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In-depth characterization of bacterial and archaeal communities present in the abandoned Kettara pyrrhotite mine tailings (Morocco)

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Abstract

In Morocco, pollution caused by closed mines continues to be a serious threat to the environment, like the generation of acid mine drainage. Mine drainage is produced by environmental and microbial oxidation of sulfur minerals originating from mine wastes. The fundamental role of microbial communities is well known, like implication of Fe-oxidizing and to a lesser extent S-oxidizing microorganism in bioleaching. However, the structure of the microbial communities varies a lot from one site to another, like diversity depends on many factors such as mineralogy, concentration of metals and metalloids or pH, etc. In this study, prokaryotic communities in the pyrrhotite-rich tailings of Kettara mine were characterized using the Illumina sequencing. In-depth phylogenetic analysis revealed a total of 12 phyla of bacteria and 1 phyla of Archaea. The majority of sequences belonged to the phylum of Proteobacteria and Firmicutes with a predominance of Bacillus, Pseudomonas or Corynebacterium genera. Many microbial populations are implicated in the iron, sulfur and arsenic cycles, like Acidiferrobacter, Leptospirillum, or Alicyclobacillus in Fe; Acidiferrobacter and Sulfobacillus in S; and Bacillus or Pseudomonas in As. This is one of the first description of prokaryotic communities in pyrrhotite-rich mine tailings using high-throughput sequencing.

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References

  • Abdul SM, Jayasinghe SS, Chandana EPS, Jayasumana C et al (2015) Arsenic and human health effects: a review. Environ Toxicol Pharmacol 40:828–846

    Article  PubMed  Google Scholar 

  • Akcil A, Koldas S (2006) Acid mine drainage (AMD): causes, treatment and case studies. J Clean Prod 14:1139–1145

    Article  Google Scholar 

  • Anandham R, Indiragandhi P, Madhaiyan M, Ryu KY et al (2008) Chemolithoautotrophic oxidation of thiosulfate and phylogenetic distribution of sulfur oxidation gene (soxB) in rhizobacteria isolated from crop plants. Res Microbiol 159:579–589

    Article  CAS  PubMed  Google Scholar 

  • Auger C, Han S, Appanna VP, Thomas SC, Ulibarri G, Appanna VD (2013) Metabolic reengineering invoked by microbial systems to decontaminate aluminum: implications for bioremediation technologies. Biotechnol Adv 31:266–273

    Article  CAS  PubMed  Google Scholar 

  • Babi K, Asselin H, Benzaazoua M (2015) Stakeholders’ perceptions of sustainable mining in Morocco: a case study of the abandoned Kettara mine. Extr Ind Soc 1:185–192

    Google Scholar 

  • Bachate SP, Khapare RM, Kodam KM (2012) Oxidation of arsenite by two β-proteobacteria isolated from soil. Appl Microbiol Biotechnol 93:2135–2145

    Article  CAS  PubMed  Google Scholar 

  • Bachate SP, Nandre VS, Ghatpande NS, Kodam KM (2013) Simultaneous reduction of Cr(VI) and oxidation of As(III) by Bacillus firmus TE7 isolated from tannery effluent. Chemosphere 90:2273–2278

    Article  CAS  PubMed  Google Scholar 

  • Bachy C, Worden AZ (2014) Microbial ecology: finding structure in the rare biosphere. Curr Biol 24:R315–R317

    Article  CAS  PubMed  Google Scholar 

  • Bahar MM, Megharaj M, Naidu R (2012) Arsenic bioremediation potential of new arsenic oxidizing bacterium Stenotrophomonas sp. MM-7 isolated from soil. Biodegradation 23:803–812

    Article  CAS  PubMed  Google Scholar 

  • Bahar MM, Megharaj M, Naidu R (2013a) Bioremediation of arsenic-contaminated water: recent advances and future prospects. Water Air Soil Pollut 224:1722

    Article  Google Scholar 

  • Bahar MM, Megharaj M, Naidu R (2013b) Kinetics of arsenite oxidation by Variovorax sp. MM-1 isolated from a soil containing low arsenic and identification of arsenite oxidase gene. J Hazard Mater 262:997–1003

    Article  CAS  PubMed  Google Scholar 

  • Banerjee S, Majumdar J, Samal AC, Bhattachariya P et al (2013) Biotransformation and bioaccumulation of arsenic by Brevibacillus brevis isolated from arsenic contaminated region of West Bengal. IOSR J Environ Sci Toxicol Food Technol 3:1–10

    Article  Google Scholar 

  • Bates ST, Berg-Lyons D, Caporaso JG et al (2011) Examining the global distribution of dominant archaeal populations in soil. ISME J 5:908–917

    Article  CAS  PubMed  Google Scholar 

  • Behera BC, Patra M, Dutta SK, Thatoi HN (2014) Isolation and characterisation of sulphur oxidising bacteria from mangrove soil of Mahanadi River Delta and their sulphur oxidising ability. J Appl Environ Microbiol 2:1–5

    Google Scholar 

  • Bhatnagar L, Henriquet M, Zeikus JG, Aubert JP (1984) Utilization of mercapto-2-ethanol as a medium reductant for determination of the metabolic response of methanogens towards inorganic sulfur compounds. FEMS Microbiol Lett 22:155–158

    Article  CAS  Google Scholar 

  • Blum JS, Bindi AB, Buzelli J, Stolz JF, Oremland RS (1998) Bacillus arsenicoselenatis, sp. nov., and Bacillus selenitireducens, sp. nov.: two haloalkaliphiles from Mono Lake, California that respire oxyanions. Arch Microbiol 171:19–30

    Article  CAS  Google Scholar 

  • Bridge TAM, Johnson DB (1998) Reduction of soluble iron and reductive dissolution of ferric iron-containing minerals by moderately thermophilic iron-oxidizing bacteria. Appl Environ Microbiol 64:2181–2186

    CAS  PubMed  PubMed Central  Google Scholar 

  • Campos VL, Escalante G, Yañez J, Zaror CA et al (2009) Isolation of arsenite-oxidizing bacteria from a natural biofilm associated to volcanic rocks of Atacama Desert, Chile. J Basic Microbiol 49:S93–S97

    Article  PubMed  Google Scholar 

  • Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D et al (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci 108:4516–4522

    Article  CAS  PubMed  Google Scholar 

  • Chang J-S, Lee J-H, Kim I-S (2011) Bacterial aox genotype from arsenic contaminated mine to adjacent coastal sediment: evidences for potential biogeochemical arsenic oxidation. J Hazard Mater 193:233–242

    Article  CAS  PubMed  Google Scholar 

  • Chen LX, Li JT, Chen YT, Huang LN et al (2013) Shifts in microbial community composition and function in the acidification of a lead/zinc mine tailings. Environ Microbiol 15:2431–2444

    Article  CAS  PubMed  Google Scholar 

  • Das S, Jean J-S, Kar S, Chou M-L et al (2014) Screening of plant growth-promoting traits in arsenic-resistant bacteria isolated from agricultural soil and their potential implication for arsenic bioremediation. J Hazard Mater 272:112–120

    Article  CAS  PubMed  Google Scholar 

  • Diaby N, Dold B, Pfeifer HR, Holliger C, Johnson DB, Hallberg KB (2007) Microbial communities in a porphyry copper tailings impoundment and their impact on the geochemical dynamics of the mine waste. Environ Microbiol 9:298–307

    Article  CAS  PubMed  Google Scholar 

  • Dopson M, Johnson DB (2012) Biodiversity, metabolism and applications of acidophilic sulfur-metabolizing microorganisms. Environ Microbiol 14:2620–2631

    Article  CAS  PubMed  Google Scholar 

  • Duan M, Wang Y, Xie X, Su C et al (2013) Arsenite oxidizing bacterium isolated from high arsenic groundwater aquifers from Datong Basin, Northern China. Proc Earth Planet Sci 7:232–235

    Article  CAS  Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC, Quince C et al (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fisher J, Hollibaugh JT (2008) Selenate-dependent anaerobic arsenite oxidation by a bacterium from Mono Lake, California. Appl Environ Microbiol 74:2588–2594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Friedrich CG, Mitrenga G (1981) Oxidation of thiosulfate by Paracoccus denitrificans and other hydrogen bacteria. FEMS Microbiol Lett 10:209–212

    Article  CAS  Google Scholar 

  • Galand PE, Casamayor EO, Kirchman DL, Lovejoy C (2009) Ecology of the rare microbial biosphere of the Arctic Ocean. Proc Natl Acad Sci USA 106:22427–22432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garcia Balboa C, Bedoya IC, González F, Blázquez ML, Muñoz JA, Ballester A (2010) Bio-reduction of Fe(III) ores using three pure strains of Aeromonas hydrophila, Serratia fonticola and Clostridium celerecrescens and a natural consortium. Biores Technol 101:7864–7871

    Article  CAS  Google Scholar 

  • Hakkou R, Benzaazoua M, Bussière B (2008a) Acid mine drainage at the abandoned Kettara mine (Morocco): 1. Environmental characterization. Mine Water Environ 27:145–159

    Article  CAS  Google Scholar 

  • Hakkou R, Benzaazoua M, Bussière B (2008b) Acid mine drainage at the abandoned Kettara mine (Morocco): 2. Mine waste geochemical behavior. Mine Water Environ 27:160–170

    Article  CAS  Google Scholar 

  • Hallberg KB (2010) New perspectives in acid mine drainage microbiology. Hydrometallurgy 104:448–453

    Article  CAS  Google Scholar 

  • Hallberg KB, Hedrich S, Johnson DB (2011) Acidiferrobacter thiooxydans, gen. nov. sp. nov.; an acidophilic, thermo-tolerant, facultatively anaerobic iron-and sulfur-oxidizer of the family Ectothiorhodospiraceae. Extremophiles 15:271–279

    Article  CAS  PubMed  Google Scholar 

  • Han Y, Wang JB, Zhu XY, Guo NN (2012) Stable isotope and REE geological and geochemical characteristics of the calcite in the Fankou Zinc-Lead deposit, Guangdong Province, China. In Adv Mater Res 524:205–212

    Article  Google Scholar 

  • Huang LN, Zhou WH, Hallberg KB, Wan CY, Li J, Shu WS (2011) Spatial and temporal analysis of the microbial community in the tailings of a Pb-Zn mine generating acidic drainage. Appl Environ Microbiol 77:5540–5544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huse SM, Welch DM, Morrison HG, Sogin ML (2010) Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ Microbiol 12:1889–1898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang CY, Liu Y, Liu YY, You XY, Guo X, Liu SJ (2008) Alicyclobacillus ferrooxydans sp. nov., a ferrous-oxidizing bacterium from solfataric soil. Int J Syst Evol Microbiol 58:2898–2903

    Article  CAS  PubMed  Google Scholar 

  • Johnson DB, Bridge TAM (2002) Reduction of ferric iron by acidophilic heterotrophic bacteria: evidence for constitutive and inducible enzyme systems in Acidiphilium spp. J Appl Microbiol 92:315–321

    Article  CAS  PubMed  Google Scholar 

  • Johnson DB, Hallberg KB (2008) Carbon, iron and sulfur metabolism in acidophilic micro-organisms. Adv Microb Physiol 54:201–255

    Article  Google Scholar 

  • Justice NB, Norman A, Brown CT, Singh A, Thomas BC, Banfield JF (2014) Comparison of environmental and isolate Sulfobacillus genomes reveals diverse carbon, sulfur, nitrogen, and hydrogen metabolisms. BMC Genomics 15:1107

    Article  PubMed  PubMed Central  Google Scholar 

  • Karavaiko GI, Bogdanova TI, Tourova TP, Kondrat’eva TF et al (2005) Reclassification of ‘Sulfobacillus thermosulfidooxidans subsp thermotolerans’ strain K1 as Alicyclobacillus tolerans sp. nov. and Sulfobacillus disulfidooxidans Dufresne et al 1996 as Alicyclobacillus disulfidooxidans comb. nov., and emended description of the genus Alicyclobacillus. Int J Syst Evol Microbiol 55:941–947

    Article  CAS  PubMed  Google Scholar 

  • Katayama Y, Hiraishi A, Kuraishi H (1995) Paracoccus thiocyanatus sp. nov., a new species of thiocyanate-utilizing facultative chemolithotroph, and transfer of Thiobacillus versutus to the genus Paracoccus as Paracoccus versutus comb. nov. with emendation of the genus. Microbiology 141:1469–1477

    Article  CAS  PubMed  Google Scholar 

  • Khalil K, Hanich L, Bannari A, Zouhri L et al (2013) Assessment of soil contamination around an abandoned mine in a semi-arid environment using geochemistry and geostatistics: pre-work of geochemical process modeling with numerical models. J Geochem Explor 125:117–129

    Article  CAS  Google Scholar 

  • Kock D, Schippers A (2008) Quantitative microbial community analysis of three different sulfidic mine tailing dumps generating acid mine drainage. Appl Environ Microbiol 74:5211–5219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Korehi H, Blöthe M, Schippers A (2014) Microbial diversity at the moderate acidic stage in three different sulfidic mine tailings dumps generating acid mine drainage. Res Microbiol 165:713–718

    Article  CAS  PubMed  Google Scholar 

  • Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79:5112–5120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumaraswamy R, Sjollema K, Kuenen G, Van Loosdrecht M, Muyzer G (2006) Nitrate-dependent [Fe(II) EDTA]2− oxidation by Paracoccus ferrooxidans sp. nov., isolated from a denitrifying bioreactor. Syst Appl Microbiol 29:276–286

    Article  CAS  PubMed  Google Scholar 

  • Lghoul M, Teixidó T, Peña JA, Hakkou R, Kchikach A, Guérin R et al (2012) Electrical and seismic tomography used to image the structure of a tailings pond at the abandoned Kettara mine, Morocco. Mine Water Environ 31:53–61

    Article  Google Scholar 

  • Lghoul M, Maqsoud A, Hakkou R, Kchikach A (2014) Hydrogeochemical behavior around the abandoned Kettara mine site, Morocco. J Geochem Explor 144:456–467

    Article  CAS  Google Scholar 

  • Liao VHC, Chu YJ, Su YC, Hsiao SY, Wei CC, Liu CW et al (2011) Arsenite-oxidizing and arsenate-reducing bacteria associated with arsenic-rich groundwater in Taiwan. J Contam Hydrol 123:20–29

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Hua ZS, Chen LX, Kuang JL, Li SJ, Shu WS, Huang LN (2014) Correlating microbial diversity patterns with geochemistry in an extreme and heterogeneous environment of mine tailings. Appl Environ Microbiol 80:3677–3686

    Article  PubMed  PubMed Central  Google Scholar 

  • Luo J, Tian G, Lin W (2013) Enrichment, isolation and identification of sulfur-oxidizing bacteria from sulfide removing bioreactor. J Environ Sci 25:1393–1399

    Article  CAS  Google Scholar 

  • Macur RE, Jackson CR, Botero LM, Mcdermott TR, Inskeep WP (2004) Bacterial populations associated with the oxidation and reduction of arsenic in an unsaturated soil. Environ Sci Technol 38:104–111

    Article  CAS  PubMed  Google Scholar 

  • Mahmood Q, Zheng P, Hu B, Jilani G, Azim MR, Wu D, Liu D (2009) Isolation and characterization of Pseudomonas stutzeri QZ1 from an anoxic sulfide-oxidizing bioreactor. Anaerobe 15:108–115

    Article  CAS  PubMed  Google Scholar 

  • Mandal BK, Suzuki KT (2002) Arsenic round the world: a review. Talanta 58:201–235

    Article  CAS  PubMed  Google Scholar 

  • Mathieu C, Pieltain F (2003) Analyse chimique des sols. In: Méthode choisis. Ed Lavoisier, Tec and Doc

  • Mendez MO, Neilson JW, Maier RM (2008) Characterization of a bacterial community in an abandoned semiarid lead-zinc mine tailing site. Appl Environ Microbiol 74:3899–3907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muehe EM, Gerhardt S, Schink B, Kappler A (2009) Ecophysiology and the energetic benefit of mixotrophic Fe(II) oxidation by various strains of nitrate-reducing bacteria. FEMS Microbiol Ecol 70:335–343

    Article  CAS  PubMed  Google Scholar 

  • Needleman SB, Wunsch CD (1970) A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol 48:443–453

    Article  CAS  PubMed  Google Scholar 

  • Norris PR, Clark DA, Owen JP, Waterhouse S (1996) Characteristics of Sulfobacillus acidophilus sp. nov. and other moderately thermophilic mineral-sulphide-oxidizing bacteria. Microbiology 142:775–783

    Article  CAS  PubMed  Google Scholar 

  • Okamura K, Kawai A, Wakao N, Yamada T, Hiraishi A (2015) Acidiphilium iwatense sp. nov., isolated from an acid mine drainage treatment plant, and emendation of the genus Acidiphilium. Int J Syst Evol Microbiol 65:42–48

    Article  CAS  PubMed  Google Scholar 

  • Omori T, Monna LISA, Saiki Y, Kodama T (1992) Desulfurization of dibenzothiophene by Corynebacterium sp. strain SY1. Appl Environ Microbiol 58:911–915

    CAS  PubMed  PubMed Central  Google Scholar 

  • Oremland RS, Stolz JF (2003) The ecology of arsenic. Science 300:939–944

    Article  CAS  PubMed  Google Scholar 

  • Osborne FH, Ehrlich HL (1976) Oxidation of arsenite by a soil isolate of Alcaligenes. J Appl Microbiol 41:295–305

    CAS  Google Scholar 

  • Paul D, Poddar S, Sar P (2014) Characterization of arsenite-oxidizing bacteria isolated from arsenic-contaminated groundwater of West Bengal. J Environ Sci Health Part A-Toxic/Hazard Subst Environ Eng 49:1481–1492

    Article  CAS  Google Scholar 

  • Pina RG, Cervantes C (1996) Microbial interactions with aluminium. BioMetals 9:311–316

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org

  • Rawlings DE, Johnson DB (2007) The microbiology of biomining: development and optimization of mineral-oxidizing microbial consortia. Microbiology 153:315–324

    Article  CAS  PubMed  Google Scholar 

  • Sallam A, Steinbüchel A (2009) Clostridium sulfidigenes sp. nov., a mesophilic, proteolytic, thiosulfate-and sulfur-reducing bacterium isolated from pond sediment. Int J Syst Evol Microbiol 59:1661–1665

    Article  CAS  PubMed  Google Scholar 

  • Sanchez Andrea I, Rodriguez N, Amils R, Sanz JL (2011) Microbial diversity in anaerobic sediments at Rio Tinto, a naturally acidic environment with a high heavy metal content. Appl Environ Microbiol 77:6085–6093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santini JM, Sly LI, Schnagl RD, Macy JM (2000) A new chemolithoautotrophic arsenite-oxidizing bacterium isolated from a gold mine: phylogenetic, physiological, and preliminary biochemical studies. Appl Environ Microbiol 66:92–97

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sarkar A, Kazy KS, Sar P (2014) Studies on arsenic transforming groundwater bacteria and their role in arsenic release from subsurface sediment. Environ Sci Pollut Res 21:8645–8662

    Article  CAS  Google Scholar 

  • Schippers A, Sand W (1999) Bacterial leaching of metal sulfides proceeds by two indirect mechanisms via thiosulfate or via polysulfides and sulfur. Appl Environ Microbiol 65:319–321

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schippers A, Kock D, Schwartz M, Böttcher ME, Vogel H, Hagger M (2007) Geomicrobiological and geochemical investigation of a pyrrhotite-containing mine waste tailings dam near Selebi-Phikwe in Botswana. J Geochem Explor 92:151–158

    Article  CAS  Google Scholar 

  • Schippers A, Breuker A, Blazejak A, Bosecker K, Kock D, Wright TL (2010) The biogeochemistry and microbiology of sulfidic mine waste and bioleaching dumps and heaps, and novel Fe(II)-oxidizing bacteria. Hydrometallurgy 104:342–350

    Article  CAS  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schloss PD, Gevers D, Westcott SL (2011) Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6:e27310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simate GS, Ndlovu S (2014) Acid mine drainage: challenges and opportunities. J Environ Chem Eng 2:1785–1803

    Article  CAS  Google Scholar 

  • Singer PC, Stumm W (1970) Acid mine drainage: the rate-determining step. Science 167:1121–1123

    Article  CAS  PubMed  Google Scholar 

  • Sorokin DY, Teske A, Robertson LA, Kuenen JG (1999) Anaerobic oxidation of thiosulphate to tetrathionate by obligately heterotrophic bacteria, belonging to the Pseudomonas stutzeri complex. FEMS Microbiol Ecol 30:113–123

    Article  CAS  PubMed  Google Scholar 

  • Stolz JF, Basu P, Santini JM, Oremland RS (2006) Arsenic and selenium in microbial metabolism. Annu Rev Microbiol 60:107–130

    Article  CAS  PubMed  Google Scholar 

  • Takahashi Y, Suto K, Inoue C (2010) Polysulfide reduction by Clostridium relatives isolated from sulfate-reducing enrichment cultures. J Biosci Bioeng 109:372–380

    Article  CAS  PubMed  Google Scholar 

  • Tan GL, Shu WS, Hallberg KB, Li F, Lan CY, Zhou WH, Huang LN (2008) Culturable and molecular phylogenetic diversity of microorganisms in an open-dumped, extremely acidic Pb/Zn mine tailings. Extremophiles 12:657–664

    Article  CAS  PubMed  Google Scholar 

  • Thermo Scientific NITON (2008) Thermo Scientific NITON® XL3t 900 Series Product specifications. http://www.thermo.com/niton (last accessed 3 Nov 2014)

  • Toughzaoui S, El Amari K, Benkaddour A, Hibti M, Essarraj S (2015) Hydrogeochemical and isotopic studies of the Kettara mine watershed, Morocco. Mine Water Environ 34:308–319

    Article  CAS  Google Scholar 

  • Turner AW (1954) Bacterial oxidation of arsenite. I. Description of bacteria isolated from arsenical cattle-dipping fluids. Aust J Biol Sci 7:452–476

    Article  CAS  PubMed  Google Scholar 

  • Ventura BA, González F, Ballester A, Blázquez ML, Muñoz JA (2015) Bioreduction of iron compounds by Aeromonas hydrophila. Int Biodeterior Biodegrad 103:69–76

    Article  CAS  Google Scholar 

  • Vera M, Schippers A, Sand W (2013) Progress in bioleaching: fundamentals and mechanisms of bacterial metal sulfide oxidation. Part A. Appl Microbiol Biotechnol 97:7529–7541

    Article  CAS  PubMed  Google Scholar 

  • Vikromvarasiri N, Boonyawanich S, Pisutpaisal N (2015) Optimizing sulfur oxidizing performance of Paracoccus pantotrophus isolated from leather industry wastewater. Energy Proc 79:629–633

    Article  CAS  Google Scholar 

  • Wang GW, Chen TH, Yue ZB, Zhou YF, Wang J (2014a) Isolation and characterization of Pseudomonas stutzeri capable of reducing Fe(III) and nitrate from skarn-type copper mine tailings. Geomicrobiol J 31:509–518

    Article  Google Scholar 

  • Wang P, Sun G, Jia Y, Meharg AA, Zhu Y (2014b) A review on completing arsenic biogeochemical cycle: microbial volatilization of arsines in environment. J Environ Sci 26:371–381

    Article  Google Scholar 

  • Weber KA, Achenbach LA, Coates JD (2006) Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction. Nat Rev Microbiol 4:752–764

    Article  CAS  PubMed  Google Scholar 

  • Xiu W, Guo H, Liu Q, Liu Z, Zhang B (2015) Arsenic removal and transformation by Pseudomonas sp. strain GE-1-induced ferrihydrite: co-precipitation versus adsorption. Water Air Soil Pollut 226:1–14

    Article  CAS  Google Scholar 

  • Xu XJ, Chen C, Guo HL, Wang AJ, Ren NQ, Lee DJ (2016) Characterization of a newly isolated strain Pseudomonas sp. C27 for sulfide oxidation: reaction kinetics and stoichiometry. Sci Rep 6:21032. doi:10.1038/srep21032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamamura S, Amachi S (2014) Microbiology of inorganic arsenic: from metabolism to bioremediation. J Biosci Bioeng 118:1–9

    Article  CAS  PubMed  Google Scholar 

  • Zeikus JG, Wolfe RS (1972) Methanobacterium thermoautotrophicum sp. nov., an anaerobic, autotrophic, extreme thermophile. J Bacteriol 109:707–713

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors thank the International Research Chairs Initiative funded by the International Development Research Centre (IDRC), Canada, and by the Canada Research Chairs program and the IRD (Institut de Recherche pour le Développement) for supporting this research.

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Bruneel, O., Mghazli, N., Hakkou, R. et al. In-depth characterization of bacterial and archaeal communities present in the abandoned Kettara pyrrhotite mine tailings (Morocco). Extremophiles 21, 671–685 (2017). https://doi.org/10.1007/s00792-017-0933-3

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