Elsevier

Geochimica et Cosmochimica Acta

Volume 218, 1 December 2017, Pages 237-256
Geochimica et Cosmochimica Acta

Biologically induced formation of realgar deposits in soil

https://doi.org/10.1016/j.gca.2017.09.023Get rights and content

Abstract

The formation of realgar (As4S4) has recently been identified as a prominent As sequestration pathway in the naturally As-enriched wetland soil at the Mokrsko geochemical anomaly (Czech Republic). Here we used bulk soil and pore water analyses, synchrotron X-ray absorption spectroscopy, S isotopes, and DNA extractions to determine the distribution and speciation of As as a function of soil depth and metabolic properties of microbial communities in wetland soil profiles. Total solid-phase analyses showed that As was strongly correlated with organic matter, caused by a considerable As accumulation (up to 21 g kg–1) in an organic-rich soil horizon artificially buried in 1980 at a depth of ∼80 cm. Extended X-ray absorption fine structure spectroscopy revealed that As in the buried organic horizon was predominantly present as realgar occurring as nanocrystallites (50–100 nm) in millimeter-scale deposits associated with particulate organic matter. The realgar was depleted in the 34S isotope by 9–12.5‰ relative to the aqueous sulfate supplied to the soil, implying its biologically induced formation. Analysis of the microbial communities by 16S rDNA sequencing showed that realgar deposits formed in strictly anaerobic organic-rich domains dominated by sulfate-reducing and fermenting metabolisms. In contrast, realgar deposits were not observed in similar domains with even small contributions of oxidative metabolisms. No association of realgar with specific microbial species was observed. Our investigation shows that strongly reducing microenvironments associated with buried organic matter are significant biogeochemical traps for As, with an estimated As accumulation rate of 61 g As m–2 yr–1. Nevertheless the production of biologically induced realgar in these microenvironments is too slow to lower As groundwater concentrations at our field site (∼6790 mg L–1). Our study demonstrates the intricate link between geochemistry and microbial community dynamics in wetland soils, and provides insights into the conditions necessary to promote As sulfide precipitation in engineered wetlands for the treatment of As-rich waters.

Introduction

The natural contamination of groundwater with As is widely acknowledged as a major global threat to human health (Nordstrom, 2002, Ravenscroft et al., 2009). Despite the widespread poisoning of humans by the use of As-contaminated groundwater and resulting attention to subsurface As sources and cycling, the biogeochemical processes leading to As sequestration in, or release from, anoxic groundwater systems still remain elusive.

The cycle in which reduced forms of As are oxidized, liberated from primary sulfide or arsenide phases, and incorporated into oxidized, secondary phases such as Fe(III) (oxyhydr)oxides and metal arsenates can also run in reverse: Under reducing conditions, oxidized forms of As can be mobilized via a variety of processes; for example, microbial respiration of Fe(III) (oxyhydr)oxide and other secondary oxidized phases coupled to the degradation of natural organic matter (NOM) (Rochette et al., 1998, Cummings et al., 1999, Nickson et al., 2000). Depending on the geochemical conditions prevalent in the reducing system, As can remain in solution or be re-sequestered in secondary reduced phases such as Fe sulfides or mixed-valence Fe hydroxides. Previous studies have postulated that As can react with dissolved sulfide to form aqueous (oxy)thioarsenates and, hence, may increase As mobility under anoxic conditions (Couture and Van Cappellen, 2011, Burton et al., 2013). Arsenic can be further sequestered either by co-precipitation with, or adsorption onto, pyrite (FeS2), greigite (Fe3S4), and mackinawite (FeS) (Belzile and Lebel, 1986, Wilkin and Ford, 2006, Lowers et al., 2007, Kirk et al., 2010, Burton et al., 2014, Stuckey et al., 2015); alternatively, it can precipitate as arsenopyrite (FeAsS), löllingite (FeAs2), orpiment (As2S3) or realgar (As4S4) phases (Rittle et al., 1995, Tazaki et al., 2003, O'Day et al., 2004, Demergasso et al., 2007, Langner et al., 2012, Langner et al., 2013).

The speciation and transport of As is thus closely related to the biogeochemical cycling of Fe, S, and organic C, and controlled by the relative abundances of these elements (O'Day et al., 2004, Chow and Taillefert, 2009, Langner et al., 2013, Couture et al., 2013, Burton et al., 2014). In soils and sediments with sulfate reducing conditions Fe monosulfides (e.g., mackinawite) would precipitate first; these phases precipitate rapidly and have lower solubilities than As sulfides (Morse and Rickard, 2004, O'Day et al., 2004, Kirk et al., 2010), thus removing Fe and sulfide from solution. Sorption of As onto Fe monosulfides is more effective at slightly acidic pH, and likely occurs through the formation of a sorption complex resembling realgar- or orpiment-like phases (Gallegos et al., 2007, Gallegos et al., 2008, Renock et al., 2009, Han et al., 2011, Root et al., 2013, Burton et al., 2014). Fe monosulfides are metastable with respect to pyrite in most low-temperature geochemical environments (Rickard, 1975, Rickard and Luther, 1997, Morse and Rickard, 2004) and may transform to arsenian pyrite, with As incorporation levels of up to 1.3 wt.% (Lowers et al., 2007). The remaining free sulfide is available for As complexation, allowing for the precipitation of As sulfide minerals. In this regard, the factors governing the formation of realgar and orpiment phases are still poorly understood. Reaction path modeling indicated that realgar precipitation is favored in environments where the sulfide activity is buffered by the coexistence of Fe sulfides and Fe(II/III) (oxyhydr)oxides, whereas orpiment stability was predicted in Fe-poor environments that do not effectively buffer dissolved sulfide, and thus allow its concentration to increase to levels high enough for orpiment precipitation (O'Day et al. 2004). Furthermore, the proportion of orpiment in As sulfide precipitates increases with pH and redox potential (Han et al., 2011, Rodriguez-Freire et al., 2014). However, Le Pape et al. (2017) proposed that realgar does not form via direct interaction of arsenite with dissolved sulfide. In their incubation experiment, As first precipitated as amorphous orpiment, which further transformed into realgar due to the reduction of As(III) to As(II) by biogenic H2S. Although these facts stress the key influence of Fe and S on the geochemical behavior of As, with organic C being considered as only an energy source for microbial metabolism, it has recently been shown that particulate NOM in wetlands may efficiently sequester As through the binding of arsenite to sulfhydryl groups of NOM (Hoffmann et al., 2012, Langner et al., 2012, Couture et al., 2013). Sorption of arsenite to NOM appears to be favored by a combination of abundant reduced organic S, with comparatively low amounts of dissolved As preventing the formation of secondary As sulfides (Langner et al., 2013).

Hitherto, there is scant field evidence showing recent formation of As sulfides in low-temperature environments. The in-situ formation of realgar and orpiment in shallow subsurface environments so far has only been observed in an aquifer sediment from a former pesticide manufacturing facility near San Francisco Bay (California, USA) (O'Day et al., 2004, Root et al., 2009), a naturally As-enriched minerothropic peatland at Gola di Lago (canton Ticino, Switzerland) (Langner et al., 2012, Langner et al., 2013), and a wetland soil at the Mokrsko geochemical anomaly (Czech Republic) (Drahota et al., 2013b). Recent evidence has demonstrated the biological nature of the formation of As sulfides. Newman et al. (1997) first showed that the precipitation of As trisulfide was due to microbial reduction of arsenate and sulfate. Many other incubation experiments with microorganisms isolated from As-rich environments have further reinforced As sulfide biogenesis in Fe-poor systems (Huber et al., 2000, Ledbetter et al., 2007, Lee et al., 2007, Jiang et al., 2009, Focardi et al., 2010, Rodriguez-Freire et al., 2014, Rodriguez-Freire et al., 2016). Furthermore, Demergasso et al. (2007) have demonstrated the biological origin of As-S phases in the Ascotán borate deposit from an Andean salt flat (Chile) by analyzing S isotopes in both chemically and biologically formed As sulfides and then comparing them with the isotopic S signatures of the sediment. It seems likely that microbial sulfate reduction also caused the precipitation of As sulfides in other borate deposits, such as those in Turkey (Palmer et al., 2004, García-Veigas et al., 2011). All these findings suggest that microbial As-sulfide precipitation reactions contributed to the early-stage (low-temperature) formation of sediment-hosted ore deposits containing As sulfides (Palmer et al., 2004, Demergasso et al., 2007, Dekov et al., 2013), and that biogenic As-sulfide mineralization is a particularly important process in the biogeochemical As cycle in As-rich wetland systems characterized by abundant NOM and microbial activity.

This study expands our earlier work on microbially mediated AsS precipitation (Drahota et al., 2013b) and reports on the distribution and speciation of As in a naturally As-enriched wetland located in the most contaminated sub-watershed (0.13 km2) of the Mokrsko geochemical anomaly (Czech Republic). Previous soil analyses in the sub-watershed revealed As concentrations up to 4.37 g kg−1 (x¯: 0.45 g kg−1, n = 75) (Drahota et al., 2006). High aqueous As concentrations in combination with macroscopic deposits of realgar-like phases in the organic-rich soils (Drahota et al., 2013b) render this wetland a key locality to explore As sulfidization processes under low-temperature conditions. Our main objectives were to (1) provide information on the distribution and speciation of As in these wetland soils, (2) elucidate the role of soil microorganisms and NOM for the speciation and distribution of As, (3) gain insights into the mechanisms of As sulfide formation (abiotic vs. biotic), and (4) determine whether soil NOM represents a source or sink for groundwater As. Of particular interest was the development of a greater understanding of the relationship between biogeochemical As, S, and Fe cycling in wetland systems and its implications for the long-term stability of As in these low-temperature environments.

Section snippets

Field site description

The study site is a 100 m2 wetland located in the central Czech Republic (49 °44′43″N, 14 °20′01′'E; Fig. S1a). This region has a mild climate, with average monthly temperatures ranging from −2.5 °C in January to 17.3 °C in July, and a 555 mm average annual rainfall (Drahota et al., 2013a). Prior to 1980, the study site was a densely overgrown wetland with natural vegetation (Alnus sp., Eleocharis spp. and Typha spp.), and displayed poor drainage. In 1980, an open drain with a subsurface drainage

Mineralogy and chemistry of soil profiles

The wetland soils collected on the banks of the open drain were classified as a Dystric Gleysols (IUSS Working Group WRB, 2006). The upper soil layer (≤60–80 cm depth) represents artificial soil material from the surrounding area which has been deposited onto the original soil surface during the installation of the open drain (September, 1980). The buried soil is characterized by an approximately 40 cm-thick black organic soil horizon (cores A, B: 60–100 cm depth; core C: 80–110 cm depth) with a

Speciation of wetland soil arsenic

X-ray absorption spectroscopy, together with supporting electron microscopy and XRD analyses, showed changes in As speciation on a centimeter scale and revealed two principal As speciation patterns as a function of soil depth. In the near-surface artificial soil, the major species comprised As(V) associated with Fe(III) (oxyhydr)oxides and minerals from the pharmacosiderite group. In the buried soil, realgar almost completely dominated the As speciation. Because arsenopyrite has been identified

Conclusions

Wetland soils have been recognized as important sinks for As; yet the sources and immobilization mechanisms of As often vary in these environments. In this study, an organic-rich wetland soil artificially buried in 1980 provided the biogeochemical requirements for the extensive formation of realgar that led to a substantial As enrichment relative to the underlying and overlying soils. Microbiological and S isotope results indicated that realgar was generated by in-situ microbial reduction of

Acknowledgements

This research was supported by Grant GACR 16-09352S from the Czech Science Foundation. Use of the Stanford Synchrotron Radiation Lightsource, SLAC National Accelerator Laboratory, is supported by the U.S. Department of Energy, Office of Science, Office of Basic Energy Sciences under Contract No. DE-AC02-76SF00515. We are indebted to Ryan Davis, Erik Nelson, and Matthew Latimer for their support at beamline 4-1. Part of the laboratory equipment for this study was purchased from the Operational

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