- Research article
- Open Access
Vertical profiles of arsenic and arsenic species transformations in deep-sea sediment, Nankai Trough, offshore Japan
© The Author(s). 2019
- Received: 30 April 2018
- Accepted: 27 January 2019
- Published: 21 March 2019
Concentrations of arsenic (As) and its chemical forms were determined on deep-sea sediments drilled at three sites of Nankai Trough, off the Kii Peninsula, Japan. Those sediments were analyzed to document the behavior of As in relation to methane hydrate formation and the deep biosphere.
The analytical results showed the total As concentration of interstitial water (IW) and squeezed cake (SC) ranged from 0.9 to 380 ppb and from 3 to 14 ppm (average, 6.4 ppm), respectively. The sediments from Site C0002, of which sediment column was the longest down to 2200 m below the seafloor (mbsf) among the studied three drilling sites, were analyzed for the host phase transformation of As. The total concentration of As of IW and SC from 200 to 500 mbsf, where methane hydrate zone was included, was higher than those from the uppermost 200 m. Concentration of As was ultimately controlled by pH. Also, organoarsenicals, such as methylarsonic acid (MMA) and arsenobetaine (AsB), were detected in the sediment column, implying that these organoarsenicals appeared in relation to the in situ microbial activities. These observations suggest that As becomes mobilized directly or indirectly as a result of microbial activity in deep-sea sediments.
- Nankai Trough
- Deep biosphere
- Convergent margin
Distribution and behavior of arsenic (As), one of the most common toxic elements, in the hydrosphere and subareal and under-water shallow sediments have been well documented as a part of geologic cycle of arsenic in the Earth’s surface and crust (e.g., Masuda 2018, and references therein). The As is generally present in clean, open-ocean water at an average concentration of 1.5 μg/L (e.g., Andreae 1979). Marine organisms, particularly photosynthetic organisms, take up As from seawater and accumulate it in their bodies, where metabolic reactions result in As species transformations. Biogeochemical processes affecting As in ocean water have been well documented (e.g., Neff 2002, and references therein); in marine organisms, As is present as both inorganic species such as arsenate (AsV) and arsenite (AsIII) (e.g., Sanders 1979; Raab et al. 2005; Duncan et al. 2015) and organic species, such as arsenosugars in marine algae (e.g., Morita and Shibata 1990; Edmonds et al. 1997; Raab et al. 2005) and arsenobetaine in marine animals (e.g., Edmonds et al. 1977; Duncan et al. 2015).
In general, the dominant As phases in sediments are the inorganic species: that is, arsenite in reducing environments and arsenate in oxidizing environments (Neff 2002). Unpolluted nearshore marine and estuarine sediments usually contain from 5 to 15 μg/g As, but deep-sea sediments occasionally contain much higher concentrations, probably owing to precipitation from submarine hydrothermal solutions. Neff (2002) documented As phase changes in marine sediments due to microbial decomposition and synthesis of organoarsenicals and reported that sulfides such as realgar (As4S) and pyrite (FeS2), in which As was included as an impurity element, and oxides such as arsenolite (As2O3) are the main final inorganic products fixed in the sediments.
In coastal areas, As in sediments and interstitial water has been studied mainly in relation to biotoxicity. In deep-sea environments, although As has been documented in seafloor surface sediments (e.g., Francesconi and Edmonds 1996) and in hydrothermal sediments (e.g., Handley and Lloyd, 2013), vertical profiles of As in deep-sea sediments have not been systematically studied. In this study, we first traced concentrations and chemical forms of As in deep-sea sediments from the seafloor surface, through a methane hydrate layer, and down to 2200 mbsf. Then, we examined the sources of As and effect of microbial activity on its behavior in deep-sea sediments.
Drilling sites and studied cores
Site C0021, located on the basin slope seaward of the splay fault, is composed of dominantly silty clay sediments that were relocated by a submarine landslide (Moore et al. 2013). The chlorinity of the IW, which was the same as that of seawater, was uniform from the seafloor to 200 mbsf (Fig. 3g), probably as a result of homogenization of the collapsed sediments.
Most core samples used for our As analyses were collected by IODP Expedition 338 (October 2012 to January 2013) from Hole C0021B (drilled interval 0-204 mbsf), Hole C0022B (drilled interval 0–204 mbsf), Holes C0002K, L (200–505 mbsf), and holes C0002J and H (902–940 and 1100.5–1120 mbsf, respectively) (Moore et al. 2013). Both stored and newly recovered cores from Site C0002 were analyzed to document As behavior from the seafloor to as deep as possible in the ocean bottom sediments. Sediment samples from 0 to 204 mbsf and 475–1057 mbsf in Holes C0002D and B, respectively, were collected by Expedition 315 (November–December 2007) (Ashi et al. 2008), and those from 2110 to 2220 mbsf in Holes C0002P were collected by Expedition 348 (September 2013 to January 2014) (Expedition 348 Scientists and Scientific Participants 2014).
In order to examine As in coexisting water and solids, we analyzed As in both IW and the squeezed cake (SC, residual sediment after extraction of IW). IW was extracted from the sediment cores on board with a Manheim-type titanium squeezer (Manheim 1966), filtered through a polytetrafluoroethylene (PTFE) membrane filter (0.45 μm mesh), preserved with HCl in a plastic vial (Nalgene), and stored at room temperature. The SC was stored onboard at − 20 °C during the cruises. Then, in the shore-based laboratory, the SC was freeze-dried and powdered manually for the analyses. In our analyses, we used stored IW from shallow sediments above 200 mbsf in Site C0002 that had previously been used for onboard analysis of alkalinity. Among the samples taken during Expedition 348, we analyzed only the SC, because these core samples rarely contained an extractable amount of IW.
We determined total As concentrations in the bulk sediment (i.e., SC) and dissolved in the IW, As species extracted from the sediments by a sequential chemical extraction method, and As species in the sediments separated by high-performance liquid chromatography (HPLC) as described below.
Total As concentration
One gram of powdered sediment was fused with NaCO3 at 900 °C until the silicates were completely melted, and then the residue was dissolved in 0.05 M HNO3. IW was diluted with 0.05 M HNO3 to make a 1/300 solution. Total As concentrations in the sample solutions were quantified by inductively coupled plasma-mass spectrometry (ICP-MS; SPQ9700, Hitachi), with H2 gas used to prevent the formation of ArCl+. Commercially distributed standard As solution (FUJIFILM Wako Pure Chemical Corp.) was used for the calibration. Accuracy of the results was checked by using rock standard samples (JSd-1, As 2.42 ppm; JSd-2, 38.6 ppm; and JSl-1, 14.9 ppm) from AIST (National Institute of Advanced Industrial Science and Technology), which were prepared in a similar manner to the studied samples. The analytical error was ± 8% at maximum.
Sequential chemical extraction of As
The BCR sequential chemical extraction method (Rauret et al. 1999) was used to separate chemical phases of As in sediment. This method cannot accurately specify the As host phases, but As behaviors associated with changes in the environmental redox condition can be roughly evaluated. As phases were extracted in five steps. In step 1, 1 g of sediment powder was put in a PTFE centrifuge tube, which was shaken with 20 ml 0.22 M acetic acid (pH adjusted to 5 with HNO3) for 16 h at room temperature. Then, the mixture was centrifuged at 10,000 rpm for 10 min to extract acid-soluble phases, namely, components weakly adsorbed onto detrital materials or contained in carbonates into the supernatant fluid. In step 2, the residual sediment was washed with ultra-pure water; then, 20 ml 0.5 M hydroxylammonium chloride (NH3OHCl, pH adjusted to 2 with HNO3) was added and the mixture was shaken for 16 h at room temperature to extract As fixed in reducible phases, mainly, Fe-oxyhydroxides and Mn-oxides. In step 3, the residue from the previous step was heated with 20 ml 0.1 M sodium pyrophosphate solution for 2 h and then shaken with 5 M ammonium acetate (CH3COONH4, pH 2) for 16 h. This reagent cannot completely decompose sulfide minerals, so the most probable phase dissolved at this step is organic matter. Then, the mixture of residue and solution was centrifuged to separate. In step 4, the residue from step 3 was shaken with a mixture of concentrated nitric and perchloric acid for 16 h, then gently heated for 24 h, and centrifuged. Most insoluble phases, silicates, and sulfides were decomposed at this step. In step 5, the residue from the previous step was decomposed by alkaline fusion to decompose minerals resistant to the reagents used in steps 1–4. The As extracted at each step was quantified by ICP-MS as described in the previous section.
As species in sediments
Water-soluble As compounds in SC from Sites C0002 and C0022 were extracted by the method of Ellwood and Maher (2003). The sediment sample was mixed with a solution of 0.1 M hydroxylammonium chloride and 0.5 M phosphoric acid in a PTFE centrifuge tube and shaken at 25 °C for 1 h. The hydroxylammonium chloride solution is reductant and can decompose amorphous and weakly crystalized Fe-oxyhydroxides (e.g., ferrihydrite and goethite) and Mn-oxides, and the phosphoric acid helps to preserve AsIII and AsV species, especially in solutions containing high amounts of Fe and Mn (Ellwood and Maher 2003). Frozen sediment was used for this analysis, because dried samples may become oxidized, changing the chemical form of the As. After the reaction, the solid phase was separated by centrifugation (1880×g for 10 min) and removed by filtration through a PTFE membrane filter (0.45 μm mesh). The obtained solution was analyzed by HPLC–ICP-MS at the National Institute for Environmental Studies (8800 ICP-QQQ, Agilent Technologies, Inc., USA) to determine the concentrations of each separated As phase. Eight As compounds (commercially distributed by FUJIFILM Wako Pure Chemical Corp.), As(III), As(V), methylarsonic acid (MMA), dimethylarsinic acid (DMA), arsenobetaine (AsB), trimethylarsine oxide (TMO), tetramethylarsonium salt (TMAO), and arsenocholine (AsC), were separated in a GL-Science InertSil AS column (4.6 i.d. × 250 mm long), using an eluent composed of 10 mM butane-1-sulfonic acid sodium salt, 4 mM malonic acid, 4 mM tetramethylammonium hydroxide, and 0.05% methanol. The flow rate was 1.0 ml/min at 40 °C.
Bulk As concentration
Total arsenic concentration of squeezed cake and interstitial water of sediments from the Sites C0002, C0021 and C0022 at Nankai Trough
The highest As concentration was measured in SC from 116 mbsf, at the bottom of Unit I (13.5 ppm), but the As concentration range in SC from other parts of Unit I was low (3–5 ppm). In the upper half of Unit II, between 110 and 500 mbsf (referred to as Unit II-1 hereafter), the As concentration was > 5 ppm, and a maximum concentration of 13.2 ppm was observed at 320 mbsf. Arsenic concentrations of SC from below 600 mbsf in Hole C0002 were mostly < 5 ppm, similar to those of SC from Unit I. The bulk As concentration in sediments from below 2000 mbsf was also mostly < 6 ppm, while it increased in the deeper part and the maximum concentration was up to 11 ppm (Table 1). Although only bulk As concentrations were obtained from the deepest sediments, we inferred that As behavior did not largely change below ~ 500 mbsf in Hole C0002.
The total dissolved As concentration of IW from Hole C0002 ranged from 0.9 to 379 ppb (average 50 ppb). The total As concentration was low in the Unit I sediments and in the sediments from below 500 mbsf (Units II-2 and III), whereas it was high in the Unit II-1 sediments (Fig. 2b). The relationship between the SC concentration and the IW concentration varied with depth (Fig. 2c): for example, As peaks in IW were observed at 200 and 400 mbsf, whereas sediment peaks were observed at 116 and < 350 mbsf. The low As concentrations in SC from Unit I (excepting three samples from the bottom of the unit) and from below 500 mbsf did not change with depth. Owing to the insoluble host phases of the As and the physico-chemical conditions of the ambient IW, As in these depth intervals would not be easily mobilized.
At Site C0022, the drilled hole penetrated the fracture zone of a splay fault at around 100 mbsf (Fig. 3). The chlorinity of the IW increased with depth from 550 mM, that of ambient seawater, to 600 mM in the fracture zone, reflecting the upwelling of deep-seated water, in which dissolved salts had been concentrated via hydration reactions, along the fault (Strasser et al. 2014). The total As concentration in SC and IW ranged from 3 to 11 ppm and 4 to 94 ppb, respectively. The total concentration in SC did not change with depth, whereas that in IW increased below 100 mbsf and reached a peak at 110–130 mbsf, below the fracture zone.
Total As concentrations of SC and IW from Hole C0021 were from 4 to 7 ppm and from 7 to 36 ppb, respectively, except the deepest sample (22.7 ppm and 94 ppb), and did not change substantially with depth (Fig. 3). This site is located on the forearc slope, and the cored sediments consist of landslide deposits. The chlorinity is stable with depth and the same as that of seawater, probably because the sediment and IW were homogenized during relocation by the landslide. Thus, except in the deepest samples (from 180 mbsf), the As concentrations in the sediment (4–9 ppm) and IW (5–20 ppb) can be regarded as averaged shallow sediment values.
Host phases of As in the sediments
Arsenic concentrations of sequentially extracted fractions of sediments from Site C0002 at Nankai Trough
As concentration (ppm)
As species in sediments separated by HPLC
Arsenic concentrations of soluble fractions extracted by hydroxylammonium chloride and phosphoric acid solution
In Unit I, reduction of SO42− occurred just beneath the seafloor, leading to a low SO42− concentration there. The Fe concentration is also low in Unit I, probably owing to the precipitation of FeS2 (pyrite), because framboidal pyrite was observed throughout the sediment column (Strasser et al. 2014). Br−, PO43−, and NH4+ increase with depth in Unit I; these results can be plausibly attributed to the decomposition of organic matter. Peak concentrations of these three components were observed in the uppermost part of Unit II; below that, their concentrations decreased with depth down to 400 mbsf. The SO42− concentrations of Unit II are higher than those of the Unit I, in which SO42− reduction occurs just beneath the ocean bottom surface (Fig. 6). The similar decrease (3–6 mbsf) and increase (> 400 mbsf) of SO42− concentrations were observed in the deep-sea sediments at IODP Sites 1173 and 1174 at Nankai Trough, about 100 km SW from this study site. In those sediment columns, high SO42− was supplied from diffusive flux of sulfate from the oceanic basement into the overlaying sediments (e.g., Shipboard Scientific Party 2001a, b; Heuer et al. 2017). It would not be the case for the sediment column studied here, since the upward migration of deep fluid was limited (Toki et al. 2017). However, the SO42− would be derived diffusive flux of seawater and/or deep-sourced fluid (BG, described in the next paragraph).
The Br− concentration (Fig. 6b), but not the Cl− concentration, of IW increased with depth in Unit I, probably because Br was released from sediments by the decomposition of Br-containing organic matter derived from algae and marine animals, some of which concentrate Br in various, mostly toxic, compounds such as bromoperoxidases (Hewson and Hager 1980), bromoform, and dobromoacetic acid (DBA) (e.g., Paul et al. 2006). Further, alkyl bromide compounds (Ma et al. 2010) have been extracted from algae, and 2,4-dibromophenol is produced by animal activity in coastal sediments (King 1988). Dehalogenation bacteria were recovered from the sediment column of Hole C0002 down to 150 mbsf, and Futagami et al. (2013) observed dehalogenation (bromide release) of 2,4,6-tribromophenol in an incubation experiment conducted with sediment from 4.7 mbsf. The freshwater derived from the dissociation of methane hydrate is not only low in Cl− but also in Br− (Fig. 7a). The BG end member is slightly depleted in Cl− but not in Br− compared with SW. IW from Unit II was a mixture of MH, SW, and BG. The Br− concentration increased with increasing PO43− in Units I and II-1. High Br− and PO43− concentrations are probably attributable to the decomposition of algae, and the relationship between them showed different trends between Units I and II-1. Moreover, the relationship between NH4+ and PO43− in IW showed different trends even more clearly between Units I and II-1. These differences between Units I and II-1 suggest that the sources of Br−, PO43−, and NH4+ differed between these Units (Fig. 7c, d). IW was depleted PO43− in Unit III and IV, and the relationship to Br− and NH4+ can be explained by the mixing of BG and MH.
The high bulk As concentrations in both sediment and IW in Unit II-1 (Fig. 2), along with the high Br−, PO43−, and NH4+ concentrations of IW, imply that these components had similar sources, i.e., marine biology especially such as algae. In Unit II-1, the As concentration increased with increasing pH (Fig. 7g) but not in relation to either PO43− or Fe (Fig. 7f, h). From the combined results of sequential extraction and leaching analyses, we can infer that a considerable amount of AsV was associated with Fe-oxyhydroxides and that the As concentration of IW was largely controlled by the pH. The adsorption–desorption affinity of As onto Fe-oxyhydroxides is mainly controlled by the solution pH; adsorption of arsenate (AsV) occurs at pH 5–6, whereas desorption becomes dominant at higher pH (e.g., Pearce and Moore 1982; Bowell et al. 1994; Dixit and Hering 2003).
MMA, one of the simplest organoarsenicals, is derived from the decomposition of arsenosugars contained in phytoplankton and algae (Edmonds et al. 1997; Morita and Shibata 1990). AsB (arsenobetaine), the simplest protein containing As, is derived from marine animals (e.g., Francesconi and Edmonds 1996). Decomposition rates of organic As in sediments are high: Takeuchi et al. (2005) observed that in surface sediments from a coastal area, which were plausibly more oxic than the deep-sea sediments studied here, organic As was largely decomposed within approximately 60 years. The ages of the sediments from 200 to 500 mbsf in Hole C0002K and C0002L, corresponding to Unit II-1 in this study, were constrained from 1.04 to 1.34 Ma by biostratigraphy and magnetostratigraphy conducted during Expedition 315 (Strasser et al. 2014; Expedition 315 Scientists 2009). MMA can form in situ by microbial methylation (Reimer and Thompson 1988) in conjunction with methane formation. Sulfate-reducing and nitrogen-fixing bacteria were detected with methanogen, which mostly uses CO2 and H2 for producing CH4, from the sediments down to 193.29 mbsf at IODP Site 1173, located in the Nankai Trough and about 100 km SW of our study site (Newberry et al. 2004). In the same sediment column down to 194 mbsf, epsilon-proteobacterial clones, of which species used a diverse spectrum of electron accepters, such as O2 in low concentrations, NO3−, S°, and S2O32−, were also detected, and it was notable that these clones could also respire with Fe(III) and arsenate (Kormas et al. 2003). The similar microbial assemblage would be expected in the Unit II-1 of our studied column, of which IW contained SO42−. AsB, an organic As compound that is synthesized and degraded in biotransformation cycles, is ubiquitous in marine, terrestrial, and deep-sea hydrothermal systems (Hoffmann et al. 2018). In light of the results reported by Hoffmann et al. (2018), we can infer that the AsB in the deep-sea sediments studied here was also a product of in situ microbial activity. Thus, the detection of organic As compounds suggests that considerable amounts of mobile As in the studied sediment column may have been derived in relation to microbial activity via both degradation and synthesis of organic As compounds in the sediment column.
Arsenic is actively released into IW at depths of methane hydrate layer of deep-sea sediments of the Nankai Trough, offshore Japan. The release of As accompanies the degradation of organic matter and following change of redox condition to control the adsorption/desorption affinity of As onto the Fe-oxyhydroxides. The sources of the As in the sediment column are not clear at present. However, a considerable amount of mobile As must be derived from marine organisms. It is notable that As mobilization in deep-sea sediments is associated with microbial activity in deep-sea sediments where methane hydrate appears.
The authors sampled the studied sediments and IW in collaboration with the crews and onboard scientists of Expeditions 338 and 348. The stored samples taken during Expedition 315 were provided by the Kochi Core Center, which is directed by Dr. Lalan Gupta. T. Shimonaka and K. Okazaki supported for conducting shore-based laboratory analyses. The comments from Dr. T. Kakegawa and two anonymous reviewers were helpful to improve the manuscript. We thank to all of them. This study was financially supported by post-cruise IODP studies to HM, SF and EE, and KAKENHI (No. 17K18810).
Samples were collected on Drilling Vessel “Chikyu” under IODP program during Expeditions 338 and 348.
Post cruise research fund from JAMSTEC for HM, SF and EE and KAKENHI (No. 17K18810) were used for As analyses.
Availability of data and materials
All data newly obtained from this study is in the manuscript and data sharing is not applicable.
HM carried out the sample collection and pretreatments on Exp. 338, helped in the analysis of water-soluble As, wrote the manuscript, and drew the figures. HY helped in the analyses of As of interstitial water and sediments. SF helped in the sample collection and pretreatments on Exp. 348, analysis of water-soluble As with HY, and discussion. TT helped in the sample collection and pretreatments on Exp. 338, and discussion. EE contributed to the sample collection and pretreatments on Exp. 348. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
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