Microbial Communities in Peruvian Acid Mine Drainages: Low-Abundance Sulfate-Reducing Bacteria With High Metabolic Activity

References

• Alazard D, Joseph M, Battaglia-Brunet F, Cayol JL, Ollivier B. 2010. Desulfosporosinus acidiphilus sp. nov.: a moderately acidophilic sulfate-reducing bacterium isolated from acid mining drainage sediments: new taxa: Firmicutes (Class Clostridia, Order Clostridiales, Family Peptococcaceae). Extremophiles 14(3):305–312.
   PubMed Web of Science ®Google Scholar
• Auld RR, Mykytczuk NCS, Leduc LG, Merritt TJS. 2017. Seasonal variation in an acid mine drainage microbial community. Can J Microbiol 63(2):137–152.
   PubMed Web of Science ®Google Scholar
• Ayangbenro AS, Olanrewaju OS, Babalola OO. 2018. Sulfate-reducing bacteria as an effective tool for sustainable acid mine bioremediation. Front Microbiol 9:1986.
   PubMed Web of Science ®Google Scholar
• Baker BJ, Banfield JF. 2003. Microbial communities in acid mine drainage. FEMS Microbiol Ecol 44(2):139–152.
   PubMed Web of Science ®Google Scholar
• Bartsch S, Gensch A, Stephan S, Doetsch A, Gescher J. 2017. Metallibacterium scheffleri: genomic data reveal a versatile metabolism. FEMS Microbiol Ecol 93(3):fix011.
   PubMed Web of Science ®Google Scholar
• Battaglia-Brunet F, Achbouni HE, Quemeneur M, Hallberg KB, Kelly DP, Joulian C. 2011. Proposal that the arsenite-oxidizing organisms Thiomonas cuprina and “‘Thiomonas arsenivorans' be reclassified as strains of Thiomonas delicata, and emended description of Thiomonas delicata”. Int J Syst Evol Microbiol 61(Pt 12):2816–2821.
   PubMed Web of Science ®Google Scholar
• Bhowal S, Chakraborty R. 2011. Five novel acid-tolerant oligotrophic thiosulfate-metabolizing chemolithotrophic acid mine drainage strains affiliated with the genus Burkholderia of Betaproteobacteria and identification of two novel soxB gene homologues. Res Microbiol 162(4):436–445.
   PubMed Web of Science ®Google Scholar
• Bomberg M, Arnold M, Kinnunen P. 2015. Characterization of the bacterial and sulphate reducing community in the alkaline and constantly cold water of the closed Kotalahti mine. Minerals 5(3):452–472.
   Google Scholar
• Bomberg M, Mäkinen J, Salo M, Kinnunen P. 2019. High diversity in iron cycling microbial communities in acidic, iron-rich water of the Pyhäsalmi mine, Finland. Geofluids 2019:1–17.
   Web of Science ®Google Scholar
• Brantner JS, Haake ZJ, Burwick JE, Menge CM, Hotchkiss ST, Senko JM. 2014. Depth-dependent geochemical and microbiological gradients in Fe(III) deposits resulting from coal mine-derived acid mine drainage. Front Microbiol 5:215.
   PubMed Web of Science ®Google Scholar
• Bryan CG, Marchal M, Battaglia-Brunet F, Kugler V, Lemaitre-Guillier C, Lièvremont D, Bertin PN, Arsène-Ploetze F. 2009. Carbon and arsenic metabolism in Thiomonas strains: differences revealed diverse adaptation processes. BMC Microbiol 9:127.
   PubMed Web of Science ®Google Scholar
• Canchaya S. 1990. In Stratabound Ore Deposits in the Andes. New York (NY): Springer-Verlag Berlin Heidelberg. p569–582.
   Google Scholar
• Chen L, Huang L, Méndez-García C, Kuang J, Hua Z, Liu J, Shu W. 2016. Microbial communities, processes and functions in acid mine drainage ecosystems. Curr Opin Biotechnol 38:150–158.
   PubMed Web of Science ®Google Scholar
• Church CD, Wilkin RT, Alpers CN, Rye RO, Blaine RB. 2007. Microbial sulfate reduction and metal attenuation in pH 4 acid mine water. Geochem Trans 8:10.
   PubMed Web of Science ®Google Scholar
• Cline JD. 1969. Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr 14(3):454–458.
   Web of Science ®Google Scholar
• Dar SA, Kleerebezem R, Stams AJM, Kuenen JG, Muyzer G. 2008. Competition and coexistence of sulfate-reducing bacteria, acetogens and methanogens in a lab-scale anaerobic bioreactor as affected by changing substrate to sulfate ratio. Appl Microbiol Biotechnol 78(6):1045–1055.
   PubMed Web of Science ®Google Scholar
• Diez-Ercilla M, Sánchez-España J, Yusta I, Wendt-Potthoff K, Koschorreck M. 2014. Formation of biogenic sulphides in the water column of an acidic pit lake: biogeochemical controls and effects on trace metal dynamics. Biogeochemistry 121(3):519–536.
   Web of Science ®Google Scholar
• Dold B. 2014. Evolution of acid mine drainage formation in sulphidic mine tailings. Minerals 4(3):621–641.
   Web of Science ®Google Scholar
• Dopson M, Holmes DS. 2014. Metal resistance in acidophilic microorganisms and its significance for biotechnologies. Appl Microbiol Biotechnol 98(19):8133–8144.
   PubMed Web of Science ®Google Scholar
• [DIGESA] Dirección General de Salud ambiental. 2012. Accessed September 10, 2021. Available at http://www.digesa.minsa.gob.pe/DEPA/vigilancia_recursos_hidricos.asp
   Google Scholar
• Eisen S, Poehlein A, Johnson DB, Daniel R, Schlömann M, Mühling M. 2016. Genome sequence of the acidophilic iron oxidizer Ferrimicrobium acidiphilum strain T23T. Genome Announc 3(2):383–398.
   Google Scholar
• Falagán C, Johnson DB. 2014. Acidibacter ferrireducens gen. nov., sp. nov.: an acidophilic ferric iron-reducing gammaproteobacterium. Extremophiles 18(6):1067–1073.
   PubMed Web of Science ®Google Scholar
• Falagán C, Sánchez-España J, Johnson DB. 2014. New insights into the biogeochemistry of extremely acidic environments revealed by a combined cultivation-based and culture-independent study of two stratified pit lakes. FEMS Microbiol Ecol 87(1):231–243.
   PubMed Web of Science ®Google Scholar
• Fang Y, Xu M, Chen X, Sun G, Guo J, Wu W, Liu X. 2015. Modified pretreatment method for total microbial DNA extraction from contaminated river sediment. Front Environ Sci Eng. 9(3):444–452.
   Web of Science ®Google Scholar
• Ferreira ML, Ramirez SA, Vullo DL. 2018. Chemical characterization and ligand behaviour of Pseudomonas veronii 2E siderophores. World J Microbiol Biotechnol 34(9):1–12.
   Web of Science ®Google Scholar
• Fichtel K, Mathes F, Könneke M, Cypionka H, Engelen B, Teske A, Loy A. 2012. Isolation of sulfate-reducing bacteria from sediments above the deep-subseafloor aquifer. Front Microbiol 3:65.
   PubMed Web of Science ®Google Scholar
• García-Moyano A, Austnes A, Lanzén A, González-Toril E, Aguilera Á, Øvreås L. 2015. Novel and unexpected microbial diversity in acid mine drainage in Svalbard (78° N), revealed by culture-independent approaches. Microorganisms 3(4):667–694.
   PubMedGoogle Scholar
• Gavrilov SN, Korzhenkov AA, Kublanov IV, Bargiela R, Zamana LV, Popova AA, Toshchakov SV, Golyshin PN, Golyshina OV. 2019. Microbial communities of polymetallic deposits’ acidic ecosystems of continental climatic zone with high temperature contrasts. Front Microbiol 10:1573.
   PubMed Web of Science ®Google Scholar
• Giovannoni SJ, Schabtach E, Castenholz RW. 1987. Isosphaera pallida, gen. and comb. nov., a gliding, budding eubacterium from hot springs. Arch Microbiol 147(3):276–284.
   Web of Science ®Google Scholar
• González D, Liu Y, Villa Gomez D, Southam G, Hedrich S, Galleguillos P, Colipai C, Nancucheo I. 2019. Performance of a sulfidogenic bioreactor inoculated with indigenous acidic communities for treating an extremely acidic mine water. Min Eng 131:370–375.
   Web of Science ®Google Scholar
• González-Toril E, Aguilera Á, Souza-Egipsy V, López Pamo E, Sánchez España J, Amils R. 2011. Geomicrobiology of La Zarza-Perrunal acid mine effluent (Iberian Pyritic Belt, Spain). Appl Environ Microbiol 77(8):2685–2694.
   PubMed Web of Science ®Google Scholar
• Grettenberger CL, Pearce AR, Bibby KJ, Jones DS, Burgos WD, Macalady JL. 2017. Efficient low-pH iron removal by a microbial iron oxide mound ecosystem at scalp level run. Appl Environ Microbiol 83(7):e00015–17.
   PubMed Web of Science ®Google Scholar
• Hallbeck L, Pedersen K. 2014. The family Gallionellaceae. In: Rosenberg, E, DeLong, EF, Lory, S, Stackebrandt, E, Thompson, F, editors. The Prokaryotes: Alphaproteobacteria and Betaproteobacteria. 4th ed. London: Springer-Verlag Berlin Heidelberg, p853–858.
   Google Scholar
• Hausmann B, Pelikan C, Herbold CW, Köstlbacher S, Albertsen M, Eichorst SA, Glavina del Rio T, Huemer M, Nielsen PH, Rattei T, et al. 2018. Peatland Acidobacteria with a dissimilatory sulfur metabolism. ISME J 12(7):1729–1742.
   PubMed Web of Science ®Google Scholar
• Hausmann B, Pelikan C, Rattei T, Loy A, Pester M, Mark Bailey EJ. 2019. Long-term transcriptional activity at zero growth of a cosmopolitan rare biosphere member. mBio 10(1):e02189–18.
   PubMed Web of Science ®Google Scholar
• Heidelberg JF, Seshadri R, Haveman SA, Hemme CL, Paulsen IT, Kolonay JF, Eisen JA, Ward N, Methe B, Brinkac LM, et al. 2004. The genome sequence of the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. Nat Biotechnol 22(5):554–559.
   PubMed Web of Science ®Google Scholar
• Iakovleva E, Mäkilä E, Salonen J, Sitarz M, Wang S, Sillanpää M. 2015. Acid mine drainage (AMD) treatment: Neutralization and toxic elements removal with unmodified and modified limestone. Ecol Eng 81:30–40.
   Web of Science ®Google Scholar
• Islam FS, Boothman C, Gault AG, Polya DA, Lloyd JR. 2005. Potential role of the Fe(III)-reducing bacteria Geobacter and Geothrix in controlling arsenic solubility in Bengal delta sediments. Mineral Mag 69(5):865–875.
   Web of Science ®Google Scholar
• Jew AD, Behrens SF, Rytuba JJ, Kappler A, Spormann AM, Brown GE. Jr. 2014. Microbially enhanced dissolution of HgS in an acid mine drainage system in the California coast range. Geobiology 12(1):20–33.
   PubMed Web of Science ®Google Scholar
• Johnson DB, Hallberg KB. 2003. The microbiology of acidic mine waters. Res Microbiol 154(7):466–473.
   PubMed Web of Science ®Google Scholar
• Kaksonen AH, Franzmann PD, Puhakka JA. 2004. Effects of hydraulic retention time and sulfide toxicity on ethanol and acetate oxidation in sulfate-reducing metal-precipitating fluidized-bed reactor. Biotechnol Bioeng 86(3):332–343.
   PubMed Web of Science ®Google Scholar
• Kaksonen AH, Puhakka JA. 2007. Sulfate reduction based bioprocesses for the treatment of acid mine drainage and the recovery of metals. Eng Life Sci 7(6):541–564.
   Web of Science ®Google Scholar
• Karakashev D, Batstone DJ, Trably E, Angelidaki I. 2006. Acetate oxidation is the dominant methanogenic pathway from acetate in the absence of Methanosaetaceae. Appl Environ Microbiol 72(7):5138–5141.
   PubMed Web of Science ®Google Scholar
• Karimian N, Johnston SG, Burton ED. 2018. Iron and sulfur cycling in acid sulfate soil wetlands under dynamic redox conditions: a review. Chemosphere 197:803–816.
   PubMed Web of Science ®Google Scholar
• Karnachuk OV, Kurganskaya IA, Avakyan MR, Frank YA, Ikkert OP, Filenko RA, Danilova EV, Pimenov NV. 2015. An acidophilic Desulfosporosinus isolated from the oxidized mining wastes in the Transbaikal area. Microbiology 84(5):677–686.
   Web of Science ®Google Scholar
• Kelly DP, Uchino Y, Huber H, Amils R, Wood AP. 2007. Reassessment of the phylogenetic relationships of Thiomonas cuprina. Int J Sys Evol Microbiol. 57(11):2720–2724.
   PubMed Web of Science ®Google Scholar
• Kim BC, Jeon BS, Kim S, Kim H, Um Y, Sang BI. 2015. Caproiciproducens galactitolivorans gen. nov., sp. nov., a bacterium capable of producing caproic acid from galactitol, isolated from a wastewater treatment plant. Int J Syst Evol Microbiol 65(12):4902–4908.
   PubMed Web of Science ®Google Scholar
• Kimura S, Hallberg KB, Johnson DB. 2006. Sulfidogenesis in low pH (3.8–4.2) media by a mixed population of acidophilic bacteria. Biodegradation 17(2):159–167.
   PubMed Web of Science ®Google Scholar
• Koschorreck M. 2008. Microbial sulphate reduction at a low pH. FEMS Microbiol Ecol 64(3):329–342.
   PubMed Web of Science ®Google Scholar
• Lee KC, Dunfield P F, Stott MB. 2014. The Phylum Armatimonadetes. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F, editors. The prokaryotes: Other Major Lineages of Bacteria and The Archaea. 4th ed. London: Springer-Verlag Berlin Heidelberg; p. 447–458.
   Google Scholar
• Lu S, Gischkat S, Reiche M, Akob DM, Hallberg KB, Küsel K. 2010. Ecophysiology of Fe-cycling bacteria in acidic sediments. Appl Environ Microbiol 76(24):8174–8183.
   PubMed Web of Science ®Google Scholar
• Lucheta AR, Otero XL, Macías F, Lambais MR. 2013. Bacterial and archaeal communities in the acid pit lake sediments of a chalcopyrite mine. Extremophiles 17(6):941–951.
   PubMed Web of Science ®Google Scholar
• Madigan MT, Martinko JM, Bender KS, Buckley DH, Stahl D. 2015. Brock biology of microorganisms. 14th ed. USA: Pearson Education, Inc.; p493–497.
   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(4):108–115.
   PubMed Web of Science ®Google Scholar
• Mardanov AV, Panova IA, Beletsky AV, Avakyan MR, Kadnikov VV, Antsiferov DV, Banks D, Frank YA, Pimenov NV, Ravin NV, et al. 2016. Genomic insights into a new acidophilic, copper-resistant Desulfosporosinus isolate from the oxidized tailings area of an abandoned gold mine. FEMS Microbiol Ecol 92(8):fiw111.
   PubMed Web of Science ®Google Scholar
• Meier J, Piva A, Fortin D. 2012. Enrichment of sulfate-reducing bacteria and resulting mineral formation in media mimicking pore water metal ion concentrations and pH conditions of acidic pit t lakes. FEMS Microbiol Ecol 79(1):69–84.
   PubMed Web of Science ®Google Scholar
• Méndez-García C, Peláez AI, Mesa V, Sánchez J, Golyshina OV, Ferrer M. 2015. Microbial diversity and metabolic networks in acid mine drainage habitats. Front Microbiol 6:475.
   PubMed Web of Science ®Google Scholar
• Mesa V, Gallego JLR, González-Gil R, Lauga B, Sánchez J, Méndez-García C, Peláez AI. 2017. Bacterial, archaeal, and eukaryotic diversity across distinct microhabitats in an acid mine drainage. Front Microbiol 8:1756.
   PubMed Web of Science ®Google Scholar
• Muyzer G, Stams AJM. 2008. The ecology and biotechnology of sulphate-reducing bacteria. Nat Rev Microbiol 6(6):441–454.
   PubMed Web of Science ®Google Scholar
• Neal AL, Techkarnjanaruk S, Dohnalkova A, McCready D, Peyton BM, Geesey GG. 2001. Iron sulfides and sulfur species produced at hematite surfaces in the presence of sulfate-reducing bacteria. Geochim Cosmochim Acta 65(2):223–235.
   Web of Science ®Google Scholar
• Nordstrom DK, Alpers CN. 1999. Geochemistry of acid mine waters. In: Plumlee, GS, Logsdon, MJ, editors. The Environmental Geochemistry of Mineral Deposits, Part A: Processes, Techniques, and Health Issues. Littleton: Society of Economic Geologists; p133–160.
   Google Scholar
• Portielje R, Lijklema L. 1995. The effect of reaeration and benthic algae on the oxygen balance of an artificial ditch. Ecol Model 79(1–3):35–48.
   Web of Science ®Google Scholar
• Prieto-Barajas CM, Valencia-Cantero E, Santoyo G. 2018. Microbial mat ecosystems: structure types, functional diversity, and biotechnological application. Electron J Biotechnol 31:48–56.
   Web of Science ®Google Scholar
• Puente-Sánchez F, Arce-Rodríguez A, Oggerin M, García-Villadangos M, Moreno-Paz M, Blanco Y, Rodríguez N, Bird L, Lincoln SA, Tornos F, et al. 2018. Viable cyanobacteria in the deep continental subsurface. Proc Natl Acad Sci USA. 115(42):10702–10707.
   PubMed Web of Science ®Google Scholar
• Rabus R, Hansen TA, Widdel F. 2013. Dissimilatory sulfate- and sulfur-reducing prokaryotes. In: Rosenberg, E, DeLong, EF, Lory, S, Stackebrandt, E, Thompson, F, editors. The Prokaryotes: Prokaryotic Physiology and Biochemistry. 4th ed. London: Springer-Verlag Berlin Heidelberg; p309–404.
   Google Scholar
• Ramiro-Garcia J, Hermes GDA, Giatsis C, Sipkema D, Zoetendal EG, Schaap PJ, Smidt H. 2016. NG-Tax, a highly accurate and validated pipeline for analysis of 16S rRNA amplicons from complex biomes. F1000Res 5:1791.
   PubMedGoogle Scholar
• Reis MAM, Lemos PC, Almeida JS, Carrondo MJT. 1990. Influence of produced acetic acid on growth of sulfate reducing bacteria. Biotechnol Lett 12(2):145–148.
   Web of Science ®Google Scholar
• Rowe OF, Sánchez-España J, Hallberg KB, Johnson DB. 2007. Microbial communities and geochemical dynamics in an extremely acidic, metal-rich stream at an abandoned sulfide mine (Huelva, Spain) underpinned by two functional primary production systems. Environ Microbiol 9(7):1761–1771.
   PubMed Web of Science ®Google Scholar
• Sajjad W, Zheng G, Zhang G, Ma X, Xu W, Ali B, Rafiq M. 2018. Diversity of prokaryotic communities indigenous to acid mine drainage and related rocks from Baiyin open-pit copper mine stope, china. Geomicrobiol J 35(7):580–600.
   Web of Science ®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(Pt 7):1661–1665.
   PubMed Web of Science ®Google Scholar
• Sánchez España J, López Pamo E, Santofimia E, Aduvire O, Reyes J, Barettino D. 2005. Acid mine drainage in the Iberian pyrite belt (Odiel river watershed, Huelva, SW Spain): geochemistry, mineralogy and environmental implications. J Appl Geochem 20(7):1320–1356.
   Web of Science ®Google Scholar
• Sánchez-Andrea I, Guedes IA, Hornung B, Boeren S, Lawson CE, Sousa DZ, Bar-Even A, Claassens NJ, Stams AJM. 2020. The reductive glycine pathway allows autotrophic growth of Desulfovibrio desulfuricans. Nat Commun 11(1):1–12.
   PubMed Web of Science ®Google Scholar
• Sánchez-Andrea I, Knittel K, Amann R, Amils R, Luis Sanz J. 2012. Quantification of Tinto River sediment microbial communities: importance of sulfate-reducing bacteria and their role in attenuating acid mine drainage. Appl Environ Microbiol 78(13):4638–4645.
   PubMed Web of Science ®Google Scholar
• Sánchez-Andrea I, Rodríguez 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(17):6085–6093.
   PubMed Web of Science ®Google Scholar
• Sánchez-Andrea I, Sanz JL, Bijmans MF, Stams AJ. 2014a. Sulfate reduction at low pH to remediate acid mine drainage. J Hazard Mater 269:98–109.
   PubMed Web of Science ®Google Scholar
• Sánchez-Andrea I, Sanz JL, Stams AM. 2014b. Microbacter margulisiae gen. nov., sp. nov., a propionigenic bacterium isolated from sediments of an acid rock drainage pond. Int J Syst Evol Microbiol 64(Pt 12):3936–3942.
   PubMed Web of Science ®Google Scholar
• Sánchez-Andrea I, Stams AJM, Hedrich S, Ňancucheo I, Johnson DB. 2015. Desulfosporosinus acididurans sp. nov.: an acidophilic sulfate-reducing bacterium isolated from acidic sediments. Extremophiles 19(1):39–47.
   PubMed Web of Science ®Google Scholar
• Sánchez-Andrea I, Stams AJM, Amils R, Sanz JL. 2013. Enrichment and isolation of acidophilic sulfate-reducing bacteria from Tinto River sediments. Environ Microbiol Rep 5(5):672–678.
   PubMed Web of Science ®Google Scholar
• Sánchez-España J, Yusta I, Ilin A, van der Graaf C, Sánchez-Andrea I. 2020. Microbial geochemistry of the acidic saline pit lake of Brunita mine (La Unión, SE Spain). Mine Water Environ 39(3):535–555.
   Web of Science ®Google Scholar
• Sani RK, Peyton BM, Smith WA, Apel WA, Petersen JN. 2002. Dissimilatory reduction of Cr(VI), Fe(III), and U(VI) by Cellulomonas isolates. Appl Microbiol Biotechnol 60(1–2):192–199.
   PubMed Web of Science ®Google Scholar
• Santos AL, Johnson DB. 2017. The effects of temperature and pH on the kinetics of an acidophilic sulfidogenic bioreactor and indigenous microbial communities. Hydrometallurgy 168:116–120.
   Web of Science ®Google Scholar
• Sato Y, Hamai T, Hori T, Aoyagi T, Inaba T, Kobayashi M, Habe H, Sakata T. 2019. Desulfosporosinus spp. were the most predominant sulfate-reducing bacteria in pilot- and laboratory-scale passive bioreactors for acid mine drainage treatment. Appl Microbiol Biotechnol 103(18):7783–7793.
   PubMed Web of Science ®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(3–4):342–350.
   Web of Science ®Google Scholar
• Schnürer A, Schink B, Svensson BH. 1996. Clostridium ultunense sp. nov., a mesophilic bacterium oxidizing acetate in syntrophic association with a hydrogenotrophic methanogenic bacterium. Int J Syst Bacteriol 46(4):1145–1152.
   PubMedGoogle Scholar
• Stams AJ, Van Dijk JB, Dijkema C, Plugge CM. 1993. Growth of syntrophic propionate-oxidizing bacteria with fumarate in the absence of methanogenic bacteria. Appl Environ Microbiol 59(4):1114–1119.
   PubMed Web of Science ®Google Scholar
• Suzuki Y, Kelly SD, Kemner KM, Banfield JF. 2003. Microbial populations stimulated for hexavalent uranium reduction in uranium mine sediment. Appl Environ Microbiol 69(3):1337–1346.
   PubMed Web of Science ®Google Scholar
• Teitzel GM, Parsek MR. 2003. Heavy metal resistance of biofilm and planktonic Pseudomonas aeruginosa. Appl Microbiol Biotechnol. 69(4):2313–2320.
   Google Scholar
• Tuffnell S. 2017. Acid drainage: the global environmental crisis you’ve never heard of. [UK]: The Conversation. Accessed January 30, 2020. Available at https://www.history.ox.ac.uk/article/acid-drainage-global-environmental-crisis-youve-never-heard.
   Google Scholar
• van der Graaf CM, Sánchez-España J, Yusta I, Ilin A, Shetty SA, Bale NJ, Villanueva L, Stams AJM, Sánchez-Andrea I. 2020. Biosulfidogenesis mediates natural attenuation in acidic mine pit lakes. Microorganisms 8(9):1275.
   PubMed Web of Science ®Google Scholar
• Ward N, Staley JT, Fuerst JA, Giovannoni S, Schlesner H, Stackebrandt E. 2006. The order Planctomycetales, including the genera Planctomyces, Pirellula, Gemmata and Isosphaera and the candidatus genera Brocadia, Kuenenia and Scalindua. Prokaryotes 7:757–793.
   Google Scholar
• Weijma J, Gubbels F, Hulshoff Pol LW, Stams AJ, Lens P, Lettinga G. 2002. Competition for H2 between sulfate reducers, methanogens and homoacetogens in a gas-lift reactor. Water Sci Technol. 45(10):75–80.
   Google Scholar
• Weiss JV, Rentz JA, Plaia T, Neubauer SC, Merrill-Floyd M, Lilburn T, Bradburne C, Megonigal JP, Emerson D. 2007. Characterization of Neutrophilic Fe(II)-Oxidizing Bacteria Isolated from the Rhizosphere of Wetland Plants and Description of Ferritrophicum radicicola gen. nov. sp. nov., and Sideroxydans paludicola sp. nov. Geomicrobiol J 24(7–8):559–570.
   Google Scholar
• Widdel F, Bak F. 1992. Gram-negative mesophilic sulfate-reducing bacteria. In: Balows, A, Trüper, HG, Dworkin, M, Harder, W, Schleifer, KH, editors. The Prokaryotes. 2nd ed. New York: Springer Science Bussiness Media; p3352–3378.
   Google Scholar
• Xia D, Yi X, Lu Y, Huang W, Xie Y, Ye H, Dang Z, Tao X, Li L, Lu G. 2019. Dissimilatory iron and sulfate reduction by native microbial communities using lactate and citrate as carbon sources and electron donors. Ecotoxicol Environ Saf 174:524–531.
   PubMed Web of Science ®Google Scholar
• Yu H, Jiang Z, Lu Y, Yao X, Han C, Ouyang Y, Wang H, Guo C, Ling F, Dang Z. 2020. Transcriptome analysis of the acid stress response of Desulfovibrio vulgaris ATCC 7757. Curr Microbiol 77(10):2702–2711.
   PubMed Web of Science ®Google Scholar
• Ziegler S, Waidner B, Itoh T, Schumann P, Spring S, Gescher J. 2013. Metallibacterium scheffleri gen. nov., sp. nov., an alkalinizing gammaproteobacterium isolated from an acidic biofilm. Int J Syst Evol Microbiol 63(Pt_4):1499–1504.
   PubMed Web of Science ®Google Scholar