Biologically induced formation of realgar deposits in soil
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 (: 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
References (99)
- et al.
Precipitation of arsenic sulphide from acidic water in a fixed-film bioreactor
Water Res.
(2012) - et al.
Capture of arsenic by pyrite in near-shore marine-sediments
Chem. Geol.
(1986) - et al.
Alteration of As-bearing phases in a small watershed located on a high grade arsenic-geochemical anomaly (French Massif Central)
Appl. Geochem.
(2010) - et al.
Coupling of arsenic mobility to sulfur transformations during sulfate reduction in the presence and absence of humic acid
Chem. Geol.
(2013) Isotope fractionation by natural populations of sulfate-reducing bacteria
Geochim. Cosmochim. Acta
(2001)- et al.
Effect of arsenic concentration on microbial iron reduction and arsenic speciation in an iron-rich freshwater sediment
Geochim. Cosmochim. Acta
(2009) - et al.
Reassessing the role of sulfur geochemistry on arsenic speciation in reducing environments
J. Hazard. Mater.
(2011) - et al.
Inorganic and biogenic As-sulfide precipitation at seafloor hydrothermal fields
Mar. Geol.
(2013) - et al.
Weathering and erosion fluxes of arsenic in watershed mass budgets
Sci. Total Environ.
(2006) - et al.
Mineralogical and geochemical controls of arsenic speciation and mobility under different redox conditions in soil, sediment and water at the Mokrsko-West gold deposit, Czech Republic
Sci. Total Environ.
(2009)
Diel variation of arsenic, molybdenum and antimony in a stream draining natural As geochemical anomaly
Appl. Geochem.
Microbial effect on the release and attenuation of arsenic in the shallow subsurface of a natural geochemical anomaly
Environ. Pollut.
Mineralogical speciation of arsenic in soils above the Mokrsko-west gold deposit, Czech Republic
Geoderma
Mineralogy, diagenesis and hydrochemical evolution in a probertite-glauberite-halite saline lake (Miocene, Emet Basin, Turkey)
Chem. Geol.
Sulfur isotope fractionation during bacterial sulfate reduction in organic-rich sediments
Geochim. Cosmochim. Acta
X-ray absorption and photoelectron spectroscopic study of the association of As(III) with nanoparticulate FeS and FeS-coated sand
Water Res.
Oligomerization in As(III) sulfide solution: theoretical constraints and spectroscopic evidence
Geochim. Cosmochim. Acta
Respiration of arsenate and selenate by hyperthermophilic archaea
Syst. Appl. Microbiol.
Mechanisms of dissolved arsenic removal by biochemical reactors: a bench- and field-scale study
Appl. Geochem.
Geochemical exploration in the Jílové belt: case history of the Celina deposit, Bohemian Massif, Czechoslovakia
J. Geochem. Explor.
Experimental analysis of arsenic precipitation during microbial sulfate and iron reduction in model aquifer sediment reactors
Geochim. Cosmochim. Acta
Consistent indexing of s (set of) SAED pattern(s) with the process diffraction program
Ultramicroscopy
Complete removal of arsenic and zinc from heavily contaminated acid mine drainage via an indigenous SRB consortium
J. Hazard. Mater.
Arsenic incorporation into authigenic pyrite, Bengal Basin sediment, Bangladesh
Geochim. Cosmochim. Acta.
Mechanism of arsenic release to groundwater, Bangladesh and West Bengal
Appl. Geochem.
Sulphur, sulphate oxygen and strontium isotope composition of Cenozoic Turkish evaporates
Chem. Geol.
Sorption of As(V) on green rust (Fe4(II)Fe2(III)(OH)12SO4·3H2O) and lepidocrocite (γ-FeOOH): Surface complexes from EXAFS spectroscopy
Geochim. Cosmochim. Acta
Chemical and structural characterization of As immobilization by nanoparticles of mackinawite (FeSm)
Chem. Geol.
Kinetics of pyrite formation by the H2S oxidation of iron(II) monosulfide in aqueous solutions between 25 and 125 C: the mechanism
Geochim. Cosmochim. Acta
Biomineralization of arsenate to arsenic sulfides is greatly enhanced at mildly acidic conditions
Water Res.
Speciation and natural attenuation of arsenic in a tidally influenced shallow aquifer
Geochim. Cosmochim. Acta
Surface complexation of arsenic(V) to iron(III) (hydr)oxides: structural mechanism from ab initio molecular geometries and EXAFS spectroscopy
Geochim. Cosmochim. Acta
Peat formation concentrated arsenic within sediment deposits of the Mekong Delta
Geochim. Cosmochim. Acta
Surface chemistry of ferrihydrite: Part 1. EXAFS studies of the geometry of coprecipitated and adsorbed arsenate
Geochim. Cosmochim. Acta
Arsenic solid-phase partitioning in reducing sediments of a contaminated wetland
Chem. Geol.
The Mokrsko-West gold deposit, Bohemian Massif, Czech Republic: mineralogy, deposit settings and classification
Ore Geol. Rev.
Multiple fluid sources/pathways and severe thermal gradients during formation of the Jílové orogenic gold deposits, Bohemian Massif, Czech Republic
Ore Geol. Rev.
Real-space multiple-scattering calculation and interpretation of x-ray-absorption near-edge structure
Phys. Rev. B
Command-Line Tools for Processing Biological Sequencing Data
Patterns of sulfur isotope fractionation during microbial sulfate reduction
Geobiology
The structure and composition of pharmacosiderite
Z. Kristallogr.
Arsenic mobility during flooding of contaminated soil: the effect of microbial sulfate reduction
Environ. Sci. Technol.
The production of 34S-depleted sulfide during bacterial disproportionation of elemental sulfur
Science
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms (short communication)
ISME J.
Arsenic binding to organic and inorganic sulfur species during microbial sulfate reduction: a sediment flow-through reactor experiment
Environ. Chem.
Arsenic mobilization by the dissimilatory Fe(III)-reducing bacterium Shewanella alga BrY
Environ. Sci. Technol.
Microbial precipitation of arsenic sulfides in Andean salt flats
Geomicrobiol J.
UPARSE: highly accurate OTU sequences from microbial amplicon reads
Nat. Methods
UCHIME improves sensitivity and speed of chimera detection
Bioinformatics
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