Vertical profiles of arsenic and arsenic species transformations in deep-sea sediment, Nankai Trough, offshore Japan

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 (As^V) and arsenite (As^III) (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.

We examined the factors controlling As behavior in deep-sea sediments mainly on the basis of the analytical results for the cored sediments from Hole C0002. Vertical profiles of As and other chemical components in IW from the sediment column at Site C0002 are shown in Fig. 6 (Moore et al. 2013). As described above, chlorinity decreases linearly in Units I, III, and IV, whereas in Unit II, freshwater derived from the dissociation of methane hydrate diluted the IW, lowering the chlorinity of that unit. Here, we first discuss differences in the vertical variation of chemical components likely controlled by in situ microbial activity; later, we discuss sources of the IW.

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).

We examined variations of IW chemistry in relation to the end-member composition of the IW (Fig. 7). Toki et al. (2017) inferred that IW at Site C0002 is a mixture of three end members: SW (seawater); MH, freshwater derived from the dissociation of methane hydrate; and BG, defined as a deep-sourced fluid probably formed by ultrafiltration during burial diagenesis of IW in the old accretionary prism (Fig. 7a). SW, MH, and BG are characterized by chlorinity values of 550, 140, and 460 mM, respectively, and δ¹⁸O values of 0‰, + 1‰, and − 2.5‰, respectively. These three end members are typically found at the seafloor surface, around the methane hydrate concentration peak at about 400 mbsf, and below 1000 mbsf, respectively. Toki et al. (2017) suggested that the IW initially formed by the mixing of SW and BG via slow advection and was later modified by the addition of MH to the mixture. Most IW from Units I, III, and IV represents a mixture of SW and BG, whereas IW from Unit II is a mixture of MH with pre-existing SW–BG mixture. Concentrations of dissolved components associated with microbial activity and redox conditions are not just a simple function of the mixing ratios of the three end members. Figure 7 shows relationships among chemical components plausibly vary associated with As. Some components show contrasting distributions in four separate depth intervals: for example, Br⁻ is enriched but the Cl⁻ concentration is unchanged from that of SW in Unit I, both Cl⁻ and Br⁻ are depleted in MH, and Cl⁻ is depleted with no change in the Br⁻ concentration in BG (in Units III and IV) (Fig. 7b). Br⁻, PO₄³⁻, and NH₄⁺ show weakly positive correlations in Unit I, whereas those components show strongly positive correlations in Unit II-1. IW from Units III and IV is characterized by low PO₄³⁻ without changes in Br⁻ and NH₄⁺ concentrations (Fig. 7c, d). In Unit II-1, the Fe concentration seems to increase with the PO₄³⁻ concentration (Fig. 7e). These features suggest that the IW geochemistry reflects the degree of biological degradation, and that microbial activity was most active in Unit II-1.

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 As^V 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 (As^V) 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.