Theoretical constraints of physical and chemical properties of hydrothermal fluids on variations in chemolithotrophic microbial communities in seafloor hydrothermal systems
© Nakamura and Takai; licensee Springer. 2014
Received: 8 November 2013
Accepted: 15 March 2014
Published: 22 April 2014
In the past few decades, chemosynthetic ecosystems at deep-sea hydrothermal vents have received attention as plausible analogues to the early ecosystems of Earth, as well as to extraterrestrial ecosystems. These ecosystems are sustained by chemical energy obtained from inorganic redox substances (e.g., H2S, CO2, H2, CH4, and O2) in hydrothermal fluids and ambient seawater. The chemical and isotope compositions of the hydrothermal fluid are, in turn, controlled by subseafloor physical and chemical processes, including fluid–rock interactions, phase separation and partitioning of fluids, and precipitation of minerals. We hypothesized that specific physicochemical principles describe the linkages among the living ecosystems, hydrothermal fluids, and geological background in deep-sea hydrothermal systems. We estimated the metabolic energy potentially available for productivity by chemolithotrophic microorganisms at various hydrothermal vent fields. We used a geochemical model based on hydrothermal fluid chemistry data compiled from 89 globally distributed hydrothermal vent sites. The model estimates were compared to the observed variability in extant microbial communities in seafloor hydrothermal environments. Our calculations clearly show that representative chemolithotrophic metabolisms (e.g., thiotrophic, hydrogenotrophic, and methanotrophic) respond differently to geological and geochemical variations in the hydrothermal systems. Nearly all of the deep-sea hydrothermal systems provide abundant energy for organisms with aerobic thiotrophic metabolisms; observed variations in the H2S concentrations among the hydrothermal fluids had little effect on the energetics of thiotrophic metabolism. Thus, these organisms form the base of the chemosynthetic microbial community in global deep-sea hydrothermal environments. In contrast, variations in H2 concentrations in hydrothermal fluids significantly impact organisms with aerobic and anaerobic hydrogenotrophic metabolisms. Particularly in H2-rich ultramafic rock-hosted hydrothermal systems, anaerobic and aerobic hydrogenotrophy is more energetically significant than thiotrophy. The CH4 concentration also has a considerable impact on organisms with aerobic and anaerobic methanotrophic metabolisms, particularly in sediment-associated hydrothermal systems. Recently clarified patterns and functions of existing microbial communities and their metabolisms are generally consistent with the results of our thermodynamic modeling of the hydrothermal mixing zones. These relationships provide important directions for future research addressing the origin and early evolution of life on Earth as well as for the search for extraterrestrial life.
KeywordsDeep-sea hydrothermal systems Chemosynthetic ecosystems Hydrothermal fluid chemistry Host rock geochemistry Geochemical modeling Bioavailable energy yield
Deep-sea hydrothermal vents host some of the most diverse microbial communities on Earth (Takai and Nakamura 2011). Since the first discovery of black smoker vents inhabited by dense and unique chemosynthetic macrofaunal communities (Spiess et al. 1980), submarine hydrothermal systems and their associated biota have attracted great interest (e.g., Humphris et al. 1995; Van Dover 2000; Wilcock et al. 2004). Unlike most biological communities, in which photosynthetic organisms are the base of the food web, deep-sea hydrothermal vent ecosystems are dependent on primary production by symbiotic and free-living chemolithoautotrophic microorganisms that obtain energy from inorganic redox substances (e.g., H2S, CO2, H2, CH4, and O2) in hydrothermal fluids and ambient seawater (Karl, 1995; Kelley et al. 2002). Because of the unique features of deep-sea hydrothermal vent ecosystems, they are considered plausible analogues to the early ecosystems of Earth and also to extraterrestrial life on other planets and moons (e.g., Jannasch and Mottl 1985; Nealson et al. 2005; Takai et al. 2006a).
To date, more than 300 high-temperature hydrothermal vent systems have been identified at mid-ocean ridges (MOR), island arcs, and back-arc spreading centers (Hannington et al. 2011). Deep-sea hydrothermal fluids vary greatly in their chemical compositions due to subseafloor physical and chemical processes such as fluid-rock interactions, magmatic volatile inputs, and phase separation of hydrothermal fluids (Von Damm 1995; Butterfield et al. 2003; German and Von Damm 2004; Tivey 2007). Compositional variations in hydrothermal fluids (particularly energy and carbon sources) in turn affect biomass production and the diversity of hydrothermal vent-endemic communities. Consequently, clarifying the relationships among the geological background of hydrothermal environments, physical and chemical variations in hydrothermal fluids, and the compositional and functional diversity of chemosynthetic ecosystems has provided important information on the diversification and development of extant deep-sea hydrothermal ecosystems as well as the generation and sustenance of early ecosystems and possible extraterrestrial life forms.
In deep-sea hydrothermal vents, rapid mixing between hot reduced hydrothermal fluids and cold oxidized seawater provides chemical energy for microbial activity and biomass production. To quantify the in situ energetics of chemolithotrophic microorganisms in hydrothermal mixing environments, a thermodynamic model was first proposed and applied to a basalt-hosted hydrothermal system at 21° N on the East Pacific Rise (EPR) (McCollom and Shock 1997). Using batch-mixing models modified from this original model, thermodynamic calculations have been conducted for several hydrothermal vent systems at MOR and arc-backarc (ABA) hydrothermal systems (Shock and Holland 2004; Tivey 2004; McCollom 2007; Amend et al. 2011). These studies have demonstrated differing patterns in the potential energy yields of various in situ metabolic reactions in the mixing zones of these habitats, providing the theoretical basis for relationships between hydrothermal fluid chemistry and the diversity of hydrothermal vent-endemic biological communities. However, the hydrothermal systems studied were quite limited. In addition, the structures and functions of extant chemosynthetic biological communities, which have been characterized in many previous investigations, have not yet been integrated into development of these theoretical relationships.
Many studies have identified high compositional and functional diversity of chemosynthetic ecosystems in geographically and geologically diverse hydrothermal systems (e.g., in reviews by Huber and Holden 2008; Nakagawa and Takai 2008; Takai et al. 2006b). Some of these studies have noted possible relationships between the metabolic abundances and compositions of hydrothermal vent-endemic microbial communities and the chemical characteristics of hydrothermal vent fluids in deep-sea hydrothermal systems (Perner et al. 2007, 2010; Reysenbach and Shock 2002; Takai and Horikoshi 1999; Takai et al. 2001, 2004a). However, most of these studies were qualitative and focused mainly on the genetic and phylogenetic diversity of microbial communities and their constituents. Thus, the relationships between the abundance and composition of chemolithotrophic microbial communities and the geological and geochemical environments of global deep-sea hydrothermal systems remain unclear.
Takai and Nakamura ( 2010, 2011) first provided clear evidence of biogeochemical relationships among microbiological community development, the chemical composition of hydrothermal fluids, and the geological environment of deep-sea hydrothermal systems through both thermodynamic calculations of the potential energy yields of various in situ metabolic reactions and observed compositional and functional diversity of chemosynthetic ecosystems in the mixing zones of these habitats. However, examples of hydrothermal systems for this comparison were still scarce; thus, only microbial populations in chimney habitats adjacent to high-temperature hydrothermal fluids were characterized by quantitative cultivation techniques and included. In the present study, we conducted a more comprehensive evaluation of the relationships among variations in geology, geochemistry, and microbial metabolisms and the diversity of communities in global deep-sea hydrothermal environments, based on compilation of a substantial hydrothermal fluid chemistry data set and microbial communities in the mixing zones of a wide variety of habitats.
Metabolic reactions for chemolithoautotrophy considered in this study
Overall chemical reaction
Identified (I)/cultured (C)
ΔG r° 2, 250(kJ) a
CH4 + 2O2 = CO2 + 2H2O
I and C
Hydrogenotrophic O2 reduction
H2 + 1/2O2 = H2O
I and C
Thiotrophic (H2S-oxidizing) O2 reduction
H2S + 2O2 = SO4 2- + 2H+
I and C
Fe(II)-oxidizing O2 reduction
Fe2+ + 1/4O2 + H+ = Fe3+ + 1/2H2O
I and C
H2 + 1/4CO2 = 1/4CH4 + 1/2H2O
I and C
Hydrogenotrophic SO4 reduction
H2 + 1/4SO4 2- + 1/2H+ = 1/4H2S + H2O
I and C
Hydrogenotrophic Fe(III) reduction
H2 + 2Fe3+ = 2Fe2+ + 2H+
I and C
Anoxic methanotrophy with SO4 reduction
CH4 + SO4 2- = HCO3 - + HS- + H2O
I but not yet C
where ΔG r is the Gibbs free energy of the reaction, ΔG r ° is the standard-state Gibbs free energy of the reaction, R is the universal gas constant, T is the temperature in Kelvin, and Q r is the activity quotient of the compounds involved in the reaction. The Q r term takes into account the contribution of the fluid composition to the Gibbs free energy of each reaction, determined based on the chemical composition of the mixed fluid estimated from the reaction path calculations. The energy available from the metabolic reactions as a function of temperature (equivalent to the mixing ratio) was calculated by multiplying the calculated Gibbs free energy for the reaction at each temperature by the concentrations of the reactants in the mixed fluid. This method takes into account the stoichiometry of the reaction and the reactants that are limiting, multiplied by the total amount of mixed fluid at that temperature (McCollom and Shock 1997; McCollom 2007).
This calculation yields an estimate of the maximum energy that is potentially available from the metabolic reactions per kilogram of mixed fluid. We used the average ΔG r values for four temperature ranges: <25°C, 25°C to 45°C, 45°C to 80°C, and 80°C to 125°C, representing the chemolithotrophic metabolisms of psychrophilic, mesophilic, thermophilic, and hyperthermophilic microbial organisms, respectively.
Geological settings and geochemical characteristics of seafloor hydrothermal systems
As noted above, we compiled data for 89 deep-sea hydrothermal vent sites located in various geological settings (Figure 1), including MOR, ABA, and SED hydrothermal systems. These can be further subdivided into the following six categories: basalt-hosted systems in MOR settings (MOR-B), ultramafic rock-associated systems in MOR settings (MOR-U), mafic rock-hosted systems in ABA settings (ABA-M), felsic rock-hosted systems in ABA settings (ABA-F), SED systems in MOR settings (SED-MOR), and SED systems in ABA settings (SED-ABA).
MOR hydrothermal systems
The global MOR system is the largest mountain chain in the world, with a total length of more than 60,000 km. Magma production in the MOR system far exceeds that in any other tectonic environment, accounting for more than 60% by volume of the total annual flux of magma from the mantle to the crust (Fisher and Schmincke 1984; Schmincke 2004). Therefore, the MOR system is the locus of the greatest amount of hydrothermal activity on Earth. Most MOR hydrothermal vents are hosted by basalt (often termed mid-ocean-ridge basalt). Therefore, many studies of deep-sea hydrothermal systems have focused mainly on basalt-hosted hydrothermal systems (Karl 1995; Kelley et al. 2002). However, in recent years, increasing attention has been paid to hydrothermal systems associated with ultramafic rocks present in the MOR (Kelley et al. 2001, 2005; Früh-Green et al. 2004), because the geochemical characteristics of ultramafic rock-hosted hydrothermal fluids are significantly different from those of basalt-hosted ones (Charlou et al. 2002).
Hydrothermal fluids from basalt-hosted systems are characterized by enrichment in base metals, a generally neutral or weakly acidic in situ pH, and strongly reducing conditions compared to seawater, due to subseafloor hydrothermal reactions between basaltic rocks and seawater at high temperature and pressure (Seyfried et al. 1991; Wetzel and Shock 2000). However, the fluids from ultramafic rock-associated systems are often characterized by an abundance of dissolved H2 and CH4 compared to basalt-hosted hydrothermal fluids (Figure 2) (Charlou et al. 1998, 2002). This is attributed to differences in the mineralogy and bulk chemistry of the rocks, resulting in a substantially different alteration reaction known as serpentinization (Janecky and Seyfried 1986; Wetzel and Shock 2000; Allen and Seyfried 2003). H2 concentrations of 12 to 16 mmol/kg (roughly 1 to 2 orders of magnitude higher than in basalt-hosted hydrothermal fluids) due to serpentinization have been reported in ultramafic rock-hosted deep-sea hydrothermal vent fluids (Additional file 1) (Charlou et al. 2002; Kelley et al. 2005). In addition, enrichment of CH4 in ultramafic rock-associated systems is likely associated with reduction of CO2 to CH4 under highly reducing (high H2) conditions.
ABA hydrothermal systems
Although significant global magma production occurs in the MOR, the second most active volcanic area is the subduction zone (Fisher and Schmincke 1984; Schmincke 2004), where ABA volcanic systems develop. Some arc volcanoes are subaerial, particularly in continental arc settings, whereas more than 40% of volcanic arcs are oceanic island arcs where most volcanoes are submarine (Leat and Larter 2003). In oceanic island arcs and associated back-arc basins, many deep-sea hydrothermal vent sites hosted by active submarine ABA volcanisms have been discovered (Ishibashi and Urabe 1995; Gamo et al. 2006). The chemical characteristics of these ABA hydrothermal systems are significantly different from those of MOR hydrothermal systems, although they share many common features derived from the basic reactions and processes of subseafloor hydrothermal circulation. In particular, ABA hydrothermal fluids are characterized by large variations in chemical composition (Ishibashi and Urabe 1995; Gamo et al. 2006). This chemical variability is primarily attributed to a variety of host-rock compositions (from basaltic to rhyolitic), abundant input of volatile elements from magmas (e.g., CO2 and SO2), and the variable water depth (shallow to deep) of the submarine volcanoes.
SED hydrothermal systems
Some hydrothermal vent sites are covered with sediments, which influence the chemical composition of their hydrothermal fluids. SED hydrothermal systems are found in both MOR (e.g., Juan de Fuca, Middle Valley, Escanaba Trough, and Guaymas Basin) and ABA (e.g., Okinawa Trough) settings in which hydrothermal vent sites are in close proximity to continental runoff sources. Irrespective of differences in tectonic setting or host-rock composition, SED hydrothermal systems have characteristic chemical compositions, e.g., relatively high pH, low metal content, and high CH4 and NH3 concentrations (German and Von Damm 2004). There are only minor differences in chemical composition between SED hydrothermal systems in MOR and ABA settings (Figure 2). Thus, the chemical features of SED hydrothermal vent fluids are more strongly affected by the sediment than by the tectonic setting or host-rock composition.
Factors controlling hydrothermal fluid chemistry
It is believed that hydrothermal fluid flux is primarily controlled by the crust (magma) production rate, because magmatic heat derived from creation of new oceanic crust (cooling from 1,200°C to 350°C) heats hydrothermal fluids from 2°C to 350°C (e.g., Elderfield and Schultz 1996). Based on this, Kawahata et al. ( 2001) estimated that the maximum volume of high-temperature hydrothermal fluid is twice that of the upper oceanic crust (the volcanic and sheeted dike sequence) and if 65% to 85% of the rocks are altered to secondary minerals, the volumetric water/rock ratio would be 2.3 to 3.1. This clearly suggests that high-temperature hydrothermal fluids are generated under rock-dominated (low water/rock ratio) conditions (Kawahata et al. 2001). Therefore, the chemical compositions of hydrothermal fluids are predominantly controlled by water-rock reactions and fluid-mineral equilibria (Seyfried et al. 1991; Shock 1992; Seyfried and Ding 1995). Thus, host-rock geochemistry is one of the most important factors controlling hydrothermal fluid chemistry. In addition to the chemical compositions of host rocks, however, other processes such as input of volatiles from magmas, phase separation of hydrothermal fluids, and interactions with sediment also have a significant impact on the observed compositions of hydrothermal fluids.
Chemical composition of host rocks
Differences in the rock types in the reaction zone can lead to large variations in the hydrothermal fluid chemistry, because the bulk chemical composition and primary minerals in the source rock control the reaction sequences and their chemical equilibria.
Mafic rocks Most ocean basins (including MOR and ABA settings) are of mafic composition (mainly basaltic). The chemical systematics of mafic rock-seawater systems (particularly basalt-seawater systems) have been well characterized based on field observations, hydrothermal experiments, and theoretical studies (Bischoff and Dickson 1975; Mottl and Holland 1978; Seyfried and Mottl 1982; Mottl 1983; Reed 1983; Bowers and Taylor 1985; Seyfried 1987; Von Damm 1990, 1995; Seyfried et al. 1988, 1991; Shock 1992; Saccocia et al. 1994; Wetzel and Shock 2000; Butterfield et al. 2003; Nakamura et al. 2007).
Basalt-hosted hydrothermal fluids have relatively low pH at 25°C and 1 atm (generally 3 to 4) and notable enrichment in base metals (e.g., Fe and Mn) and dissolved gases (e.g., H2, CO2, and CH4) compared to seawater (Figure 2). The in situ pH of the basalt-hosted vent fluids are neutral to weakly acidic, significantly different from the pH measured at 25°C and 1 atm in laboratory experiments (German and Von Damm 2004). This discrepancy is mainly caused by dissociation of H+-bearing aqueous complexes (e.g., HCl0) due to cooling during sample processing (Shock et al. 1989; Seyfried et al. 1991; Ding and Seyfried 1992; Ding et al. 2005). Another possible mechanism of pH change is precipitation of metal sulfides below the seafloor, producing protons (German and Von Damm 2004).
In high-temperature MOR vent fluids, most metals are enriched by up to 7 to 8 orders of magnitude compared to seawater. The stability of chloride complexes (e.g., FeCl2 0) increases with increasing temperature, and therefore, most metal ions are present in high-temperature fluids as chloride complexes (Helgeson et al. 1981; Ding and Seyfied 1992). The substantial increase in the metal solubility produces the high concentrations in the vent fluids.
Basalt-hosted hydrothermal fluids are also highly reducing, as evidenced by the presence of H2S rather than SO4, as well as by significant amounts of H2, CH4, Fe2+, and Mn2+. These chemical features are generally consistent with phase-equilibrium calculations involving the observed primary and secondary minerals (feldspar, chlorite, epidote, quartz, magnetite, anhydrite, pyrite, and pyrrhotite) and seawater at in situ hydrothermal fluid temperatures and pressures (Bowers et al. 1988; Seyfried et al. 1988, 1999; Saccocia and Seyfried 1990; Seyfried and Ding 1995; McCollum and Shock 1998; Wetzel and Shock 2000). Time-series measurements of chemical compositions of hydrothermal fluids in MOR regions have indicated steady-state concentrations of dissolved species (Campbell et al. 1988; Bowers et al. 1988; Butterfield et al. 1994; Von Damm 1988, 1995, 2000), reflecting clear solubility control by mineral phases in the subseafloor reaction zones and recharge zones.
Ultramafic rocks Compared with hydrothermal fluids in mafic rock-hosted systems, ultramafic rock-associated hydrothermal fluids are characterized by conspicuous enrichment in H2 in the presence or absence of phase separation processes (Figure 2). Production of H2 during serpentinization of ultramafic rocks results from reaction of water with Fe2+-bearing minerals, primarily olivine and pyroxene. In these reactions, Fe2+ is partially oxidized to Fe3+ by the water, resulting in precipitation of magnetite in the serpentinite. The water reduced by the Fe2+ also produces H2. One of the important chemical features of ultramafic rocks that constrains abundant H2 production during serpentinization is relatively low Al concentrations. Low Al activity results in formation of alteration minerals (particularly serpentines and brucite) that have a tendency to exclude Fe2+ from their structure. This leads to oxidation of Fe2+ by water to form magnetite. In contrast, because mafic rocks have higher Al contents than ultramafic rocks, a much greater proportion of the Fe2+ is sequestered in Al-bearing alteration minerals (e.g., chlorite), limiting oxidation of Fe2+ to Fe3+. Thus, hydrothermal alteration of mafic rocks generates much lower amounts of H2 and magnetite than serpentinization of ultramafic rocks, even though the Fe content of basaltic rocks is higher than that of ultramafic rocks. Basaltic rock-hosted vent fluids typically exhibit H2 concentrations of <1 mmol/kg, whereas >10 mmol/kg H2 has frequently been reported for ultramafic rock-associated fluids (Additional file 1). The potential for even higher H2 concentrations (>100 mmol/kg) has been suggested by both petrological (Frost 1985; Alt and Shanks 1998) and experimental (Berndt et al. 1996; McCollom and Seewald 2001) studies.
In addition, ultramafic rock-associated hydrothermal fluids are often characterized by CH4 enrichment (Figure 2). Although the origin of CH4 in these fluids is controversial, it is generally thought to be derived from reduction of CO2 by high concentrations of H2 through abiotic methanogenesis (Nakamura et al. 2009). However, the hydrothermal fluid CH4 concentrations are always disequilibrated with the concomitant H2 and CO2 concentrations, suggesting that the subseafloor hydrothermal circulation system is an open system with respect to CH4 content. Enriched CH4 (>0.5 mmol/kg) has also been observed in hydrothermal fluids from certain basalt-hosted systems at the MOR (Figure 2; Lucky Strike and Menez Gwen hydrothermal fields) (Additional file 1). Both of these fields are located in the northern Mid-Atlantic Ridge, where several ultramafic rock-associated hydrothermal systems have been discovered. Based on geological and geochemical lines of evidence, it has been suggested that the high CH4 concentrations in these basalt-hosted hydrothermal fluids were caused by serpentinization of ultramafic rocks somewhere in the subseafloor (Charlou et al. 2000).
Felsic rocks Hydrothermal systems hosted by felsic rocks have been identified only in ABA settings (Figure 1). Felsic rock-hosted hydrothermal fluids are characterized by relatively low pH and enrichment in H2S, CO2, K, Mn, and Fe compared to mafic rock-hosted fluids (Figure 2). The chemical characteristics of felsic rock-hosted hydrothermal fluids are generally consistent with experimental results for seawater-felsic rock interactions (e.g., Hajash and Chandler 1981). For example, felsic rocks contain high concentrations of incompatible elements such as K. Enrichment of K in felsic rock-hosted fluids originates from the bulk rock composition. In addition, the lower pH is attributed to the low ability of felsic rocks to consume H+ in solution. The pH of a hydrothermal solution is lowered by removal of Mg2+ via precipitation of Mg-hydroxysulfate during heating of the seawater (Bischoff and Seyfried 1978) and by formation of Mg-bearing alteration minerals (e.g., smectite and chlorite) during seawater-rock interactions (Mottl 1983). In a basalt–seawater system, the H+ generated in the fluid is consumed by dissolution of Ca from the reacted rocks (Seyfried and Mottl 1982; Mottl 1983). Mg-Ca exchange reactions control the fluid pH to approximately neutral under in situ conditions (Seyfried and Mottl 1982; Wetzel and Shock 2000). However, because felsic rocks are relatively depleted in Ca, their ability to buffer pH changes is significantly lower than that of their mafic counterparts.
Inputs of magmatic volatiles
Enrichment of H2S and CO2 in felsic rock-hosted hydrothermal fluids cannot be explained only by water-rock interactions. Instead, enrichment in these volatiles can be caused by inputs of magmatic volatiles into hydrothermal systems. ABA magmas (particularly those that are felsic in composition) have very high concentrations of volatile elements and molecules, and hydrothermal fluids that are highly enriched in sulfur and/or CO2 have been observed in ABA hydrothermal systems, mainly hosted by more siliceous rocks, e.g., andesite, calcite, and rhyolite rather than by basalt (Gamo et al. 1997; Sakai et al. 1990; Inagaki et al. 2006; Lupton et al. 2006, 2008). Therefore, enrichment in CO2 and H2S of felsic rock-hosted hydrothermal fluids is likely due to significant inputs of magmatic volatiles into these hydrothermal systems.
Compared to that for SO2 (see below), the dissociation constant of this reaction is much smaller, particularly under high-temperature conditions. It is therefore believed that the effect of CO2 on the fluid pH is not very significant. However, segregation of CO2 from upwelling hydrothermal fluids in the subseafloor can result in consumption of H+ in the fluid, increasing the pH. Even a small pH increase during ascent of the hydrothermal fluid can cause subseafloor precipitation of metal-sulfide minerals, resulting in low heavy metal concentrations in the hydrothermal fluids. This process would be expected in hydrothermal systems with significant inputs of CO2 but not SO2 from magma, such as hot spot-influenced MOR hydrothermal systems and basalt-hosted arc-backarc hydrothermal systems.
Once the of the hydrothermal fluid reaches the sulfate-sulfide boundary via reaction (3), sulfuric acid is produced by reaction (4). The presence of sulfuric acid can cause a significant decrease in pH. Because the solubility of heavy metals is quite sensitive to pH, the pH decrease caused by SO2 promotes dissolution of heavy metals from the reacted rocks. Volatile inputs from magmas occur intermittently, and even during such activity, the chemistry of hydrothermal fluids is controlled by reactions induced by both volatile inputs and water-rock interactions. Therefore, it is likely that the chemical composition of the fluids, as is typical of open and dynamic systems, significantly varies with space and time. Nevertheless, felsic rock-hosted hydrothermal systems affected by magmatic volatile inputs clearly exhibit high concentrations of base metals and low pH (Figure 4).
As described above, the concentrations of all components in hydrothermal fluids exhibited positive or negative correlations with Cl, except for H2, CO2, and CH4 in several samples affected by serpentinization of ultramafic rocks, CO2 inputs from magma, and CH4 inputs from sedimentary organic matter and/or microbial processes (Figure 2). Deep-sea hydrothermal fluids often reach temperatures high enough that they separate into vapor and brine phases. The phase separation temperature depends primarily on the pressure conditions (i.e., water depth) of the hydrothermal system. The observed temperatures of hydrothermal fluids from various vent sites were clearly limited by the two-phase boundary of seawater (Bischoff and Pitzer 1989) (Figure 3). Phase separation and subsequent remixing of the vapor and brine phases produce hydrothermal fluids with a wide range of salinities, from 1 order of magnitude lower to several times higher than that of seawater (Figure 2).
Presence of sediments
SED hydrothermal systems have chemical compositions distinct from those of other hydrothermal fluids. Compared to those of sediment-starved MOR and ABA hydrothermal systems, SED hydrothermal fluids generally have relatively high pH, lower heavy metal contents, and higher CH4 and NH4 + concentrations (Figure 2) (German and Von Damm, 2004). The very high CH4 concentrations of hydrothermal fluids in SED systems are attributed to thermal decomposition of organic matter at high temperatures during hydrothermal reactions at discharge zones and/or microbial methanogenesis at relatively low temperatures at sedimentary recharge zones (Lilley et al. 1993; Kawagucci et al. 2011, 2013). Likewise, the source of NH4 + in SED hydrothermal systems is considered to be thermal decomposition and microbial ammonification of organic matter (Kawagucci et al. 2011, 2013). High concentrations of NH4 + in these hydrothermal fluids provide an NH3/NH4 + buffer that maintains the relatively high pH of the fluid (German and Von Damm, 2004). This greatly decreases the solubility of metal-sulfide minerals, leading to low heavy metal concentrations in the hydrothermal-vent fluids.
Effects of hydrothermal fluid chemistry on the bioavailable energy yield
The chemosynthetic primary producers that sustain deep-sea hydrothermal vent ecosystems utilize inorganic substances (e.g., H2S, CO2, H2, and CH4) derived from hydrothermal vent fluids as energy and carbon sources. Thus, deep-sea hydrothermal vent ecosystems should be at least partially controlled by the chemical composition of the hydrothermal fluids. The effects of hydrothermal fluid compositions on deep-sea hydrothermal vent ecosystems based on the energy yields available to various chemolithotrophic metabolisms are described below.
Hydrogen sulfide (H2S)
The exception is in hydrothermal plumes, where much higher seawater mixing ratios (>1000) and low temperatures (up to several degrees Celsius) are found. In hydrothermal plume environments, the concentration of H2S in the source hydrothermal fluid, rather than the seawater-dissolved O2, becomes the limiting factor for sulfur-oxidizing chemolithotrophic metabolism.
In contrast to H2S, variations in the H2 concentration directly affected the potential energy for the chemolithotrophic microbial population, not only for aerobic H2 oxidation but also for most anaerobic energy metabolisms other than anaerobic methane oxidation. This feature is partially attributed to the wide range of H2 concentrations in hydrothermal fluids. For example, typical basalt-hosted hydrothermal fluids had H2 concentrations of <1 mmol/kg (Figure 2). In contrast, ultramafic rock-hosted hydrothermal fluids had H2 concentrations 1 to 2 orders of magnitude higher, whereas hydrothermal fluids in ABA settings had H2 concentrations 1 order of magnitude lower (Figure 2). Thus, potential energy yields for aerobic and anaerobic H2-oxidizing (H2-trophic) metabolisms were directly correlated with H2 concentrations in the end-member hydrothermal fluids (Figure 6B, C, D). For aerobic H2-oxidizing metabolism, nearly the same amount of metabolic energy was available irrespective of the H2 concentration in the end-member hydrothermal fluid (Figure 6B), when the H2 concentration exceeded approximately 1 mmol/kg (for hyperthermophiles at relatively high temperatures) to approximately 10 mmol/kg (for psychrophiles to hyperthermophiles at all temperature ranges). As with H2S oxidation, this occurs because seawater-dissolved O2 rather than H2 becomes the limiting factor for aerobic H2-oxidizing metabolism.
However, because most seafloor hydrothermal fluids had H2 concentrations <1 mmol/kg, except for ultramafic rock-hosted and highly vapor phase-enriched hydrothermal fluids (Figure 2), variations in the H2 concentration of the end-member hydrothermal fluid significantly affected the potential energy yields of nearly all H2-trophic chemolithotrophs (Figure 6B, C, D). This variation is expected to have a strong impact on biomass production and the compositional structure of most H2-trophic microbial populations as well as the entire microbial community. As described above, the abundance of H2S in hydrothermal fluids is relatively constant among most hydrothermal systems, tectonic settings, and geological conditions. In addition, H2S is coupled only to aerobic (both O2- and NO3-reducing) sulfur-oxidizing metabolisms. In contrast, the abundance of H2 in end-member hydrothermal fluids is highly variable and constrains various aerobic and anaerobic chemolithotrophic energy metabolisms for primary production.
Although ultramafic rock-associated hydrothermal fluids are significantly enriched in H2 (Charlou et al. 2002), in several phase separation-influenced (vapor phase-abundant) hydrothermal fluids hosted by MOR-B, H2 can also be comparably enriched (Lilley et al. 2003) (Figure 2). In these hydrothermal systems, therefore, the energy yield of H2-trophic metabolisms was similar to that in ultramafic rock-hosted hydrothermal systems (Figure 6B, C, D). However, the abundant availability of H2 (as well as other gaseous species) induced by phase separation in MOR-B-hosted hydrothermal fluids is generally transient and lasts several weeks to several months (Lilley et al. 2003). Thus, the effect of temporal enrichment of hydrothermal fluid H2 on biomass production and compositional structure of the entire microbial community is likely transient and minor.
The CH4 concentration in seafloor hydrothermal fluids was also variable, ranging from the nanomole per kilogram level in ABA hydrothermal fluids to the millimole per kilogram level in SED and ultramafic rock-hosted fluids. Variations in the CH4 concentration in hydrothermal fluids could affect both aerobic and anaerobic methane oxidizers (Figure 6E, F).
The potential metabolic energy from anaerobic CH4 oxidation (methanotrophy) was directly correlated with the CH4 concentration in the hydrothermal fluid (Figure 6F), suggesting that the anaerobic methanotrophic population is likely affected by CH4 concentrations in end-member hydrothermal fluids. This is attributable to the large amount of SO4 2- in seawater; these high levels of SO4 2- are always present in seawater-hydrothermal fluid mixing zones in all habitable temperature ranges. For aerobic CH4 oxidation reactions, the potential energy yield was also affected by the CH4 concentration in end-member hydrothermal fluids, except for hydrothermal fluids with high CH4 concentrations (>0.2 mmol/kg for hyperthermophiles to >2 mmol/kg for psychrophiles) (Figure 6E).
Variation in the Fe2+ concentration of the hydrothermal fluids was also large, from the nanomole per kilogram level to the millimole per kilogram level (comparable to the ranges for H2 and CH4 concentrations). This variation in the Fe2+ concentration of the hydrothermal fluids could affect aerobic iron-oxidizing chemolithotrophy. The potential energy yield from the aerobic Fe oxidation reaction was well correlated with the Fe2+ concentration in the hydrothermal fluid (Figure 6G). However, for highly Fe2+-enriched hydrothermal fluids (>0.2 mmol/kg for hyperthermophiles to >2 mmol/kg for psychrophiles), the amount of available metabolic energy was saturated with respect to the Fe2+ concentration in the end-member hydrothermal fluid (Figure 6G). The metabolic energy yield potentially obtained from aerobic oxidation of 1 mol of Fe2+ was several times smaller than that from aerobic oxidation of 1 mol of H2S, H2, or CH4 (Figure 6). This may affect the relative abundance of aerobic Fe-oxidizer populations in deep-sea hydrothermal vent ecosystems.
In contrast to aerobic Fe-oxidizing chemolithotrophy, there was an essentially negligible energy yield predicted for anaerobic Fe3+ reduction using H2 or CH4 for all types of deep-sea hydrothermal fluids and systems. This is attributed to an extremely low concentration of Fe3+ in both seawater and hydrothermal fluids.
Effect of the geological setting of the hydrothermal system on the bioavailable energy yield
In the MOR-B and ABA-M settings, aerobic oxidation of H2 and CH4 were the second most available metabolic reactions, particularly at higher temperatures (lower mixing ratios). On the other hand, in the ABA-F setting, aerobic Fe2+ oxidation was the second most favorable chemolithotrophic metabolism (Figure 8A). These differences are directly related to the different chemical compositions of the end-member hydrothermal fluids (e.g., H2, CH4, and Fe2+ concentrations) in these settings, ultimately derived from the oxidation state of the magmas and/or volatile (particularly SO2) inputs into the hydrothermal fluids. Relatively little energy was predicted to be available from anaerobic chemolithotrophic metabolisms for these settings, except for temporally and spatially limited habitats induced by phase separation of hydrothermal fluids (Figure 8B).
In the MOR-U and SED settings, the potential energy from aerobic oxidation of H2 or CH4 exceeded that from aerobic sulfur oxidation at higher temperatures (lower mixing ratios) (Figure 8A). More importantly, in these settings, considerable energy for primary production can be obtained from anaerobic chemolithotrophic metabolisms and populations (Figure 8B). Particularly in high-temperature habitats, anaerobic chemolithotrophs are expected to play a prominent role as primary producers (Figure 8A, B). This represents a marked difference in potential chemolithotrophic microbial communities between the MOR-U and SED settings and the more common MOR-B and ABA settings.
In the MOR-U setting, because of the high H2 concentrations in end-member fluids, both aerobic and anaerobic H2-trophic population reducers were energetically dominant primary producers (Figure 8A, B). In addition, the total potentially bioavailable energy yields in the mixing zones were greater in the MOR-U setting than in the typical MOR-B and ABA settings (Figure 8A, B). Thus, the MOR-U deep-sea hydrothermal environments may supply more abundant and diverse energy sources for biological production.
In the SED setting, aerobic methanotrophy could be competitive with aerobic sulfur oxidation in all temperature ranges (Figure 8A). Interestingly, among all possible chemolithotrophic metabolisms, anaerobic (sulfate-reducing) methanotrophy was by far the most favorable energy-generating metabolism, particularly in high-temperature habitats (Figure 8B). The total amount of potentially bioavailable energy yield in the mixing zones of habitats in the SED setting was also greater than in the typical MOR-B and ABA settings.
Comparison of existing chemolithotrophic microbial communities with the results of thermodynamic modeling
Above, we have provided the theoretical basis for relationships between the geological environments of hydrothermal activity (e.g., tectonic settings, basement-rock geochemistry, abundance of sediments, magmatic volatile input, and phase separation related to subseafloor hydrothermal processes), physical and chemical variations in hydrothermal fluids, and the compositional diversity of potentially bioavailable energy for various vent-endemic chemolithotrophic metabolisms estimated using thermodynamic models. We have shown that the abundance and composition of chemolithotrophic energy metabolisms in hydrothermal vent biological communities is directly constrained by the physical and chemical characteristics of the hydrothermal mixing zones of habitats, which are subject to the physical and chemical properties of end-member hydrothermal fluids. Furthermore, the physical and chemical characteristics of the end-member hydrothermal fluids are substantially controlled by the geological settings that host the hydrothermal systems. Thus, it seems likely that the abundance and composition of chemolithotrophic energy metabolisms in microbial communities located in a given deep-sea hydrothermal system could be systematized in terms of geological backgrounds based on the results of the thermodynamic models.
In typical mixing zones in deep-sea hydrothermal habitats, chemolithotrophic microbial communities consist of organisms with three typical lifestyles: surface-attached or biofilm-forming free-living entities, planktonic free-living entities, and symbiotic entities. Here, we discuss potential patterns in chemolithotrophic microbial community development delineated by recent microbiological investigations (biogeochemical, ecological, and molecular approaches) for representative hydrothermal mixing zones of habitats in which the predominant organisms have different lifestyles.
Hydrothermal plumes are typical of mixing zone habitats that host planktonic free-living microbial communities and are characterized by low temperatures and quite low mixing ratios of hydrothermal fluids (<0.1%). In hydrothermal plumes, the SUP05 group of Gammaproteobacteria is the most abundant and geographically widespread microbial component (Sunamura et al. 2004; Dick and Tebo 2010; German et al. 2010). The deep-sea vent Epsilonproteobacteria (Sunamura et al. 2004; Nakagawa et al. 2005a; German et al. 2010), methanotrophic Gammaproteobacteria (Lam et al. 2008), and ammonia-oxidizing Betaproteobacteria and Thaumarchaeota (Lam et al. 2008; Takai et al. 2004b) have been identified as other dominant microbial populations.
Although microbial communities in hydrothermal plumes have variable abundances and compositions of chemolithotrophic metabolisms, there have been few quantitative studies or functional characterizations of these communities. Thus, we still do not know much about how these microbial communities and their metabolisms respond to the varying physical and chemical states of hydrothermal plume habitats or how they are related to the geological backgrounds that produce the source hydrothermal fluids. Nevertheless, the general landscape of metabolic abundance and composition in hydrothermal plume microbial communities has been established via biogeochemical (Cowen et al. 1986; de Angelis et al. 1993; Mandernack and Tebo, 1993; Dick et al. 2009) and microbial ecology (Sunamura et al. 2004; Takai et al. 2004b; Nakagawa et al. 2005a; Lam et al. 2008; Dick and Tebo 2010; Lesniewski et al. 2012) investigations. For example, dominance of the sulfur-oxidizing SUP05 group of Gammaproteobacteria and the deep-sea vent Epsilonproteobacteria is commonly observed in geographically and geologically diverse deep-sea hydrothermal systems. These organisms primarily sustain themselves via aerobic sulfur oxidation; considerable populations occasionally utilize aerobic H2 oxidation for additional energy conversion if metabolically available H2 is present. In addition, much smaller but ubiquitous populations of phylogenetically diverse bacteria also utilize Fe2+ and Mn2+ oxidation for biomass production. In contrast, in hydrothermal plumes highly enriched in CH4 and NH4 +, particularly in SED hydrothermal systems, the methanotrophic Gammaproteobacteria and ammonia-oxidizing Betaproteobacteria and Thaumarchaeota dominate the microbial communities in spatially and temporally varying hydrothermal plume habitats.
An increasing number of recent observations appear consistent with our conclusions based on thermodynamic estimates of bioavailable energy yields in low-temperature mixing zones: (1) aerobic sulfur oxidation is the most common and basic chemolithotrophic energy metabolism in global deep-sea hydrothermal systems, (2) aerobic Fe2+ and Mn2+ oxidation are less abundant but widespread metabolisms, and (3) aerobic methanotrophy and ammonia oxidizer are dominant in SED systems, respectively.
Diffusing hydrothermal fluids
Microbial communities in relatively low-temperature diffusing hydrothermal fluids have been investigated in a wide variety of geographically diverse hydrothermal systems (Huber and Holden 2008; Huber et al. 2009; Perner et al. 2011, 2013a, 2013b; Akerman et al. 2013; Campbell et al. 2013). These are mainly planktonic free-living communities under conditions in which the end-member fluids have already mixed with infiltrated seawater in relatively shallow subseafloor environments in the recharge and discharge regions of hydrothermal fluids (Bemis et al. 2012). In addition to planktonic free-living populations, these microbial communities also include detached epilithic and biofilm-forming components entrained by the fluid flows.
Hydrothermal fluids diffusing at the seafloor would be expected to combine all growing, living, and dead populations and components within the entire subseafloor fluid flow path in the discharge. This differs from microbial communities in hydrothermal plume habitats in which most microbial populations are indigenously growing from planktonic origins in deep-sea water (Lesniewski et al. 2012). Thus, it is challenging to clearly understand the relationships between the diversity and composition of the observed microbial populations and hydrothermal fluid chemistry based on existing biological and geochemical data for diffusing fluid habitats. However, several studies have recently suggested the dominance of sulfur oxidizers in typical MOR-B settings and the presence of hydrogen oxidizers in MOR-U settings (Perner et al. 2011, 2013a; Akerman et al. 2013). These results are generally consistent with our thermodynamic predictions of relationships among microbial metabolisms and functions, hydrothermal fluid chemistry, and geological background.
On the other hand, a very recent study producing function-focused quantitative estimates, based on H2 and sulfide consumption and CO2 assimilation activities as well as metagenomic 16S rRNA and functional gene analyses, has indicated that even in H2-poor hydrothermal fluids in MOR-B settings, H2 oxidation-based primary production is highly attractive despite the low H2 content (Perner et al. 2013b). This leads us to consider that low-temperature diffusing flow is the product of complex subseafloor processes (including seawater-hydrothermal fluid mixing, conductive cooling, various redox reactions, and mineral precipitation), and thus, the simple batch-mixing model employed in this study may not be able to accurately reproduce all of these processes.
Geochemical data sets for low-temperature diffusing flows remain scarce. Thus, further quantitative estimates combined with in situ or detailed chemical measurements will be needed to more accurately describe interactions among the physical and chemical processes, bioavailable energy yields from chemolithotrophic metabolisms, and community development in diffusing hydrothermal fluids.
Chemolithotrophic symbionts hosted by deep-sea vent-endemic chemosynthetic invertebrates represent important primary producers in global deep-sea hydrothermal ecosystems. Their biomass production and functions may be constrained by the energy states of the habitats of both the symbionts and the host animals (Dubilier et al. 2008), as productivity and energy metabolism in a tight symbiotic association are strongly regulated by the interaction of the symbiont with the physiology and ecology of the host animal (Dubilier et al. 2008). There have been numerous studies of the basic relationships between the in situ physical and chemical conditions of habitats and the abundance and composition of energy metabolisms in deep-sea hydrothermal chemosynthetic symbioses (Beinart et al. 2012; Petersen et al. 2011; Suzuki et al. 2006; Watsuji et al. 2010, 2014). However, the energy conversion yield of the primary production of chemolithotrophic symbionts is likely one of the most important factors in the establishment of chemosynthetic symbioses, affecting the selection, acquisition, and breeding of specific bacterial counterparts. In particular, episymbioses and horizontally transmitted endosymbioses, in which symbionts are acquired from the proximal environments of habitats in their larval and adult stages in each generation, would be expected to be more strongly affected by the energy states of chemolithotrophic symbiont metabolisms than vertically transmitted endosymbioses.
Recently, several studies have been conducted of the relationship between the activity of chemolithotrophic symbionts and hydrothermal fluid chemistry, e.g., a series of studies on epibiotic microbial communities in the galatheid crab Shinkaia crosnieri in Okinawa Trough (Watsuji et al. 2010, 2012, 2014). The epibiotic microbial communities of S. crosnieri abdominal setae consist primarily of the sulfur-oxidizing Epsilonproteobacteria and Gammaproteobacteria and methanotrophic Gammaproteobacteria (Watsuji et al. 2010, 2012, 2014). These results are generally consistent with the results of our thermodynamic modeling, indicating high bioavailable energy yields from both sulfur- and CH4-oxidizing reactions at low temperatures (high seawater mixing ratios) in the Okinawa Trough (Figure 8). The abundance of epibiotic methanotrophic gammaproteobacterial populations and methanotrophic activity vary among the S. crosnieri populations recovered from different hydrothermal fields (Iheya North and Hatoma Knoll fields) (Watsuji et al. 2010). As suggested by our model calculations, these variations are likely correlated with the in situ CH4 concentrations in the S. crosnieri colonies. This may, in turn, be associated with the CH4 concentrations in the end-member hydrothermal fluids, although CH4 concentrations in the Hatoma fluids have not yet been published.
Another notable example is the dual endosymbiotic (thiotrophic and methanotrophic) populations of vent mussels living in different geological settings of deep-sea hydrothermal vent sites in the MAR and the Eastern Pacific (Petersen et al. 2011). Based on thermodynamic modeling of preferred H2-trophic energy metabolism, genetic characterization of a key enzyme gene for H2-trophic energy metabolism, and functional analyses of H2 consumption and CO2 fixation of endosymbionts in Bathymodiolus puteoserpentis in a typical MOR-U hydrothermal system (Logatchev field), Peterson et al. ( 2011) clearly demonstrated that the thiotrophic population in dual endosymbiosis of the Logatchev B. puteoserpentis use H2 and H2S comparably as energy sources for primary production. This was the first reported example of chemosynthetic symbiosis sustained by an inorganic energy source (H2) other than H2S (reduced sulfur species) or CH4. In other words, this study first revealed that compositional variations in H2, H2S, and CH4 in the mixing zones of chemosynthetic macrofaunal habitats affect the patterns and functions of episymbioses and endosymbioses in chemosynthetic microbial-faunal associations. Peterson et al. ( 2011) also showed that the thio- and H2-trophic endosymbionts hosted by different Bathymodiolus populations living in geographically and geologically distinct hydrothermal systems of the MAR and Pacific (all H2-starved MOR-B hydrothermal systems) had much lower specific H2 consumption activities than the endosymbiotic population from the H2-abundant MOR-U hydrothermal system (Logatchev field). Although not fully quantitative, these results provide strong evidence that the metabolic activity of chemolithotrophic symbionts is controlled by hydrothermal fluid chemistry and is related to the geological background of the hydrothermal system, as suggested by our model calculations.
Recently, metagenomic and metatranscriptomic approaches have also been used to study possible biogeochemical associations with Alviniconcha (deep-sea hydrothermal-vent snail) holobionts (host/symbiont associations) that dwell in a broad region of the Eastern Lau Spreading Center (ELSC) (Beinart et al. 2012; Sanders et al. 2013). Different holobiont patterns have been found in the Alviniconcha populations obtained from the mixing zones of colonies in four different hydrothermal systems in the ELSC. The endosymbionts were classified into three groups: Sulfurimonas-type Epsilonproteobacteria, gamma-1-type Gammaproteobacteria, and gamma-Lau-type Gammaproteobacteria (Beinart et al. 2012), all of which are known to be typical sulfur (and H2) oxidizers. The Alviniconcha holobiont and endosymbiont distributions varied from the northern to the southern region of the ELSC, which have somewhat different geological settings (Beinart et al. 2012). The ELSC has been well characterized from north to south in terms of geological properties (such as the spreading stage and rate, magmatic productivity, geochemistry, and host-rock geochemistry) (Tivey et al. 2012). Reflecting the change in geological setting, the chemical compositions of the end-member hydrothermal fluids also change from relatively reduced and H2- and H2S-enriched (approximately 500 μM and approximately 5 mM, respectively) in the north to relatively oxidized and H2- and H2S-depleted (approximately 30 μM and approximately 3 mM, respectively) in the south (Beinart et al. 2012). The endosymbiont species shift from predominantly Sulfurimonas-type Epsilonproteobacteria in the north to predominantly gamma-1-type Gammaproteobacteria and finally to both types of Gammaproteobacteria in the south (Beinart et al. 2012). Interestingly, the compositional abundance of both the endosymbiotic microbial components and the expressed key gene transcripts for various energy metabolisms vary with the regional geochemical gradient (Sanders et al. 2013). Under relatively reduced and H2- and H2S-enriched conditions, the compositional abundance of mRNAs related to H2- and sulfur-oxidizing metabolisms throughout the entire endosymbiont transcriptome is highly elevated (Sanders et al. 2013). The compositional abundances of the mRNAs of these energy metabolisms throughout the entire endosymbiont transcriptome are likely associated with the activities of these energy metabolisms in the endosymbiotic populations of the Alviniconcha host individuals.
Our geochemical modeling suggests that changes in the H2S concentration from north to south in the ELSC (approximately 5 mM to approximately 3 mM) should not significantly affect sulfur-oxidizing metabolisms, whereas H2-oxidizing metabolisms could be affected by the change in H2 concentration (approximately 500 μM to approximately 30 μM) (Figure 6). Indeed, based on differences in the expression of hydrogenases between Epsilonproteobacteria and Gammaproteobacteria individuals, Sanders et al. ( 2013) suggested that H2 oxidation may play a larger role in the energy metabolism of holobionts with Epsilonproteobacteria. Thus, the change in H2 concentration, rather than the H2S concentration, may account for differences in the holobiont patterns found in the Alviniconcha populations in the ELSC. Although future studies are needed to elucidate the degree to which Epsilonproteobacteria endosymbionts rely on H2 for energy production, this may be additional evidence supporting the relationship between geological constraints on hydrothermal fluid chemistry and the compositions and functions of chemosynthetic microbial symbionts in deep-sea hydrothermal environments.
Chimney structures and sediments
The compositional and functional diversity of microbial communities has been most extensively explored in deep-sea vent chimney structures that host high-temperature hydrothermal fluid emissions (Nakagawa and Takai 2008; Takai and Nakamura 2010, 2011; Takai et al. 2006b). These microbial communities consist of typical epilithic (mineral surface-attached) and/or biofilm-forming populations and are sustained by the redox disequilibria formed in the chimney wall via diffusive mixing between the internal hydrothermal fluid and external seawater. Thus, the abundance and composition of chemolithotrophic energy metabolisms in the chimney microbial communities are directly controlled by the energy states of the chimney habitats, resulting in good approximations by the thermodynamic calculations of the simple batch-mixing model.
Using data for both end-member hydrothermal fluids and chimney microbial communities obtained from six deep-sea hydrothermal systems with different geological settings, Takai and Nakamura ( 2010, 2011) constructed intra-field and inter-field comparisons between the abundance and composition of chemolithotrophic energy metabolisms predicted by thermodynamic modeling and the microbial community composition determined through quantitative cultivation methods. Based on both the thermodynamic modeling and microbiological characterization, statistically significant correlations between the H2 concentration in the hydrothermal fluid or the estimated potential energy yield of H2-trophic methanogenesis and the cultivatable population size of hydrogenotrophic methanogens were found. More recently, in addition to quantitative cultivation methods, statistical phylotype compositional analyses of 16S rRNA and other functional genes have also been used to demonstrate significant correlations between H2-trophic chemolithotrophy in chimney microbial communities and hydrothermal fluid H2 concentrations, particularly in MOR-U hydrothermal systems (Flores et al. 2011; Roussel et al. 2011). Our geochemical model provides consistent explanations for the results of these studies. Specifically, the energy yields of anaerobic (and aerobic, in most cases) H2-trophic reactions were well correlated with the H2 concentrations of hydrothermal fluids (Figure 6). In addition, thermophilic H2-trophic methanogens and sulfate/sulfur reducers are predominantly found in H2-enriched deep-sea hydrothermal systems in the MOR-U setting (Figure 8). It is thus very likely that serpentinization-driven H2 enrichment in hydrothermal fluids is an important geochemical factor that directly controls the thermodynamic energy potential, biomass, and productivity of H2-trophic chemolithotrophs.
Similar to the apparent relationship between H2 concentrations in hydrothermal fluids and the abundance of H2-trophic chemolithotroph populations, our thermodynamic calculations also identified a possible relationship between CH4 enrichment and the abundance of anaerobic methanotroph populations (particularly thermophilic methanotrophic sulfate reducers) in SED hydrothermal systems (Figure 8). In low-temperature habitats (e.g., hydrothermal plumes, diffusing fluids, and chemosynthetic animal symbioses), many molecular signals and metabolic activities of aerobic methanotrophy have been observed. However, the existence of anaerobic thermophilic methanotrophic sulfate reducers has been inferred only from lipid biomarker signals (Schouten et al. 2003). Recently, thermophilic anoxic CH4-oxidizing SO4-reducing activities have been directly verified at up to 70°C in the sediments of the Guaymas Basin hydrothermal field (Holler et al. 2011). In addition, possible microbial components of thermophilic anaerobic methane oxidizers, consortia of ANME-1a Archaea and HotSeep-1 cluster Deltaproteobacteria, have been identified via FISH analysis (Holler et al. 2011). Similar phylotypes of potentially thermophilic ANME-1a Archaea have also been found in hydrothermal sediments and diffusing fluids of SED hydrothermal systems such as the Axial Seamount and Endeavour Segment fields in the Juan de Fuca Ridge and the Yonaguni Knoll IV field in the Okinawa Trough (Nunoura et al. 2010; Merkel et al. 2013). Because these phylotypes of thermophilic anaerobic methanotrophic Archaea remain resistant to cultivation, quantitative cultivation methods are not feasible. However, other quantitative techniques targeting 16S rRNA and functional gene transcripts together with direct metabolic activity measurements are now available (e.g., Beal et al. 2009; Watsuji et al. 2012, 2014). Such quantitative estimates will provide multiple lines of evidence for the relationship between CH4 enrichment in SED hydrothermal systems and the abundance of thermophilic methanotrophic sulfate reducers in mixing zone habitats.
Takai and Nakamura ( 2010) have also noted that phase separation has a considerable impact on intra-field variations in hydrothermal fluid chemistry. In microbiological studies of the Iheya North field in the middle Okinawa Trough and the Mariner field in the Lau Basin, increased populations of anaerobic and aerobic H2-trophic chemolithotrophs (e.g., Methanococcales and Aquificales) were observed, potentially due to phase separation of hydrothermal fluids (Nakagawa et al. 2005b; Takai et al. 2008). However, in studies of the Yonaguni Knoll IV field in the Southern Okinawa Trough, H2-trophic (and thiotrophic) chemolithotrophs (e.g., Methanococcales, Desulfurococcales, Nautiliaceae, and Thioreductoraceae) were the dominant microbial components in both vapor- and brine-rich hydrothermal fluids (Nunoura and Takai 2009). Although H2S concentration data for the Yonaguni Knoll IV fluid have not yet been reported, our geochemical model calculations indicate that if the H2 concentrations of the end-member hydrothermal fluids were well below approximately 1 mmol/kg, the metabolic energy available from both aerobic and anaerobic H2-trophic reactions would be directly correlated with the H2 concentration of the fluids (Figure 6). The H2 concentrations in the vapor- and brine-rich hydrothermal fluids venting at the Iheya North field (0.045 and 0.096 mmol/kg, respectively) and the Mariner field (0.012 and 0.13 mmol/kg, respectively) are well below approximately 1 mmol/kg and thus, phase separation-induced H2 variations may directly affect the available energy yields from aerobic and anaerobic H2-trophic reactions. In contrast, the H2 concentrations in the fluids at the Yonaguni Knoll IV field (0.8 to 3.6 mmol/kg) are mostly above approximately 1 mmol/kg, resulting in saturation of the metabolic energy available from aerobic hydrogenotrophic reactions, particularly at higher temperatures (Figure 6). In addition, the bioavailable energy yield from hyperthermophilic anaerobic reactions is nearly comparable to that from aerobic thiotrophic reactions, even in brine-rich hydrothermal fluids (Figure 6). This may explain why there are no major differences in abundance or composition of microbial communities between the vapor- and brine-rich hydrothermal fluids in the Yonaguni Knoll IV field (Nunoura and Takai, 2009).
We have provided an overview of variations in the geology, geochemistry, microbial energy metabolisms, and community development associated with global deep-sea hydrothermal systems. Relationships among the geological backgrounds of hydrothermal activities (e.g., tectonic settings, basement rock geochemistry, abundance of sediments, magmatic volatile inputs, and phase separation related to subseafloor hydrothermal processes), physical and chemical variations in hydrothermal fluids, and compositional diversity of potentially bioavailable energy for various vent-endemic chemolithotrophic metabolisms have been elucidated through thermodynamic modeling of redox states in hydrothermal mixing zone habitats. In addition, these relationships have been empirically substantiated by recent multidisciplinary biogeochemical and microbiological studies of existing microbial communities and their metabolic functions in representative deep-sea hydrothermal systems in different geographic locations and geological settings.
However, thermodynamic estimates of potential energy for possible chemolithotrophic metabolisms are based on certain simplifications, particularly with respect to quantitative representations of mixing of source hydrothermal fluids and seawater and the kinetic effects of abiotic reactions, cellular uptake and excretion of energy sources, and enzymatic functions on energy metabolism. These shortcomings may result in differences between the theoretical predictions and actual configurations and patterns in some cases. To characterize the in situ physical and chemical characteristics of hydrothermal mixing zone habitats at high spatial and temporal resolution, several electrochemical sensors have been developed and applied to various habitats such as diffusing hydrothermal fluids and chemosynthetic animal colonies. However, these sensors have some technical challenges, including multiple chemical interferences, relatively narrow dynamic ranges, and the need for in situ calibration (Luther et al. 2012). A deep-sea in situ membrane inlet mass spectrometry (MIMS) method has also been developed and used for in situ measurement of volatile and time-sensitive chemical species (Wankel et al. 2010). These newly developed in situ measurement tools will enable more precise estimates of the energy states of habitats of chemolithotrophic microbial communities. Improvement and development of biogeochemical and microbiological characterization techniques are also necessary to understand the functional and metabolic abundance and composition of microbial communities in deep-sea hydrothermal environments. It is a significant challenge to quantify the biomass, productivity, and functions of dominant microbial components in deep-sea vents. Comprehensive characterizations of in situ mRNA assemblages using such tools as GeoChip technology (Wang et al. 2009) and the metatranscriptomic approach (Dahle et al. 2013) will likely prove more objective, quantitative, and effective than employing elaborate quantitative cultivations using numerous media for intra-field and inter-field comparisons of microbial communities and their functions. Successfully overcoming these challenges is essential for clarifying the relationships between geology, geochemistry, microbial energy metabolisms, and community development associated with global deep-sea hydrothermal activities.
felsic rock-hosted hydrothermal system in an arc-backarc setting
mafic rock-hosted hydrothermal system in an arc-backarc setting
basalt-hosted hydrothermal system in a mid-ocean ridge setting
ultramafic rock-hosted hydrothermal system in a mid-ocean ridge setting
sediment-associated hydrothermal system in an arc-backarc setting
sediment-associated hydrothermal system in a mid-ocean ridge setting.
We would like to thank the two anonymous reviewers for their constructive and helpful comments, which have significantly improved the manuscript. This research was financially supported by the Ministry of Education, Culture, Science, and Technology (MEXT) of Japan through the special coordination fund Project TAIGA: Trans-crustal Advection and In situ Biogeochemical Processes of Global Subseafloor Aquifer.
- Akerman NH, Butterfield DA, Huber JA: Phylogenetic diversity and functional gene patterns of sulfur-oxidizing subseafloor Epsilonproteobacteria in diffuse hydrothermal vent fluids. Front Microbiol 2013., 4: doi:10.3389/fmicb.2013.00185 doi:10.3389/fmicb.2013.00185Google Scholar
- Allen DE, Seyfried WE Jr: Compositional controls on vent fluids from ultramafic-hosted hydrothermal systems at mid-ocean ridges: an experimental study at 400°C 500 bars. Gechim Cosmochim Acta 2003, 67: 1531–1542. 10.1016/S0016-7037(02)01173-0Google Scholar
- Alt JC, Shanks WC: Sulfur in serpentinized oceanic peridotites: serpentinization processes and microbial sulfate reduction. J Geophys Res 1998, 103: 9917–9929. 10.1029/98JB00576Google Scholar
- Amend JP, McCollom TM, Hentscher M, Bach W: Catabolic and anabolic energy for chemolithoautotrophs in deep-sea hydrothermal systems hosted in different rock types. Gechim Cosmochim Acta 2011, 75: 5736–5748. 10.1016/j.gca.2011.07.041Google Scholar
- Beal EJ, House CH, Orphan VJ: Manganese- and iron-dependent marine methane oxidation. Science 2009, 325: 184–187. 10.1126/science.1169984Google Scholar
- Beinart RA, Sanders JG, Faure B, Sylva SP, Lee RW, Becker EL, Gartman A, Luther GW III, Seewald JS, Fisher CR, Girguis PR: Evidence for the role of endosymbionts in regional-scale habitat partitioning by hydrothermal vent symbioses. Proc Natl Acad Sci U S A 2012, 109: E3241-E3250. 10.1073/pnas.1202690109Google Scholar
- Bemis K, Lowell RP, Farough A: Diffuse flow on and around hydrothermal vents at mid-ocean ridges. Oceanography 2012, 25: 182–191. 10.5670/oceanog.2012.16Google Scholar
- Berndt ME, Allen DE, Seyfried WE Jr: Reduction of CO 2 during serpentinization of olivine at 300°C and 500 bar. Geology 1996, 24: 351–354. 10.1130/0091-7613(1996)024<0351:ROCDSO>2.3.CO;2Google Scholar
- Bischoff JL, Dickson FW: Seawater-basalt interaction at 200°C and 500 bars implications for origin of seafloor heavy-metal deposits and regulations of seawater chemistry. Earth Planet Sci Lett 1975, 25: 385–397. 10.1016/0012-821X(75)90257-5Google Scholar
- Bischoff JL, Seyfried WE Jr: Hydrothermal chemistry of seawater from 25° to 350°C. Am J Sci 1978, 278: 838–860. 10.2475/ajs.278.6.838Google Scholar
- Bischoff JL, Pitzer KS: Liquid-vapor relations for the system NaCl-H 2 O summary of the P-T-x surface from 300 to 500°C. Am J Sci 1989, 289: 217–248. 10.2475/ajs.289.3.217Google Scholar
- Bowers TS, Taylor HP Jr: An integrated chemical and stable isotope model of the origin of mid-ocean ridge hot spring systems. J Geophys Res 1985, 90: 12583–12606. 10.1029/JB090iB14p12583Google Scholar
- Bowers TS, Campbell AC, Measures CI, Spivack AJ, Khadem M, Edmond JM: Chemical controls on the composition of vent fluids at 13°-11°N and 21°N East Pacific Rise. J Geophys Res 1988, 93: 4522–4536. 10.1029/JB093iB05p04522Google Scholar
- Butterfield DA, McDuff RE, Mottl MJ, Lilley MD, Lupton JE, Massoth GJ: Gradients in the composition of hydrothermal fluids from the Endeavour Ridge vent field: phase separation and brine loss. J Geophys Res 1994, 99: 9561–9583. 10.1029/93JB03132Google Scholar
- Butterfield DA, Seyfried WE Jr, Lilley MD: Composition and evolution of hydrothermal fluids. In Energy and Mass Transfer in Marine Hydrothermal Systems. Edited by: Halbach PE, Tunnicliffe V, Hein JR. Berlin: Dahlem University Press; 2003.Google Scholar
- Campbell AC, Palmer MR, Klinkhammer GP, Bowers TS, Edmond JM, Lawrence JR, Casey JF, Thompson G, Humphris S, Rona P, Karson JA: Chemistry of hot springs on the Mid-Atlantic Ridge. Nature 1988, 335: 514–519. 10.1038/335514a0Google Scholar
- Campbell BJ, Polson SW, Allen LZ, Williamson SJ, Lee CK, Wommack KE, Cary SC: Diffuse flow environments within basalt- and sediment-based hydrothermal vent ecosystems harbor specialized microbial communities. Front Microbiol 2013., 4: doi:10.3389/fmicb201300182 doi:10.3389/fmicb201300182Google Scholar
- Charlou JL, Fouquet Y, Bougauit H, Donval JP, Etoubleau J, Jean-Baptiste P, Dapoigny A, Appriou P, Rona PA: Intense CH 4 plumes generated by serpentinization of ultra-mafic rocks at the intersection of the 15°20’N fracture zone and the Mid-Atlantic Ridge. Geochim Cosmochim Acta 1998, 62: 2323–2333. 10.1016/S0016-7037(98)00138-0Google Scholar
- Charlou JL, Donval JP, Jean-Baptiste P, Radford-Knoery J, Fouquet Y, Dapoigny A, Stievenard M: Compared geochemical signatures and the evolution of Menez Gwen (37°50’N) and Lucky Strike (37°17’N) hydrothermal fluids south of the Azores Triple Junction on the Mid-Atlantic Ridge. Chem Geol 2000, 171: 49–75. 10.1016/S0009-2541(00)00244-8Google Scholar
- Charlou JL, Donval JP, Fouquet Y, Jean-Baptiste P, Holm N: Geochemistry of high H 2 and CH 4 vent fluids issuing from ultramafic rocks at the rainbow hydrothermal field (36°14’M MAR). Chem Geol 2002, 191: 345–359. 10.1016/S0009-2541(02)00134-1Google Scholar
- Cowen JP, Massoth GJ, Baker ET: Bacterial scavenging of Mn and Fe in a mid- to far-field hydrothermal particle plume. Nature 1986, 322: 169–171. 10.1038/322169a0Google Scholar
- Dahle H, Roalkvam I, Thorseth IH, Pedersen RB, Steen IH: The versatile in situ gene expression of an Epsilonproteobacteria-dominated biofilm from a hydrothermal chimney. Environ Microbiol Repts 2013, 5: 282–290. 10.1111/1758-2229.12016Google Scholar
- de Angelis MA, Lilley MD, Olson EJ, Baross JA: Methane oxidation in deep-sea hydrothermal plumes of the endeavour segment of the Juan de Fuca Ridge. Deep-Sea Res I 1993, 40: 1169–1186. 10.1016/0967-0637(93)90132-MGoogle Scholar
- Dick GJ, Tebo BM: Microbial diversity and biogeochemistry of the Guaymas Basin deep-sea hydrothermal plume. Environ Microbiol 2010, 12: 1334–1347. 10.1111/j.1462-2920.2010.02177.xGoogle Scholar
- Dick GJ, Clement BG, Fodrie FJ, Webb SM, Bargar JR, Tebo BM: Enzymatic microbial Mn(II) oxidation and Mn biooxide production in the Guaymas Basin hydrothermal plume. Geochim Cosmochim Acta 2009, 73: 6517–6530. 10.1016/j.gca.2009.07.039Google Scholar
- Ding K, Seyfried WE Jr: Determination of Fe-Cl complexing in the low pressure supercritical region (NaCl) Fe solubility constraints on the pH of subseafloor hydrothermal fluids. Geochim Cosmochim Acta 1992, 59: 4769–4773.Google Scholar
- Ding K, Seyfried WE Jr, Tivey MK, Von Damm KL, Bradley AM, Zhang Z: In situ pH measurement of hydrothermal fluids at mid-ocean ridges. Earth Planet Sci Lett 2005, 237: 167–174. 10.1016/j.epsl.2005.04.041Google Scholar
- Dubilier N, Bergin C, Lott C: Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat Rev Microbiol 2008, 6: 725–740. 10.1038/nrmicro1992Google Scholar
- Elderfield H, Schults A: Mid-ocean ridge hydrothermal fluxes and the chemical composition of the ocean. Ann Rev Earth Planet Sci 1996, 24: 191–224. 10.1146/annurev.earth.24.1.191Google Scholar
- Embley RW, Baker ET, Butterfield DA, Chadwick WW Jr, Lupton JE, Resing JA, de Ronde CEJ, Nakamura K, Tunnicliffe V, Dower JF, Merle SG: Exploring the submarine ring of fire Mariana Arc-Western Pacific. Oceanography 2007, 20: 68–79. 10.5670/oceanog.2007.07Google Scholar
- Fisher RV, Schmincke H-U: Pyroclastic Rocks. Berlin: Springer; 1984.Google Scholar
- Flores GE, Campbell JH, Kirshtein JD, Meneghin J, Podar M, Steinberg JI, Seewald JS, Tivey MK, Voytek MA, Yang ZK, Reysenbach AL: Microbial community structure of hydrothermal deposits from geochemically different vent fields along the Mid-Atlantic Ridge. Environ Microbiol 2011, 13: 2158–2171. 10.1111/j.1462-2920.2011.02463.xGoogle Scholar
- Foustoukos DI, Seyfried WE Jr: Fluid phase separation processes in submarine hydrothermal systems. Rev Mineral Geochem 2007, 65: 213–239. 10.2138/rmg.2007.65.7Google Scholar
- Frost RB: On the stability of sulfides oxides and native metals in serpentinite. J Petrol 1985, 26: 31–63. 10.1093/petrology/26.1.31Google Scholar
- Früh-Green GL, Connolly JA, Plas A, Kelley DS, Grobety B: Serpentinization of oceanic peridotites: implications for geochemical cycles and biological activity. In The Subseafloor Biosphere at mid-Ocean Ridges. Edited by: Wilcock WS, DeLong EF, Kelley DS, Baross JA, Cary SC. Washington, DC: Geophys Monogr Ser 144, AGU; 2004.Google Scholar
- Gamo T, Okamura K, Charlou JL, Urabe T, Auzende JM, Ishibashi J, Shitashima K, Chiba H, Shipboard Scientific Party of the ManusFlux Cruise: Acidic and sulfate-rich hydrothermal fluids from the Manus back-arc basin, Papua New Guinea. Geology 1997, 25: 139–142. 10.1130/0091-7613(1997)025<0139:AASRHF>2.3.CO;2Google Scholar
- Gamo T, Ishibashi J, Tsunogai U, Okamura K, Chiba H: Unique geochemistry of submarine hydrothermal fluids from arc-back-arc settings of the western Pacific. In Back-arc Spreading Systems—Geological, Biological, Chemical, and Physical Interactions. Edited by: Christie DM, Fisher CR, Lee SM, Givens S. Washington, DC: Geophys Monogr Ser 166, AGU; 2006.Google Scholar
- German CR, Von Damm KL: Hydrothermal processes. In The Treatise on Geochemistry Chapter 6.07. Edited by: Turekian KK, Holland HD. New York: Elsevier; 2004.Google Scholar
- German CR, Bowen A, Coleman ML, Honig DL, Huber JA, Jakuba MV, Kinsey JC, Kurz MD, Leroy S, McDermott JM, de Lepinay BM, Nakamura K, Seewald JS, Smith JL, Sylva SP, Van Dover CL, Whitcomb LL, Yoerger DR: Diverse styles of submarine venting on the ultraslow spreading Mid-Cayman Rise. Proc Natl Acad Sci U S A 2010, 107: 14020–14025. 10.1073/pnas.1009205107Google Scholar
- Hajash A, Chandler GW: An experimental investigation of high-temperature interactions between seawater and rhyolite andesite basalt and peridotite. Contrib Mineral Petrol 1981, 78: 240–254.Google Scholar
- Hannington M, Jamieson J, Monecke T, Petersen S, Beaulieu S: The abundance of seafloor massive sulfide deposits. Geology 2011, 39: 1155–1158. 10.1130/G32468.1Google Scholar
- Helgeson HC, Kirkham DH, Flowers GC: Theoretical prediction of the thermodynamic behavior of aqueous electrolytes at high pressures and temperatures IV: calculation of activity coefficients osmotic coefficients and relative partial molal properties to 600°C and 5 kb. Am J Sci 1981, 281: 1249–1516. 10.2475/ajs.281.10.1249Google Scholar
- Holler T, Widde F, Knittel K, Amann R, Kellermann MY, Hinrichs KU, Teske A, Boetius A, Wegener G: Thermophilic anaerobic oxidation of methane by marine microbial consortia. ISME J 2011, 5: 1946–1956. 10.1038/ismej.2011.77Google Scholar
- Huber JA, Holden JF: Modeling the impact of diffuse vent microorganisms along mid-ocean ridges and flanks. In Magma to Microbe: Modeling Hydrothermal Processes at Oceanic Spreading Centers. Edited by: Lowell RP, Seewald JS, Metaxas A, Perfit MR. Washington, DC: Geophys Monogr Ser 178, AGU; 2008.Google Scholar
- Huber JA, Morrison HG, Huse SM, Neal PR, Sogin ML, Mark Welch DB: Effect of PCR amplicon size on assessments of clone library microbial diversity and community structure. Environ Microbiol 2009, 11: 1292–1302. 10.1111/j.1462-2920.2008.01857.xGoogle Scholar
- Humphris SE, Zierenberg RA, Mullineaux LS, Thomson RE: Seafloor Hydrothermal Systems—Physical, Chemical, Biological, and Geological Interactions. Washington, DC: Geophys Monogr Ser 91, AGU; 1995.Google Scholar
- Inagaki F, Kuypers MMM, Tsunogai U, Ishibashi J, Nakamura K, Treude T, Ohkubo S, Nakaseama M, Gena K, Chiba H, Hirayama H, Nunoura T, Takai K, Jorgensen BB, Horikoshi K, Boetius A: Microbial community in a sediment-hosted CO 2 lake of the southern Okinawa Trough hydrothermal. Proc Natl Acad Sci U S A 2006, 103: 14164–14169. 10.1073/pnas.0606083103Google Scholar
- Ishibashi J, Urabe T: Hydrothermal activity related to arc-backarc magmatism in the western Pacific. In Backarc Basins: Tectonics and Magmatism. Edited by: Taylor B. New York: Plenum; 1995.Google Scholar
- Janecky DR, Seyfried WE Jr: Hydrothermal serpentinization of peridotite within the oceanic crust: experimental investigations of mineralogy and major element chemistry. Geochim Cosmochim Acta 1986, 50: 1357–1378. 10.1016/0016-7037(86)90311-XGoogle Scholar
- Jannasch HW, Mottl MJ: Geomicrobiology of deep-sea hydrothermal vents. Science 1985, 229: 717–725. 10.1126/science.229.4715.717Google Scholar
- Karl DM: Ecology of free-living hydrothermal vent microbial communities. In Microbiology of Deep-sea Hydrothermal Vents. Edited by: Karl DM. Boca Raton: CRC; 1995.Google Scholar
- Kawagucci S, Chiba C, Ishibashi J, Yamanaka T, Toki T, Muramatsu Y, Ueno Y, Makabe A, Inoue K, Yoshida N, Nakagawa S, Nunoura T, Takai K, Takahata N, Sano Y, Narita T, Teranishi G, Obata H, Gamo T: Hydrothermal fluid geochemistry at the Iheya North field in the mid-Okinawa trough: implication for origin of methane in subseafloor fluid circulation systems. Gechem J 2011, 45: 109–124. 10.2343/geochemj.1.0105Google Scholar
- Kawagucci S, Ueno Y, Takai K, Toki T, ito M, Inoue K, Makabe A, Yoshida N, Muramatsu Y, Takahata N, Sano Y, Narita T, Teranishi G, Obata H, Nakagawa S, Nunoura T, Gamo T: Geochemical origin of hydrothermal fluid methane in sediment-associated fluids and its relevance to the geographical distribution of whole hydrothermal circulation. Chem Geol 2013, 339: 213–225.Google Scholar
- Kawahata H, Nohara M, Ishizuka H, Hasebe S, Chiba H: Sr isotope geochemistry and hydrothermal alteration of the Oman ophiolite. J Geophys Res 2001, 106: 11083–11099. 10.1029/2000JB900456Google Scholar
- Kelley DS, Karson JA, Blackman DK, Fruh-Green GL, Butterfield DA, Lilley MD, Oison EJ, Schrenk MO, Roe KK, Lebon GT, Rivizzigno P, the AT3–60 Shipboard Party: An off-axis hydrothermal vent field discovered near the Mid-Atlantic Ridge at 30°N. Nature 2001, 412: 145–149. 10.1038/35084000Google Scholar
- Kelley DS, Baross JA, Delaney JR: Volcanoes fluids and life at mid-ocean ridge spreading centers. Annu Rev Earth Planet Sci 2002, 30: 385–491. 10.1146/annurev.earth.30.091201.141331Google Scholar
- Kelley DS, Karson JA, Fruh-Green GL, Yoerger DR, Shank TM, Butterfield DA, Hayes JM, Schrenk MO, Oison EJ, Proskurowski G, Jakuba M, Bradley A, Larson B, Ludwig K, Glickson D, Buckman K, Bradley AS, Brazelton WJ, Roe K, Elend MJ, Delacour A, Bernasconi SM, Lilley MD, Baross JA, Summons RE, Sylva SP: A serpentinite-hosted ecosystem: the lost city hydrothermal field. Science 2005, 307: 1428–1434. 10.1126/science.1102556Google Scholar
- Lam P, Cowen JP, Popp BN, Jones RD: Microbial ammonia oxidation and enhanced nitrogen cycling in the Endeavour hydrothermal plume. Geochim Cosmochim Acta 2008, 72: 2268–2286. 10.1016/j.gca.2008.01.033Google Scholar
- Leat PT, Larter RD: Intra-oceanic subduction systems introduction. In Intra-Oceanic Subduction Systems Tectonic and Magmatic Processes. Edited by: Larter RD, Leat PT. London: Geol Soc London Spec Publ; 2003.Google Scholar
- Lesniewski RA, Jain S, Anantharaman K, Schloss PD, Dick GJ: The metatranscriptome of a deep-sea hydrothermal plume is dominated by water column methanotrophs and lithotrophs. ISME J 2012, 6: 2257–2268. 10.1038/ismej.2012.63Google Scholar
- Lilley MD, Butterfield DA, Olson EJ, Lupton JE, Macko SA, McDuff RE: Anomalous CH 4 and NH 4 -concentrations at an unsedimented mid-ocean-ridge hydrothermal system. Nature 1993, 364: 45–47. 10.1038/364045a0Google Scholar
- Lilley MD, Butterfield DA, Lupton JE, Olson EJ: Magmatic events can produce rapid changes in hydrothermal vent chemistry. Nature 2003, 422: 878–881. 10.1038/nature01569Google Scholar
- Lupton J, Butterfield D, Lilley M, Evans L, Nakamura K, Chadwick W Jr, Resing J, Embley R, Olson E, Proskurowski G, Baker E, de Ronde C, Roe K, Greene R, Lebon G, Young C: Submarine venting of liquid carbon dioxide on a Mariana Arc volcano. Geochem Geophys Geosys 2006, 7: Q08007. doi:10.1029/2005GC001152 doi:10.1029/2005GC001152Google Scholar
- Lupton J, Lilley M, Butterfield D, Evans L, Embley R, Massoth G, Christenson B, Nakamura K, Schmidt M: Venting of a separate CO 2 -rich gas phase from submarine arc volcanoes: examples from the Mariana and Tonga-Kermadec arcs. J Geophys Res 2008, 113: B08S12. doi:10.1029/2007JB005467 doi:10.1029/2007JB005467Google Scholar
- Luther GW, Gartman A, Yucel M, Madison AS, Moore RS, Nees HA, Nuzzio DB, Sen A, Lutz RA, Shank TM, Fisher CR: Chemistry temperature and faunal distributions at diffuse flow hydrothermal vents comparisons of two geologically distinct ridge systems. Oceanography 2012, 25: 234–245. 10.5670/oceanog.2012.22Google Scholar
- Mandernack KW, Tebo BM: Manganese scavenging and oxidation at hydrothermal vents and in vent plumes. Geochim Cosmochim Acta 1993, 57: 3907–3923. 10.1016/0016-7037(93)90343-UGoogle Scholar
- McCollom TM: Geochemical constraints on sources of metabolic energy for chemolithoautotrophy in ultramafic-hosted deep-sea hydrothermal systems. Astrobiology 2007, 7: 933–950. 10.1089/ast.2006.0119Google Scholar
- McCollom TM, Shock EL: Geochemical constraints on chemolithoautotrophic metabolism by microorganisms in deep-sea hydrothermal systems. Geochim Cosmochim Acta 1997, 61: 4375–4391. 10.1016/S0016-7037(97)00241-XGoogle Scholar
- McCollom TM, Shock EL: Fluid-rock interactions in the lower oceanic crust: thermodynamic models of hydrothermal alteration. J Geophys Res 1998, 103: 547–575. 10.1029/97JB02603Google Scholar
- McCollom TM, Seewald JS: A reassessment of the potential for reduction of dissolved CO 2 to hydrocarbons during serpentinization of olivine. Geochim Cosmochim Acta 2001, 65: 3769–3778. 10.1016/S0016-7037(01)00655-XGoogle Scholar
- Merkel AY, Huberb JA, Chernyha NA, Bonch-Osmolovskayaa EA, Lebedinskya AV: Detection of putatively thermophilic anaerobic methanotrophs in diffuse hydrothermal vent fluids. Appl Environ Microbiol 2013, 79: 915–923. 10.1128/AEM.03034-12Google Scholar
- Mottl MJ: Hydrothermal processes at seafloor spreading centers: application of basalt-seawater experimental results. In Hydrothermal Processes at Seafloor Spreading Centers. Edited by: Rona PA, Bostrom K, Laubier L, Smith KL. New York: Plenum; 1983.Google Scholar
- Mottl MJ, Holland HD: Chemical exchange during hydrothermal alteration of basalt by seawater—I: experimental results for major and minor components of seawater. Geochim Cosmochim Acta 1978, 42: 1103–1115. 10.1016/0016-7037(78)90107-2Google Scholar
- Nakagawa S, Takai K: Deep-sea vent chemoautotrophs diversity biochemistry and ecological significance. FEMS Microbiol Ecol 2008, 65: 1–14. 10.1111/j.1574-6941.2008.00502.xGoogle Scholar
- Nakagawa S, Takai K, Inagaki F, Hirayama H, Nunoura T, Horikoshi K, Sako Y: Distribution phylogenetic diversity and physiological characteristics of epsilon-proteobacteria in a deep-sea hydrothermal field. Environ Microbiol 2005, 7: 1619–1632. 10.1111/j.1462-2920.2005.00856.xGoogle Scholar
- Nakagawa S, Takai K, Inagaki F, Chiba H, Ishibashi J, Kataoka S, Hirayama H, Nunoura T, Horikoshi K, Sako Y: Variability in microbial community and venting chemistry in a sediment-hosted backarc hydrothermal system: impacts of subseafloor phase-separation. FEMS Microbiol Ecol 2005, 54: 141–155. 10.1016/j.femsec.2005.03.007Google Scholar
- Nakamura K, Kato Y, Tamaki K, Ishii T: Geochemistry of hydrothermally altered basaltic rocks from the Southwest Indian Ridge near the Rodriguez Triple Junction. Mar Geol 2007, 239: 125–141. 10.1016/j.margeo.2007.01.003Google Scholar
- Nakamura K, Morishita T, Bach W, Klein F, Hara K, Okino K, Takai K, Kumagai H: Serpentinized troctolites exposed near the Kairei hydrothermal field Central Indian Ridge: insights into the origin of the Kairei hydrothermal fluid supporting a unique microbial ecosystem. Earth Planet Sci Lett 2009, 280: 128–136. 10.1016/j.epsl.2009.01.024Google Scholar
- Nealson KH, Inagaki F, Takai K: Hydrogen-driven subsurface lithoautotrophic microbial ecosystems (SLiMEs): do they exist and why should we care? TRENDS Microbiol 2005, 13: 405–410. 10.1016/j.tim.2005.07.010Google Scholar
- Nunoura T, Takai K: Comparison of microbial communities associated with phase-separation-induced hydrothermal fluids at the Yonaguni Knoll IV hydrothermal field, the Southern Okinawa Trough. FEMS Microbiol Ecol 2009, 67: 351–370. 10.1111/j.1574-6941.2008.00636.xGoogle Scholar
- Nunoura T, Oida H, Nakaseama M, Kosaka A, Ohkubo SB, Kikuchi T, Kazama H, Hosoi-Tanabe S, Nakamura K, Kinoshita M, Hirayama H, Inagaki F, Tsunogai U, Ishibashi J, Takai K: Archaeal diversity and distribution along thermal and geochemical gradients in hydrothermal sediments at the Yonaguni Knoll IV hydrothermal field in the Southern Okinawa Trough. Appl Environ Microbiol 2010, 76: 1198–1211. 10.1128/AEM.00924-09Google Scholar
- Perner M, Kuever J, Seifert R, Pape T, Koschinsky A, Schmidt K, Strauss H, Imhoff JF: The influence of ultramafic rocks on microbial communities at the Logatchev hydrothermal field, located 15°N on the Mid-Atlantic Ridge. FEMS Microbiol Ecol 2007, 61: 97–109. 10.1111/j.1574-6941.2007.00325.xGoogle Scholar
- Perner M, Petersen JM, Zielinski F, Gennerich H-H, Seifert R: Geochemical constraints on the diversity and activity of H 2 -oxidizing microorganisms in diffuse hydrothermal fluids from a basalt- and an ultramafic-hosted vent. FEMS Microbiol Ecol 2010, 74: 55–71. 10.1111/j.1574-6941.2010.00940.xGoogle Scholar
- Perner M, Hentscher M, Rychlik N, Seifert R, Strauss H, Bach W: Driving forces behind the biotope structures in the low-temperature venting at 5°S and 9°S MAR. Environ Microbiol Repts 2011, 3: 727–737. 10.1111/j.1758-2229.2011.00291.xGoogle Scholar
- Perner M, Gonella G, Hourdez S, Böhnke S, Kurtz S, Girguis P: In-situ chemistry and microbial community compositions in five deep-sea hydrothermal fluid samples from Irina II in the Logatchev field. Environ Microbiol 2013, 15: 1551–1560. 10.1111/1462-2920.12038Google Scholar
- Perner M, Hansen M, Seifert R, Strauss H, Koschinsky A, Petersen S: Linking geology fluid chemistry and microbial activity of basalt- and ultramafic-hosted deep-sea hydrothermal vent environments. Geobiology 2013, 11: 340–355. 10.1111/gbi.12039Google Scholar
- Petersen JM, Zielinski FU, Pape T, Seifert R, Moraru C, Amann R, Hourdez S, Girguis PR, Wankel SD, Barbe V, Pellerier E, Fink D, Borowski C, Bach W, Dubiller N: Hydrogen is an energy source for hydrothermal vent symbioses. Nature 2011, 476: 176–180. 10.1038/nature10325Google Scholar
- Reysenbach A-L, Shock E: Merging genomes with geochemistry in hydrothermal ecosystems. Science 2002, 296: 1077–1082. 10.1126/science.1072483Google Scholar
- Reed MH: Seawater-basalt reaction and the origin of greenstones and related ore deposits. Econ Geol 1983, 78: 466–485. 10.2113/gsecongeo.78.3.466Google Scholar
- Roussel EG, Konn C, Charlou JL, Donval JP, Fouquet Y, Querellou J, Prieur D, Bonavita MAC: Comparison of microbial communities associated with three Atlantic ultramafic hydrothermal systems. FEMS Microbiol Ecol 2011, 77: 647–665. 10.1111/j.1574-6941.2011.01161.xGoogle Scholar
- Saccocia J, Seyfried WE Jr: Talc-quartz equilibria and the stability of magnesium chloride complexes in NaCl-MgCl 2 solutions at 300, 350, and 400°C 500 bars. Geochim Cosmochim Acta 1990, 54: 3283–3295. 10.1016/0016-7037(90)90285-SGoogle Scholar
- Saccocia PJ, Ding K, Berndt ME, Seewald JS, Seyfried WE Jr: Experimental and theoretical perspectives on crustal alteration at mid-ocean ridges. In Alteration and Alteration Processes Associated With ore-Forming Systems. Edited by: Lentz D. Québec: Geological Association of Canada Short Course Notes; 1994.Google Scholar
- Sakai H, Gamo T, Kim ES, Tsutsumi M, Tanaka T, Ishibashi J, Wakita H, Yamano M, Oomori T: Venting of carbon dioxide-rich fluid and hydrate formation in mid-Okinawa Trough backarc basin. Science 1990, 248: 1093–1096. 10.1126/science.248.4959.1093Google Scholar
- Sanders JG, Beinart RA, Stewart FJ, Delong EF, Girguis PR: Metatranscriptomics reveal differences in in situ energy and nitrogen metabolism among hydrothermal vent snail symbionts. ISME J 2013, 7: 1556–1567. 10.1038/ismej.2013.45Google Scholar
- Schmincke H-U: Volcanism. Berlin: Springer; 2004.Google Scholar
- Schouten S, Wakeham SG, Hopmans EC, Damsté JSS: Biogeochemical evidence that thermophilic Archaea mediate the anaerobic oxidation of methane. Appl Environ Microbiol 2003, 69: 1680–1686. 10.1128/AEM.69.3.1680-1686.2003Google Scholar
- Seyfried WE Jr: Experimental and theoretical constraints on hydrothermal alteration processes at mid-ocean ridges. Annu Rev Earth Planet Sci 1987, 5: 317–335.Google Scholar
- Seyfried WE Jr, Mottl MJ: Hydrothermal alterations of basalt by seawater under seawater-dominated conditions. Geochim Cosmochim Acta 1982, 46: 985–1002. 10.1016/0016-7037(82)90054-0Google Scholar
- Seyfried WE Jr, Ding K: Phase equilibria in subseafloor hydrothermal systems: a review of the role of redox temperature pH and dissolved Cl on the chemistry of hot spring fluids at mid-ocean ridges. In Seafloor Hydrothermal Systems: Physical, Chemical, Biological, and Geological Interactions. Edited by: Humphris S, Mullineaux L, Zierenberg R, Thomson R. Washington, DC: Geophys Monogr Ser, vol. 91, AGU; 1995:248–273.Google Scholar
- Seyfried WE Jr, Berndt ME, Seewald JS: Hydrothermal alteration processes at mid-ocean ridges—constraints from diabase alteration experiments, hot spring fluids and composition of the oceanic crust. Can Mineral 1988, 26: 787–804.Google Scholar
- Seyfried WE Jr, Ding K, Berndt ME: Phase equilibria constraints on the chemistry of hot spring fluids at mid-ocean ridges. Geochim Cosmochim Acta 1991, 55: 3559–3580. 10.1016/0016-7037(91)90056-BGoogle Scholar
- Seyfried WE Jr, Ding K, Berndt ME, Chen X: Experimental and theoretical controls on the composition of mid-ocean ridge hydrothermal fluids. Rev Econ Geol 1999, 8: 181–200.Google Scholar
- Shock EL: Chemical environments of submarine hydrothermal systems. Origin Life Evol Biosphere 1992, 22: 67–107. 10.1007/BF01808019Google Scholar
- Shock EL, Holland ME: Geochemical energy sources that support the subsurface biosphere. In The Subseafloor Biosphere at mid-Ocean Ridges. Edited by: Wilcock WSD, DeLong EF, Kelley DS, Baross JA, Cary SC. Washington, DC: Geophys Monogr Ser vol. 144, AGU; 2004:153–165.Google Scholar
- Shock EL, Helgeson HC, Sverjensky DA: Calculation of the thermodynamic and transport properties of aqueous species at high pressures and temperatures: standard partial molal properties of inorganic neutral species. Geochim Cosmochim Acta 1989, 53: 2157–2183. 10.1016/0016-7037(89)90341-4Google Scholar
- Spiess FN, Macdonald KC, Atwater T, Ballard R, Carranza A, Cordoba D, Cox C, Diaz Garcia VM, Francheteau J, Guerrero J, Hawkins J, Haymon R, Hessler R, Juteau T, Kastner M, Larson R, Luyendyk B, Macdougall JD, Miller S, Normark W, Orcutt J, Rangin C: East Pacific Rise: Hot springs and Geophysical experiments. Science 1980, 207: 1421–1433. 10.1126/science.207.4438.1421Google Scholar
- Sunamura M, Higashi Y, Miyako C, Ishibashi J, Maruyama A: Two bacteria phylotypes are predominant in the Suiyo seamount hydrothermal plume. Appl Environ Microbiol 2004, 70: 1190–1198. 10.1128/AEM.70.2.1190-1198.2004Google Scholar
- Suzuki Y, Kojima S, Sasaki T, Suzuki M, Utsumi T, Watanabe H, Urakawa H, Tsuchida S, Nunoura T, Hirayama H, Takai K, Nealson KH, Horikoshi K: Host-symbiont relationships in hydrothermal vent gastropods of the genus Alviniconcha from the Southwest Pacific. Appl Environ Microbiol 2006, 72: 1388–1393. 10.1128/AEM.72.2.1388-1393.2006Google Scholar
- Takai K, Horikoshi K: Genetic diversity of Archaea in deep-sea hydrothermal vent environments. Genetics 1999, 152: 1285–1297.Google Scholar
- Takai K, Nakamura K: Compositional physiological and metabolic variability in microbial communities associated with geochemically diverse deep-sea hydrothermal vent fluids. In Geomicrobiology: Molecular and Environmental Perspective. Edited by: Barton LL, Mandl M, Loy A. Berlin: Springer; 2010:251–283.Google Scholar
- Takai K, Nakamura K: Archaeal diversity and community development in deep-sea hydrothermal vents. Curr Opin Microbiol 2011, 14: 282–291. 10.1016/j.mib.2011.04.013Google Scholar
- Takai K, Komatsu T, Inagaki F, Horikoshi K: Distribution of archaea in a black smoker chimney structure. Appl Environ Microbiol 2001, 67: 3618–3629. 10.1128/AEM.67.8.3618-3629.2001Google Scholar
- Takai K, Gamo T, Tsunogai U, Nakayama N, Hirayama H, Nealson KH, Horikoshi K: Geochemical and microbiological evidence for a hydrogen-based, hyperthermophilic subsurface lithoautotrophic microbial ecosystem (HyperSLiME) beneath an active deep-sea hydrothermal field. Extremophiles 2004, 8: 269–282.Google Scholar
- Takai K, Oida H, Suzuki Y, Hirayama H, Nakagawa S, Nunoura T, Inagaki F, Nealson KH, Horikoshi K: Spatial distribution of marine Crenarchaeota group I in the vicinity of deep-sea hydrothermal systems. Appl Environ Microbiol 2004, 70: 2404–2413. 10.1128/AEM.70.4.2404-2413.2004Google Scholar
- Takai K, Nakamura K, Suzuki K, Inagaki F, Nealson KH, Kumagai H: Ultramafics-Hydrothermalism-Hydrogenesis-Hyperslime (UltraH 3 ) linkage: a key insight into early microbial ecosystem in the archean deep-sea hydrothermal systems. Paleontol Res 2006a, 10: 269–282. 10.2517/prpsj.10.269Google Scholar
- Takai K, Nakagawa S, Reysenbach AL, Hoek J: Microbial ecology of mid-ocean ridges and back-arc basins. In Back-arc Spreading Systems: Geological, Biological, Chemical, and Physical Interactions. Edited by: Christie DM, Fisher CR, Lee SM, Givens S. Washington, DC: Geophys Monogr Ser vol 166, AGU; 2006b:185–213.Google Scholar
- Takai K, Nunoura T, Ishibashi J, Lupton J, Suzuki R, Hamasaki H, Ueno Y, Kawagucci S, Gamo T, Suzuki Y, Hirayama H, Horikoshi K: Variability in the microbial communities and hydrothermal fluid chemistry at the newly discovered Mariner hydrothermal field southern Lau Basin. J Geophys Res 2008, 113: G02031. doi:0201001029/02007JG000636 doi:0201001029/02007JG000636Google Scholar
- Tivey MK: Environmental conditions within active seafloor vent structures: sensitivity to vent fluid composition and fluid flow. In Subseafloor Biosphere at mid-Ocean Ridges. Edited by: Wilcock WS, DeLong EF, Kelley DS, Baross JA, Craig Cary S. Washington, DC: Geophys Monogr Ser vol. 144, AGU; 2004:137–152.Google Scholar
- Tivey MK: Generation of seafloor hydrothermal vent fluids and associated mineral deposits. Oceanography 2007, 20: 50–65. 10.5670/oceanog.2007.80Google Scholar
- Tivey MK, Becker E, Beinart R, Fisher CR, Girguis PR, Langmuir CH, Michael PJ, Reysenbach AL: Links from mantle to microbe at the Lau Integrated Study Site: insights from a back-arc spreading center. Oceanography 2012, 25: 62–77. 10.5670/oceanog.2012.04Google Scholar
- Van Dover CL: The Ecology of Deep-sea Hydrothermal Vents. New Jersey: Princeton University Press; 2000.Google Scholar
- Von Damm KL: Systematics of and postulated controls on submarine hydrothermal solution chemistry. J Geophys Res 1988, 93: 4551–4561. 10.1029/JB093iB05p04551Google Scholar
- Von Damm KL: Seafloor hydrothermal activity: black smoker chemistry and chimneys. Ann Rev Earth Planet Sci 1990, 18: 173–204. 10.1146/annurev.ea.18.050190.001133Google Scholar
- Von Damm KL: Controls on the chemistry and temporal variability of seafloor hydrothermal fluids. In Seafloor Hydrothermal Systems: Physical, Chemical, Biological, and Geological Interactions. Edited by: Humphris SE, Zierenberg RA, Mullineaux LS, Thomson RE. Washington, DC: Geophys Monogr Ser vol 91, AGU; 1995:222–247.Google Scholar
- Von Damm KL: Chemistry of hydrothermal vent fluids from 9°-10°N, East Pacific Rise: "Time zero" the immediate posteruptive period. J Geophys Res 2000, 105: 11203–11222. 10.1029/1999JB900414Google Scholar
- Wallace PJ, Edmonds M: The sulfur budget in magmas: evidence from melt inclusions submarine glasses and volcanic gas emissions. Rev Mineral Geochem 2011, 73: 215–246. 10.2138/rmg.2011.73.8Google Scholar
- Wang F, Zhou H, Meng J, Peng X, Jiang L, Sun P, Zhang C, Van Nostrand JDV, Deng Y, He Z, Wu L, Zhou J, Xiao X: GeoChip-based analysis of metabolic diversity of microbial communities at the Juan de Fuca Ridge hydrothermal vent. Proc Natl Acad Sci U S A 2009, 106: 4840–4845. 10.1073/pnas.0810418106Google Scholar
- Wankel SD, Joye SB, Samarkin VA, Shah SR, Friederich G, Melas-Kyriazi J, Girguis PR: New constraints on methane fluxes and rates of anaerobic methane oxidation in a Gulf of Mexico brine pool via in situ mass spectrometry. Deep-Sea Res II 2010, 57: 2022–2029. 10.1016/j.dsr2.2010.05.009Google Scholar
- Watsuji T, Nakagawa S, Tsuchida S, Toki T, Hirota A, Tsunogai U, Takai K: Diversity and function of epibiotic microbial communities on the galatheid crab Shinkaia crosnieri . Microbes Environ 2010, 25: 288–294. 10.1264/jsme2.ME10135Google Scholar
- Watsuji T, Nishizawa M, Morono Y, Hirayama H, Kawagucci S, Takahata N, Sano Y, Takai K: Cell-specific thioautotrophic productivity of epsilon-proteobacterial epibionts associated with Shinkaia crosnieri . PLoS One 2012, 7: e46282. doi:10.1371/journal.pone.0046282 doi:10.1371/journal.pone.0046282 10.1371/journal.pone.0046282Google Scholar
- Watsuji T, Yamamoto A, Takaki Y, Ueda K, Kawagucci S, Takai K: Diversity and methane oxidation of active epibiotic methanotrophs on live Shinkaia crosnieri . ISME J 2014. doi:10.1038/ismej.2013.226 doi:10.1038/ismej.2013.226Google Scholar
- Wetzel LR, Shock EL: Distinguishing ultra-mafic from basalt-hosted submarine hydrothermal systems by comparing calculated vent fluid compositions. J Geophys Res 2000, 105: 8319–8340. 10.1029/1999JB900382Google Scholar
- Wilcock WW, DeLong E, Kelley DS, Baross JA, Cary SC: The Subseafloor Biosphere at mid-Ocean Ridges. Washington, DC: Geophys Monogr Ser vol. 144, AGU; 2004.Google Scholar
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