Skip to main content
Log in

Diversity and Heavy Metal Tolerance of Fungi Associated with Different Coal Overburden Strata of Tikak Colliery, Assam

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Coal mine overburdens are generally highly acidic and contaminated with toxic heavy metals. Here, we studied the culturable fungal diversity associated with different coal overburden strata (OBS) of Assam, India, and assessed their heavy metal tolerance ability against five different heavy metals viz., As3+, Cd2+, Cr6+, Cu2+, and Ni2+. Among 15 distinct coal OBS considered in this study which spans a depth of ~ 35 m from the ground surface, the isolation of fungi was successful only from 11 OBS samples and the colony-forming unit (CFU) counts were highly variable among the samples. A total of 66 fungal pure cultures were isolated which belong to 18 genera (17 known and 1 unknown) under 15 families and two divisions i.e., Ascomycota (89.4%) and Basidiomycota (10.6%). Acidiella bohemica was found relatively the most abundant species followed by Rhodotorula toruloides. A good number of fungal isolates was found tolerant to the test heavy metals at concentrations ≥ 1 mM. Findings of some multi-metallotolerant fungal isolates along with a tolerance up to 5 mM concentration of As3+, and up to 10 mM each of Cu2+, Cr6+, Ni2+ and Cd2+ were noteworthy in the present study that could be useful in the management of heavy metal pollution or stress.

Graphical Abstract

Cultivable fungal diversity of coal mine overburden strata of Tikak colliery, Margherita, Assam, India. It shows a photograph of the coal mining site as the background, front view of the fungal colonies in the upper section, and a graphical representation of heavy metal tolerance of the isolates at different concentrations of As, Cd, Cr, Cu, and Ni in the lower section.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Akob DM, Kusel K (2011) Where microorganisms meet rocks in the Earth’s Critical Zone. Biogeosciences 8(12):3531–3543. https://doi.org/10.5194/bg-8-3531-2011

    Article  CAS  Google Scholar 

  2. Jin L, Ravella R, Ketchum B, Bierman PR, Heaney P, White T, Brantley SL (2010) Mineral weathering and elemental transport during hillslope evolution at the Susquehanna/Shale Hills Critical Zone Observatory. Geochim Cosmochim Acta 74(13):3669–3691. https://doi.org/10.1016/j.gca.2010.03.036

    Article  CAS  Google Scholar 

  3. Singh KN, Narzary D (2021) Geochemical characterization of mine overburden strata for strategic overburden-spoil management in an opencast coal mine. Environ Chall 3:100060. https://doi.org/10.1016/j.envc.2021.100060

    Article  CAS  Google Scholar 

  4. Ehrlich HL (2006) Geomicrobiology: relative roles of bacteria and fungi a geomicrobial agents. In: Gadd GM (ed) Fungi in biogeochemical cycles. Cambridge University Press, Cambridge, pp 1–27

    Google Scholar 

  5. Reitner J, GabrielaPedersen S K (2006) Fungi in subterranean environments. In: Gadd GM (ed) Fungi in biogeochemical cycles. Cambridge University Press, Cambridge, p 377

    Chapter  Google Scholar 

  6. Ehrlich HL (2002) Geomicrobiology, 4th edn. Marcel Dekker Publisher, New York

    Book  Google Scholar 

  7. Gadd GM (2006) Fungi in biogeochemical cycles. Cambridge University Press

    Book  Google Scholar 

  8. Ehrlich HL (1997) Microbes and metals. Appl Microbiol Biotechnol 48(6):687–692

    Article  CAS  Google Scholar 

  9. Ehrlich HL (2002) How microbes mobilize metals in ores: a review of current understandings and proposals for further research. Min Metall Explor 19(4):220–224

    CAS  Google Scholar 

  10. Dobson AP, Bradshaw AD, Baker AJM (1997) Hopes for the future: restoration ecology and conservation biology. Science 277(5325):515–522. https://doi.org/10.1126/science.277.5325.515

    Article  CAS  Google Scholar 

  11. Dowarah J, Deka Boruah HP, Gogoi J, Pathak N, Saikia N, Handique AK (2009) Eco-restoration of a high-sulfur coal mine overburden dumping site in northeast India: a case study. J Earth Syst Sci 118:597–608. https://doi.org/10.1007/s12040-009-0042-5

    Article  Google Scholar 

  12. Daniels W, Zipper C (2010) Creation and management of productive mine soils. Virginia Cooperative Extension. 460: 121. https://vtechworks.lib.vt.edu/handle/10919/55040

  13. Willscher S, Hertwig T, Frenzel M, Felix M, Starke S (2010) Results of remediation of hard coal overburden and tailing dumps after a few decades: insights and conclusions. Hydrometallurgy 104(3–4):506–517. https://doi.org/10.1016/j.hydromet.2010.03.031

    Article  CAS  Google Scholar 

  14. Li F, Li X, Hou L, Shao A (2018) Impact of the coal mining on the spatial distribution of potentially toxic metals in farmland tillage soil. Sci Rep 8(1):14925. https://doi.org/10.1038/s41598-018-33132-4

    Article  CAS  Google Scholar 

  15. Grant CD, Koch J (2007) Decommissioning Western Australia’s first bauxite mine: co-evolving vegetation restoration techniques and targets. Ecol Manag Restor 8(2):92–105. https://doi.org/10.1111/j.1442-8903.2007.00346.x

    Article  Google Scholar 

  16. Skousen J, Zipper C (2014) Post-mining policies and practices in the Eastern USA coal region. Int J Coal Sci Technol 1:135–151

    Article  Google Scholar 

  17. Jaynes DB, Rogowski AS, Pionke HB (1984) Acid mine drainage from reclaimed coal strip mines 1. Model description. Water Resour Res 20(2):233–242. https://doi.org/10.1029/WR020i002p00233

    Article  CAS  Google Scholar 

  18. Zafar S, Aqil F, Ahmad I (2007) Metal tolerance and biosorption potential of filamentous fungi isolated from metal contaminated agricultural soil. Bioresour Technol 98(13):2557–2561. https://doi.org/10.1016/j.biortech.2006.09.051

    Article  CAS  Google Scholar 

  19. Ezzouhri L, Castro E, Moya M, Espinola F, Lairini K (2009) Heavy metal tolerance of filamentous fungi isolated from polluted sites in Tangier. Morocco Afr J Microbiol Res 3(2):35–48

    CAS  Google Scholar 

  20. Ho Joo J, Hussein KA (2012) Heavy metal tolerance of fungi isolated from contaminated soil. Korean J Soil Sci Fertil 45(4):565–571. https://doi.org/10.7745/KJSSF.2012.45.4.565

    Article  Google Scholar 

  21. Kumari D, Pan X, Achal V, Zhang D, Al-Misned FA, Golam Mortuza M (2015) Multiple metal-resistant bacteria and fungi from acidic copper mine tailings of Xinjiang. China Environ Earth Sci 74(4):3113–3121. https://doi.org/10.1007/s12665-015-4349-z

    Article  CAS  Google Scholar 

  22. Rose PK, Devi R (2018) Heavy metal tolerance and adaptability assessment of indigenous filamentous fungi isolated from industrial wastewater and sludge samples. Beni-Suef Univ J Basic Appl Sci 7(4):688–694. https://doi.org/10.1016/j.bjbas.2018.08.001

    Article  Google Scholar 

  23. Hassan A, Periathamby A, Ahmed A, Innocent O, Hamid FS (2020) Effective bioremediation of heavy metal–contaminated landfill soil through bioaugmentation using consortia of fungi. J Soils Sediments 20(1):66–80. https://doi.org/10.1007/s11368-019-02394-4

    Article  CAS  Google Scholar 

  24. Gadd GM (1994) Interactions of fungi with toxic metals. In: Powell KA, Renwick A, Peberdy JF (eds) The Genus Aspergillus. Springer, Cham, pp 361–374. https://doi.org/10.1007/978-1-4899-0981-7_28

    Chapter  Google Scholar 

  25. Belly RT, Brock TD (1974) Ecology of iron-oxidizing bacteria in pyritic materials associated with coal. J Bacteriol 117(2):726–732. https://doi.org/10.1128/jb.117.2.726-732.1974

    Article  CAS  Google Scholar 

  26. Ngugi MR, Fechner N, Neldner VJ, Dennis PG (2020) Successional dynamics of soil fungal diversity along a restoration chronosequence post-coal mining. Restor Ecol 28(3):543–552. https://doi.org/10.1111/rec.13112

    Article  Google Scholar 

  27. Dangi SR, Stahl PD, Wick AF, Ingram LJ, Buyer JS (2012) Soil microbial community recovery in reclaimed soils on a surface coal mine site. Soil Sci Soc Am J 76(3):915–924. https://doi.org/10.2136/sssaj2011.0288

    Article  CAS  Google Scholar 

  28. Singh KN, Narzary D (2021) Heavy metal tolerance of bacterial isolates associated with overburden strata of an open-cast coal mine of Assam (India). Environ Sci Pollut Res 28(44):63111–63126. https://doi.org/10.1007/s11356-021-15153-1

    Article  CAS  Google Scholar 

  29. Rayment GE, Lyons DJ (2011) Soil chemical methods: Australasia, vol 3. CSIRO Publishing, Clayton

    Google Scholar 

  30. Cenis JL (1992) Rapid extraction of fungal DNA for PCR amplification. Nucleic Acids Res 20(9):2380. https://doi.org/10.1093/nar/20.9.2380

    Article  CAS  Google Scholar 

  31. White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press Inc, New York, pp 315–322

    Google Scholar 

  32. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  33. Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 35(6):1547–1549

    Article  CAS  Google Scholar 

  34. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797. https://doi.org/10.1093/nar/gkh340

    Article  CAS  Google Scholar 

  35. Selbmann L, de Hoog GS, Mazzaglia A, Friedmann EI, Onofri S (2005) Fungi at the edge of life: cryptoendolithic black fungi from Antarctic desert. Stud Mycol 51:1–32

    Google Scholar 

  36. Zucconi L, Selbmann L, Buzzini P, Turchetti B, Guglielmin M, Frisvad JC, Onofri S (2012) Searching for eukaryotic life preserved in Antarctic permafrost. Polar Biol 35(5):749–757. https://doi.org/10.1007/s00300-011-1119-6

    Article  Google Scholar 

  37. Baker BJ, Lutz MA, Dawson SC, Bond PL, Banfield JF (2004) Metabolically active eukaryotic communities in extremely acidic mine drainage. Appl Environ Microbiol 70(10):6264–6271. https://doi.org/10.1128/AEM.70.10.6264-6271.2004

    Article  CAS  Google Scholar 

  38. Nagai K (1998) Studies on the distribution of alkalophilic and alkali-tolerant soil fungi II: fungal flora in two limestone caves in Japan. Mycoscience 39(3):293–298. https://doi.org/10.1007/bf02464011

    Article  CAS  Google Scholar 

  39. Gunde-Cimerman N, Zalar P, Hoog S, Plemenitas A (2000) Hypersaline waters in salterns—Natural ecological niches for halophilic black yeasts. FEMS Microbiol Ecol 32(3):235–240. https://doi.org/10.1111/j.1574-6941.2000.tb00716.x

    Article  CAS  Google Scholar 

  40. Coleine C, Stajich JE, De Los RA, Selbmann L (2021) Beyond the extremes: rocks as ultimate refuge for fungi in drylands. Mycologia 113(1):108–133. https://doi.org/10.1080/00275514.2020.1816761

    Article  Google Scholar 

  41. Liu C-H, Huang X, Xie T-N, Duan N, Xue Y-R, Zhao T-X, Lever MA, Hinrichs K-U, Inagaki F (2017) Exploration of cultivable fungal communities in deep coal-bearing sediments from∼ 1.3 to 2.5 km below the ocean floor. Environ Microbiol 19(2):803–818. https://doi.org/10.1111/1462-2920.13653

    Article  CAS  Google Scholar 

  42. Elhottová D, Krištůfek V, Frouz J, Nováková A, Chroňáková A (2006) Screening for microbial markers in Miocene sediment exposed during open-cast brown coal mining. Antonie Leeuwenhoek 89:459–463. https://doi.org/10.1007/s10482-005-9044-8

    Article  Google Scholar 

  43. Sharma A, Sumbali G (2017) Prevalence of fungal flora in the acidic environment of anthracite and lignite coal mines of Jammu. Bull Environ Pharmacol Life Sci 6:86–93

    Google Scholar 

  44. de Goes KCGP, da Silva JJ, Lovato GM, Iamanaka BT, Massi FP, Andrade DS (2017) Talaromyces sayulitensis, Acidiella bohemica and Penicillium citrinum in Brazilian oil shale by-products. Antonie Leeuwenhoek 110:1637–1646. https://doi.org/10.1007/s10482-017-0913-8

    Article  CAS  Google Scholar 

  45. Lawrey JD (1977) Soil fungal populations and soil respiration in habitats variously influenced by coal strip-mining. Environ Pollut 14(3):195–205. https://doi.org/10.1016/0013-9327(77)90119-7

    Article  CAS  Google Scholar 

  46. Fresquez PR, Aldon EF, Lindemann WC (1987) Diversity and composition of soil fungi associated with reclaimed coal mine spoils and soils. Proceedings of the American Society of Mining and Reclamation, pp 107–114

  47. Khan R, Gupta AK (2017) Screening and characterization of acid-producing fungi from different mine areas of Chhattisgarh region. KAVAKA 49:45–49

    Google Scholar 

  48. Tulsiyan RK, Sinha NK, Kumar V (2017) Isolation and identification of fungi from coal mines near Hazaribagh and their diversity study. J Cell Sci Apoptosis 1:1–3

    Google Scholar 

  49. Hujslová M, Kubátová A, Kostovčík M, Kolařík M (2013) Acidiella bohemica gen. et sp. nov. and Acidomyces spp. (Teratosphaeriaceae), the indigenous inhabitants of extremely acidic soils in Europe. Fungal Divers 58(1):33–45. https://doi.org/10.1007/s13225-012-0176-7

    Article  Google Scholar 

  50. Weil RR, Brady NC (2017) The soils around us. The nature and properties of soils, 14th edn. Pearson Prentice Hall, New Jersey and Ohio, pp 1–31

    Google Scholar 

  51. Castro-Silva MA, De Souza Lima AO, Gerchenski AV, Jaques DB, Rodrigues AL, De Souza PL, Rörig LR (2003) Heavy metal resistance of microorganisms isolated from coal mining environments of Santa Catarina. Braz J Microbiol 34:45–47. https://doi.org/10.1590/S1517-83822003000500015

    Article  Google Scholar 

  52. Fomina M, Burford EP, Gadd GM (2006) Fungal dissolution and transformation of minerals: significance for nutrient and metal mobility. In: Gadd GM (ed) Fungi in biogeochemical cycles. Cambridge University Press, Cambridge, p 236

    Chapter  Google Scholar 

  53. Gadd GM (2010) Metals minerals and microbes: geomicrobiology and bioremediation. Microbiology 156:609–643

    Article  CAS  Google Scholar 

  54. Bosecker K (1997) Bioleaching: metal solubilisation by microorganisms. FEMS Microbiol Rev 20(3–4):591–604. https://doi.org/10.1016/S0168-6445(97)00036-3

    Article  CAS  Google Scholar 

  55. Joshi PK, Swarup A, Maheshwari S, Kumar R, Singh N (2011) Bioremediation of heavy metals in liquid media through fungi isolated from contaminated sources. Indian J Microbiol 51(4):482–487. https://doi.org/10.1007/s12088-011-0110-9

    Article  CAS  Google Scholar 

  56. Fukuda T, Ishino Y, Ogawa A, Tsutsumi K, Morita H (2008) Cr(VI) reduction from contaminated soils by Aspergillus sp. N2 and Penicillium sp. N3 isolated from chromium deposits. J Gen Appl Microbiol 54(5):295–303. https://doi.org/10.2323/jgam.54.295

    Article  CAS  Google Scholar 

  57. Gadd GM, Mowll JL (1985) Copper uptake by yeast-like cells, hyphae and chlamydospores of Aureobasidium pullulans. Exp Mycol 9(3):230–240

    Article  CAS  Google Scholar 

  58. Cecchi G, Marescotti P, Di Piazza S, Zotti M (2017) Native fungi as metal remediators: Silver myco-accumulation from metal contaminated waste-rock dumps (Libiola Mine, Italy). J Environ Sci Health B 52(3):191–195. https://doi.org/10.1080/03601234.2017.1261549

    Article  CAS  Google Scholar 

  59. Jambhulkar HP, Kumar MS (2019) Eco-restoration approach for mine spoil overburden dump through biotechnological route. Environ Monit Assess 191(12):1–16. https://doi.org/10.1007/s10661-019-7873-6

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank the Department of Botany, Gauhati University for providing the research facilities that are supported by the DST-FIST and UGC-SAP. KNS is thankful to the CSIR, Govt. of India for the research fellowship (Award Ref. No. 09/059(0059)/2017-EMR-I). The authors also thank Coal India Ltd., Margherita for permission and logistic support to explore the mining sites for the microbiological study.

Funding

This research was funded by the Department of Biotechnology, Ministry of Science and Technology, Govt. of India (Sanction Order No. BT/408/NE/U-Excel/2013) and CSIR-HRDC, Govt. of India (Award Ref. No. 09/059(0059)-2017-EMR-I)

Author information

Authors and Affiliations

Authors

Contributions

DN conceptualized the research project. KNS conducted the experimental works. KNS drafted and DN finalized the manuscript.

Corresponding author

Correspondence to Diganta Narzary.

Ethics declarations

Conflict of interest

Authors declare no conflict of interests.

Ethical Approval

Not applicable.

Consent to Participate

Not applicable.

Consent for Publication

Both authors read the final manuscript and agreed to publish.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Deposition in repositories: Nucleotide sequences of nrDNA-ITS regions were submitted to the DNA Database of Japan (DDBJ) and the sequences are also accessible through the NCBI.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 72 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Singh, K.N., Narzary, D. Diversity and Heavy Metal Tolerance of Fungi Associated with Different Coal Overburden Strata of Tikak Colliery, Assam. Curr Microbiol 80, 72 (2023). https://doi.org/10.1007/s00284-022-03170-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00284-022-03170-3

Navigation