Skip to main content

Advertisement

Log in

Thermoplasmata and Nitrososphaeria as dominant archaeal members in acid mine drainage sediment of Malanjkhand Copper Project, India

  • Short Communication
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Acid mine drainage (AMD) harbors all three life forms in spite of its toxic and hazardous nature. In comparison to bacterial diversity, an in-depth understanding of the archaeal diversity in AMD and their ecological significance remain less explored. Archaeal populations are known to play significant roles in various biogeochemical cycles within the AMD ecosystem, and it is imperative to have a deeper understanding of archaeal diversity and their functional potential in AMD system. The present study is aimed to understand the archaeal diversity of an AMD sediment of Malanjkhand Copper Project, India through archaea specific V6 region of 16S rRNA gene amplicon sequencing. Geochemical data confirmed the acidic, toxic, heavy metal-rich nature of the sample. Archaea specific V6-16S rRNA gene amplicon data showed a predominance of Thermoplasmata (BSLdp215, uncultured Thermoplasmata, and Thermoplasmataceae) and Nitrososphaeria (Nitrosotaleaceae) members constituting ~ 95% of the archaeal community. Uncultured members of Bathyarchaeia, Group 1.1c, Hydrothermarchaeota, and Methanomassiliicoccales along with Methanobacteriaceae, Methanocellaceae, Haloferaceae, Methanosaetaceae, and Methanoregulaceae constituted the part of rare taxa. Analysis of sequence reads indicated that apart from their close ecological relevance, members of the Thermoplasmata present in Malanjkhand AMD were mostly involved in chemoheterotrophy, Fe/S redox cycling, and with heavy metal resistance, while the Nitrososphaeria members were responsible for ammonia oxidation and fixation of HCO3 through 3-hydroxypropionate/4-hydroxybutyrate cycle at low pH and oligotrophic environment which subsequently played an important role in nitrification process in AMD sediment. Overall, the present study elucidated the biogeochemical significance of archaeal populations inhabiting the toxic AMD environment.

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

Availability of data and materials

Amplicon sequences are submitted in NCBI under Bioproject number PRJNA479957. Accession numbers of the V6 and V4 regions of the sample were SRR12489631 and SRR7511722, respectively.

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(1):42–50

    PubMed  Google Scholar 

  • Baker BJ, Comolli LR, Dick GJ, Hauser LJ, Hyatt D, Dill BD, Land ML, VerBerkmoes NC, Hettich RL, Banfield JF (2010) Enigmatic, ultrasmall, uncultivated Archaea. Proc Natl Acad Sci USA 107(19):8806–8811

    CAS  PubMed  PubMed Central  Google Scholar 

  • Berg IA, Kockelkorn D, Buckel W, Fuchs G (2007) A 3-hydroxypropionate/4-hydroxybutyrate autotrophic carbon dioxide assimilation pathway in Archaea. Science 318(5857):1782–1786

    CAS  PubMed  Google Scholar 

  • Bomberg M, Mäkinen J, Salo M, Kinnunen P (2019) High diversity in iron cycling microbial communities in acidic, iron-rich water of the Pyhäsalmi Mine, Finland. Geofluids. https://doi.org/10.1155/2019/7401304

    Article  Google Scholar 

  • Brantner JS, Haake ZJ, Burwick JE, Menge CM, Hotchkiss ST, Senko JM (2014) Depth-dependent geochemical and microbiological gradients in Fe (III) deposits resulting from coal mine-derived acid mine drainage. Front Microbiol 5:215

    PubMed  PubMed Central  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336

    CAS  PubMed  PubMed Central  Google Scholar 

  • Carr SA, Jungbluth SP, Eloe-Fadrosh EA, Stepanauskas R, Woyke T, Rappé MS, Orcutt BN (2019) Carboxydotrophy potential of uncultivated Hydrothermarchaeota from the subseafloor crustal biosphere. ISME J 13(6):1457–1468

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cataldo DA, Maroon M, Schrader LE, Youngs VL (1975) Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid. Commun Soil Sci Plant Anal 6(1):71–80

    CAS  Google Scholar 

  • Chen LX, Huang LN, Méndez-García C, Kuang JL, Hua ZS, Liu J, Shu WS (2016) Microbial communities, processes and functions in acid mine drainage ecosystems. Curr Opin Biotechnol 38:150–158

    CAS  PubMed  Google Scholar 

  • Chesnin L, Yien CH (1951) Turbidimetric determination of available sulfates 1. Soil Sci Soc Am J 15(C):149–151

    CAS  Google Scholar 

  • Comolli LR, Banfield JF (2014) Inter-species interconnections in acid mine drainage microbial communities. Front Microbiol 5:367

    PubMed  PubMed Central  Google Scholar 

  • Dutta A, Sar P, Sarkar J, Dutta Gupta S, Gupta A, Bose H, Mukherjee A, Roy S (2019) Archaeal communities in deep terrestrial subsurface underneath the Deccan traps. India Front Microbiol 10:1362

    Google Scholar 

  • Golyshina OV, Lünsdorf H, Kublanov IV, Goldenstein NI, Hinrichs KU, Golyshin PN (2016a) The novel extremely acidophilic, cell-wall-deficient archaeon Cuniculiplasma divulgatum gen. nov., sp. nov. represents a new family, Cuniculiplasmataceae fam. nov, of the order Thermoplasmatales. Int J Syst Evol Micrbiol 66(Pt 1):332

    CAS  Google Scholar 

  • Golyshina OV, Kublanov IV, Tran H, Korzhenkov AA, Lünsdorf H, Nechitaylo TY, Gavrilov SN, Toshchakov SV, Golyshin PN (2016b) Biology of archaea from a novel family Cuniculiplasmataceae (Thermoplasmata) ubiquitous in hyperacidic environments. Sci Rep 6:39034

    CAS  PubMed  PubMed Central  Google Scholar 

  • Golyshina OV, Bargiela R, Golyshin PN (2019) Cuniculiplasmataceae, their ecogenomic and metabolic patterns, and interactions with ‘ARMAN.’ Extremophiles 23(1):1–7

    PubMed  Google Scholar 

  • Gupta A, Dutta A, Sarkar J, Panigrahi MK, Sar P (2018) Low-abundance members of the Firmicutes facilitate bioremediation of soil impacted by highly acidic mine drainage from the Malanjkhand copper project, India. Front Microbiol 9:2882

    PubMed  PubMed Central  Google Scholar 

  • Gupta A, Dutta A, Panigrahi MK, Sar P (2020) Geomicrobiology of mine tailings from malanjkhand copper project, India. Geomicrobiol J. https://doi.org/10.1080/01490451.2020.1817197

    Article  Google Scholar 

  • He H, Zhen Y, Mi T, Fu L, Yu Z (2018) Ammonia-oxidizing Archaea and Bacteria differentially contribute to ammonia oxidation in sediments from adjacent waters of Rushan Bay, China. Front Microbiol 9:116

    PubMed  PubMed Central  Google Scholar 

  • Huang LN, Kuang JL, Shu WS (2016) Microbial ecology and evolution in the acid mine drainage model system. Trends Microbiol 24(7):581–593

    CAS  PubMed  Google Scholar 

  • Johnson DB (2012) Geomicrobiology of extremely acidic subsurface environments. FEMS Microbiol Ecol 81(1):2–12

    CAS  PubMed  Google Scholar 

  • Justice NB, Pan C, Mueller R, Spaulding SE, Shah V, Sun CL, Yelton AP, Miller CS, Thomas BC, Shah M, VerBerkmoes N (2012) Heterotrophic archaea contribute to carbon cycling in low-pH, suboxic biofilm communities. Appl Environ Microbiol 78(23):8321–8330

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kato S, Nakano S, Kouduka M, Hirai M, Suzuki K, Itoh T, Ohkuma M, Suzuki Y (2019) Metabolic potential of as-yet-uncultured archaeal lineages of Candidatus Hydrothermarchaeota thriving in deep-sea metal sulfide deposits. Microbes Environ 34(3):293–303

    PubMed  PubMed Central  Google Scholar 

  • Kerou M, Alves RJ, Schleper C (2016) Nitrososphaeria. In: Whitman WB (ed) Bergey’s manual of systematics of archaea and bacteria. Wiley, Hoboken

    Google Scholar 

  • Korzhenkov AA, Toshchakov SV, Bargiela R, Gibbard H, Ferrer M, Teplyuk AV, Jones DL, Kublanov IV, Golyshin PN, Golyshina OV (2019) Archaea dominate the microbial community in an ecosystem with low-to-moderate temperature and extreme acidity. Microbiome 7(1):1–4

    Google Scholar 

  • Kuang JL, Huang LN, Chen LX, Hua ZS, Li SJ, Hu M, Li JT, Shu WS (2013) Contemporary environmental variation determines microbial diversity patterns in acid mine drainage. ISME J 7(5):1038–1050

    CAS  PubMed  Google Scholar 

  • Lazar CS, Baker BJ, Seitz KW, Teske AP (2017) Genomic reconstruction of multiple lineages of uncultured benthic archaea suggests distinct biogeochemical roles and ecological niches. ISME J 11(5):1118–1129

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lehtovirta-Morley LE (2018) Ammonia oxidation: ecology, physiology, biochemistry and why they must all come together. FEMS Microbiol Lett 365(9):fny058

    Google Scholar 

  • Louca S, Parfrey LW, Doebeli M (2016) Decoupling function and taxonomy in the global ocean microbiome. Science 353(6305):1272–1277

    CAS  PubMed  Google Scholar 

  • Massello FL, Chan CS, Chan KG, Goh KM, Donati E, Urbieta MS (2020) Meta-analysis of microbial communities in hot springs: recurrent taxa and complex shaping factors beyond pH and temperature. Microorganisms 8(6):906

    CAS  PubMed Central  Google Scholar 

  • Méndez-García C, Mesa V, Sprenger RR, Richter M, Diez MS, Solano J, Gallego JR (2014) Microbial stratification in low pH oxic and suboxic macroscopic growths along an acid mine drainage. ISME J 8(6):1259–1274

    PubMed  PubMed Central  Google Scholar 

  • Méndez-García C, Peláez AI, Mesa V, Sánchez J, Golyshina OV, Ferrer M (2015) Microbial diversity and metabolic networks in acid mine drainage habitats. Front Microbiol 6:475

    PubMed  PubMed Central  Google Scholar 

  • Mesa V, Gallego JL, González-Gil R, Lauga B, Sánchez J, Méndez-García C, Peláez AI (2017) Bacterial, archaeal, and eukaryotic diversity across distinct microhabitats in an acid mine drainage. Front Microbiol 8:1756

    PubMed  PubMed Central  Google Scholar 

  • Murphy JA, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36

    CAS  Google Scholar 

  • Pan J, Zhou Z, Béjà O, Cai M, Yang Y, Liu Y, Gu JD, Li M (2020) Genomic and transcriptomic evidence of light-sensing, porphyrin biosynthesis, Calvin-Benson-Bassham cycle, and urea production in Bathyarchaeota. Microbiome 8:1–2

    CAS  Google Scholar 

  • Qiu GZ, Wan MX, Qian L, Huang ZY, Liu K, Liu XD, Shi WY, Yang Y (2008) Archaeal diversity in acid mine drainage from Dabaoshan Mine, China. J Basic Microbiol 48(5):401–409

    CAS  PubMed  Google Scholar 

  • Ramanathan B, Boddicker AM, Roane TM, Mosier AC (2017) Nitrifier gene abundance and diversity in sediments impacted by acid mine drainage. Front Microbiol 8:2136

    PubMed  PubMed Central  Google Scholar 

  • Sanz JL, Rodríguez N, Díaz EE, Amils R (2011) Methanogenesis in the sediments of Rio Tinto, an extreme acidic river. Environ Microbiol 13(8):2336–2341

    CAS  PubMed  Google Scholar 

  • Volant A, Desoeuvre A, Casiot C, Lauga B, Delpoux S, Morin G, Personné JC, Héry M, Elbaz-Poulichet F, Bertin PN, Bruneel O (2012) Archaeal diversity: temporal variation in the arsenic-rich creek sediments of Carnoulès Mine, France. Extremophiles 16(4):645–657

    CAS  PubMed  Google Scholar 

  • Weber EB, Lehtovirta-Morley LE, Prosser JI, Gubry-Rangin C (2015) Ammonia oxidation is not required for growth of group 1.1 c soil Thaumarchaeota. FEMS Microbiol Ecol 91(3):fiv001

    PubMed  PubMed Central  Google Scholar 

  • Xiang X, Wang R, Wang H, Gong L, Man B, Xu Y (2017) Distribution of Bathyarchaeota communities across different terrestrial settings and their potential ecological functions. Sci Rep 7:45028

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Y, Yang LI, 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(10):3332–3342

    CAS  Google Scholar 

  • Yelton AP, Comolli LR, Justice NB, Castelle C, Denef VJ, Thomas BC, Banfield JF (2013) Comparative genomics in acid mine drainage biofilm communities reveals metabolic and structural differentiation of co-occurring archaea. BMC Genom 14(1):485

    CAS  Google Scholar 

  • Zhang LM, Hu HW, Shen JP, He JZ (2012) Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. ISME J 6(5):1032–1045

    CAS  PubMed  Google Scholar 

  • Zhou Z, Pan J, Wang F, Gu JD, Li M (2018) Bathyarchaeota: globally distributed metabolic generalists in anoxic environments. FEMS Microbiol Rev 42(5):639–655

    CAS  PubMed  Google Scholar 

  • Zou D, Pan J, Liu Z, Zhang C, Liu H, Li M (2020) The distribution of Bathyarchaeota in surface sediments of the Pearl river estuary along salinity gradient. Front Microbiol 11:285

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Authors would like to thank the Department of Biotechnology, Govt. of India for funding the project (Grant ID BT/PR7533/BCE/8/959/2013) and MCP authority for sample collection. Authors thank the IIT Kharagpur for the in-house NGS facility (Ion S5 platform) through SGBSI challenge grant (IIT/SRIC/BT/ODM/2015-16/141). AG thanks Department of Biotechnology Govt. of India for DBT-JRF fellowship (DBT/2014/IITKH/113). AS thanks IIT Kharagpur for the Fellowship.

Funding

Authors would like to thank the Department of Biotechnology, Govt. of India for funding the project (Grant ID BT/PR7533/BCE/8/959/2013). Authors thank the IIT Kharagpur for the in-house NGS facility (Ion S5 platform) through SGBSI challenge grant (IIT/SRIC/BT/ODM/2015-16/141).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Pinaki Sar.

Ethics declarations

Conflict of interest

Authors declare no conflict of interest.

Additional information

Communicated by Kristina Beblo-Vranesevic.

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file 1 (DOCX 345 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gupta, A., Saha, A. & Sar, P. Thermoplasmata and Nitrososphaeria as dominant archaeal members in acid mine drainage sediment of Malanjkhand Copper Project, India. Arch Microbiol 203, 1833–1841 (2021). https://doi.org/10.1007/s00203-020-02130-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-020-02130-4

Keywords

Navigation