Effect of exogenous and endogenous sulfide on the production and the export of methylmercury by sulfate-reducing bacteria.

Cysteine Mercury Mercury partitioning Microbial mercury transformations Sulfur-containing molecules hgcA expression

Journal

Environmental science and pollution research international
ISSN: 1614-7499
Titre abrégé: Environ Sci Pollut Res Int
Pays: Germany
ID NLM: 9441769

Informations de publication

Date de publication:
Jan 2023
Historique:
received: 24 11 2021
accepted: 19 07 2022
pubmed: 12 8 2022
medline: 7 2 2023
entrez: 11 8 2022
Statut: ppublish

Résumé

Mercury (Hg) is a global pollutant of environmental and health concern; its methylated form, methylmercury (MeHg), is a potent neurotoxin. Sulfur-containing molecules play a role in MeHg production by microorganisms. While sulfides are considered to limit Hg methylation, sulfate and cysteine were shown to favor this process. However, these two forms can be endogenously converted by microorganisms into sulfide. Here, we explore the effect of sulfide (produced by the cell or supplied exogenously) on Hg methylation. For this purpose, Pseudodesulfovibrio hydrargyri BerOc1 was cultivated in non-sulfidogenic conditions with addition of cysteine and sulfide as well as in sulfidogenic conditions. We report that Hg methylation depends on sulfide concentration in the culture and the sulfides produced by cysteine degradation or sulfate reduction could affect the Hg methylation pattern. Hg methylation was independent of hgcA expression. Interestingly, MeHg production was maximal at 0.1-0.5 mM of sulfides. Besides, a strong positive correlation between MeHg in the extracellular medium and the increase of sulfide concentrations was observed, suggesting a facilitated MeHg export with sulfide and/or higher desorption from the cell. We suggest that sulfides (exogenous or endogenous) play a key role in controlling mercury methylation and should be considered when investigating the impact of Hg in natural environments.

Identifiants

pubmed: 35953752
doi: 10.1007/s11356-022-22173-y
pii: 10.1007/s11356-022-22173-y
doi:

Substances chimiques

Methylmercury Compounds 0
Cysteine K848JZ4886
Mercury FXS1BY2PGL
Sulfides 0
Sulfates 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

3835-3846

Subventions

Organisme : Agence Nationale de la Recherche
ID : iSITE -E2S GoBeam

Informations de copyright

© 2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.

Références

Adediran GA, Liem-Nguyen V, Song Y et al (2019) Microbial biosynthesis of thiol compounds: implications for speciation, cellular uptake, and methylation of Hg(II). Environ Sci Technol 53:8187–8196. https://doi.org/10.1021/acs.est.9b01502
doi: 10.1021/acs.est.9b01502
Andrei A, Öztürk Y, Khalfaoui-Hassani B et al (2020) Cu homeostasis in bacteria: the ins and outs. Membranes 10:242. https://doi.org/10.3390/membranes10090242
doi: 10.3390/membranes10090242
Andrews SC, Robinson AK, Rodríguez-Quiñones F (2003) Bacterial iron homeostasis. FEMS Microbiol Rev 27:215–237. https://doi.org/10.1016/S0168-6445(03)00055-X
doi: 10.1016/S0168-6445(03)00055-X
Atchison WD, Hare MF (1994) Mechanisms of methylmercury-induced neurotoxicity. FASEB J 8:622–629. https://doi.org/10.1096/fasebj.8.9.7516300
doi: 10.1096/fasebj.8.9.7516300
Benoit JM, Gilmour CC, Mason RP, Heyes A (1999a) Sulfide controls on mercury speciation and bioavailability to methylating bacteria in sediment pore waters. Environ Sci Technol 33:951–957. https://doi.org/10.1021/es9808200
doi: 10.1021/es9808200
Benoit JM, Mason RP, Gilmour CC (1999b) Estimation of mercury-sulfide speciation in sediment pore waters using octanol-water partitioning and implications for availability to methylating bacteria: mercury-sulfide speciation. Environ Toxicol Chem 18:2138–2141. https://doi.org/10.1002/etc.5620181004
doi: 10.1002/etc.5620181004
Benoit JM, Gilmour CC, Mason RP (2001a) The influence of sulfide on solid-phase mercury bioavailability for methylation by pure cultures of Desulfobulbus propionicus (1pr3). Environ Sci Technol 35:127–132. https://doi.org/10.1021/es001415n
doi: 10.1021/es001415n
Benoit JM, Gilmour CC, Mason RP (2001b) Aspects of bioavailability of mercury for methylation in pure cultures of Desulfobulbus propionicus (1pr3). Appl Environ Microbiol 67:51–58. https://doi.org/10.1128/AEM.67.1.51-58.2001
doi: 10.1128/AEM.67.1.51-58.2001
Bouchet S, Goñi-Urriza M, Monperrus M et al (2018) Linking microbial activities and low-molecular-weight thiols to hg methylation in biofilms and periphyton from high-altitude tropical lakes in the Bolivian Altiplano. Environ Sci Technol 52:9758–9767. https://doi.org/10.1021/acs.est.8b01885
doi: 10.1021/acs.est.8b01885
Boudou A, Ribeyre F (1997) Mercury in the food web: accumulation and transfer mechanisms. Met Ions Biol Syst 34:289–319
Bravo AG, Zopfi J, Buck M et al (2018) Geobacteraceae are important members of mercury-methylating microbial communities of sediments impacted by waste water releases. ISME J 12:802–812. https://doi.org/10.1038/s41396-017-0007-7
doi: 10.1038/s41396-017-0007-7
Bridou R, Monperrus M, Gonzalez PR et al (2011) Simultaneous determination of mercury methylation and demethylation capacities of various sulfate-reducing bacteria using species-specific isotopic tracers. Environ Toxicol Chem 30:337–344. https://doi.org/10.1002/etc.395
doi: 10.1002/etc.395
Cline JD (1969) Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr 14:454–458. https://doi.org/10.4319/lo.1969.14.3.0454
doi: 10.4319/lo.1969.14.3.0454
Compeau GC, Bartha R (1985) Sulfate-reducing bacteria: principal methylators of mercury in anoxic estuarine sediment. Appl Environ Microbiol 50(2):498–502. https://doi.org/10.1128/aem.50.2.498-502.1985
doi: 10.1128/aem.50.2.498-502.1985
Deonarine A, Hsu-Kim H (2009) Precipitation of mercuric sulfide nanoparticles in NOM-containing water: implications for the natural environment. Environ Sci Technol 43:2368–2373. https://doi.org/10.1021/es803130h
doi: 10.1021/es803130h
Drott A, Lambertsson L, Björn E, Skyllberg U (2007) Importance of dissolved neutral mercury sulfides for methyl mercury production in contaminated sediments. Environ Sci Technol 41:2270–2276. https://doi.org/10.1021/es061724z
doi: 10.1021/es061724z
Farina M, Rocha JBT, Aschner M (2011) Mechanisms of methylmercury-induced neurotoxicity: Evidence from experimental studies. Life Sci 89:555–563. https://doi.org/10.1016/j.lfs.2011.05.019
doi: 10.1016/j.lfs.2011.05.019
Findlay AJ (2016) Microbial impact on polysulfide dynamics in the environment. FEMS Microbiol Let 363:fnw103. https://doi.org/10.1093/femsle/fnw103
doi: 10.1093/femsle/fnw103
Findlay AJ, Kamyshny A (2017) Turnover rates of intermediate sulfur species (Sx2-, S0, S2O32-, S4O62-, SO32-) in anoxic freshwater and sediments. Front Microbiol 8. https://doi.org/10.3389/fmicb.2017.02551
Gentès S, Taupiac J, Colin Y et al (2017) Bacterial periphytic communities related to mercury methylation within aquatic plant roots from a temperate freshwater lake (South-Western France). Environ Sci Pollut Res 24:19223–19233. https://doi.org/10.1007/s11356-017-9597-x
doi: 10.1007/s11356-017-9597-x
Gerbig CA, Kim CS, Stegemeier JP et al (2011) Formation of nanocolloidal metacinnabar in mercury-DOM-sulfide systems. Environ Sci Technol 45:9180–9187. https://doi.org/10.1021/es201837h
doi: 10.1021/es201837h
Gilmour CC, Henry EA (1991) Mercury methylation in aquatic systems affected by acid deposition. Environ Pollut 71:131–169. https://doi.org/10.1016/0269-7491(91)90031-Q
doi: 10.1016/0269-7491(91)90031-Q
Gilmour CC, Elias DA, Kucken AM et al (2011) Sulfate-reducing bacterium Desulfovibrio desulfuricans ND132 as a model for understanding bacterial mercury methylation. Appl Environ Microbiol 77:3938–3951. https://doi.org/10.1128/AEM.02993-10
doi: 10.1128/AEM.02993-10
Gilmour CC, Podar M, Bullock AL et al (2013) Mercury methylation by novel microorganisms from new environments. Environ Sci Technol 47:11810–11820. https://doi.org/10.1021/es403075t
doi: 10.1021/es403075t
Gilmour CC, Bullock AL, McBurney A et al (2018) Robust mercury methylation across diverse methanogenic archaea. mBio 9:e02403-17. https://doi.org/10.1128/mBio.02403-17
doi: 10.1128/mBio.02403-17
Goñi-Urriza M, Corsellis Y, Lanceleur L et al (2015) Relationships between bacterial energetic metabolism, mercury methylation potential, and hgcA/hgcB gene expression in Desulfovibrio dechloroacetivorans BerOc1. Environ Sci Pollut Res 22:13764–13771. https://doi.org/10.1007/s11356-015-4273-5
doi: 10.1007/s11356-015-4273-5
Goñi-Urriza M, Klopp C, Ranchou-Peyruse M et al (2020) Genome insights of mercury methylation among Desulfovibrio and Pseudodesulfovibrio strains. Res Microbiol 171:3–12. https://doi.org/10.1016/j.resmic.2019.10.003
doi: 10.1016/j.resmic.2019.10.003
Graham AM, Aiken GR, Gilmour CC (2012a) Dissolved organic matter enhances microbial mercury methylation under sulfidic conditions. Environ Sci Technol 46:2715–2723. https://doi.org/10.1021/es203658f
doi: 10.1021/es203658f
Graham AM, Bullock AL, Maizel AC et al (2012b) Detailed assessment of the kinetics of Hg-cell association, Hg methylation, and methylmercury degradation in several Desulfovibrio species. Appl Environ Microbiol 78:7337–7346. https://doi.org/10.1128/AEM.01792-12
doi: 10.1128/AEM.01792-12
Graham AM, Aiken GR, Gilmour CC (2013) Effect of dissolved organic matter source and character on microbial Hg methylation in Hg–S–DOM solutions. Environ Sci Technol 47:5746–5754. https://doi.org/10.1021/es400414a
doi: 10.1021/es400414a
Hellal J, Schäfer J, Vigouroux R et al (2020) Impact of old and recent gold mining sites on mercury fluxes in suspended particulate matter, water and sediment in French Guiana. Appl Sci 10:7829. https://doi.org/10.3390/app10217829
doi: 10.3390/app10217829
Higueras P, Oyarzun R, Lillo J et al (2006) The Almadén district (Spain): anatomy of one of the world’s largest Hg-contaminated sites. Sci of the Tot Environ 356:112–124. https://doi.org/10.1016/j.scitotenv.2005.04.042
doi: 10.1016/j.scitotenv.2005.04.042
Isaure M-P, Albertelli M, Kieffer I et al (2020) Relationship between Hg speciation and Hg methylation/demethylation processes in the sulfate-reducing bacterium Pseudodesulfovibrio hydrargyri: evidences from HERFD-XANES and nano-XRF. Front Microbiol 11:584715. https://doi.org/10.3389/fmicb.2020.584715
doi: 10.3389/fmicb.2020.584715
Jensen S, Jernelöv A (1969) Biological methylation of mercury in aquatic organisms. Nature 223:753–754. https://doi.org/10.1038/223753a0
doi: 10.1038/223753a0
Joe-Wong C, Shoenfelt E, Hauser EJ, et al (2012) Estimation of reactive thiol concentrations in dissolved organic matter and bacterial cell membranes in aquatic systems. Environ Sci Technol 120831120231009.  https://doi.org/10.1021/es301381n
Jørgensen BB, Findlay AJ, Pellerin A (2019) The biogeochemical sulfur cycle of marine sediments. Front Microbiol 10. https://doi.org/10.3389/fmicb.2019.00849
Kanzler CR, Lian P, Trainer EL, et al (2018) Emerging investigator series: methylmercury speciation and dimethylmercury production in sulfidic solutions. Environ Sci: Process Impacts 20.  https://doi.org/10.1039/C7EM00533D
Kerin EJ, Gilmour CC, Roden E et al (2006) Mercury methylation by dissimilatory iron-reducing bacteria. Appl Environ Microbiol 72:7919–7921. https://doi.org/10.1128/AEM.01602-06
doi: 10.1128/AEM.01602-06
Liem-Nguyen V, Skyllberg U, Björn E (2017a) Thermodynamic modeling of the solubility and chemical speciation of mercury and methylmercury driven by organic thiols and micromolar sulfide concentrations in boreal wetland soils. Environ Sci Technol 51:3678–3686. https://doi.org/10.1021/acs.est.6b04622
doi: 10.1021/acs.est.6b04622
Liem-Nguyen V, Skyllberg U, Nam K et al (2017b) Thermodynamic stability of mercury(II) complexes formed with environmentally relevant low-molecular-mass thiols studied by competing ligand exchange and density functional theory. Environ Chem 14:243–253. https://doi.org/10.1071/EN17062
doi: 10.1071/EN17062
Lin H, Lu X, Liang L, Gu B (2015) Thiol-facilitated cell export and desorption of methylmercury by anaerobic bacteria. Environ Sci Technol Lett 2:292–296. https://doi.org/10.1021/acs.estlett.5b00209
doi: 10.1021/acs.estlett.5b00209
Liu Y-R, Lu X, Zhao L et al (2016) Effects of cellular sorption on mercury bioavailability and methylmercury production by Desulfovibrio desulfuricans ND132. Environ Sci Technol 50:13335–13341. https://doi.org/10.1021/acs.est.6b04041
doi: 10.1021/acs.est.6b04041
Monperrus M, Tessier E, Veschambre S et al (2005) Simultaneous speciation of mercury and butyltin compounds in natural waters and snow by propylation and species-specific isotope dilution mass spectrometry analysis. Anal Bioanal Chem 381:854–862. https://doi.org/10.1007/s00216-004-2973-7
doi: 10.1007/s00216-004-2973-7
Ndu U, Barkay T, Schartup AT et al (2016) The effect of aqueous speciation and cellular ligand binding on the biotransformation and bioavailability of methylmercury in mercury-resistant bacteria. Biodegrad 27:29–36. https://doi.org/10.1007/s10532-015-9752-3
doi: 10.1007/s10532-015-9752-3
Norambuena J, Miller M, Boyd JM, Barkay T (2020) Expression and regulation of the mer operon in Thermus thermophilus. Environ Microbiol 22:1619–1634. https://doi.org/10.1111/1462-2920.14953
doi: 10.1111/1462-2920.14953
Overmann J, Fischer U, Pfennig N (1992) A new purple sulfur bacterium from saline littoral sediments. Arch Microbiol 157:329–335. https://doi.org/10.1007/BF00248677
Parks JM, Johs A, Podar M et al (2013) The genetic basis for bacterial mercury methylation. Sci 339:1332–1335. https://doi.org/10.1126/science.1230667
doi: 10.1126/science.1230667
Pederick VG, Eijkelkamp BA, Begg SL et al (2015) ZnuA and zinc homeostasis in Pseudomonas aeruginosa. Sci Rep 5:13139. https://doi.org/10.1038/srep13139
doi: 10.1038/srep13139
Pedrero Z, Bridou R, Mounicou S et al (2012) Transformation, localization, and biomolecular binding of Hg species at subcellular level in methylating and nonmethylating sulfate-reducing bacteria. Environ Sci Technol 46:11744–11751. https://doi.org/10.1021/es302412q
doi: 10.1021/es302412q
Pham AL-T, Morris A, Zhang T et al (2014) Precipitation of nanoscale mercuric sulfides in the presence of natural organic matter: structural properties, aggregation, and biotransformation. Geochim Et Cosmochim Acta 133:204–215. https://doi.org/10.1016/j.gca.2014.02.027
doi: 10.1016/j.gca.2014.02.027
Qian C, Chen H, Johs A et al (2018) Quantitative proteomic analysis of biological processes and responses of the bacterium Desulfovibrio desulfuricans ND132 upon deletion of its mercury methylation Genes. PROTEOM 18:1700479. https://doi.org/10.1002/pmic.201700479
doi: 10.1002/pmic.201700479
Ranchou-Peyruse A, Moppert X, Hourcade E et al (2004) Characterization of brackish anaerobic bacteria involved in hydrocarbon degradation: a combination of molecular and culture-based approaches. Ophelia 58:255–262. https://doi.org/10.1080/00785236.2004.10410233
doi: 10.1080/00785236.2004.10410233
Ranchou-Peyruse M, Monperrus M, Bridou R et al (2009) Overview of mercury methylation capacities among anaerobic bacteria including representatives of the sulphate-reducers: implications for environmental studies. Geomicrobiol J 26:1–8. https://doi.org/10.1080/01490450802599227
doi: 10.1080/01490450802599227
Ranchou-Peyruse M, Goñi-Urriza M, Guignard M et al (2018) Pseudodesulfovibrio hydrargyri sp. nov., a mercury-methylating bacterium isolated from a brackish sediment. Int J System Evol Microbiol 68:1461–1466. https://doi.org/10.1099/ijsem.0.002173
doi: 10.1099/ijsem.0.002173
Rice KM, Walker EM, Wu M et al (2014) Environmental mercury and its toxic effects. J Prev Med Public Health 47:74–83. https://doi.org/10.3961/jpmph.2014.47.2.74
doi: 10.3961/jpmph.2014.47.2.74
Rimondi V, Chiarantini L, Lattanzi P et al (2015) Metallogeny, exploitation and environmental impact of the Mt. Amiata mercury ore district (Southern Tuscany, Italy). Italian Journal of Geosci 134:323–336. https://doi.org/10.3301/IJG.2015.02
doi: 10.3301/IJG.2015.02
Schaefer JK, Morel FMM (2009) High methylation rates of mercury bound to cysteine by Geobacter sulfurreducens. Nature Geosci 2:123–126. https://doi.org/10.1038/ngeo412
doi: 10.1038/ngeo412
Silver S (1996) Bacterial resistances to toxic metal ions - a review. Gene 179:9–19. https://doi.org/10.1016/S0378-1119(96)00323-X
doi: 10.1016/S0378-1119(96)00323-X
Silver S, Phung LT (2005) Genes and enzymes involved in bacterial oxidation and reduction of inorganic arsenic. Appl Environ Microbiol 71:599–608. https://doi.org/10.1128/AEM.71.2.599-608.2005
doi: 10.1128/AEM.71.2.599-608.2005
Stenzler BR, Zhang R, Semrau JD et al (2022) Diffusion of H2S from anaerobic thiolated ligand biodegradation rapidly generates bioavailable mercury. Environ Microbiol in Press. https://doi.org/10.1111/1462-2920.16078
doi: 10.1111/1462-2920.16078
Thomas SA, Gaillard J-F (2017) Cysteine addition promotes sulfide production and 4-fold Hg(II)–S coordination in actively metabolizing Escherichia coli. Environ Sci Technol 51:4642–4651. https://doi.org/10.1021/acs.est.6b06400
doi: 10.1021/acs.est.6b06400
Thomas SA, Rodby KE, Roth EW et al (2018) Spectroscopic and microscopic evidence of biomediated HgS species formation from Hg(II)–cysteine complexes: implications for Hg(II) bioavailability. Environ Sci Technol 52:10030–10039. https://doi.org/10.1021/acs.est.8b01305
doi: 10.1021/acs.est.8b01305
Thomas SA, Catty P, Hazemann J-L et al (2019) The role of cysteine and sulfide in the interplay between microbial Hg(ii) uptake and sulfur metabolism. Metallomics 11:1219–1229. https://doi.org/10.1039/c9mt00077a
doi: 10.1039/c9mt00077a
Thomas SA, Mishra B, Myneni SCB (2020) Cellular mercury coordination environment, and not cell surface ligands, influence bacterial methylmercury production. Environ Sci Technol 54:3960–3968. https://doi.org/10.1021/acs.est.9b05915
doi: 10.1021/acs.est.9b05915
Trüper HG, Pfennig N (1992) The Family Chlorobiaceae. In: Balows A, Trüper HG, Dworkin M et al (eds) The prokaryotes: a handbook on the biology of bacteria: ecophysiology, isolation, identification, applications. Springer, New York, pp 3583–3592
Widdel F, Bak F (1992) Gram-negative mesophilic sulfate-reducing bacteria. In: Balows A, Trüper HG, Dworkin M et al (eds) The prokaryotes. Springer, New York, pp 3352–3378
doi: 10.1007/978-1-4757-2191-1_21
Yoshida E, Toyama T, Shinkai Y et al (2011) Detoxification of methylmercury by hydrogen sulfide-producing enzyme in mammalian cells. Chem Res Toxicol 24:1633–1635. https://doi.org/10.1021/tx200394g
doi: 10.1021/tx200394g
Zhang T, Kim B, Levard C et al (2012) Methylation of mercury by bacteria exposed to dissolved, nanoparticulate, and microparticulate mercuric sulfides. Environ Sci Technol 46:6950–6958. https://doi.org/10.1021/es203181m
doi: 10.1021/es203181m
Zhang T, Kucharzyk K, Kim B, et al (2014) Net methylation of mercury in estuarine sediment microcosms amended with dissolved, nanoparticulate, and microparticulate mercuric sulfides. Environ Sci Technol 48. https://doi.org/10.1021/es500336j
Zhang Z, Si R, Lv J et al (2020) Effects of extracellular polymeric substances on the formation and methylation of mercury sulfide nanoparticles. Environ Sci Technol 54:8061–8071. https://doi.org/10.1021/acs.est.0c01456
doi: 10.1021/acs.est.0c01456

Auteurs

Sophie Barrouilhet (S)

Universite de Pau Et Des Pays de L'Adour, E2S UPPA, CNRS, IPREM UMR 5254, Pau, France.

Mathilde Monperrus (M)

Universite de Pau Et Des Pays de L'Adour, E2S UPPA, CNRS, IPREM UMR 5254, Anglet, France.

Emmanuel Tessier (E)

Universite de Pau Et Des Pays de L'Adour, E2S UPPA, CNRS, IPREM UMR 5254, Pau, France.

Bahia Khalfaoui-Hassani (B)

Universite de Pau Et Des Pays de L'Adour, E2S UPPA, CNRS, IPREM UMR 5254, Pau, France.

Rémy Guyoneaud (R)

Universite de Pau Et Des Pays de L'Adour, E2S UPPA, CNRS, IPREM UMR 5254, Pau, France.

Marie-Pierre Isaure (MP)

Universite de Pau Et Des Pays de L'Adour, E2S UPPA, CNRS, IPREM UMR 5254, Pau, France.

Marisol Goñi-Urriza (M)

Universite de Pau Et Des Pays de L'Adour, E2S UPPA, CNRS, IPREM UMR 5254, Pau, France. marisol.goni@univ-pau.fr.

Articles similaires

Populus Soil Microbiology Soil Microbiota Fungi
Aerosols Humans Decontamination Air Microbiology Masks
Coal Metagenome Phylogeny Bacteria Genome, Bacterial
Semiconductors Photosynthesis Polymers Carbon Dioxide Bacteria

Classifications MeSH