Register      Login
Soil Research Soil Research Society
Soil, land care and environmental research
Shopping Cart: ( empty )
You are here: Home > Journals > SR > SR22135
RESEARCH ARTICLE
Contents Vol 61(8)

Bacterial succession in an abandoned circum-neutral opencast coal mine in India

Sohini Banerjee https://orcid.org/0000-0002-2911-2650 A B C , Arijit Misra A , Abhijit Sar A , Srikanta Pal A , Shibani Chaudhury B and Bomba Dam https://orcid.org/0000-0003-2417-2088 A *
+ Author Affiliations
- Author Affiliations

A Microbiology Laboratory, Department of Botany (DST-FIST & UGC-DRS Funded), Institute of Science, Visva-Bharati (A Central University), Santiniketan, West Bengal 731235, India.

B Department of Environmental Studies, Institute of Science, Visva-Bharati (A Central University), Santiniketan, West Bengal 731235, India.

C Present Address: Department of Molecular Virology and Microbiology, Baylor College of Medicine, Houston, TX 77030, USA.

* Correspondence to: bomba.dam@visva-bharati.ac.in

Handling Editor: Nathan Basiliko

Soil Research 61(8) 831-842 https://doi.org/10.1071/SR22135
Submitted: 29 July 2022  Accepted: 21 August 2023  Published: 15 September 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Context

Abandoned mines provide an ideal opportunity to study the succession of microbial communities, which is crucial for the development and stability of the soil.

Aims

We examined the diversity and temporal succession of the microbial community in an abandoned coal mine.

Methods

We investigated soil geochemical parameters and microbial succession using high-throughput 16S rRNA gene amplicon sequences over a 4-year period in a derelict opencast circum-neutral coal mine in Tasra colliery, Jharkhand, India.

Results

Soil pH (4.46–6.13), organic carbon (0.86–4.53%), available nitrogen (0.001–0.003%) and total cultivable heterotrophic microbial load increased, and concentrations of chloride (24 865–15 067 ppm), sulfate (26 417–417 ppm) and heavy metals reduced over the period of 4 years. The 16S rRNA gene sequences identified Proteobacteria as the dominant phylum across samples except for the fourth year, where Actinobacteria was predominant. Chlorobi, WPS-2 and Spirochaetes were exclusively identified in the first year. Twelve phyla present in the first year were completely absent by the end. In the fourth year, an abundance of nitrogen-fixing members such as Burkholderiales, Rhizobiales, Roseiflexales and Actinomycetales was noted and semi-quantitative PCR suggested that nitrogenases were predominately vanadium dependent (relative to molybdenum). Gradual shifts from purportedly chemolithotrophic to heterotrophic metabolic strategies were also observed.

Conclusion

This work establishes that soil improvement in abandoned coal mines involves the dynamic interplay of physicochemical parameters and shifts in microbial communities and dominant metabolic guilds. This knowledge can be used to plan and monitor remediation measures in such sites.

Keywords: 16S rDNA amplicon sequencing, abandoned coal mine, alternative nitrogenase, microbial communities, nutrients in soil, rehabilitation, soil microbial ecology, temporal succession.

References

Andrews S (2010) FastQC: a quality control tool for high throughput sequence data. Available at http://www.bioinformatics.babraham.ac.uk/projects/fastqc

Baker BJ, Banfield JF (2003) Microbial communities in acid mine drainage. FEMS Microbiology Ecology 44, 139-152.
| Crossref | Google Scholar |

Banerjee S, Sar A, Misra A, Pal S, Chakraborty A, Dam B (2018) Increased productivity in poultry birds by sub-lethal dose of antibiotics is arbitrated by selective enrichment of gut microbiota, particularly short-chain fatty acid producers. Microbiology 164, 142-153.
| Crossref | Google Scholar |

Banerjee S, Misra A, Chaudhury S, Dam B (2019) A Bacillus strain TCL isolated from Jharia coalmine with remarkable stress responses, chromium reduction capability and bioremediation potential. Journal of Hazardous Materials 367, 215-223.
| Crossref | Google Scholar | PubMed |

Banerjee S, Misra A, Sar A, Pal S, Chaudhury S, Dam B (2020) Poor nutrient availability in opencast coalmine influences microbial community composition and diversity in exposed and underground soil profiles. Applied Soil Ecology 152, 103544.
| Crossref | Google Scholar |

Banks D, Younger PL, Arnesen R-T, Iversen ER, Banks SB (1997) Mine-water chemistry: the good, the bad and the ugly. Environmental Geology 32, 157-174.
| Crossref | Google Scholar |

Bechtold R, Sharma NK, Vega M, Datta S, Arruda J, Ghosh A (2020) Isolation and characterization of soil bacteria from an abandoned coal mine in Southeast Kansas. Transactions of the Kansas Academy of Science 123, 371-385.
| Crossref | Google Scholar |

Boyd ES, Hamilton TL, Peters JW (2011) An alternative path for the evolution of biological nitrogen fixation. Frontiers in Microbiology 2, 205.
| Crossref | Google Scholar | PubMed |

Bremner JM (1960) Determination of nitrogen in soil by the Kjeldahl method. The Journal of Agricultural Science 55, 11-33.
| Crossref | Google Scholar |

Caporaso JG, Kuczynski J, Stombaugh J, et al. (2010a) QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7, 335-336.
| Crossref | Google Scholar | PubMed |

Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2010b) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26, 266-267.
| Crossref | Google Scholar | PubMed |

Chen M, Ma LQ (1998) Comparison of four USEPA digestion methods for trace metal analysis using certified and Florida soils. Journal of Environmental Quality 27, 1294-1300.
| Crossref | Google Scholar |

Claassens S, Jansen Van Rensburg PJ, Maboeta MS, van Rensburg L (2008) Soil microbial community function and structure in a post-mining chronosequence. Water, Air, and Soil Pollution 194, 315-329.
| Crossref | Google Scholar |

Cravotta CA III, Kirby CS (2004) Acidity and alkalinity in mine drainage: practical considerations. In ‘Proceedings of the 21st ASMR and the 25th West Virginia surface mine drainage task force symposium, Morgantown, WV’. pp. 334–365. (ASMR)

De Mandal S, Chatterjee R, Kumar NS (2017) Dominant bacterial phyla in caves and their predicted functional roles in C and N cycle. BMC Microbiology 17, 90.
| Crossref | Google Scholar | PubMed |

DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Applied and Environmental Microbiology 72, 5069-5072.
| Crossref | Google Scholar |

Ding W, Stewart DI, Humphreys PN, Rout SP, Burke IT (2016) Role of an organic carbon-rich soil and Fe(III) reduction in reducing the toxicity and environmental mobility of chromium(VI) at a COPR disposal site. Science of The Total Environment 541, 1191-1199.
| Crossref | Google Scholar | PubMed |

Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461.
| Crossref | Google Scholar | PubMed |

Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods 10, 996-998.
| Crossref | Google Scholar | PubMed |

Edwards KJ, Gihring TM, Banfield JF (1999) Seasonal variations in microbial populations and environmental conditions in an extreme acid mine drainage environment. Applied and Environmental Microbiology 65, 3627-3632.
| Crossref | Google Scholar | PubMed |

EPA US (1996) Microwave assisted acid digestion of siliceous and organically based matrices. OHW, Method 3052. EPA.

Ezeokoli OT, Bezuidenhout CC, Maboeta MS, Khasa DP, Adeleke RA (2020) Structural and functional differentiation of bacterial communities in post-coal mining reclamation soils of South Africa: bioindicators of soil ecosystem restoration. Scientific Reports 10, 1759.
| Crossref | Google Scholar |

Fierer N, Nemergut D, Knight R, Craine JM (2010) Changes through time: integrating microorganisms into the study of succession. Research in Microbiology 161, 635-642.
| Crossref | Google Scholar | PubMed |

Fosso-Kankeu E, Manyatshe A, Waanders F (2017) Mobility potential of metals in acid mine drainage occurring in the Highveld area of Mpumalanga Province in South Africa: implication of sediments and efflorescent crusts. International Biodeterioration & Biodegradation 119, 661-670.
| Crossref | Google Scholar |

Gaby JC, Buckley DH (2012) A comprehensive evaluation of PCR primers to amplify the nifH gene of nitrogenase. PLoS ONE 7, e42149.
| Crossref | Google Scholar |

Ghose MK (2004) Effect of opencast mining on soil fertility. Journal of Scientific and Industrial Research 63, 1006-1009.
| Google Scholar |

Guo Y, Fujimura R, Sato Y, Suda W, Kim S-W, Oshima K, Hattori M, Kamijo T, Narisawa K, Ohta H (2014) Characterization of early microbial communities on volcanic deposits along a vegetation gradient on the island of Miyake, Japan. Microbes and Environments 29, 38-49.
| Crossref | Google Scholar | PubMed |

Halter D, Cordi A, Gribaldo S, Gallien S, Goulhen-Chollet F, Heinrich-Salmeron A, Carapito C, Pagnout C, Montaut D, Seby F, Van Dorsselaer A, Schaeffer C, Bertin PN, Bauda P, Arsène-Ploetze F (2011) Taxonomic and functional prokaryote diversity in mildly arsenic-contaminated sediments. Research in Microbiology 162, 877-887.
| Crossref | Google Scholar | PubMed |

Hariharan J, Sengupta A, Grewal P, Dick WA (2017) Functional predictions of microbial communities in soil as affected by long-term tillage practices. Agricultural & Environmental Letters 2, 170031.
| Crossref | Google Scholar |

Hua Z-S, Han Y-J, Chen L-X, Liu J, Hu M, Li S-J, Kuang J-L, Chain PSG, Huang L-N, Shu W-S (2015) Ecological roles of dominant and rare prokaryotes in acid mine drainage revealed by metagenomics and metatranscriptomics. The ISME Journal 9, 1280-1294.
| Crossref | Google Scholar | PubMed |

Jamal A, Dhar BB, Ratan S (1991) Acid mine drainage control in an opencast coal mine. Mine Water and the Environment 10, 1-16.
| Crossref | Google Scholar |

Janzen C, Tobin-Janzen T (2008) Microbial communities in fire-affected soils. In ‘Microbiology of extreme soils’. (Eds P Dion, CS Nautiyal) pp. 299–316. (Springer)

Jitesh Kumar M, Amiya Kumar P (2013) Physico-chemical characterization and mine soil genesis in age series coal mine overburden spoil in chronosequence in a dry tropical environment. Journal of Phylogenetics & Evolutionary Biology 1, 101.
| Crossref | Google Scholar |

Johnson CD, Skousen JG (1995) Minesoil properties of 15 abandoned mine land sites in West Virginia. Journal of Environmental Quality 24, 635-643.
| Crossref | Google Scholar |

King GM, Weber CF (2008) Interactions between bacterial carbon monoxide and hydrogen consumption and plant development on recent volcanic deposits. The ISME Journal 2, 195-203.
| Crossref | Google Scholar | PubMed |

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. Research in Microbiology 165, 713-718.
| Crossref | Google Scholar | PubMed |

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. The ISME Journal 7, 1038-1050.
| Crossref | Google Scholar | PubMed |

Kumbhare SV, Dhotre DP, Dhar SK, Jani K, Apte DA, Shouche YS, Sharma A (2015) Insights into diversity and imputed metabolic potential of bacterial communities in the continental shelf of Agatti Island. PLoS ONE 10, e0129864.
| Crossref | Google Scholar | PubMed |

Langille MGI, Zaneveld J, Caporaso JG, et al. (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nature Biotechnology 31, 814-821.
| Crossref | Google Scholar | PubMed |

Li S-J, Hua Z-S, Huang L-N, Li J, Shi S-H, Chen L-X, Kuang J-L, Liu J, Hu M, Shu W-S (2014) Microbial communities evolve faster in extreme environments. Scientific Reports 4, 6205.
| Crossref | Google Scholar | PubMed |

Li J, Liu F, Chen J (2016) The effects of various land reclamation scenarios on the succession of soil bacteria, Archaea, and Fungi over the short and long term. Frontiers in Ecology and Evolution 4, 32.
| Crossref | Google Scholar |

Lindsay MBJ, Condon PD, Jambor JL, Lear KG, Blowes DW, Ptacek CJ (2009) Mineralogical, geochemical, and microbial investigation of a sulfide-rich tailings deposit characterized by neutral drainage. Applied Geochemistry 24, 2212-2221.
| Crossref | Google Scholar |

Loveless TM, Bishop PE (1999) Identification of genes unique to Mo-independent nitrogenase systems in diverse diazotrophs. Canadian Journal of Microbiology 45, 312-317.
| Crossref | Google Scholar | PubMed |

Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Applied and Environmental Microbiology 71, 8228-8235.
| Crossref | Google Scholar | PubMed |

Maharana JK, Patel AK (2015) Assessment of microbial diversity associated with chronosequence coal mine overburden spoil using random amplified polymorphic DNA markers. International Journal Recent Scientific Research 6, 4291-4301.
| Google Scholar |

Muchowska KB, Varma SJ, Chevallot-Beroux E, Lethuillier-Karl L, Li G, Moran J (2017) Metals promote sequences of the reverse Krebs cycle. Nature Ecology & Evolution 1, 1716-1721.
| Crossref | Google Scholar | PubMed |

Mus F, Alleman AB, Pence N, Seefeldt LC, Peters JW (2018) Exploring the alternatives of biological nitrogen fixation. Metallomics 10, 523-538.
| Crossref | Google Scholar | PubMed |

Nemergut DR, Anderson SP, Cleveland CC, Martin AP, Miller AE, Seimon A, Schmidt SK (2007) Microbial community succession in an unvegetated, recently deglaciated soil. Microbial Ecology 53, 110-122.
| Crossref | Google Scholar | PubMed |

Nieto JM, Sarmiento AM, Canovas CR, Olias M, Ayora C (2013) Acid mine drainage in the Iberian Pyrite Belt: 1. Hydrochemical characteristics and pollutant load of the Tinto and Odiel rivers. Environmental Science and Pollution Research 20, 7509-7519.
| Crossref | Google Scholar | PubMed |

Parks DH, Tyson GW, Hugenholtz P, Beiko RG (2014) STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30, 3123-3124.
| Crossref | Google Scholar | PubMed |

Pasayat M, Patel AK (2015) Assessment of physico-chemical properties influencing mine spoil genesis in chronosequence iron mine overburden spoil and implications of soil quality. International Journal of Current Microbiology and Applied Sciences 4, 1095-1110.
| Google Scholar |

Pereira LB, Vicentini R, Ottoboni LMM (2014) Changes in the bacterial community of soil from a neutral mine drainage channel. PLoS ONE 9, e96605.
| Crossref | Google Scholar | PubMed |

Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson FL (2014) ‘The Prokaryotes: Actinobacteria.’ (Springer)

Rout TK, Masto RE, Padhy PK, Ram LC, George J, Joshi G (2015) Heavy metals in dusts from commercial and residential areas of Jharia coal mining town. Environmental Earth Sciences 73, 347-359.
| Crossref | Google Scholar |

Scharer JM, Pettit CM, Kirkaldy JL, Bolduc L, Halbert BE, Chambers DB (2000) Leaching of metals from sulphide mine wastes at neutral pH. In ‘ICARD 2000 Proceedings from the Fifth International Conference on Acid Rock Drainage, Vol. I’. (Society for Mining, Metallurgy, and Exploration, Inc.)

Sheoran V, Sheoran AS, Poonia P (2010) Soil reclamation of abandoned mine land by revegetation: a review. International Journal of Soil, Sediment and Water 3, 13.
| Google Scholar |

Shivlata L, Satyanarayana T (2015) Thermophilic and alkaliphilic Actinobacteria: biology and potential applications. Frontiers in Microbiology 6, 1014.
| Crossref | Google Scholar | PubMed |

Staley C, Gould TJ, Wang P, Phillips J, Cotner JB, Sadowsky MJ (2014) Core functional traits of bacterial communities in the Upper Mississippi River show limited variation in response to land cover. Frontiers in Microbiology 5, 414.
| Crossref | Google Scholar |

Tessier A, Campbell PGC, Bisson M (1979) Sequential extraction procedure for the speciation of particulate trace metals. Analytical Chemistry 51, 844-851.
| Crossref | Google Scholar |

Tordoff GM, Baker AJM, Willis AJ (2000) Current approaches to the revegetation and reclamation of metalliferous mine wastes. Chemosphere 41, 219-228.
| Crossref | Google Scholar | PubMed |

Tripathy DP, Panigrahi DC, Singh G (2009) Determination of soil pollution index and soil infiltration rates in some non-fire and fire areas of Jharia coal field. In ‘Ninth International Mine Ventilation Congress, New Delhi, 10–13 November 2009’. (Indian School of Mines)

Urbanová M, Kopecký J, Valášková V, Ságová-Marečková M, Elhottová D, Kyselková M, Moënne-Loccoz Y, Baldrian P (2011) Development of bacterial community during spontaneous succession on spoil heaps after brown coal mining. FEMS Microbiology Ecology 78, 59-69.
| Crossref | Google Scholar |

Walkley A (1947) A critical examination of a rapid method for determining organic carbon in soils – effect of variations in digestion conditions and of inorganic soil constituents. Soil Science 63, 251-264.
| Crossref | Google Scholar |

Weber CF, King GM (2010) Distribution and diversity of carbon monoxide-oxidizing bacteria and bulk bacterial communities across a succession gradient on a Hawaiian volcanic deposit. Environmental Microbiology 12, 1855-1867.
| Crossref | Google Scholar | PubMed |