Abstract
Some microorganisms have the capacity to interact with arsenic through resistance or metabolic processes. Their activities contribute to the fate of arsenic in contaminated ecosystems. To investigate the genetic potential involved in these interactions in a zone of confluence between a pristine river and an arsenic-rich acid mine drainage, we explored the diversity of marker genes for arsenic resistance (arsB, acr3.1, acr3.2), methylation (arsM), and respiration (arrA) in waters characterized by contrasted concentrations of metallic elements (including arsenic) and pH. While arsB-carrying bacteria were representative of pristine waters, Acr3 proteins may confer to generalist bacteria the capacity to cope with an increase of contamination. arsM showed an unexpected wide distribution, suggesting biomethylation may impact arsenic fate in contaminated aquatic ecosystems. arrA gene survey suggested that only specialist microorganisms (adapted to moderately or extremely contaminated environments) have the capacity to respire arsenate. Their distribution, modulated by water chemistry, attested the specialist nature of the arsenate respirers. This is the first report of the impact of an acid mine drainage on the diversity and distribution of arsenic (As)-related genes in river waters. The fate of arsenic in this ecosystem is probably under the influence of the abundance and activity of specific microbial populations involved in different As biotransformations.
Similar content being viewed by others
References
Johnson DB, Hallberg KB (2004) The microbiology of acidic mine waters. Res Microbiol 154:466–473
Hallberg KB, Johnson DB (2005) Microbiology of a wetland ecosystem constructed to remediate mine drainage from a heavy metal mine. Sci Total Environ 338:53–66
Casiot C, Leblanc M, Bruneel O, Personné JC, Koffi K, Elbaz-Poulichet F (2003) Geochemical processes controlling the formation of As-rich waters within a tailings impoundment (Carnoulès, France). Aquat Geochem 9:273–290
Egal M, Casiot C, Morin G, Elbaz-Poulichet F, Cordier MA, Bruneel O (2010) An updated insight into the natural attenuation of As concentrations in Reigous Creek (southern France). Appl Geochem 25:1949–1957
Héry M, Casiot C, Resongles E, Gallice Z, Bruneel O, Desoeuvre A, Delpoux S (2014) Release of arsenite, arsenate and methyl-arsenic species from streambed sediment affected by acid mine drainage: a microcosm study. Environ Chem 11:514
Hallberg KB (2010) New perspectives in acid mine drainage microbiology. Hydrometallurgy 104:448–453
Mohapatra BR, Douglas Gould W, Dinardo O, Koren DW (2011) Tracking the prokaryotic diversity in acid mine drainage-contaminated environments: a review of molecular methods. Miner Eng 24:709–718
Bruneel O, Duran R, Casiot C, Elbaz-Poulichet F, Personne JC (2006) Diversity of microorganisms in Fe-As-rich acid mine drainage waters of Carnoules, France. Appl Environ Microbiol 72:551–556
Volant A, Desoeuvre A, Casiot C, Lauga B, Delpoux S, Morin G, Personné JC et al (2012) Archaeal diversity: temporal variation in the arsenic-rich creek sediments of Carnoulès Mine, France. Extremophiles 16:645–657
Volant A, Bruneel O, Desoeuvre A, Héry M, Casiot C, Bru N, Delpoux S et al (2014) Diversity and spatiotemporal dynamics of bacterial communities: physicochemical and other drivers along an acid mine drainage. FEMS Microbiol Ecol 90:247–263
Bertin PN, Heinrich-Salmeron A, Pelletier E, Goulhen-Chollet F, Arsène-Ploetze F, Gallien S, Lauga B et al (2011) Metabolic diversity among main microorganisms inside an arsenic-rich ecosystem revealed by meta- and proteo-genomics. ISME J 5:1735–1747
Fahy A, Giloteaux L, Bertin P, Le Paslier D, Médigue C, Weissenbach J, Duran R et al (2015) 16S rRNA and As-related functional diversity: contrasting fingerprints in arsenic-rich sediments from an acid mine drainage. Microb Ecol 70:154–67
Rosen BP (1999) Families of arsenic transporters. Trends Microbiol 7:207–212
Yang Y, Wu S, Lilley RM, Zhang R (2015) The diversity of membrane transporters encoded in bacterial arsenic-resistance operons. Peer J 3:943
Achour AR, Bauda P, Billard P (2007) Diversity of arsenite transporter genes from arsenic-resistant soil bacteria. Res Microbiol 158:128–137
Rosen BP (2002) Biochemistry of arsenic detoxification. FEBS Lett 529:86–92
Oremland RS, Stolz JF (2003) The ecology of arsenic. Science 300:939–944
Hug K, Maher WA, Stott MB, Krikowa F, Foster S, Moreau JW (2014) Microbial contributions to coupled arsenic and sulfur cycling in the acid-sulfide hot spring Champagne Pool, New Zealand. Front Microbiol 5:569
Wang PP, Bao P, Sun GX (2015) Identification and catalytic residues of the arsenite methyltransferase from a sulfate-reducing bacterium, Clostridium sp. BXM FEMS Microbiol Let 362:1–8
Zhang J, Cao T, Tang Z, Shen Q, Rosen BP, Zhao FJ (2015) Arsenic methylation and volatilization by arsenite S-adenosylmethionine methyltransferase in Pseudomonas alcaligenes NBRC14159. Appl Environ Microbiol 81:2852–2860
Mestrot A, Feldmann J, Krupp EM, Hossain MS, Roman-Ross G, Meharg AA (2011) Field fluxes and speciation of arsines emanating from soils. Environ Sci Technol 45:1798–1804
Singh JS, Abhilash C, Singh NB, Singh R, Singh D (2011) Genetically engineered bacteria: an emerging tool for environmental remediation and future research perspectives. Gene 480:1–9
Chen J, Sun GX, Wang XX, de Lorenzo V, Rosen BP, Zhu YG (2014) Volatilization of arsenic from polluted soil by Pseudomonas putida engineered for expression of the arsM arsenic(III) S-adenosine methyltransferase gene. Environ Sci Technol 48:10337–10344
Yin XX, Chen J, Qin J, Sun GX, Rosen BP, Zhu YG (2011) Biotransformation and volatilization of arsenic by three photosynthetic cyanobacteria. PLANT Physiol 156:1631–1638
Jia Y, Huang H, Zhong M, Wang FH, Zhang LM, Zhu YG (2013) Microbial arsenic methylation in soil and rice rhizosphere. Environ Sci Technol 47:3141–3148
Zhao FJ, Harris E, Yan J, Ma J, Wu L, Liu W, McGrath S et al (2013) Arsenic methylation in soils and its relationship with microbial arsM abundance and diversity, and As speciation in rice. Environ Sci Technol 47:7147–7154
Zhang SY, Zhao FJ, Sun GX, Su JQ, Yang XR, Li H et al (2015) Diversity and abundance of arsenic biotransformation genes in paddy soils from southern China. Environ Sci Technol 49:4138–4146
Oremland RS, Stolz JF (2005) Arsenic, microbes and contaminated aquifers. Trends Microbiol 13:45–49
Ahmann D, Roberts AL, Krumholz LR, Morel FMM (1994) Microbe grows by reducing arsenic 371:750
Malasarn D, Saltikov CW, Campbell KM, Santini JM, Hering JG, Newman DK (2004) arrA is a reliable marker for As(V) respiration. Science 306:455–455
Leblanc M, Achard B, Ben Othman D, Luck JM, Bertrand-Sarfati J, Personné JC (1996) Accumulation of arsenic from acidic mine waters by ferruginous bacterial accretions (stromatolites). Appl Geochem 11:541–554
OSU OREME database, http://data.oreme.org/carnoules/home
Casiot C, Lebrun S, Morin G, Bruneel O, Personne JC, Elbaz Poulichet F (2005) Sorption and redox processes controlling arsenic fate and transport in a stream impacted by acid mine drainage. Sci Total Environ 347:122–130
Casiot C, Egal M, Elbaz-Poulichet F, Bruneel O, Bancon-Montigny C, Cordier MA, Gomez E et al (2009) Hydrological and geochemical control of metals and arsenic in a Mediterranean river contaminated by acid mine drainage (the Amous River, France); preliminary assessment of impacts on fish (Leuciscus cephalus). Appl Geochem 24:787–799
Fisher E, Dawson AM, Polshyna G, Lisak J, Crable B, Perera E, Ranganathan (2008) Transformation of inorganic and organic arsenic by Alkaliphilus oremlandii sp. nov. strain OhILAs. Ann NY Acad Sci 1125:230–241
Lear G, Song B, Gault AG, Polya DA, Lloyd JR (2007) Molecular analysis of arsenate-reducing bacteria within Cambodian sediments following amendment with acetate. Appl Environ Microbiol 73:1041–1048
Héry M, Van Dongen BE, Gill F, Mondal D, Vaughan DJ, Pancost RD, Polya DA, Lloyd JR (2010) Arsenic release and attenuation in low organic carbon aquifer sediments from West Bengal. Geobiology 8:155–168
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol Biol Evol 30:2725–2729
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541
Bruneel O, Personne JC, Casiot C, Leblanc M, Elbaz-Poulichet F, Mahler BJ, Le Fleche A et al (2003) Mediation of arsenic oxidation by Thiomonas sp. in acid-mine drainage (Carnoules, France). J Appl Microbiol 95:492–499
Duquesne K, Lieutaud A, Ratouchniak J, Muller D, Lett MC, Bonnefoy V (2008) Arsenite oxidation by a chemoautotrophic moderately acidophilic Thiomonas sp.: from the strain isolation to the gene study. Environ Microbiol 10:228–237
Marapakala K, Qin J, Rosen BP (2012) Identification of catalytic residues in the As(III) S-adenosyl methionine methyltransferase. Biochemistry 51:944–951
Páez-Espino D, Tamames J, de Lorenzo V, Cánovas D (2009) Microbial responses to environmental arsenic. BioMetals 22:117–130
Cai L, Liu G, Rensing C, Wang G (2009) Genes involved in arsenic transformation and resistance associated with different levels of arsenic-contaminated soils. BMC Microbiol 9:4
Héry M, Rizoulis A, Sanguin H, Cooke DA, Pancost RD, Polya DA, Lloyd JR (2015) Microbial ecology of arsenic-mobilizing Cambodian sediments: lithological controls uncovered by stable-isotope probing: As mobilization in contrasting Cambodian sediments. Environ Microbiol 17:1857–69
Giloteaux L, Holmes DE, Williams KH, Wrighton KC, Wilkins MJ, Montgomery A, Smith JA et al (2013) Characterization and transcription of arsenic respiration and resistance genes during in situ uranium bioremediation. ISME J 7:370–383
Lloyd JR, Gault AG, Héry M, MacRae JD (2011) Microbial transformations of arsenic in the subsurface. In: Stolz JF, Oremland RS (eds) Environmental Microbe-Metal Interactions II. ASM Press, Washington
Mumford AC, Barringer JL, Benzel WM, Reilly A, Young LY (2012) Microbial transformations of arsenic: mobilization from glauconitic sediments to water. Water Res 46:2859–2868
Mumford AC, Barringer JL, Reilly A, Eberl DD, Blum AE, Young LY (2015) Biogeochemical environments of streambed-sediment pore waters with and without arsenic enrichment in a sedimentary rock terrain, New Jersey Piedmont, USA. Sci Total Environ 505:1350–1360
Hollibaugh JT, Budinoff C, Hollibaugh RA, Ransom B, Bano N (2006) Sulfide oxidation coupled to arsenate reduction by a diverse microbial community in a soda lake. Appl Environ Microbiol 72:2043–2049
Kulp TR, Hoeft SE, Miller LG, Saltikov C, Murphy JN, Han S, Lanoil B, Oremland RS (2006) Dissimilatory arsenate and sulfate reduction in sediments of two hypersaline, arsenic-rich soda lakes: Mono and Searles Lakes, California. Appl Environ Microbiol 72:6514–6526
Kulp TR, Han S, Saltikov CW, Lanoil BD, Zargar K, Oremland RS (2007) Effects of imposed salinity gradients on dissimilatory arsenate reduction, sulfate reduction, and other microbial processes in sediments from two California soda lakes. Appl Environ Microbiol 73:5130–5137
Song B, Chyun E, Jaffé R, Ward BB (2009) Molecular methods to detect and monitor dissimilatory arsenate-respiring bacteria (DARB) in sediments: arrA gene detection in sediment. FEMS Microbiol Ecol 68:108–117
Jia Y, Huang H, Chen Z, Zhu YG (2014) Arsenic uptake by rice is influenced by microbe-mediated arsenic redox changes in the rhizosphere. Environ Sci Technol 48:1001–1007
Drewniak L, Maryan N, Lewandowski W, Kaczanowski S, Sklodowska A (2012) The contribution of microbial mats to the arsenic geochemistry of an ancient gold mine. Environ Pollut 162:190–201
Acknowledgments
We thank the University of Montpellier, the IRD, and the OSU OREME for financial support. We thank Yong-Guan Zhu, Si-Yu Zhang, and Yan Jia (Chinese Academy of Sciences) for useful discussions about arsM primers and Ludovic Giloteaux (Cornell University, USA) for useful discussion about arsB and acr3p genes. The authors wish also to thank David Karlin for his suggestions for improvement of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Electronic Supplementary Material
Below is the link to the electronic supplementary material.
ESM 1
(DOC 1032 kb)
Rights and permissions
About this article
Cite this article
Desoeuvre, A., Casiot, C. & Héry, M. Diversity and Distribution of Arsenic-Related Genes Along a Pollution Gradient in a River Affected by Acid Mine Drainage. Microb Ecol 71, 672–685 (2016). https://doi.org/10.1007/s00248-015-0710-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-015-0710-8