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Characterization of iron-metabolizing communities in soils contaminated by acid mine drainage from an abandoned coal mine in Southwest China

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Abstract

Acid mine discharge (AMD) has been demonstrated to have significant impacts on microbial community composition in the surrounding soil environment. However, their effect on adjacent soil has not been extensively studied. In this study, microbial community composition of 20 AMD-contaminated soil samples collected from an abandoned coal mine along an AMD creek was characterized using high-throughput sequencing. All samples were characterized as extremely low in pH (< 3) and relatively enriched in HCl-extractable Fe species. The dominant phylotypes were belonging to genera Ochrobactrum, Acidiphilium, Staphylococcus, Brevibacterium, and Corynebacterium. Canonical correspondence analysis results revealed that the HCl-extractable Fe(III) had a strong impact on the soil microbial assemblage. Co-occurrence network analysis revealed that Aquicella, Acidobacteriaceae, Ochrobactrum, Enhydrobacter, Sphingomonas, and Legionellales were actively correlated with other taxa. As expected, most of the abundant taxa have been reported as acidophilic Fe-metabolizing bacteria. Hence, a co-occurring sub-network and a phylogenetic tree related to microbial taxa responsible for Fe metabolism were constructed and described. The biotic interaction showed that Dechloromonas exhibited densely connections with Fe(III)-reducing bacteria of Comamonas, Burkholderia, Shewanella, Stenotrophomonas, Acidithiobacillus, and Pseudomonas. These results demonstrated that Fe-metabolizing bacteria could have an important role in the Fe biogeochemical cycling.

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References

  • Amaral-Zettler LA, Zettler ER, Theroux SM, Palacios C, Aguilera A, Amils R (2011) Microbial community structure across the tree of life in the extreme Rio Tinto. ISME J 5:42–50

    Article  Google Scholar 

  • Anna S, Wójtowicz-Sieńko J, Piela P, Zielenkiewicz U, Tomczyk-Żak K, Chojnacka A, Sikora R, Kowalczyk P, Grzesiuk E, Błaszczyk M (2011) Selection of bacteria capable of dissimilatory reduction of Fe(III) from a long-term continuous culture on molasses and their use in a microbial fuel cell. J Microbiol Biotechnol 21:305–316

    Google Scholar 

  • Ashassi-Sorkhabi H, Moradi-Haghighi M, Zarrini G, Javaherdashti R (2012) Corrosion behavior of carbon steel in the presence of two novel iron-oxidizing bacteria isolated from sewage treatment plants. Biodegradation 23:69–79

    Article  CAS  Google Scholar 

  • Barberán A, Bates ST, Casamayor EO, Fierer N (2012) Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J 6:343–351

    Article  CAS  Google Scholar 

  • Bastian M, Heymann S, Jacomy M (2009) Gephi: an open source software for exploring and manipulating networks. In: International AAAI Conference on Weblogs and Social Media, San Jose, California

  • Bridge TAM, Johnson DB (2010) Reductive dissolution of ferric iron minerals by Acidiphilium SJH. Geomicrobiol J 17:193–206

    Google Scholar 

  • Bohorquez LC, Delgado-Serrano L, López G, Osorio-Forero C, Klepac-Ceraj V, Kolter R, Junca H, Baena S, Zambrano MM (2012) In-depth characterization via complementing culture-independent approaches of the microbial community in an acidic hot spring of the Colombian Andes. Microb Ecol 63:103–115

    Article  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Dushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  Google Scholar 

  • Chakraborty A, Picardal F (2013) Induction of nitrate-dependent Fe (II) oxidation by Fe (II) in Dechloromonas sp. strain UWNR4 and Acidovorax sp. strain 2AN. Appl Environ Microbiol 79:748–752

    Article  CAS  Google Scholar 

  • Chao TT, Zhou L (1983) Extraction techniques for selective dissolution of amorphous iron oxides from soils and sediments 1. Soil Sci Soc Am J 47:225–232

    Article  CAS  Google Scholar 

  • Chen L, Li J, Chen Y, Huang L, Hua Z, Hu M, Shu W (2013) Shifts in microbial community composition and function in the acidification of a lead/zinc mine tailings. Environ Microbiol 15:2431–2444

    Article  CAS  Google Scholar 

  • Choi G, Kim J, Lee C (2016) Effect of low pH start-up on continuous mixed-culture lactic acid fermentation of dairy effluent. Appl Microbiol Biotechnol 100:10179–10191

    Article  CAS  Google Scholar 

  • Coates JD, Chakraborty R, Lack JG, O’Connor SM, Cole KA, Bender KS, Achenbach LA (2001) Anaerobic benzene oxidation coupled to nitrate reduction in pure culture by two strains of Dechloromonas. Nature 411:1039–1043

    Article  CAS  Google Scholar 

  • Coby AJ, Picardal F, Shelobolina E, Xu H, Roden EE (2011) Repeated anaerobic microbial redox cycling of iron. Appl Environ Microbiol 77:6036–6042

    Article  CAS  Google Scholar 

  • Coenye T, Vandamme P (2003) Diversity and significance of Burkholderia species occupying diverse ecological niches. Environ Microbiol 5:719–729

    Article  CAS  Google Scholar 

  • Coupland K, Johnson DB (2008) Evidence that the potential for dissimilatory ferric iron reduction is widespread among acidophilic heterotrophic bacteria. Microbiol Lett 279:30–35

    Article  CAS  Google Scholar 

  • Cummings DE, Fendorf S, Singh N, Sani RK, Peyton BM, Magnuson TS (2007) Reduction of Cr(VI) under acidic conditions by the facultative Fe(III)-reducing bacterium Acidiphilium crytum. Environ Sci Technol 41:146–152

    Article  CAS  Google Scholar 

  • Domenico S, Lucas S, Umer ZI, Juraj P, Georg HR, Philipp S, Alfred PB, Günter B, Robert LM, Alexander KTK, Andreas HF, Alexander E (2015) Bacterial diversity along a 2600 km river continuum. Environ Microbiol 17:4994–5007

    Article  CAS  Google Scholar 

  • Druschel GK, Baker BJ, Gihring TM, Banfield JF (2004) Acid mine drainage biogeochemistry at iron mountain, California. Geochem T 5:13–32

    Article  CAS  Google Scholar 

  • de Menezes AB, Prendergast-Miller MT, Richardson AE, Toscas P, Farrell M, Macdonald LM, Baker G, Wark T, Thrall PH (2015) Network analysis reveals that bacteria and fungi form modules that correlate independently with soil parameters. Environ Microbiol 17:2677–2689

    Article  CAS  Google Scholar 

  • Delvasto P, Valverde A, Ballester A, Muñoz JA, González F, Blázquez ML, Igual JM, García-Ballboa C (2008) Diversity and activity of phosphate bioleaching bacteria from a high-phosphorus iron ore. Hydrometallurgy 92:124–129

    Article  CAS  Google Scholar 

  • Edwards RA, Rodriguez-Brito B, Wegley L, Haynes M, Breitbart M, Peterson DM, Saar MO, Alexander S, Alexander EC Jr, Rohwer F (2006) Using pyrosequencing to shed light on deep mine microbial ecology. BMC Genomics 7(57):57

    Article  CAS  Google Scholar 

  • Emerson D, Moyer C (1997) Isolation and characterization of novel iron-oxidizing bacteria that grow at circumneutral pH. Appl Environ Microbiol 63:4784–4792

    CAS  Google Scholar 

  • Falagán C, Johnson DB (2014) Acidibacter ferrireducens gen. nov., sp. nov.: an acidophilic ferric iron-reducing gammaproteobacterium. Extremophiles 18:1067–1073

    Article  CAS  Google Scholar 

  • Falagán C, Foesel B, Johnson B (2017) Acidicapsa ferrireducens sp. nov., Acidicapsa acidiphila sp. nov., and Granulicella acidiphila sp. nov.: novel acidobacteria isolated from metal-rich acidic waters. Extremophiles 21:459–469

    Article  CAS  Google Scholar 

  • Farkas A, Dragan-Bularda M, Muntean V, Ciataras D, Tugan S (2013) Microbial activity in drinking water-associated biofilms. Cent Eur J Biol 8:201–214

    Google Scholar 

  • Gammons CH, Duaime TE, Parker SR, Poulson SR, Kennelly P (2010) Geochemistry and stable isotope investigation of acid mine drainage associated with abandoned coal mines in Central Montana, USA. Chem Geol 269:100–112

    Article  CAS  Google Scholar 

  • Gao P, Xu W, Sontag P, Li X, Xue G, Liu T, Sun W (2016) Correlating microbial community compositions with environmental factors in activated sludge from four full-scale municipal wastewater treatment plants in Shanghai, China. Appl Microbiol Biotechnol 100:4663–4673

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Jiang Y, Li S, Li R, Zhang J, Liu Y, Lv L, Zhu H, Wu W, Li W (2017) Plant cultivars imprint the rhizosphere bacterial community composition and association networks. Soil Biol Biochem 109:145–155

    Article  CAS  Google Scholar 

  • Johnson DB, McGinness S (1991) Ferric iron reduction by acidophilic heterotrophic bacteria. Appl Environ Microbiol 57:207–211

    CAS  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  Google Scholar 

  • Johnson DB, Hallberg KB (2003) The microbiology of acidic mine waters. Res Microbiol 154:466–473

    Article  CAS  Google Scholar 

  • Johnson DB, Hallberg KB (2005) Acid mine drainage remediation options: a review. Sci Total Environ 338:3–14

    Article  CAS  Google Scholar 

  • Johnson DB, Hallberg KB, Hedrich S (2014) Uncovering a microbial enigma: isolation and characterization of the streamer-generating, iron-oxidizing, acidophilic bacterium “Ferrovum myxofaciens”. Appl Environ Microbiol 80:672–680

    Article  CAS  Google Scholar 

  • Johnson DB, Rolfe S, Hallberg KB, Iversen E (2001) Isolation and phylogenetic characterization of acidophilic microorganisms indigenous to acidic drainage waters at an abandoned Norwegian copper mine. Environ Microbiol 3:630–637

    Article  CAS  Google Scholar 

  • Kefeni KK, Msagati TAM, Mamba BB (2017) Acid mine drainage: prevention, treatment options, and resource recovery: a review. J Clean Prod 151:475–493

    Article  CAS  Google Scholar 

  • Kimura S, Bryan CG, Hallberg KB, Johnson DB (2011) Biodiversity and geochemistry of an extremely acidic, low-temperature subterranean environment sustained by chemolithotrophy. Environ Microbiol 13:2092–2104

    Article  CAS  Google Scholar 

  • Kishimoto N, Kosako Y, Tano T (1993) Acidiphilium aminolytica sp. nov.: an acidophilic chemoorganotrophic bacterium isolated from acidic mineral environment. Curr Microbiol 27:131–136

    Article  CAS  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  Google Scholar 

  • Kuang J-L, Huang L-N, Chen L-X, Hua Z-S, Li S-J, Hu M, Li J-T, Shu W-S (2013) Contemporary environmental variation determines microbial diversity patterns in acid mine drainage. ISME J 7:1038–1050

    Article  CAS  Google Scholar 

  • Mishra S, Panda S, Pradhan N, Biswal SK, Sukla LB, Mishra BK (2015) Microbe-mineral interactions: exploring avenues towards development of a sustainable microbial technology for coal beneficiation. In: Sukla L, Pradhan N, Panda S, Mishra B (eds) Environmental microbial biotechnology. Soil biology, vol 45. Springer, Cham, pp 33–52

    Chapter  Google Scholar 

  • Moya-Beltrán A, Cárdenas JP, Covarrubias PC, Issotta F, Ossandon FJ, Grail BM, Holmes DS, Quatrini R, Johnson DB (2014) Draft genome sequence of the nominated type strain of “Ferrovum muxofaciens”, an acidophilic, iron-oxidizing betaproteobacterium. Genome Announc 2:e00834–14

    Article  Google Scholar 

  • Nemergut DR, Schmidt SK, Fukami T, O'Neill SP, Bilinski TM, Stanish LF, Knelman JE, Darcy JL, Lynch RC, Wickey P (2013) Patterns and processes of microbial community assembly. Microbiol Mol Biol R 77:342–356

    Article  Google Scholar 

  • Pesaro M, Widmer F (2002) Identification of novel Crenarchaeota and Euryarchaeota clusters associated with different depth layers of a forest soil. FEMS Microbiol Ecol 42:89–98

    Article  CAS  Google Scholar 

  • Rastogi G, Osman S, Vaishampayan PA, Andersen GL, Stetler LD, Sani RK (2010) Microbial diversity in uranium mining-impacted soils as revealed by high-density 16S microarray and clone library. Microb Ecol 59:94–108

    Article  CAS  Google Scholar 

  • Reis MP, Pinheiro FA, Costa PS, Salgado APC, Assis PS, Chartone-Souza E, Nascimento AMA (2014) Phylogeny of bacteria from steelmaking wastes and their acidic enrichment cultures. Adv Microb 4:816–828

    Article  CAS  Google Scholar 

  • Sánchez-Andrea I, Rodríguez N, Amils R, Luis Sanz J (2011) Microbial diversity in anaerobic sediments at Río Tinto, a naturally acidic environment with a high heavy metal content. Appl Environ Microbiol 77:6085–6093

    Article  CAS  Google Scholar 

  • Sánchez-Andrea I, Sanz JL, Bijmans MFM, Stams AJM (2014) Sulfate reduction at low pH to remediate acid mine drainage. J Hazard Mater 269:98–109

    Article  CAS  Google Scholar 

  • Senko JM, Wanjugi P, Lucas M, Bruns MA, Burgos WD (2008) Characterization of Fe(II) oxidizing bacterial activities and communities at two acidic Appalachian coalmine drainage-impacted sites. ISME J 2:1134–1145

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Stumm W, Lee GF (1961) Oxygenation of ferrous iron. Ind Eng Chem 53:143–146

    Article  CAS  Google Scholar 

  • Sultan S, Hasnain S (2007) Reduction of toxic hexavalent chromium by Ochrobactrum intermedium strain SDCr-5 stimulated by heavy metals. Bioresour Technol 98:340–344

    Article  CAS  Google Scholar 

  • Sun M, Xiao T, Ning Z, Xiao E, Sun W (2015a) Microbial community analysis in rice paddy soils irrigated by acid mine drainage contaminated water. Appl Microbiol Biotechnol 99:2911–2922

    Article  CAS  Google Scholar 

  • Sun W, Xiao T, Sun M, Dong Y, Ning Z, Xiao E, Tang S, Li J (2015b) Diversity of the sediment microbial community in the Aha watershed (southwest China) in response to acid mine drainage pollution gradients. Appl Environ Microbiol 81:4874–4884

    Article  CAS  Google Scholar 

  • Sun W, Yu G, Louie T, Liu T, Zhu C, Xue G, Gao P (2015c) From mesophilic to thermophilic digestion: the transitions of anaerobic bacterial, archaeal, and fungal community structures in sludge and manure samples. Appl Microbiol Biotechnol 99:10271–10282

    Article  CAS  Google Scholar 

  • Sun W, Xiao E, Krumins V, Dong Y, Xiao T, Ning Z, Chen H, Xiao Q (2016) Characterization of the microbial community composition and the distribution of Fe-metabolizing bacteria in a creek contaminated by acid mine drainage. Appl Microbiol Biotechnol 100:8523–8535

    Article  CAS  Google Scholar 

  • Sun W, Xiao E, Xiao T, Krumins V, Wang Q, Haggblom MM, Dong Y, Tang S, Hu M, Li B (2017) Response of soil microbial communities to elevated antimony and arsenic contamination indicates the relationship between the innate microbiota and contaminant fractions. Environ Sci Technol 51:9165–9175

    Article  CAS  Google Scholar 

  • Sun W, Xiao E, Häggblom M, Krumins V, Dong Y, Sun X, Li F, Wang Q, Li B, Yan B (2018a) Bacterial survival strategies in alkaline tailing site and the physiological mechanisms of dominant phylotypes as revealed by metagenomics analyses. Environ Sci Technol 52:13370–13380

    Article  CAS  Google Scholar 

  • Sun W, Xiao E, Pu Z, Krumins V, Dong Y, Li B, Hu M (2018b) Paddy soil microbial communities driven by environment- and microbe-microbe interactions: a case study of elevation-resolved microbial communities in a rice terrace. Sci Total Environ 612:884–893

    Article  CAS  Google Scholar 

  • Sun W, Krumins V, Dong Y, Gao P, Ma C, Hu M, Li B, Xia B, He Z, Xiong S (2018c) A combination of stable isotope probing, Illumina sequencing, and co-occurrence network to investigate thermophilic acetate- and lactate-utilizing bacteria. Microb Ecol 75:113–122

    Article  CAS  Google Scholar 

  • Sun W, Xiao E, Krumins V, Häggblom MM, Dong Y, Pu Z, Li B, Wang Q, Xiao T, Li F (2018d) Rhizosphere microbial response to multiple metal(loid)s in different contaminated arable soils indicates crop-specific metal-microbe interactions. Appl Environ Microbiol 84:e00701–e00718

    CAS  Google Scholar 

  • Tamura H, Goto K, Yotsuyanagi T, Nagayama M (1974) Spectrophotometric determination of iron(II) with 1,10-phenanthroline in the presence of large amounts of iron(III). Talanta 21:314–318

    Article  CAS  Google Scholar 

  • Timonen S, Bomberg M (2009) Archaea in dry soil environments. Phytochem Rev 8:505–518

    Article  CAS  Google Scholar 

  • Valverde A, Delvasto P, Peix A, Velázquez E, Santa-Regina I, Ballester A, Rodríguez-Barrueco C, García-Ballboa C, Igual JM (2006) Burkholderia ferrzriae sp. nov., isolated from an iron ore in Brazil. Int J Syst Evol Microbiol 56:2421–2425

    Article  CAS  Google Scholar 

  • Waranusantigul P, Le H, Kruatrachue M, Pokethitiyook P, Auesukaree C (2011) Isolation and characterization of lead-tolerant Ochrobactrum intermedium and its role in enhancing lead accumulation by Eucalyptus camaldulensis. Chemosphere 85:584–590

    Article  CAS  Google Scholar 

  • Weber KA, Urrutia MM, Churchill PF, Kukkadapu RK, Roden EE (2006) Anaerobic redox cycling of iron by freshwater sediment microorganisms. Environ Microbiol 8:100–113

    Article  CAS  Google Scholar 

  • White DC, Sutton SD, Ringelberg DB (1996) The genus Sphingomonas: physiology and ecology. Curr Opin Biotechnol 7:301–306

    Article  CAS  Google Scholar 

  • Wu C-Y, Zhuang L, Zhou S-G, Li F-B, Li X-M (2009) Fe(III)-enhanced anaerobic transformation of 2,4-dichlorophenoxyacetic acid by an iron-reducing bacterium Comamonas koreensis CY01. FEMS Microb Ecol 71:106–113

    Article  CAS  Google Scholar 

  • Xiao E, Krumins V, Xiao T, Dong Y, Tang S, Ning Z, Huang Z, Sun W (2017) Depth-resolved microbial community analyses in two contrasting soil cores contaminated by antimony and arsenic. Environ Pollut 221:244–255

    Article  CAS  Google Scholar 

  • Zeng X-C, E G, Wang J, Wang N, Chen X, Mu Y, Li H, Yang Y, Liu Y, Wang Y (2016) Functions and unique diversity of genes and microorganisms involved in arsenite oxidation from the tailings of a realgar mine. Appl Environ Microbiol 82:7019–7029

    Article  CAS  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 63:1499–1504

    Article  Google Scholar 

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Acknowledgements

We thank Hanna Han and her team from Shenzhen Ecogene Co., Ltd. for NGS technical service.

Funding

This research was funded by the National Natural Science Foundation of China (41771301, 41420104007), the High-level Leading Talent Introduction Program of GDAS (2016GDASRC-0103), GDAS’ Special Project of Science and Technology Development (2018GDASCX-0601 and 2017GDASCX-0106), the Science and Technology Planning Project of Guangdong Province (2016B070701015), and the Guangxi Innovation Drive Development Fund (AA17204076).

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  1. Pin Gao and Xiaoxu Sun contributed equally to this work.

Authors and Affiliations

  1. Guangdong Key Laboratory of Integrated Agro-environmental Pollution Control and Management, Guangdong Institute of Eco-Environmental Science and Technology, 808 Tianyuan Road, Guangzhou, 510650, Guangdong, China

    Pin Gao, Xiaoxu Sun, Zhixian Xu, Baoqin Li & Weimin Sun

  2. College of Environmental Science and Engineering, Textile Pollution Controlling Engineering Center of Ministry of Environmental Protection, Donghua University, Shanghai, 201620, China

    Pin Gao

  3. Innovation Center and Key Laboratory of Waters Safety and Protection in the Pearl River Delta, Ministry of Education, Guangzhou University, Guangzhou, 510006, China

    Enzong Xiao

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  1. Pin Gao
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Gao, P., Sun, X., Xiao, E. et al. Characterization of iron-metabolizing communities in soils contaminated by acid mine drainage from an abandoned coal mine in Southwest China. Environ Sci Pollut Res 26, 9585–9598 (2019). https://doi.org/10.1007/s11356-019-04336-6

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