Abstract
Antimony (Sb) contamination released from mine tailings represents a global threat to natural ecosystems and human health. The geochemical conditions of Sb tailings, which are oligotrophic and replete in sulfur (S) and Sb, may promote the coupled metabolism of Sb and S. In this study, multiple lines of evidence indicate that a novel biogeochemical process, S oxidation coupled to Sb(V) reduction, is enzymatically mediated by Desulfurivibrio spp. The distribution of Desulfurivibrio covaried with S and Sb concentrations, showing a high relative abundance in Sb mine tailings but not in samples from surrounding sites (i.e., soils, paddies, and river sediments). Further, the metabolic potential to couple S oxidation to Sb(V) reduction, encoded by a non-canonical, oxidative sulfite reductase (dsr) and arsenate reductase (arrA) or antimonate reductase (anrA), respectively, was found to be common in Desulfurivibrio genomes retrieved from metal-contaminated sites in southern China. Elucidation of enzymatically-catalyzed S oxidation coupled to Sb(V) reduction expands the fundamental understanding of Sb biogeochemical cycling, which may be harnessed to improve remediation strategies for Sb mine tailings.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
Data availability
All the amplicon and metagenomic sequences were uploaded to the NCBI database under the bioproject number PRJNA678566. The Desulfurivibrio-MAG04 and the environmental MAGs are available in the NCBI database as biosample SAMN16879573-SAMN16879577. The geochemical data associated with the incubations are available in figshare (https://doi.org/10.6084/m9.figshare.15132546.v1).
References
Scheinost AC, Rossberg A, Vantelon D, Xifra I, Kretzschmar R, Leuz AK, et al. Quantitative antimony speciation in shooting-range soils by EXAFS spectroscopy. Geochim Cosmochim Acta. 2006;70:3299–312.
United State Environmental Protection Agency. Priority pollutant list. 2014.
Council of the European Union. Council Directive 98/83/EC of 3 November 1998 on the quality of water intended for human consumption. 1998.
Warnken J, Ohlsson R, Welsh DT, Teasdale PR, Chelsky A, Bennett WW. Antimony and arsenic exhibit contrasting spatial distributions in the sediment and vegetation of a contaminated wetland. Chemosphere. 2017;180:388–95.
Beauchemin S, Kwong YTJ, Desbarats AJ, MacKinnon T, Percival JB, Parsons MB, et al. Downstream changes in antimony and arsenic speciation in sediments at a mesothermal gold deposit in British Columbia, Canada. Appl Geochem. 2012;27:1953–65.
Dovick MA, Arkle RS, Kulp TR, Pilliod DS. Extreme arsenic and antimony uptake and tolerance in toad tadpoles during development in highly591contaminated wetlands. Environ Sci Technol. 2020;54:7983–91.
He M, Wang X, Wu F, Fu Z. Antimony pollution in China. Sci Total Environ. 2012;421–422:41–50.
Filella M, Belzile N, Lett MC. Antimony in the environment: a review focused on natural waters. III. Microbiota relevant interactions. Earth-Sci Rev. 2007;80:195–217.
Li J, Wang Q, Oremland RS, Kulp TR, Rensing C, Wang G. Microbial antimony biogeochemistry: Enzymes, regulation, and related metabolic pathways. Appl Environ Microbiol. 2016;82:5482–95.
He M, Wang N, Long X, Zhang C, Ma C, Zhong Q, et al. Antimony speciation in the environment: Recent advances in understanding the biogeochemical processes and ecological effects. J Environ Sci (China). 2018;75:14–39.
Kong L, Hu X, He M. Mechanisms of Sb(III) oxidation by pyrite-induced hydroxyl radicals and hydrogen peroxide. Environ Sci Technol. 2015;49:3499–505.
Filella M, Belzile N, Chen YW. Antimony in the environment: A review focused on natural waters I. Occurence. Earth-Sci Rev. 2002;57:125–76.
Kulp TR, Miller LG, Braiotta F, Webb SM, Kocar BD, Blum JS, et al. Microbiological reduction of Sb(V) in anoxic freshwater sediments. Environ Sci Technol. 2014;48:218–26.
Abin CA, Hollibaugh JT. Dissimilatory antimonate reduction and production of antimony trioxide microcrystals by a novel microorganism. Environ Sci Technol. 2014;48:681–8.
Abin CA, Hollibaugh JT. Transcriptional response of the obligate anaerobe Desulfuribacillus stibiiarsenatis MLFW-2 T to growth on antimonate and other terminal electron acceptors. Environ Microbiol. 2019;21:618–30.
Lai CY, Wen LL, Zhang Y, Luo SS, Wang QY, Luo YH, et al. Autotrophic antimonate bio-reduction using hydrogen as the electron donor. Water Res. 2016;88:467–74.
Lai CY, Dong QY, Rittmann BE, Zhao HP. Bioreduction of antimonate by anaerobic methane oxidation in a membrane biofilm batch reactor. Environ Sci Technol. 2018;52:8693–8700.
Shi Y, Jiang Y, Wang S, Wang X, Zhu G. Biogeographic distribution of comammox bacteria in diverse terrestrial habitats. Sci Total Environ. 2020;717:137257.
Prosser JI The Ecology of Nitrifying Bacteria. Biology Nitrogen Cycle. 2007. Elsevier B.V., pp 223-43.
Kelly DP, Wood AP. The chemolithotrophic Prokaryotes. The Prokaryotes:Prokaryotic Communities and Ecophysiology. 2013. pp 275-87.
Walsh DA, Zaikova E, Howes CG, Song YC, Wright JJ, Tringe SG, et al. Metagenome of a versatile chemolithoautotroph from expanding oceanic dead zones. Science (80-). 2009;326:578–82.
Anantharaman K, Breier JA, Dick GJ. Metagenomic resolution of microbial functions in deep-sea hydrothermal plumes across the Eastern Lau Spreading Center. ISME J. 2016;10:225–39.
Emerson JB, Thomas BC, Alvarez W, Banfield JF. Metagenomic analysis of a high carbon dioxide subsurface microbial community populated by chemolithoautotrophs and bacteria and archaea from candidate phyla. Environ Microbiol. 2016;18:1686–703.
Jewell TNM, Karaoz U, Brodie EL, Williams KH, Beller HR. Metatranscriptomic evidence of pervasive and diverse chemolithoautotrophy relevant to C, S, N and Fe cycling in a shallow alluvial aquifer. ISME J. 2016;10:2106–17.
Sun X, Kong T, Häggblom MM, Kolton M, Li F, Dong Y, et al. Chemolithoautotrophic diazotrophy dominates the nitrogen fixation process in mine tailings. Environ Sci Technol. 2020;54:6082–93.
Nguyen VK, Lee JU. Isolation and characterization of antimony-reducing bacteria from sediments collected in the vicinity of an antimony factory. Geomicrobiol J. 2014;31:855–61.
Radajewski S, Ineson P, Parekh NR, Murrell JC. Stable-isotope probing as a tool in microbial ecology. Nature. 2000;403:646–9.
Viñas P, López-García I, Merino-Meroño B, Hernández-Córdoba M. Liquid chromatography-hydride generation-atomic fluorescence spectrometry hybridation for antimony speciation in environmental samples. Talanta. 2006;68:1401–5.
Zhao P, Niu J, Huan L, Gu W, Wu M, Wang G. Agar extraction from Pyropia haitanensis residue after the removal and purification of phycobiliproteins. J Appl Phycol. 2019;31:2497–505.
Neufeld JD, Vohra J, Dumont MG, Lueders T, Manefield M, Friedrich MW, et al. DNA stable-isotope probing. Nat Protoc. 2007;2:860–6.
Zhang M, Li Z, Haggblom MM, Young L, He Z, Li F, et al. Characterization of nitrate-dependent As(III)-oxidizing communities in arsenic-contaminated soil and investigation of their metabolic potentials by the combination of DNA-stable isotope probing and metagenomics. Environ Sci Technol. 2020;54:7366–77.
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–6.
Moonsamy PV, Williams T, Bonella P, Holcomb CL, Höglund BN, Hillman G, et al. High throughput HLA genotyping using 454 sequencing and the Fluidigm Access ArrayTM system for simplified amplicon library preparation. Tissue Antigens. 2013;81:141–9.
McMurdie PJ, Holmes S. Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One. 2013;8:e61217.
Delmont TO, Eren EM. Linking pangenomes and metagenomes: the Prochlorococcus metapangenome. PeerJ. 2018;2018:1–23.
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, et al. vegan: Community Ecology Package. R package version 2.4-6. https://CRAN.R-project.org/package=vegan. 2018.
Liaw A, Wiener M. randomForest: Breiman and Cutler’s random forests for classification and regression. R Packag version. 2015;4:6–10.
Díaz-Uriarte R, Alvarez de Andrés S. Gene selection and classification of microarray data using random forest. BMC Bioinforma. 2006;7:1–13.
Dhariwal A, Chong J, Habib S, King IL, Agellon LB, Xia J. MicrobiomeAnalyst: A web-based tool for comprehensive statistical, visual and meta-analysis of microbiome data. Nucleic Acids Res. 2017;45:W180–W188.
Müller H, Marozava S, Probst AJ, Meckenstock RU. Groundwater cable bacteria conserve energy by sulfur disproportionation. ISME J. 2020;14:623–34.
Sehmel GA. Cyanide and antimony thermodynamic database for the aqueous species and solids for the EPA-MINTEQ geochemical code. PNNL-6835; Pacific Northwest National Laboratory: Richland, WA, USA, 1989; pp 1–224.
Salter SJ, Cox MJ, Turek EM, Calus ST, Cookson WO, Moffatt MF, et al. Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol. 2014;12:1–12.
Ohtsuka T, Yamaguchi N, Makino T, Sakurai K, Kimura K, Kudo K, et al. Arsenic dissolution from Japanese paddy soil by a dissimilatory arsenate-reducing bacterium Geobacter sp . OR-1. Environ Sci Technol. 2013;47:6263–71.
Thorup C, Schramm A, Findlay AJ, Finster KW, Schreiber L. Disguised as a sulfate reducer: Growth of the Deltaproteobacterium Desulfurivibrio alkaliphilus by sulfide oxidation with nitrate. MBio. 2017;8:1–9.
Hoeft SE, Kulp TR, Stolz JF, Hollibaugh JT, Oremland RS. Dissimilatory arsenate reduction with sulfide as electron donor: Experiments with Mono Lake water and isolation of strain MLMS-1, a chemoautotrophic arsenate respirer. Appl Environ Microbiol. 2004;70:2741–7.
Tersteegen A, Linder D, Thauer RK, Hedderich R. Structures and functions of four anabolic 2-oxoacid oxidoreductases in Methanobacterium thermoautotrophicum. Eur J Biochem. 1997;244:862–8.
Hiller E, Lalinská B, Chovan M, Jurkovič Ľ, Klimko T, Jankulár M, et al. Arsenic and antimony contamination of waters, stream sediments and soils in the vicinity of abandoned antimony mines in the Western Carpathians, Slovakia. Appl Geochem. 2012;27:598–614.
Casiot C, Ujevic M, Munoz M, Seidel JL, Elbaz-Poulichet F. Antimony and arsenic mobility in a creek draining an antimony mine abandoned 85 years ago (upper Orb basin, France). Appl Geochem. 2007;22:788–98.
Gebel T. Aresnic and antimony: Comparative approach on mechanistic toxicology. Chem Biol Interact. 1997;107:131–44.
Belzile N, Chen YW, Wang Z. Oxidation of antimony (III) by amorphous iron and Manganese oxyhydroxides. Chem Geol. 2001;174:379–87.
Sorokin DY, Tourova TP, Mußmann M, Muyzer G. Dethiobacter alkaliphilus gen. nov. sp. nov., and Desulfurivibrio alkaliphilus gen. nov. sp. nov.: Two novel representatives of reductive sulfur cycle from soda lakes. Extremophiles. 2008;12:431–9.
Melton ED, Sorokin DY, Overmars L, Chertkov O, Clum A, Pillay M, et al. Complete genome sequence of Desulfurivibrio alkaliphilus strain AHT2T, a haloalkaliphilic sulfidogen from Egyptian hypersaline alkaline lakes. Stand Genom Sci. 2016;11:1–9.
Liu JL, Yao J, Wang F, Min N, Gu JH, Li ZF, et al. Bacterial diversity in typical abandoned multi-contaminated nonferrous metal(loid) tailings during natural attenuation. Environ Pollut. 2019;247:98–107.
Liu J, Yao J, Sunahara G, Wang F, Li Z, Duran R. Nonferrous metal (loid) s mediate bacterial diversity in an abandoned mine tailing impoundment. Environ Sci Pollut Res. 2019;26:24806–18.
Xiao E, Krumins V, Tang S, Xiao T, Ning Z, Lan X, et al. Correlating microbial community profiles with geochemical conditions in a watershed heavily contaminated by an antimony tailing pond. Environ Pollut. 2016;215:141–53.
Shi LD, Wang M, Han YL, Lai CY, Shapleigh JP, Zhao HP. Multi-omics reveal various potential antimonate reductases from phylogenetically diverse microorganisms. Appl Microbiol Biotechnol. 2019;103:9119–29.
Wang L, Ye L, Jing C. Genetic identification of antimonate respiratory reductase in Shewanella sp. ANA-3. Environ Sci Technol. 2020;54:14107–13.
Wang Q, Warelow TP, Kang YS, Romano C, Osborne TH, Lehr CR, et al. Arsenite oxidase also functions as an antimonite oxidase. Appl Environ Microbiol. 2015;81:1959–65.
Butcher BG, Deane SM, Rawlings DE. The chromosomal arsenic resistance genes of Thiobacillus ferrooxidans have an unusual arrangement and confer increased arsenic and antimony resistance to Escherichia coli. Appl Environ Microbiol. 2000;66:1826–33.
Baker BJ, Banfield JF. Microbial communities in acid mine drainage. FEMS Microbiol Ecol. 2003;44:139–52.
Chen LX, Hu M, Huang LN, Hua ZS, Kuang JL, Li SJ, et al. Comparative metagenomic and metatranscriptomic analyses of microbial communities in acid mine drainage. ISME J. 2015;9:1579–92.
Zhuang WQ, Yi S, Bill M, Brisson VL, Feng X, Men Y, et al. Incomplete Wood-Ljungdahl pathway facilitates one-carbon metabolism in organohalide-respiring Dehalococcoides mccartyi. Proc Natl Acad Sci USA. 2014;111:6419–24.
Figueroa IA, Barnum TP, Somasekhar PY, Carlström CI, Engelbrektson AL, Coates JD. Metagenomics-guided analysis of microbial chemolithoautotrophic phosphite oxidation yields evidence of a seventh natural CO2 fixation pathway. Proc Natl Acad Sci USA. 2018;115:E92–E101.
Bell E, Lamminmäki T, Alneberg J, Andersson AF, Qian C, Xiong W, et al. Active sulfur cycling in the terrestrial deep subsurface. ISME J. 2020;14:1260–72.
Ramos-Padrón E, Bordenave S, Lin S, Bhaskar IM, Dong X, Sensen CW, et al. Carbon and sulfur cycling by microbial communities in a gypsum-treated oil sands tailings pond. Environ Sci Technol. 2011;45:439–46.
Lahermo P, Alfthan GWD. Selenium and arsenic in the environment in Finland. J Env Pathol Toxicol Oncol. 1998;17:205–16.
Acknowledgements
This work was supported by the National Natural Science Foundation of China (Grant Nos. U21A2035, 32161143018, 41907212, U20A20109, and 42107285), the Science and Technology Planning Project of Guangzhou (Grant No. 202002020072), GDAS' Project of Science and Technology Development (Grant Nos. 2020GDASYL-20200102018 and 2019GDASYL-0301002), Guangdong Basic and Applied Basic Research Foundation (Grant Nos. 2021A1515011374 and 2021A1515011461), High-End Foreign Experts Project (Grant No. G20200130015), the Science and Technology Planning Project of Guangdong Province (Grant Nos. 2019B121205006 and 2020B1212060048), and Guangdong Introducing Innovative and Entrepreneurial Talents (Grant No. 2017GC010570).
Author information
Authors and Affiliations
Contributions
XS conceived and designed the experiment with input from WS, JEK, MMH and MK; WS acquired the funding needed to conduct the project. LL, TK, BL, and PG performed the field sampling and laboratory analyses; XS, TK performed the data analysis; and XS led writing the manuscript with close consultation with JEK, FL, MMH, MK, MCYLV, YD, and WS.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Rights and permissions
About this article
Cite this article
Sun, X., Kong, T., Li, F. et al. Desulfurivibrio spp. mediate sulfur-oxidation coupled to Sb(V) reduction, a novel biogeochemical process. ISME J 16, 1547–1556 (2022). https://doi.org/10.1038/s41396-022-01201-2
Received:
Revised:
Accepted:
Published:
Version of record:
Issue date:
DOI: https://doi.org/10.1038/s41396-022-01201-2
This article is cited by
-
Identification of hydrogen oxidation coupled with antimonate reduction, a novel antimony biogeochemical cycling, in two contrasting antimony-contaminated environments
Microbiome (2025)
-
Increased temperature enhances microbial-mediated lignin decomposition in river sediment
Microbiome (2025)
-
Microbial potential to mitigate neurotoxic methylmercury accumulation in farmlands and rice
Nature Communications (2025)
-
Adding labile carbon to peatland soils triggers deep carbon breakdown
Communications Earth & Environment (2024)
-
Microbial Sulfur Pathways and Outcomes in Tailings Impoundments: A Mesocosm Study
Mine Water and the Environment (2024)


