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Research in Microbiology xx (2014) 1e6 www.elsevier.com/locate/resmic
Microbial diversity at the moderate acidic stage in three different sulfidic mine tailings dumps generating acid mine drainage Hananeh Korehi, Marco Bl€ othe, Axel Schippers*
Q3
Geomicrobiology Unit, Federal Institute for Geosciences and Natural Resources (BGR), Stilleweg 2, D-30655 Hannover, Germany Received 14 April 2014; accepted 30 August 2014
Abstract In freshly deposited sulfidic mine tailings the pH is alkaline or circumneutral. Due to pyrite or pyrrhotite oxidation the pH is dropping over time to pH values pH > 3), Alicyclobacillus became the most dominant genus. At the final stage below pH 3, a dramatic shift in the microbial community composition was detected. Ferroplasma became the most dominant genus, followed by Leptospirillum, Sulfobacillus, Alicyclobacillus, and Acidithiobacillus. The relative abundance of Firmicutes, Proteobacteria, and Actinobacteria significantly decreased below pH 3 and the community became dominated by Euryarchaeota and Nitrospira. In conclusion our results show in line with the published literature that geochemical heterogeneous sulfidic mine tailings are characterized by complex bacterial communities at moderately acidic pH different to low pH communities which are dominated by acidophilic iron- and sulfur-oxidizing prokaryotes. However, other geochemical parameters besides pH
5
also determine the composition of the microbial community composition in mine tailings.
Appendix A. Supplementary data Supplementary data related to this article can be found at http://dx.doi.org/10.1016/j.resmic.2014.08.007. References [1] Kock D, Schippers A. Quantitative microbial community analysis of three different sulfidic mine tailing dumps generating acid mine drainage. Appl Environ Microbiol 2008;74(16):5211e9. [2] Dold B, Fontbote L. Element cycling and secondary mineralogy in porphyry copper tailings as a function of climate, primary mineralogy, and mineral processing, special issue: geochemical studies of mining and the environment. Geochem Explor 2001;74(1e3):3e55. [3] Blowes DW, Ptacek CJ, Jurjovec J. Mill tailings: hydrogeology and geochemistry. In: Jambor JL, Blowes DW, Ritchie AIM, editors. Environmental aspects of mine wastesvol. 31. Mineralogical Association of Canada; 2003. p. 95e116. [4] Schippers A, Breuker A, Blazejak A, Bosecker K, Kock D, Wright TL. The biogeochemistry and microbiology of sulfidic mine waste and bioleaching dumps and heaps, and novel Fe(II)-oxidizing bacteria. Hydrometallurgy 2010;104:342e50. [5] Hedrich S, Schl€omann M, Johnson DB. The iron-oxidizing proteobacteria. Microbiol J 2011;157:1551e64. [6] Schippers A, Hedrich, Vasters J, Drobe M, Sand W, Willscher S. Biomining: metal recovery from ores with microorganisms. In: Schippers A, Glombitza F, Sand W, editors. Geobiotechnology I e metal-related issues. Adv. Biochem. Eng. Biotechnol, vol. 141; 2014. p. 1e48. [7] Baker BJ, Banfield JF. Microbial communities in acid mine drainage. FEMS Microbiol Ecol 2003;44:139e52. [8] Gonzalez-Toril E, Llobet-Brossa E, Casamayor EO, Amann R, Amils R. Microbial ecology of an extreme acidic environment, the Tinto River. Appl Environ Microbiol 2003;69:4853e65. [9] Johnson DB, Hallberg KB. The microbiology of acidic mine waters. Res Microbiol 2003;154:466e73. [10] Bruneel O, Duran R, Casiot C, Elbaz-Poulichet F, Personne JC. Diversity of microorganisms in Fe-As-rich acid mine drainage waters of Carnoules, France. Appl Environ Microbiol 2006;72:551e6. [11] Johnson DB, Hallberg KB, Hedrich S. Uncovering a microbial enigma: isolation and characterization of the streamer-generating, iron-oxidizing, acidophilic bacterium “Ferrovum myxofaciens”. Appl Environ Microbiol 2014;80:672e80. [12] Remonsellez F, Galleguillos F, Moreno-Paz M, Parro V, Acosta M, Demergasso C. Dynamic of active microorganisms inhabiting a bioleaching industrial heap of low-grade copper sulfide ore monitored by real-time PCR and oligonucleotide prokaryotic acidophile microarray. Microb Biotechnol 2009;2:613e24. [13] Johnson DB. Geomicrobiology of extremely acidic subsurface environments. FEMS Microbiol Ecol 2012;81:2e12. [14] Ziegler S, Dolch K, Geiger K, Krause S, Asskamp M, Eusterhues K, et al. Oxygen-dependent niche formation of a pyrite-dependent acidophilic consortium built by archaea and bacteria. ISME J 2013;7:1725e37. [15] Southam G, Beveridge TJ. Enumeration of thiobacilli within pH-neutral and acidic mine tailings and their role in the development of secondary mineral soil. Appl Environ Microbiol 1992;58:1904e12. [16] Fortin D, Davis B, Beveridge TJ. Role of Thiobacillus and sulfatereducing bacteria in iron biocycling in oxic and acidic mine tailings. Microbiol Ecol 1996;21:11e24. [17] Wielinga B, Juliette KL, Moore JN, Seastone OF, Cannon JE. Microbiological and geochemical characterization of fluvial deposited sulfidic mine tailings. Appl Environ Microbiol 1999;65:1548e55.
Please cite this article in press as: Korehi H, et al., Microbial diversity at the moderate acidic stage in three different sulfidic mine tailings dumps generating acid mine drainage, Research in Microbiology (2014), http://dx.doi.org/10.1016/j.resmic.2014.08.007
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[18] Schippers A, Jozsa PG, Sand W, Kovacs ZM, Jelea M. Microbiological pyrite oxidation in a mine tailings heap and its relevance to the death of vegetation. Geomicrobiol J 2000;17:151e62. [19] Graupner T, Kassahun A, Rammlmair D, Meima J, Kock D, Furche M, et al. Formation of sequences of cemented layers and hardpans within sulfide-bearing mine tailings (mine district Freiberg, Germany). Appl Geochem 2007;22:2486e508. [20] Tan GL, Shu WS, Hallberg KB, Li F, Lan CY, Zhou WH, et al. Culturable and molecular phylogenetic diversity of microorganisms in an open-dumped, extremely acidic Pb/Zn mine tailings. Extremophiles 2008;12:657e64. [21] Kock D, Schippers A. Geomicrobiological investigation of two different mine waste tailings generating acid mine drainage. Hydrometallurgy 2006;83:167e75. [22] Diaby N, Dold B, Pfeifer HR, Holliger C, Johnson DB, Hallberg KB. Microbial communities in a porphyry copper tailings impoundment and their impact on the geochemical dynamics of the mine waste. Environ Microbiol 2007;9:298e307. [23] Zhang HB, Shi W, Yang MX, Sha T, Zhao ZW. Bacterial diversity at different depths in lead-zinc mine tailings as revealed by 16S rRNA gene libraries. J Microbiol 2007;45:479e84. [24] Mendez MO, Neilson JW, Maier RM. Characterization of a bacterial community in an abandoned semiarid lead-zinc mine tailings site. Appl Environ Microbiol 2008;74:3899e907. [25] Winch S, Mills HJ, Kostka JE, Fortin D, Lean DRS. Identification of sulfate-reducing bacteria in methylmercury- contaminated mine tailings by analysis of SSU rRNA genes. FEMS Microbiol Ecol 2009;68:94e107. [26] Huang LN, Zhou WH, Hallberg KB, Wan CY, Li J, Shu W-S. Spatial and temporal analysis of the microbial community in the tailings of a Pb-Zn mine generating acidic drainage. Appl Environ Microbiol 2011;77:5540e4. [27] Chen LX, Li JT, Chen YT, Huang LN, Hua ZS, Hu M, et al. Shifts in microbial community composition and function in the acidification of a lead/zinc mine tailings. Environ Microbiol 2013;15:2431e44. [28] Liu J, Hua ZS, Chen ZN, Kuang JL, Li SJ, Shu WS, et al. Correlating microbial diversity patterns with geochemistry in an extreme and heterogeneous mine tailings environment. Appl Environ Microbiol 2014;80:3677e86. [29] Korehi H, Bl€ othe M, Sitnikova MA, Dold B, Schippers A. Metal mobilization by iron- and sulfur-oxidizing bacteria in a multiple extreme mine tailings in the Atacama Desert, Chile. Environ Sci Technol 2013;47:2189e96. [30] Schippers A, Kock D, Schwartz MO, B€ottcher ME, Vogel H, Hagger M. Geomicrobiological and geochemical investigation of a pyrrhotite containing mine waste tailings dam near Selebi-Phikwe in Botswana. J Geochem Explor 2007;92:151e8.
[31] Herbert Jr RB, Schippers A. Iron isotope fractionation by biogeochemical processes in mine tailings. Environ Sci Technol 2008;42:1117e22. [32] Muyzer G, Teske A, Wirsen CO, Jannasch HW. Phylogenetic relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments. Arch Microbiol 1995;164:165e72. [33] Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: open-source, platform-independent community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 2009;75:7537e41. [34] Pruesse E, Peplies J, Gl€ockner FO. SINA: accurate high throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 2012;28:1823e9. [35] Stamatakis A, Aberer AJ, Goll C, Smith SA, Berger SA, IzquierdoCarrasco F. RAxML-light: a tool for computing terabyte Phylogenies. Bioinformatics 2012;28:2064e6. [36] Miller MA, Pfeiffer W, Schwartz T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the gateway Computing environments Workshop (GCE), 14 Nov. 2010, New Orleans, LA; 2010. p. 1e8. [37] Chen Y, Li J, Chen L, Hua J, Huang L, Liu J, et al. Biogeochemical processes governing natural pyrite oxidation and release of acid metalliferous drainage. Environ Sci Technol 2014;48:5537e45. [38] Pichtel JR, Dick WA. Sulfur, iron and solid phase transformations during biological oxidation of pyritic mine spoil. Soil Biol Biochem 1991;23:101e7. [39] Kaksonen AH, Spring S, Schumann P, Kroppenstedt RM, Puhakka JA. Desulfurispora thermophilic gen. nov., sp. nov., a thermophilic, sporeforming sulfate-reducer isolated from a sulfidogenic fluidized-bed reactor. Int J Syst Evol Microbiol 2007;57:1089e94. [40] Fortin D, Praharaj T. Role of microbial activity in Fe and S cycling in sub-oxic to anoxic sulfide-rich mine tailings: a mini-review. J Nucl Radiochem Sci 2005;6:39e42. [41] Abicht HK, Mancini S, Karnachuk OV, Solioz M. Genome sequence of Desulfosporosinus sp. OT, an acidophilic sulfate-reducing bacterium from copper mining waste in Norilsk, northern Siberia. J Bacteriol 2011;193:6104e5. [42] Pester M, Cheng JF, Tapia R, Wei CL, Markowitz V, Klenk HP, et al. Complete genome sequences of Desulfosporosinus orientis DSM765T, Desulfosporosinus youngiae DSM17734T, Desulfosporosinus meridiei DSM13257T, and Desulfosporosinus acidiphilus DSM22704T. J Bacteriol 2012;194:6300e1. [43] Navarro-Noyaa YE, Hernandez-Mendozaa E, Morales-Jimeneza J, JanRobleroa J, Martínez-Romerob E, Hernandez-Rodrígueza C. Isolation and characterization of nitrogen fixing heterotrophic bacteria from the rhizosphere of pioneer plants growing on mine tailings. Appl Soil Ecol 2012;62:52e60.
Please cite this article in press as: Korehi H, et al., Microbial diversity at the moderate acidic stage in three different sulfidic mine tailings dumps generating acid mine drainage, Research in Microbiology (2014), http://dx.doi.org/10.1016/j.resmic.2014.08.007
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MODEL
Research in Microbiology xx (2014) 1e6 www.elsevier.com/locate/resmic
Microbial diversity at the moderate acidic stage in three different sulfidic mine tailings dumps generating acid mine drainage Hananeh Korehi, Marco Bl€ othe, Axel Schippers*
Q3
Geomicrobiology Unit, Federal Institute for Geosciences and Natural Resources (BGR), Stilleweg 2, D-30655 Hannover, Germany Received 14 April 2014; accepted 30 August 2014
Abstract In freshly deposited sulfidic mine tailings the pH is alkaline or circumneutral. Due to pyrite or pyrrhotite oxidation the pH is dropping over time to pH values pH > 3), Alicyclobacillus became the most dominant genus. At the final stage below pH 3, a dramatic shift in the microbial community composition was detected. Ferroplasma became the most dominant genus, followed by Leptospirillum, Sulfobacillus, Alicyclobacillus, and Acidithiobacillus. The relative abundance of Firmicutes, Proteobacteria, and Actinobacteria significantly decreased below pH 3 and the community became dominated by Euryarchaeota and Nitrospira. In conclusion our results show in line with the published literature that geochemical heterogeneous sulfidic mine tailings are characterized by complex bacterial communities at moderately acidic pH different to low pH communities which are dominated by acidophilic iron- and sulfur-oxidizing prokaryotes. However, other geochemical parameters besides pH
5
also determine the composition of the microbial community composition in mine tailings.
Appendix A. Supplementary data Supplementary data related to this article can be found at http://dx.doi.org/10.1016/j.resmic.2014.08.007. References [1] Kock D, Schippers A. Quantitative microbial community analysis of three different sulfidic mine tailing dumps generating acid mine drainage. Appl Environ Microbiol 2008;74(16):5211e9. [2] Dold B, Fontbote L. Element cycling and secondary mineralogy in porphyry copper tailings as a function of climate, primary mineralogy, and mineral processing, special issue: geochemical studies of mining and the environment. Geochem Explor 2001;74(1e3):3e55. [3] Blowes DW, Ptacek CJ, Jurjovec J. Mill tailings: hydrogeology and geochemistry. In: Jambor JL, Blowes DW, Ritchie AIM, editors. Environmental aspects of mine wastesvol. 31. Mineralogical Association of Canada; 2003. p. 95e116. [4] Schippers A, Breuker A, Blazejak A, Bosecker K, Kock D, Wright TL. The biogeochemistry and microbiology of sulfidic mine waste and bioleaching dumps and heaps, and novel Fe(II)-oxidizing bacteria. Hydrometallurgy 2010;104:342e50. [5] Hedrich S, Schl€omann M, Johnson DB. The iron-oxidizing proteobacteria. Microbiol J 2011;157:1551e64. [6] Schippers A, Hedrich, Vasters J, Drobe M, Sand W, Willscher S. Biomining: metal recovery from ores with microorganisms. In: Schippers A, Glombitza F, Sand W, editors. Geobiotechnology I e metal-related issues. Adv. Biochem. Eng. Biotechnol, vol. 141; 2014. p. 1e48. [7] Baker BJ, Banfield JF. Microbial communities in acid mine drainage. FEMS Microbiol Ecol 2003;44:139e52. [8] Gonzalez-Toril E, Llobet-Brossa E, Casamayor EO, Amann R, Amils R. Microbial ecology of an extreme acidic environment, the Tinto River. Appl Environ Microbiol 2003;69:4853e65. [9] Johnson DB, Hallberg KB. The microbiology of acidic mine waters. Res Microbiol 2003;154:466e73. [10] Bruneel O, Duran R, Casiot C, Elbaz-Poulichet F, Personne JC. Diversity of microorganisms in Fe-As-rich acid mine drainage waters of Carnoules, France. Appl Environ Microbiol 2006;72:551e6. [11] Johnson DB, Hallberg KB, Hedrich S. Uncovering a microbial enigma: isolation and characterization of the streamer-generating, iron-oxidizing, acidophilic bacterium “Ferrovum myxofaciens”. Appl Environ Microbiol 2014;80:672e80. [12] Remonsellez F, Galleguillos F, Moreno-Paz M, Parro V, Acosta M, Demergasso C. Dynamic of active microorganisms inhabiting a bioleaching industrial heap of low-grade copper sulfide ore monitored by real-time PCR and oligonucleotide prokaryotic acidophile microarray. Microb Biotechnol 2009;2:613e24. [13] Johnson DB. Geomicrobiology of extremely acidic subsurface environments. FEMS Microbiol Ecol 2012;81:2e12. [14] Ziegler S, Dolch K, Geiger K, Krause S, Asskamp M, Eusterhues K, et al. Oxygen-dependent niche formation of a pyrite-dependent acidophilic consortium built by archaea and bacteria. ISME J 2013;7:1725e37. [15] Southam G, Beveridge TJ. Enumeration of thiobacilli within pH-neutral and acidic mine tailings and their role in the development of secondary mineral soil. Appl Environ Microbiol 1992;58:1904e12. [16] Fortin D, Davis B, Beveridge TJ. Role of Thiobacillus and sulfatereducing bacteria in iron biocycling in oxic and acidic mine tailings. Microbiol Ecol 1996;21:11e24. [17] Wielinga B, Juliette KL, Moore JN, Seastone OF, Cannon JE. Microbiological and geochemical characterization of fluvial deposited sulfidic mine tailings. Appl Environ Microbiol 1999;65:1548e55.
Please cite this article in press as: Korehi H, et al., Microbial diversity at the moderate acidic stage in three different sulfidic mine tailings dumps generating acid mine drainage, Research in Microbiology (2014), http://dx.doi.org/10.1016/j.resmic.2014.08.007
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[18] Schippers A, Jozsa PG, Sand W, Kovacs ZM, Jelea M. Microbiological pyrite oxidation in a mine tailings heap and its relevance to the death of vegetation. Geomicrobiol J 2000;17:151e62. [19] Graupner T, Kassahun A, Rammlmair D, Meima J, Kock D, Furche M, et al. Formation of sequences of cemented layers and hardpans within sulfide-bearing mine tailings (mine district Freiberg, Germany). Appl Geochem 2007;22:2486e508. [20] Tan GL, Shu WS, Hallberg KB, Li F, Lan CY, Zhou WH, et al. Culturable and molecular phylogenetic diversity of microorganisms in an open-dumped, extremely acidic Pb/Zn mine tailings. Extremophiles 2008;12:657e64. [21] Kock D, Schippers A. Geomicrobiological investigation of two different mine waste tailings generating acid mine drainage. Hydrometallurgy 2006;83:167e75. [22] Diaby N, Dold B, Pfeifer HR, Holliger C, Johnson DB, Hallberg KB. Microbial communities in a porphyry copper tailings impoundment and their impact on the geochemical dynamics of the mine waste. Environ Microbiol 2007;9:298e307. [23] Zhang HB, Shi W, Yang MX, Sha T, Zhao ZW. Bacterial diversity at different depths in lead-zinc mine tailings as revealed by 16S rRNA gene libraries. J Microbiol 2007;45:479e84. [24] Mendez MO, Neilson JW, Maier RM. Characterization of a bacterial community in an abandoned semiarid lead-zinc mine tailings site. Appl Environ Microbiol 2008;74:3899e907. [25] Winch S, Mills HJ, Kostka JE, Fortin D, Lean DRS. Identification of sulfate-reducing bacteria in methylmercury- contaminated mine tailings by analysis of SSU rRNA genes. FEMS Microbiol Ecol 2009;68:94e107. [26] Huang LN, Zhou WH, Hallberg KB, Wan CY, Li J, Shu W-S. Spatial and temporal analysis of the microbial community in the tailings of a Pb-Zn mine generating acidic drainage. Appl Environ Microbiol 2011;77:5540e4. [27] Chen LX, Li JT, Chen YT, Huang LN, Hua ZS, Hu M, et al. Shifts in microbial community composition and function in the acidification of a lead/zinc mine tailings. Environ Microbiol 2013;15:2431e44. [28] Liu J, Hua ZS, Chen ZN, Kuang JL, Li SJ, Shu WS, et al. Correlating microbial diversity patterns with geochemistry in an extreme and heterogeneous mine tailings environment. Appl Environ Microbiol 2014;80:3677e86. [29] Korehi H, Bl€ othe M, Sitnikova MA, Dold B, Schippers A. Metal mobilization by iron- and sulfur-oxidizing bacteria in a multiple extreme mine tailings in the Atacama Desert, Chile. Environ Sci Technol 2013;47:2189e96. [30] Schippers A, Kock D, Schwartz MO, B€ottcher ME, Vogel H, Hagger M. Geomicrobiological and geochemical investigation of a pyrrhotite containing mine waste tailings dam near Selebi-Phikwe in Botswana. J Geochem Explor 2007;92:151e8.
[31] Herbert Jr RB, Schippers A. Iron isotope fractionation by biogeochemical processes in mine tailings. Environ Sci Technol 2008;42:1117e22. [32] Muyzer G, Teske A, Wirsen CO, Jannasch HW. Phylogenetic relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments. Arch Microbiol 1995;164:165e72. [33] Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: open-source, platform-independent community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 2009;75:7537e41. [34] Pruesse E, Peplies J, Gl€ockner FO. SINA: accurate high throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 2012;28:1823e9. [35] Stamatakis A, Aberer AJ, Goll C, Smith SA, Berger SA, IzquierdoCarrasco F. RAxML-light: a tool for computing terabyte Phylogenies. Bioinformatics 2012;28:2064e6. [36] Miller MA, Pfeiffer W, Schwartz T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the gateway Computing environments Workshop (GCE), 14 Nov. 2010, New Orleans, LA; 2010. p. 1e8. [37] Chen Y, Li J, Chen L, Hua J, Huang L, Liu J, et al. Biogeochemical processes governing natural pyrite oxidation and release of acid metalliferous drainage. Environ Sci Technol 2014;48:5537e45. [38] Pichtel JR, Dick WA. Sulfur, iron and solid phase transformations during biological oxidation of pyritic mine spoil. Soil Biol Biochem 1991;23:101e7. [39] Kaksonen AH, Spring S, Schumann P, Kroppenstedt RM, Puhakka JA. Desulfurispora thermophilic gen. nov., sp. nov., a thermophilic, sporeforming sulfate-reducer isolated from a sulfidogenic fluidized-bed reactor. Int J Syst Evol Microbiol 2007;57:1089e94. [40] Fortin D, Praharaj T. Role of microbial activity in Fe and S cycling in sub-oxic to anoxic sulfide-rich mine tailings: a mini-review. J Nucl Radiochem Sci 2005;6:39e42. [41] Abicht HK, Mancini S, Karnachuk OV, Solioz M. Genome sequence of Desulfosporosinus sp. OT, an acidophilic sulfate-reducing bacterium from copper mining waste in Norilsk, northern Siberia. J Bacteriol 2011;193:6104e5. [42] Pester M, Cheng JF, Tapia R, Wei CL, Markowitz V, Klenk HP, et al. Complete genome sequences of Desulfosporosinus orientis DSM765T, Desulfosporosinus youngiae DSM17734T, Desulfosporosinus meridiei DSM13257T, and Desulfosporosinus acidiphilus DSM22704T. J Bacteriol 2012;194:6300e1. [43] Navarro-Noyaa YE, Hernandez-Mendozaa E, Morales-Jimeneza J, JanRobleroa J, Martínez-Romerob E, Hernandez-Rodrígueza C. Isolation and characterization of nitrogen fixing heterotrophic bacteria from the rhizosphere of pioneer plants growing on mine tailings. Appl Soil Ecol 2012;62:52e60.
Please cite this article in press as: Korehi H, et al., Microbial diversity at the moderate acidic stage in three different sulfidic mine tailings dumps generating acid mine drainage, Research in Microbiology (2014), http://dx.doi.org/10.1016/j.resmic.2014.08.007
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