Advertisement

Microbial Ecology

, Volume 78, Issue 3, pp 651–664 | Cite as

Comparative Analyses of the Microbial Communities Inhabiting Coal Mining Waste Dump and an Adjacent Acid Mine Drainage Creek

  • Weimin SunEmail author
  • Enzong Xiao
  • Valdis Krumins
  • Yiran Dong
  • Baoqin Li
  • Jie Deng
  • Qi Wang
  • Tangfu Xiao
  • Jie Liu
Environmental Microbiology

Abstract

Microbial communities inhabiting the acid mine drainage (AMD) have been extensively studied, but the microbial communities in the coal mining waste dump that may generate the AMD are still relatively under-explored. In this study, we characterized the microbial communities within these under-explored extreme habitats and compared with those in the downstream AMD creek. In addition, the interplay between the microbiota and the environmental parameters was statistically investigated. A Random Forest ensemble model indicated that pH was the most important environmental parameter influencing microbial community and diversity. Parameters associated with nitrogen cycling were also critical factors, with positive effects on microbial diversity, while S-related parameters had negative effects. The microbial community analysis also indicated that the microbial assemblage was driven by pH. Various taxa were enriched in different pH ranges: Sulfobacillus was the indicator genus in samples with pH < 3 while Acidobacteriaceae-affiliated bacteria prevailed in samples with 3 < pH < 3.5. The detection of some lineages that are seldom reported in mining areas suggested the coal mining dumps may be a reservoir of phylogenetic novelty. For example, potential nitrogen fixers, autotrophs, and heterotrophs may form diverse communities that actively self-perpetuate pyrite dissolution and acidic waste generation, suggesting unique ecological strategies adopted by these innate microorganisms. In addition, co-occurrence network analyses suggest that members of Acidimicrobiales play important roles in interactions with other taxa, especially Fe- and S-oxidizing bacteria such as Sulfobacillus spp.

Keywords

Random Forest Indicator species analysis Acidimicrobiales Acid mine drainage Ecological strategies 

Notes

Acknowledgements

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

Funding Information

This research was funded by GDAS’ Project of Science and Technology Development (2017GDASCX-0106), the National Natural Science Foundation of China (41771301, 41420104007), the High-level Leading Talent Introduction Program of GDAS (2016GDASRC-0103), the Science and Technology Planning Project of Guangdong Province (2017A070702015, 2017B030314092), GDAS’ Project of Science and Technology Development (2018GDASCX-0601, 2019GDASYL-0302006, 2019GDASYL-0301002).

Compliance with Ethical Standards

Conflict of Interest

The authors declare no conflict of interest.

Supplementary material

248_2019_1335_MOESM1_ESM.docx (811 kb)
ESM 1 (DOCX 810 kb)
248_2019_1335_MOESM2_ESM.xlsx (153 kb)
ESM 2 (XLSX 152 kb)

References

  1. 1.
    Evangelou V, Zhang Y (1995) A review: pyrite oxidation mechanisms and acid mine drainage prevention. Crit Rev Environ Sci Technol 25:141–199CrossRefGoogle Scholar
  2. 2.
    Baker BJ, Banfield JF (2003) Microbial communities in acid mine drainage. FEMS Microb Ecol 44:139–152CrossRefGoogle Scholar
  3. 3.
    Johnson DB, Bacelar-Nicolau P, Okibe N, Thomas A, Hallberg KB (2009) Ferrimicrobium acidiphilum gen. nov., sp. nov. and Ferrithrix thermotolerans gen. nov., sp. nov.: heterotrophic, iron-oxidizing, extremely acidophilic actinobacteria. Int J Syst Evol Microbiol 59:1082–1089CrossRefGoogle Scholar
  4. 4.
    Akcil A, Koldas S (2006) Acid mine drainage (AMD): causes, treatment and case studies. J Clean Prod 14:1139–1145CrossRefGoogle Scholar
  5. 5.
    Zhou C, Liu G, Wu S, Lam PKS (2014) The environmental characteristics of usage of coal gangue in bricking-making: a case study at Huainan, China. Chemosphere 95:274–280CrossRefGoogle Scholar
  6. 6.
    Johnson DB, Hallberg KB (2005) Acid mine drainage remediation options: a review. Sci Total Environ 338:3–14CrossRefGoogle Scholar
  7. 7.
    Silverman MP (1967) Mechanism of bacterial pyrite oxidation. J Bacteriol 94:1046–1051Google Scholar
  8. 8.
    Bevilaqua D, Leite A, Garcia O, Tuovinen O (2002) Oxidation of chalcopyrite by Acidithiobacillus ferrooxidans and Acidithiobacillus thiooxidans in shake flasks. Process Biochem 38:587–592CrossRefGoogle Scholar
  9. 9.
    Schrenk MO, Edwards KJ, Goodman RM, Hamers RJ, Banfield JF (1998) Distribution of Thiobacillus ferrooxidans and Leptospirillum ferrooxidans: implications for generation of acid mine drainage. Science 279:1519–1522CrossRefGoogle Scholar
  10. 10.
    Yahya A, Johnson DB (2002) Bioleaching of pyrite at low pH and low redox potentials by novel mesophilic Gram-positive bacteria. Hydrometallurgy 63:181–188CrossRefGoogle Scholar
  11. 11.
    Bond PL, Druschel GK, Banfield JF (2000a) Comparison of acid mine drainage microbial communities in physically and geochemically distinct ecosystems. Appl Environ Microbiol 66:4962–4971CrossRefGoogle Scholar
  12. 12.
    Edwards KJ, Bond PL, Gihring TM, Banfield JF (2000) An archaeal iron-oxidizing extreme acidophile important in acid mine drainage. Science 287:1796–1799CrossRefGoogle Scholar
  13. 13.
    Wakelin SA, Anand RR, Reith F, Gregg AL, Noble RRP, Goldfarb KC (2012) Bacterial communities associated with a mineral weathering profile at a sulphidic mine tailings dump in arid Western Australia. FEMS Microbiol Ecol 79:298–311CrossRefGoogle Scholar
  14. 14.
    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 10:228–237Google Scholar
  15. 15.
    Sun W, Xiao E, Dong Y, Tang S, Krumins V, Ning Z (2016a) Profiling microbial community in a watershed heavily contaminated by an active antimony (sb) mine in Southwest China. Sci Total Environ 550:297–308CrossRefGoogle Scholar
  16. 16.
    Sun W, Xiao E, Xiao T, Krumins V, Wang Q, Häggblom M (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 51:9165–9175CrossRefGoogle Scholar
  17. 17.
    Sun W, Xiao E, Pu Z, Krumins V, Dong Y, Li B (2018c) 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 612:884–893CrossRefGoogle Scholar
  18. 18.
    Xiao E, Krumins V, Xiao T, Dong Y, Tang S, Ning Z (2017) Depth-resolved microbial community analyses in two contrasting soil cores contaminated by antimony and arsenic. Environ Pollut 221:244–255CrossRefGoogle Scholar
  19. 19.
    Sun W, Xiao E, Krumins V, Häggblom MM, Dong Y, Pu Z (2018b) Rhizosphere microbial response to multiple metal (loid) s in different contaminated arable soils indicates crop-specific metal-microbe interactions. Appl Environ Microbiol 84:e00701-18Google Scholar
  20. 20.
    De Cáceres M, Legendre P, Moretti M (2010) Improving indicator species analysis by combining groups of sites. Oikos 119:1674–1684CrossRefGoogle Scholar
  21. 21.
    Bastian M, Heymann S, Jacomy M (2009) Gephi: an open source software for exploring and manipulating networks. ICWS 8:361–362Google Scholar
  22. 22.
    Csardi G, Nepusz T (2006) The igraph software package for complex network research. Int J Comp Syst 1695:1–9Google Scholar
  23. 23.
    Wang Q, Xie Z, Li F (2015) Using ensemble models to identify and apportion heavy metal pollution sources in agricultural soils on a local scale. Environ Pollut 206:227–235CrossRefGoogle Scholar
  24. 24.
    Fielding AH, Bell JF (1997) A review of methods for the assesment of prediction errors in conservation presence/absence models. Environ Conserv 24:38–49CrossRefGoogle Scholar
  25. 25.
    Huang LN, Kuang JL, Shu WS (2016) Microbial ecology and evolution in the acid mine drainage model system. Trends Microbiol 24:581–593CrossRefGoogle Scholar
  26. 26.
    Chen LX, Huang LN, Méndez GC, Kuang JL, Hua ZS, Liu J (2016) Microbial communities, processes and functions in acid mine drainage ecosystems. Curr Opin Biotechnol 38:150–158CrossRefGoogle Scholar
  27. 27.
    Hammarstrom J, Seal RR, Meier A, Kornfeld J (2005) Secondary sulfate minerals associated with acid drainage in the eastern us: recycling of metals and acidity in surficial environments. Chem Geol 215:407–431CrossRefGoogle Scholar
  28. 28.
    Chen LX, Li JT, Chen YT, Huang LN, Hua ZS, Hu M (2013) Shifts in microbial community composition and function in the acidification of a lead/zinc mine tailings. Environ Microbiol 15:2431–2444CrossRefGoogle Scholar
  29. 29.
    Li J, Sun W, Wang S, Sun Z, Lin S, Peng X (2014) Bacteria diversity, distribution and insight into their role in S and Fe biogeochemical cycling during black shale weathering. Environ Microbiol 16:3533–3547CrossRefGoogle Scholar
  30. 30.
    Kuang JL, Huang LN, Chen LX, Hua ZS, Li SJ, Hu M (2013) Contemporary environmental variation determines microbial diversity patterns in acid mine drainage. ISME J 7:1038–1050CrossRefGoogle Scholar
  31. 31.
    Sun M, Xiao T, Ning Z, Xiao E, Sun W (2015) Microbial community analysis in rice paddy soils irrigated by acid mine drainage contaminated water. Appl Microbiol Biotechnol 99:2911–2922CrossRefGoogle Scholar
  32. 32.
    Hua ZS, Han YJ, Chen LX, Liu J, Hu M, Li SJ (2015) Ecological roles of dominant and rare prokaryotes in acid mine drainage revealed by metagenomics and metatranscriptomics. ISME J 9:1280–1294CrossRefGoogle Scholar
  33. 33.
    Ngom A, Nakagawa Y, Sawada H, Tsukahara J, Wakabayashi S, Uchiumi T (2004) A novel symbiotic nitrogen-fixing member of the ochrobactrum clade isolated from root nodules of acacia mangium. J Gen Appl Microbiol 50:17–27CrossRefGoogle Scholar
  34. 34.
    Wackerow-Kouzova N (2007) Ochrobactrum intermedium anki, a nitrogen-fixing bacterium able to decolorize azobenzene. Appl Biochem Microbiol 43:403–406CrossRefGoogle Scholar
  35. 35.
    Giri S, Pati B (2004) A comparative study on phyllosphere nitrogen fixation by newly isolated Corynebacterium sp. & Flavobacterium sp. and their potentialities as biofertilizer. Acta Microbiol Immunol Hung 51:47–56CrossRefGoogle Scholar
  36. 36.
    Ho A, Angel R, Veraart AJ, Daebeler A, Jia Z, Kim SY, Kerckhof F, Boon N, Bodelier P (2016) Biotic interactions in microbial communities as modulators of biogeochemical processes: Methanotrophy as a model system. Front Microbiol 7:1285Google Scholar
  37. 37.
    Sun W, Xiao E, Häggblom M, Krumins V, Dong Y, Sun X (2018a) Bacterial survival strategies in an alkaline tailing site and the physiological mechanisms of dominant phylotypes as revealed by metagenomic analyses. Environ Sci Technol 52:13370–13380CrossRefGoogle Scholar
  38. 38.
    Clark DA, Norris PR (1996) Acidimicrobium ferrooxidans gen. nov., sp. nov.: mixed-culture ferrous iron oxidation with sulfobacillus species. Microbiology 142:785–790CrossRefGoogle Scholar
  39. 39.
    Johnson DB, Hallberg KB (2003) The microbiology of acidic mine waters. Res Microbiol 154:466–473CrossRefGoogle Scholar
  40. 40.
    Itoh T, Yoshikawa N, Takashina T (2007) Thermogymnomonas acidicola gen. nov., sp. nov., a novel thermoacidophilic, cell wall-less archaeon in the order thermoplasmatales, isolated from a solfataric soil in hakone, Japan. Int J Syst Evol Microbiol 57:2557–2561CrossRefGoogle Scholar
  41. 41.
    Fukushima J, Tojo F, Asano R, Kobayashi Y, Shimura Y, Okano K, Miyata N (2015) Complete genome sequence of the unclassified iron-oxidizing, chemolithoautotrophic Burkholderiales bacterium GJ-E10, isolated from an acidic river. Genome Announc 3:e01455-14Google Scholar
  42. 42.
    Twardowska I (2015) The role of microbial activity in sulfide oxidation at dumping sites of sulfidic wastes and in abandoned mining areas. Environ Microb Biotechnol 45:1–31Google Scholar
  43. 43.
    Kozubal M, Macur R, Korf S, Taylor W, Ackerman G, Nagy A, Inskeep W (2008) Isolation and distribution of a novel iron-oxidizing crenarchaeon from acidic geothermal springs in yellowstone national park. Appl Environ Microbiol 74:942–949CrossRefGoogle Scholar
  44. 44.
    Tat’yana IB, Tsaplina IA, Kondrat’eva TF, Duda VI, Suzina NE, Melamud VS (2006) Sulfobacillus thermotolerans sp. nov., a thermotolerant, chemolithotrophic bacterium. Int J Syst Evol Microbiol 56:1039–1042CrossRefGoogle Scholar
  45. 45.
    Watling H, Perrot F, Shiers D (2008) Comparison of selected characteristics of sulfobacillus species and review of their occurrence in acidic and bioleaching environments. Hydrometallurgy 93:57–65CrossRefGoogle Scholar
  46. 46.
    Bond PL, Smriga SP, Banfield JF (2000b) Phylogeny of microorganisms populating a thick, subaerial, predominantly lithotrophic biofilm at an extreme acid mine drainage site. Appl Environ Microbiol 66:3842–3849CrossRefGoogle Scholar
  47. 47.
    García-Moyano A, González-Toril E, Moreno-Paz M, Parro V, Amils R (2008) Evaluation of Leptospirillum spp. in the río tinto, a model of interest to biohydrometallurgy. Hydrometallurgy 94:155–161CrossRefGoogle Scholar
  48. 48.
    Falco L, Pogliani C, Curutchet G, Donati E (2003) A comparison of bioleaching of covellite using pure cultures of Acidithiobacillus ferrooxidans and Acidithiobacillus thiooxidans or a mixed culture of Leptospirillum ferrooxidans and Acidithiobacillus thiooxidans. Hydrometallurgy 71:31–36CrossRefGoogle Scholar
  49. 49.
    Zhang L, Qiu GZ, Hu YH, Sun XJ, Li JH, Gu GH (2008) Bioleaching of pyrite by A. ferrooxidans and L. ferriphilum. Trans Nonferrous Met Soc China 18:1415–1420CrossRefGoogle Scholar
  50. 50.
    Tan GL, Shu WS, Zhou WH, Li XL, Lan CY, Huang LN (2009) Seasonal and spatial variations in microbial community structure and diversity in the acid stream draining across an ongoing surface mining site. FEMS Microbiol Ecol 70:277–285CrossRefGoogle Scholar
  51. 51.
    Bhattacharyya S, Chakrabarty BK, Das A, Kundu PN, Banerjee PC (2011) Acidiphilium symbioticum sp. nov., an acidophilic heterotrophic bacteria. Can J Microbiol 37:78–85CrossRefGoogle Scholar
  52. 52.
    Regenspurg S, Gößner A, Peiffer S, Küsel K (2002) Potential remobilization of toxic anions during reduction of arsenated and chromated schwertmannite by the dissimilatory Fe(III)-reducing bacterium Acidiphilium cryptum JF-5. Water Air Soil Pollut 2:57–67CrossRefGoogle Scholar
  53. 53.
    González E, González F, Muñoz J, Blázquez ML, Ballester A (2015) Reductive dissolution of iron oxides and manganese bioleaching by Acidiphilium cryptum JF-5. Advanc Mater Res 1130:347–350Google Scholar
  54. 54.
    Rohwerder T, Sand W (2003) The sulfane sulfur of persulfides is the actual substrate of the sulfur-oxidizing enzymes from Acidithiobacillus and Acidiphilium spp. Microbiology 149:1699–1710CrossRefGoogle Scholar
  55. 55.
    Sun W, Xiao E, Häggblom M, Krumins V, Dong Y, Sun X, Li F, Wang Q, Li B, Yan B (2018) Bacterial survival strategies in an alkaline tailing site and the physiological mechanisms of dominant phylotypes as revealed by metagenomic analyses. Environ Sci Technol 52:13370–13380CrossRefGoogle Scholar
  56. 56.
    Waranusantigul P, Lee 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 85:584–590CrossRefGoogle Scholar
  57. 57.
    Rodríguez-Llorente ID, Gamane D, Lafuente A, Dary M, Hamdaoui AE, Delgadillo J (2010) Cadmium biosorption properties of the metal-resistant Ochrobactrum cytisi Azn6.2. Eng Life Sci 10:49–56CrossRefGoogle Scholar
  58. 58.
    Sultan S, Hasnain S (2007) Reduction of toxic hexavalent chromium by Ochrobactrum intermedium strain SDCr-5 stimulated by heavy metals. Bioresour Technol 98:340–344CrossRefGoogle Scholar
  59. 59.
    Motsi T, Rowson NA, Simmons MJH (2009) Adsorption of heavy metals from acid mine drainage by natural zeolite. Int J Miner Process 92:42–48CrossRefGoogle Scholar
  60. 60.
    Galán E, Gómez-Ariza JL, González I, Fernández-Caliani JC, Morales E, Giráldez (2003) Heavy metal partitioning in river sediments severely polluted by acid mine drainage in the iberian pyrite belt. Appl Geochem 18:409–421CrossRefGoogle Scholar
  61. 61.
    Sheoran AS, Sheoran V (2006) Heavy metal removal mechanism of acid mine drainage in wetlands: a critical review. Miner Eng 19:105–116CrossRefGoogle Scholar
  62. 62.
    Branco R, Francisco R, Chung AP, Morais PV (2009) Identification of an aox system that requires cytochrome c in the highly arsenic-resistant bacterium Ochrobactrum tritici SCII24. Appl Environ Microbiol 75:5141–5147CrossRefGoogle Scholar
  63. 63.
    Trujillo ME, Willems A, Abril A, Planchuelo AM, Rivas R, Ludena D (2005) Nodulation of lupinus albus by strains of Ochrobactrum lupini sp. nov. Appl Environ Microbiol 71:1318–1327CrossRefGoogle Scholar
  64. 64.
    Monciardini P, Cavaletti L, Schumann P, Rohde M, Donadio S (2003) Conexibacter woesei gen. nov., sp. nov., a novel representative of a deep evolutionary line of descent within the class Actinobacteria. Int J Syst Evol Microbiol 53:569–576CrossRefGoogle Scholar
  65. 65.
    Seki T, Matsumoto A, Shimada R, Inahashi Y, Ōmura S, Takahashi Y (2012) Conexibacter arvalis sp. nov., isolated from a cultivated field soil sample. Int J Syst Evol Microbiol 62:2400–2404CrossRefGoogle Scholar
  66. 66.
    Lee SD (2017) Conexibacter stalactiti sp. nov., isolated from stalactites in a lava cave and emended description of the genus Conexibacter. Int J Syst Evol Microbiol 67:3214–3218CrossRefGoogle Scholar
  67. 67.
    Mirete S, De Figueras CG, González-Pastor JE (2007) Novel nickel resistance genes from the rhizosphere metagenome of plants adapted to acid mine drainage. Appl Environ Microbiol 73:6001–6011CrossRefGoogle Scholar
  68. 68.
    Pukall R, Lapidus A, Del Rio TG, Copeland A, Tice H, Cheng JF (2010) Complete genome sequence of Conexibacter woesei type strain (ID131577T). Stand Genomic Sci 2:212–219CrossRefGoogle Scholar
  69. 69.
    Yang Y, Yang L, Sun QY (2014) Archaeal and bacterial communities in acid mine drainage from metal-rich abandoned tailing ponds, Tongling, China. Trans Nonferrous Met Soc China 24:3332–3342CrossRefGoogle Scholar
  70. 70.
    Yelton AP, Comolli LR, Justice NB, Castelle C, Denef VJ, Thomas BC (2013) Comparative genomics in acid mine drainage biofilm communities reveals metabolic and structural differentiation of co-occurring archaea. BMC Genomics 14:485CrossRefGoogle Scholar
  71. 71.
    Mesa V, Gallego JL, González-Gil R, Lauga B, Sánchez J, Méndez-García C (2017) Bacterial, archaeal, and eukaryotic diversity across distinct microhabitats in an acid mine drainage. Front Microbiol 8:1756CrossRefGoogle Scholar
  72. 72.
    Itoh T, Yamanoi K, Kudo T, Ohkuma M, Takashina T (2011) Aciditerrimonas ferrireducens gen. nov., sp. nov., an iron-reducing thermoacidophilic actinobacterium isolated from a solfataric field. Int J Syst Evol Microbiol 61:1281–1285CrossRefGoogle Scholar
  73. 73.
    Sun W, Xiao E, Krumins V, Dong Y, Xiao T, Ning Z (2016b) Characterization of the microbial community composition and the distribution of Fe-metabolizing bacteria in a creek contaminated by acid mine drainage. Appl Microbiol Biotechnol 100:8523–8535CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Guangdong Key Laboratory of Integrated Agro-environmental Pollution Control and ManagementGuangdong Institute of Eco-environmental Science & TechnologyGuangzhouChina
  2. 2.Key Laboratory for Water Quality and Conservation of the Pearl River Delta, Ministry of Education, School of Environmental Science and EngineeringGuangzhou UniversityGuangzhouChina
  3. 3.Department of Environmental SciencesRutgers UniversityNew BrunswickUSA
  4. 4.Institute for Genomic BiologyUniversity of IllinoisUrbanaUSA
  5. 5.School of Environmental StudiesChina University of Geosciences (Wuhan)WuhanChina
  6. 6.Shanghai Key Lab for Urban Ecological Processes and Eco-Restorations, School of Ecological and Environmental SciencesEast China Normal UniversityShanghaiChina

Personalised recommendations