, Volume 23, Issue 4, pp 421–433 | Cite as

Exploring the piezotolerant/piezophilic microbial community and genomic basis of piezotolerance within the deep subsurface Deccan traps

  • Avishek Dutta
  • Logan M. Peoples
  • Abhishek Gupta
  • Douglas H. Bartlett
  • Pinaki SarEmail author
Original Paper


The deep biosphere is often characterized by multiple extreme physical–chemical conditions, of which pressure is an important parameter that influences life but remains less studied. This geomicrobiology study was designed to understand the response of a subterranean microbial community of the Deccan traps to high-pressure conditions and to elucidate their genomic properties. Groundwater from a deep basaltic aquifer of the Deccan traps was used to ascertain the community response to 25 MPa and 50 MPa pressure following enrichment in high-salt and low-salt organic media. Quantitative PCR data indicated a decrease in bacterial and archaeal cell numbers with increasing pressure. 16S rRNA gene sequencing displayed substantial changes in the microbial community in which Acidovorax appeared to be the most dominant genus in the low-salt medium and Microbacteriaceae emerged as the major family in the high-salt medium under both pressure conditions. Genes present in metagenome-associated genomes which have previously been associated with piezotolerance include those related to nutrient uptake and extracytoplasmic stress (omp, rseC), protein folding and unfolding (dnaK, groEL and others), and DNA repair mechanisms (mutT, uvr and others). We hypothesize that these genes facilitate tolerance to high pressure by certain groups of microbes residing in subsurface Deccan traps.


Piezotolerant/piezophilic microbes Terrestrial deep biosphere Pressure adaptation Deccan traps 



This work was supported by the Ministry of Earth Sciences, India (Project ID: MoES/P.O.(Seismo)/1(181)/2013). We thank the Director and all the investigators and participants from CSIR-National Geophysical Research Institute, Hyderabad, engaged in the exploratory scientific drilling operations at the Koyna–Warna region of Deccan traps. We are grateful to Harsh Gupta (NGRI), Shailesh Nayak (MoES), B.K. Bansal (MoES) and Sukanta Roy (NGRI) for their unstinted support. Next generation sequencing facility created at PS’s laboratory was funded by the Indian Institute of Technology Kharagpur Challenge Grant (IIT/SRIC/BT/ODM/2015-16/141). The authors thankfully acknowledge the support received from Deep Carbon Observatory (DCO) for AD’s visit to Scripps Institution of Oceanography, UC San Diego and performing experiments related to high-pressure microbiology there. The authors acknowledge Prof Abhijit Mukherjee and Srimanti Dutta Gupta of School of Environmental Studies, IIT Kharagpur, for their help in geochemical analysis of the groundwater sample. AD gratefully acknowledges IIT Kharagpur for providing fellowship (IIT/ACAD (PGS&R)/F.II/2/14/BS/91R01). AG thanks the Department of Biotechnology, Government of India for providing fellowship under DBT-JRF category (DBT/2014/IITKH/113).

Supplementary material

792_2019_1094_MOESM1_ESM.pdf (156 kb)
Supplementary material 1 (PDF 155 kb)


  1. Aertsen A, Vanoirbeek K, De Spiegeleer P et al (2004) Heat shock protein-mediated resistance to high hydrostatic pressure in Escherichia coli. Appl Env Microbiol 70:2660–2666Google Scholar
  2. Ash K, Brown T, Watford T et al (2014) A comparison of the Caulobacter NA1000 and K31 genomes reveals extensive genome rearrangements and differences in metabolic potential. Open Biol 4:140128PubMedPubMedCentralGoogle Scholar
  3. Aziz RK, Bartels D, Best AA et al (2008) The RAST server: rapid annotations using subsystems technology. BMC Genom 9:75CrossRefGoogle Scholar
  4. Bankevich A, Nurk S, Antipov D et al (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477PubMedPubMedCentralGoogle Scholar
  5. Bartlett DH (1999) Microbial adaptations to the psychrosphere/piezosphere. J Mol Microbiol Biotechnol 1:93–100PubMedGoogle Scholar
  6. Bates ST, Berg-Lyons D, Caporaso JG et al (2011) Examining the global distribution of dominant archaeal populations in soil. ISME J 5:908–917PubMedGoogle Scholar
  7. Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336Google Scholar
  8. Colwell FS, D’Hondt S (2013) Nature and extent of the deep biosphere. Rev Miner Geochem 75:547–574Google Scholar
  9. Dick GJ, Anantharaman K, Baker BJ et al (2013) The microbiology of deep-sea hydrothermal vent plumes: ecological and biogeographic linkages to seafloor and water column habitats. Front Microbiol 4:124PubMedPubMedCentralGoogle Scholar
  10. Ding J, Zhang Y, Wang H et al (2017) Microbial community structure of deep-sea hydrothermal vents on the ultraslow spreading Southwest Indian ridge. Front Microbiol 8:1012PubMedPubMedCentralGoogle Scholar
  11. Duncan RA, Pyle DG (1988) Rapid eruption of the Deccan flood basalts at the Cretaceous/Tertiary boundary. Nature 333:841–843Google Scholar
  12. Dutta A, Dutta Gupta S, Gupta A et al (2018) Exploration of deep terrestrial subsurface microbiome in Late Cretaceous Deccan traps and underlying Archean basement, India. Sci Rep 8(1):17459PubMedPubMedCentralGoogle Scholar
  13. Grossart H-P, Gust G (2009) Hydrostatic pressure affects physiology and community structure of marine bacteria during settling to 4000 m: an experimental approach. Mar Ecol Prog Ser 390:97–104Google Scholar
  14. Gupta H, Rao NP, Roy S et al (2015) Investigations related to scientific deep drilling to study reservoir-triggered earthquakes at Koyna, India. Int J Earth Sci 104:1511–1522Google Scholar
  15. Gurevich A, Saveliev V, Vyahhi N, Tesler G (2013) QUAST: quality assessment tool for genome assemblies. Bioinformatics 29:1072–1075PubMedPubMedCentralGoogle Scholar
  16. Heberle H, Meirelles GV, da Silva FR et al (2015) InteractiVenn: a web-based tool for the analysis of sets through Venn diagrams. BMC Bioinform 16:169. CrossRefGoogle Scholar
  17. Jebbar M, Franzetti B, Girard E, Oger P (2015) Microbial diversity and adaptation to high hydrostatic pressure in deep-sea hydrothermal vents prokaryotes. Extremophiles 19:721–740PubMedGoogle Scholar
  18. Karatzas KAG, Valdramidis VP, Wells-Bennik MHJ (2005) Contingency locus in ctsR of Listeria monocytogenes Scott A: a strategy for occurrence of abundant piezotolerant isolates within clonal populations. Appl Environ Microbiol 71:8390–8396PubMedPubMedCentralGoogle Scholar
  19. Karatzas KAG, Zervos A, Tassou CC et al (2007) Piezotolerant small-colony variants with increased thermotolerance, antibiotic susceptibility, and low invasiveness in a clonal Staphylococcus aureus population. Appl Environ Microbiol 73:1873–1881PubMedPubMedCentralGoogle Scholar
  20. Keto-Timonen R, Hietala N, Palonen E et al (2016) Cold shock proteins: a minireview with special emphasis on Csp-family of enteropathogenic Yersinia. Front Microbiol 7:1151PubMedPubMedCentralGoogle Scholar
  21. Kieft TL (2016) Microbiology of the deep continental biosphere. Their world: a diversity of microbial environments. Springer, Cham, pp 225–249Google Scholar
  22. Lapidus A, Clum A, LaButti K et al (2011) Genomes of three methylotrophs from a single niche uncover genetic and metabolic divergence of Methylophilaceae. J Bacteriol 193(15):3757–3764PubMedPubMedCentralGoogle Scholar
  23. Lauro FM, Bartlett DH (2008) Prokaryotic lifestyles in deep sea habitats. Extremophiles 12:15–25. CrossRefPubMedGoogle Scholar
  24. Lin H-H, Liao Y-C (2016) Accurate binning of metagenomic contigs via automated clustering sequences using information of genomic signatures and marker genes. Sci Rep 6:24175PubMedPubMedCentralGoogle Scholar
  25. Marietou A, Bartlett DH (2014) Effects of high hydrostatic pressure on coastal bacterial community abundance and diversity. Appl Environ Microbiol 80:5992–6003PubMedPubMedCentralGoogle Scholar
  26. Meersman F, Daniel I, Bartlett DH et al (2013) High-pressure biochemistry and biophysics. Rev Mineral Geochem 75:607–648Google Scholar
  27. Miettinen H, Kietäväinen R, Sohlberg E et al (2015) Microbiome composition and geochemical characteristics of deep subsurface high-pressure environment,Pyhäsalmi mine Finland. Front Microbiol 6:1203PubMedPubMedCentralGoogle Scholar
  28. Misra S, Roy S, Bartakke V et al (2017) Fissures and fractures in the Koyna seismogenic zone, western India. J Geol Soc India 90:131–137Google Scholar
  29. Mukherjee S, Stamatis D, Bertsch J et al (2017) Genomes OnLine Database (GOLD) vol 6: data updates and feature enhancements. Nucleic Acids Res 45:D446–D456. CrossRefPubMedGoogle Scholar
  30. Mustakhimov I, Kalyuzhnaya MG, Lidstrom ME, Chistoserdova L (2013) Insights into denitrification in Methylotenera mobilis from denitrification pathway and methanol metabolism mutants. J Bacteriol 195:2207–2211PubMedPubMedCentralGoogle Scholar
  31. Nyyssönen M, Hultman J, Ahonen L et al (2014) Taxonomically and functionally diverse microbial communities in deep crystalline rocks of the Fennoscandian shield. ISME J 8:126–138PubMedGoogle Scholar
  32. Onstott TC, McGown DJ, Bakermans C et al (2009) Microbial communities in subpermafrost saline fracture water at the Lupin Au Mine, Nunavut, Canada. Microb Ecol 58:786–807PubMedGoogle Scholar
  33. Oosterkamp MJ, Veuskens T, Plugge CM et al (2011) Genome sequences of Alicycliphilus denitrificans strains BC and K601T. J Bacteriol 193:5028–5029PubMedPubMedCentralGoogle Scholar
  34. Parks DH, Imelfort M, Skennerton CT et al (2015) CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 25:1043–1055PubMedPubMedCentralGoogle Scholar
  35. Pedersen K (2012) Subterranean microbial populations metabolize hydrogen and acetate under in situ conditions in granitic groundwater at 450 m depth in the Äspö Hard Rock Laboratory, Sweden. FEMS Microbiol Ecol 81:217–229PubMedGoogle Scholar
  36. Peoples LM, Bartlett DH (2017) Ecogenomics of deep-ocean microbial bathytypes. Microbial ecology of extreme environments. Springer, Cham, pp 7–50Google Scholar
  37. Poli A, Finore I, Romano I et al (2017) Microbial diversity in extreme marine habitats and their biomolecules. Microorganisms 5:25PubMedCentralGoogle Scholar
  38. Purkamo L, Bomberg M, Kietäväinen R et al (2016) Microbial co-occurrence patterns in deep Precambrian bedrock fracture fluids. Biogeosciences 13:3091–3108. CrossRefGoogle Scholar
  39. Purkamo L, Bomberg M, Nyyssönen M et al (2017) Response of deep subsurface microbial community to different carbon sources and electron acceptors during ~ 2 months incubation in microcosms. Front Microbiol 8:232PubMedPubMedCentralGoogle Scholar
  40. Quast C, Pruesse E, Yilmaz P et al (2012) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596PubMedPubMedCentralGoogle Scholar
  41. Rabinovitch-Deere CA, Parales RE (2012) Three types of taxis used in the response of Acidovorax sp. strain JS42 to 2-nitrotoluene. Appl Environ Microbiol 78:2306–2315PubMedPubMedCentralGoogle Scholar
  42. Rampelotto PH (2013) Extremophiles and extreme environments. Life 3:482–485PubMedPubMedCentralGoogle Scholar
  43. Reasoner DJ, Geldreich EE (1985) A new medium for the enumeration and subculture of bacteria from potable water. Appl Environ Microbiol 49:1–7PubMedPubMedCentralGoogle Scholar
  44. Schoene B, Samperton KM, Eddy MP et al (2015) U-Pb geochronology of the Deccan Traps and relation to the end-Cretaceous mass extinction. Science 347:182–184PubMedGoogle Scholar
  45. Scoma A, Boon N (2016) Osmotic stress confers enhanced cell integrity to hydrostatic pressure but impairs growth in Alcanivorax borkumensis SK2. Front Microbiol 7:729PubMedPubMedCentralGoogle Scholar
  46. Simonato F, Campanaro S, Lauro FM et al (2006) Piezophilic adaptation: a genomic point of view. J Biotechnol 126:11–25PubMedGoogle Scholar
  47. Stoddard SF, Smith BJ, Hein R et al (2015) rrn DB: improved tools for interpreting rRNA gene abundance in bacteria and archaea and a new foundation for future development. Nucleic Acids Res 43:D593–D598PubMedGoogle Scholar
  48. Subbarao KV, Courtillot V (2017) Deccan Basalts in and around Koyna–Warna region, Maharashtra: some reflections. J Geol Soc India 90:653–662Google Scholar
  49. Tanaka T, Burgess J, Wright P (2001) High-pressure adaptation by salt stress in a moderately halophilic bacterium obtained from open seawater. Appl Microbiol Biotechnol 57:200–204PubMedGoogle Scholar
  50. Vezzi A, Campanaro S, D’angelo M et al (2005) Life at depth: photobacterium profundum genome sequence and expression analysis. Science 307:1459–1461PubMedGoogle Scholar
  51. Wang Y (2002) The function of OmpA in Escherichia coli. Biochem Biophys Res Commun 292:396–401PubMedGoogle Scholar
  52. Wang F, Wang J, Jian H et al (2008) Environmental adaptation: genomic analysis of the piezotolerant and psychrotolerant deep-sea iron reducing bacterium Shewanella piezotolerans WP3. PLoS One 3:e1937PubMedPubMedCentralGoogle Scholar
  53. Wu X, Holmfeldt K, Hubalek V et al (2015) Microbial metagenomes from three aquifers in the Fennoscandian shield terrestrial deep biosphere reveal metabolic partitioning among populations. ISME J 10:1192PubMedPubMedCentralGoogle Scholar
  54. Yang X-W, Jian H-H, Wang F-P (2015) pSW2, a novel low-temperature-inducible gene expression vector based on a filamentous phage of the deep-sea bacterium Shewanella piezotolerans WP3. Appl Environ Microbiol 81:5519–5526PubMedPubMedCentralGoogle Scholar
  55. Yayanos AA (1995) Microbiology to 10,500 meters in the deep sea. Annu Rev Microbiol 49:777–805PubMedGoogle Scholar
  56. ZoBell CE (1941) Studies on marine bacteria. I. The cultural requirements of heterotrophic aerobes. J Mar Res 4:41–75Google Scholar

Copyright information

© Springer Japan KK, part of Springer Nature 2019

Authors and Affiliations

  • Avishek Dutta
    • 1
    • 2
  • Logan M. Peoples
    • 3
  • Abhishek Gupta
    • 1
  • Douglas H. Bartlett
    • 3
  • Pinaki Sar
    • 1
    Email author
  1. 1.Environmental Microbiology and Genomics Laboratory, Department of BiotechnologyIndian Institute of Technology KharagpurKharagpurIndia
  2. 2.School of BioscienceIndian Institute of Technology KharagpurKharagpurIndia
  3. 3.Marine Biology Research Division, Scripps Institution of OceanographyUniversity of California San DiegoSan DiegoUSA

Personalised recommendations