Deep Biosphere: Microbiome of the Deep Terrestrial Subsurface

  • Pinaki Sar
  • Avishek Dutta
  • Himadri Bose
  • Sunanda Mandal
  • Sufia K. Kazy


Deep biosphere represents an unexplored realm of planetary life residing underneath the continental and oceanic crusts that constitutes majorly of prokaryotic life forms bacteria and archaea. Microbial communities which reside within various deep subsurface environments form a significant but largely unknown portion of the Earth’s biosphere. While the shallow aquifer and sedimentary rock microbiome might get access to the nutrient pool available above ground, deep subterranean habitats hosted by crystalline rocks are severely constrained by the availability of photosynthetically derived nutrients. Deep subsurface microbiome underneath the continental crusts not only showed variations based on their geographic locations but also with respect to the abundance of various microbial populations and their metabolic properties. It is estimated that the deep biosphere microorganisms represent the largest pool of carbon, nitrogen, and phosphorous and constitute a critical component of biogeochemical engine of our planet. The aphotic deep dark microbial realm that has evolved possibly billions of years ago has developed unique metabolic repertoire for their survival. The deep biosphere microbiome is considered to be a portion of planetary life with extraordinary life-supporting system that works beyond our notion about biological and physical constraints. Advancement of techniques in microbial ecology has enabled us to decipher deep subsurface microbiome which resides up to several kilometers below the surface using both cultivation-dependent and cultivation-independent techniques. In this chapter, we have summarized our understanding of the deep biosphere microbiome within terrestrial subsurface. Habitability of life within the deep subsurface has been discussed considering the major metabolic routes deployed by the microorganisms. Cultivation-dependent and cultivation-independent studies and their requirement and outcome from various exploratory researches have been documented. Techniques used for sampling the subsurface microbiome are discussed, highlighting the role of possible contamination during drilling and subsequent postcore extraction processes. Lastly, applications of deep subsurface microbiome research in achieving better sustainability and biotechnological innovations are discussed.


Deep biosphere Metabolic processes Metagenomics Enrichment Drilling process-contamination CO2 sequestration Waste repository Bioprospecting 


  1. Åhäll KI (2007) Final deposition of high-level nuclear waste in very deep boreholes. An evaluation based on recent research of bedrock conditions at great depths (No. MKG-R--2). Swedish NGO Office for Nuclear Waste Review (MKG)Google Scholar
  2. Baas-Becking LGM (1934) Geobiologie; of inleiding tot de milieukunde. WP Van Stockum & Zoon NVGoogle Scholar
  3. Basen M, Schut GJ, Nguyen DM, Lipscomb GL, Benn RA, Prybol CJ, Vaccaro BJ, Poole FL, Kelly RM, Adams MW (2014) Single gene insertion drives bioalcohol production by a thermophilic archaeon. Proc Natl Acad Sci U S A 111:17618–17623PubMedPubMedCentralCrossRefGoogle Scholar
  4. Bassham JA, Calvin M (1957) The path of carbon in photosynthesis. Prentice-Hall, Englewood Cliffs. 104 ppGoogle Scholar
  5. Beeman RE, Suflita JM (1989) Evaluation of deep subsurface sampling procedures using serendipitous microbial contaminants as tracer organisms. Geomicrobiol J 7:223–233CrossRefGoogle Scholar
  6. Benson SM, Cole DR (2008) CO2 sequestration in deep sedimentary formations. Elements 4:325–331CrossRefGoogle Scholar
  7. Beswick J (2008) Status of technology for deep borehole disposal. Report for NDA, Contract NP, 1185Google Scholar
  8. Bomberg M, Nyyssönen M, Pitkänen P, Lehtinen A, Itävaara M (2015). Active microbial communities inhabit sulphate-methane interphase in deep bedrock fracture fluids in Olkiluoto, Finland. Biomed Res Int.Google Scholar
  9. Borgonie G, Linage-Alvarez B, Ojo A, Shivambu S, Kuloyo O, Cason ED, Maphanga S, Vermeulen J-G, Litthauer D, Ralston CD (2015) Deep subsurface mine stalactites trap endemic fissure fluid Archaea, Bacteria, and Nematoda possibly originating from ancient seas. Front Microbiol 6:833PubMedPubMedCentralCrossRefGoogle Scholar
  10. Bouquet S, Gendrin A, Labregere D, Le Nir I, Dance T, Xu J, Cinar Y (2009) CO2CRC Otway Project, Australia: parameters influencing dynamic modelling of CO2 injection into a depleted gas reservoir. SPE Offshore Europe Oil & Gas Conference & Exhibition, AberdeenGoogle Scholar
  11. Brady PV, Arnold BW, Freeze GA, Swift PN, Bauer SJ, Kanney JL, Rechard RP, Stein JS (2009) Deep borehole disposal of high level radioactive waste, SAND2009-4401, Sandia National Laboratories, AlbuquerqueGoogle Scholar
  12. Brady PV, Arnold BW, Mackinnon RJ (2012). Deep borehole disposal of nuclear waste (No. SAND2014-18766PE). Sandia National Lab.(SNL-NM), Albuquerque, NM (United States)Google Scholar
  13. Cassan A, Kubas D, Beaulieu J-P, Dominik M, Horne K, Greenhill J, Wambsganss J, Menzies J, Williams A, Jørgensen UG (2012) One or more bound planets per Milky Way star from microlensing observations. Nature 481:167PubMedCrossRefGoogle Scholar
  14. Chapelle FH, Lovley D (1990) Rates of microbial metabolism in deep coastal plain aquifers. Appl Environ Microbiol 56:1865–1874PubMedPubMedCentralGoogle Scholar
  15. Chivian D, Brodie EL, Alm EJ, Culley DE, Dehal PS, DeSantis TZ, Gihring TM, Lapidus A, Lin L-H, Lowry SR (2008) Environmental genomics reveals a single-species ecosystem deep within Earth. Science 322:275–278PubMedCrossRefGoogle Scholar
  16. Coker JA (2016) Extremophiles and biotechnology: current uses and prospects. F1000Res. 5(F1000 Faculty Rev):396Google Scholar
  17. Coker BMO, Olumagin A (1995) Waste drilling-fluid-utilising microorganisms in a tropical mangrove swamp oilfield location. Bioresour Technol 53:211–215CrossRefGoogle Scholar
  18. Colman DR, Poudel S, Stamps BW, Boyd ES, Spear JR (2017) The deep, hot biosphere: twenty-five years of retrospection. Proc Natl Acad Sci U S A 114:6895–6903PubMedPubMedCentralCrossRefGoogle Scholar
  19. Colwell RR (1997) Microbial diversity: the importance of exploration and conservation. J Ind Microbiol Biotechnol 18:302–307PubMedCrossRefGoogle Scholar
  20. Colwell FS, D’Hondt S (2013) Nature and extent of the deep biosphere. Rev Mineral Geochem 75:547–574CrossRefGoogle Scholar
  21. Colwell FS, Onstott TC, Delwiche ME, Chandler D, Fredrickson JK, Yao Q-J, McKinley JP, Boone DR, Griffiths R, Phelps TJ (1997) Microorganisms from deep, high temperature sandstones: constraints on microbial colonization. FEMS Microbiol Rev 20:425–435CrossRefGoogle Scholar
  22. Cragg, BA, Parkes RJ, Fry JC, Herbert RA, Wimpenny JWT, Getliff JM.(1990) Bacterial biomass and activity profiles within deep sediment layers. In: Suess E, von Huene R (eds.) Proceedings of the Ocean Drilling Program, Scientific Results, Vol. 112. Ocean Drilling Program, College Station, TX, pp 607–619Google Scholar
  23. Cui M, Ma A, Qi H, Zhuang X, Zhuang G (2015) Anaerobic oxidation of methane: an “active” microbial process. Microbiology 4:1–11Google Scholar
  24. D’Hondt S, Jorgensen BB, Miller DJ, Batzke A, Blake R, Cragg BA, Cypionka H, Dickens GR, Ferdelman T, Hinrichs KU, Holm NG, Mitterer R, Spivack A, Wang G, Bekins B, Engelen B, Ford K, Gettemy G, Rutherford SD, Sass H, Skilbeck CG, Aiello IW, Guèrin G, House CH, Inagaki F, Meister P, Naehr T, Niitsuma S, Parkes RJ, Schippers A, Smith DC, Teske A, Wiegel J, Padilla CN, Acosta JL (2004) Distributions of microbial activities in deep subseafloor sediments. Science 306:2216–2221PubMedCrossRefGoogle Scholar
  25. Davidson MM, Silver BJ, Onstott TC, Moser DP, Gihring TM, Pratt LM, Boice EA, Sherwood Lollar B, Lippmann-Pipke J, Pfiffner SM, Kieft TL, Symore W, Ralston C (2011) Capture of planktonic microbial diversity in fractures by long-term monitoring of flowing boreholes, Evander Basin, South Africa. Geomicrobiol J 28:275–300CrossRefGoogle Scholar
  26. De Silva GPD, Ranjith PG, Perera MSA (2015) Geochemical aspects of CO2 sequestration in deep saline aquifers: a review. Fuel 155:128–143CrossRefGoogle Scholar
  27. Dong Y, Kumar CG, Chia N, Kim PJ, Miller PA, Price ND, Cann IK, Flynn TM, Sanford RA, Krapac IG, Locke RA (2014) Halomonas sulfidaeris-dominated microbial community inhabits a 1.8 km-deep subsurface Cambrian Sandstone reservoir. Environ Microbiol 16:1695–1708PubMedCrossRefGoogle Scholar
  28. Dutta A, Gupta A, Sar P (2018a) Comparative analysis of microbial diversity and possibilities of dispersal of microbial cells across different subterranean systems of Deccan traps. EGU 20:2018-3836-1,Google Scholar
  29. Dutta A, Dutta Gupta S, Gupta A, Sarkar J, Roy S, Mukherjee A, Sar P (2018b) Exploration of deep terrestrial subsurface microbiome in late cretaceous Deccan traps and underlying Archean basement, India. Sci Rep 8:17459Google Scholar
  30. Dziewit L, Pyzik A, Szuplewska M, Matlakowska R, Mielnicki S, Wibberg D, Schlüter A, Pühler A, Bartosik D (2015) Diversity and role of plasmids in adaptation of bacteria inhabiting the Lubin copper mine in Poland, an environment rich in heavy metals. Front Microbiol 6:152PubMedPubMedCentralGoogle Scholar
  31. Edwards KJ, Rogers DR, Wirsen CO, McCollom TM (2003) Isolation and characterization of novel psychrophilic, neutrophilic, Fe-oxidizing, chemolithoautotrophic α-and γ-Proteobacteria from the deep sea. Appl Environ Microbiol 69:2906–2913PubMedPubMedCentralCrossRefGoogle Scholar
  32. Edwards KJ, Becker K, Colwell F (2012) The deep, dark energy biosphere: intraterrestrial life on earth. Annu Rev Earth Planet Sci 40:551–568CrossRefGoogle Scholar
  33. Eisenlord SD, Zak DR, Upchurch RA (2012) Dispersal limitation and the assembly of soil Actinobacteria communities in a long-term chronosequence. Ecol Evol 2:538–549PubMedPubMedCentralCrossRefGoogle Scholar
  34. Erzinger J, Wiersberg T, Zimmer M (2006) Real-time mud gas logging and sampling during drilling. Geofluids 6:225–233Google Scholar
  35. Firoozabadi A, Myint PC (2010) Prospects for subsurface CO2 sequestration. AICHE J 56:1398–1405CrossRefGoogle Scholar
  36. Fredrickson JK, Balkwill DL (2006) Geomicrobial processes and biodiversity in the deep terrestrial subsurface. Geomicrobiol J 23:345–356CrossRefGoogle Scholar
  37. Friese A, Kallmeyer J, Axel Kitte J, Montaño Martínez I, Bijaksana S, Wagner D (2017) A simple and inexpensive technique for assessing contamination during drilling operations. Limnol Oceanogr Methods 15:200–211CrossRefGoogle Scholar
  38. Fry NK, Fredrickson JK, Fishbain S, Wagner M, Stahl DA (1997) Population structure of microbial communities associated with two deep, anaerobic, alkaline aquifers. Appl Environ Microbiol 63:1498–1504PubMedPubMedCentralGoogle Scholar
  39. Fry JC, Parkes RJ, Cragg BA, Weightman AJ, Webster G (2008) Prokaryotic biodiversity and activity in the deep subseafloor biosphere. FEMS Microbiol Ecol 66:181–196PubMedCrossRefGoogle Scholar
  40. Fukuda A, Hagiwara H, Ishimura T, Kouduka M, Ioka S, Amano Y, Tsunogai U, Suzuki Y, Mizuno T (2010) Geomicrobiological properties of ultra-deep granitic groundwater from the Mizunami underground research laboratory (MIU), Central Japan. Microb Ecol 60:214–225PubMedCrossRefGoogle Scholar
  41. Gascoyne S, Schippers A, Schwyn B, Poulain S, Sergeant C, Simonoff M, McKenzie J (2007) Microbial community analysis of Opalinus clay drill core samples from the Mont Terri underground research laboratory, Switzerland. Geomicrobiology J 24:1–17CrossRefGoogle Scholar
  42. Gihring TM, Moser DP, Lin L-H, Davidson M, Onstott TC, Morgan L, Milleson M, Kieft TL, Trimarco E, Balkwill DL (2006) The distribution of microbial taxa in the subsurface water of the Kalahari Shield, South Africa. Geomicrobiol J 23:415–430CrossRefGoogle Scholar
  43. Gniese C, Bombach P, Rakoczy J, Hoth N, Schlömann M, Richnow HH, Krüger M (2013) Relevance of deep-subsurface microbiology for underground gas storage and geothermal energy production. In: Schippers A, Glombitza F, Sand W (eds) Geobiotechnology II. Advances in Biochemical Engineering/Biotechnology. Springer, Berlin/Heidelberg, pp 95–121Google Scholar
  44. Gold T (1992) The deep, hot biosphere. Proc Natl Acad Sci U S A 89:6045–6049PubMedPubMedCentralCrossRefGoogle Scholar
  45. Green JL, Bohannan BJM, Whitaker RJ (2008) Microbial biogeography: from taxonomy to traits. Science 320:1039–1043PubMedCrossRefGoogle Scholar
  46. Haldeman DL, Amy PS, Russell CE, Jacobson R (1995) Comparison of drilling and mining as methods for obtaining microbiological samples from the deep subsurface. J Microbiol Methods 21:305–316CrossRefGoogle Scholar
  47. Hallbeck L, Pedersen K (2008) Characterization of microbial processes in deep aquifers of the Fennoscandian Shield. Appl Geochem 23:1796–1819CrossRefGoogle Scholar
  48. Hallbeck L, Pedersen K (2012) Culture-dependent comparison of microbial diversity in deep granitic groundwater from two sites considered for a Swedish final repository of spent nuclear fuel. FEMS Microbiol Ecol 81:66–77PubMedCrossRefGoogle Scholar
  49. Ham B, Choi B-Y, Chae G-T, Kirk MF, Kwon MJ (2017) Geochemical influence on microbial communities at CO2-leakage analog sites. Front Microbiol 8:2203PubMedPubMedCentralCrossRefGoogle Scholar
  50. Haveman SA, Pedersen K, Ruotsalainen P (1999) Distribution and metabolic diversity of microorganisms in deep igneous rock aquifers of Finland. Geomicrobiol J 16:277–294CrossRefGoogle Scholar
  51. Hernsdorf AW, Amano Y, Miyakawa K, Ise K, Suzuki Y, Anantharaman K, Probst A, Burstein D, Thomas BC, Banfield JF (2017) Potential for microbial H2 and metal transformations associated with novel bacteria and archaea in deep terrestrial subsurface sediments. ISME J 11:1915PubMedPubMedCentralCrossRefGoogle Scholar
  52. Hippel VD, Hayes P (2009) Deep borehole disposal of nuclear spent fuel and high level waste as a focus of regional East Asia nuclear fuel cycle cooperation. Nautilus Institute AustraliaGoogle Scholar
  53. Hoehler TM, Jørgensen BB (2013) Microbial life under extreme energy limitation. Nat Rev Microbiol 11:83–94PubMedCrossRefGoogle Scholar
  54. House CH, Cragg BA, Teske A, Party SS (2003) Drilling contamination tests during ODP Leg 201 using chemical and particulate tracers. In Proceedings of the Ocean Drilling Program, initial reports, College Station, TX: Ocean Drilling Program. 201:1–19Google Scholar
  55. Ijiri A, Inagaki F, Kubo Y, Adhikari RR, Hattori S, Hoshino T, Imachi H, Kawagucci S, Morono Y, Ohtomo Y, Ono S, Sakai S, Takai K, Toki T, Wang DT, Yoshinaga MY, Arnold GL, Ashi J, Case DH, Feseker T, Hinrichs KU, Ikegawa Y, Ikehara M, Kallmeyer J, Kumagai H, Lever MA, Morita S, Nakamura K, NakamuraY NM, Orphan VJ, Røy H, Schmidt F, Tani A, Tanikawa W, Terada T, Tomaru H, Tsuji T, Tsunogai U, Yamaguchi YT, Yoshida N (2018) Deep-biosphere methane production stimulated by geofluids in the Nankai accretionary complex. Sci Adv 4:4631CrossRefGoogle Scholar
  56. Inagaki F, Hinrichs KU, Kubo Y, Bowles MW, Heuer VB, Hong WL, Hoshino T, Ijiri A, Imachi H, Ito M, Kaneko M (2015) Exploring deep microbial life in coal-bearing sediment down to~ 2.5 km below the ocean floor. Science 349:420–424PubMedCrossRefGoogle Scholar
  57. Ino K, Konno U, Kouduka M, Hirota A, Togo YS, Fukuda A, Komatsu D, Tsunogai U, Tanabe AS, Yamamoto S (2016) Deep microbial life in high-quality granitic groundwater from geochemically and geographically distinct underground boreholes. Environ Microbiol Rep 8:285–294PubMedCrossRefGoogle Scholar
  58. Istok JD, Park M, Michalsen M, Spain AM, Krumholz LR, Liu C, McKinley J, Long P, Roden E, Peacock AD, Baldwin B (2010) A thermodynamically-based model for predicting microbial growth and community composition coupled to system geochemistry: application to uranium bioreduction. Jour of Contam Hydro 112:1–14CrossRefGoogle Scholar
  59. Itävaara M, Nyyssönen M, Kapanen A, Nousiainen A, Ahonen L, Kukkonen I (2011) Characterization of bacterial diversity to a depth of 1500 m in the Outokumpu deep borehole, Fennoscandian Shield. FEMS Microbiol Ecol 77:295–309PubMedCrossRefPubMedCentralGoogle Scholar
  60. Jannasch HW, Eimhjellen K, Farmanfarmalan A (1971) Microbial degradation of organic matter in the deep sea. Science 171:672–675PubMedCrossRefPubMedCentralGoogle Scholar
  61. Jørgensen SL, Zhao R (2016) Microbial inventory of deeply buried oceanic crust from a young ridge flank. Front Microbiol 7:820PubMedPubMedCentralCrossRefGoogle Scholar
  62. Joseph SJ, Hugenholtz P, Sangwan P, Osborne CA, Janssen PH (2003) Laboratory cultivation of widespread and previously uncultured soil Bacteria. Appl Environ Microbiol 69(12):7210–7215PubMedPubMedCentralCrossRefGoogle Scholar
  63. Jungbluth SP, Bowers RM, Lin H-T, Cowen JP, Rappé MS (2016) Novel microbial assemblages inhabiting crustal fluids within mid-ocean ridge flank subsurface basalt. ISME J 10:2033–2047PubMedPubMedCentralCrossRefGoogle Scholar
  64. Kallmeyer J, Mangelsdorf K, Cragg B, Horsfield B (2006) Techniques for contamination assessment during drilling for terrestrial subsurface sediments. Geomicrobiol J 23:227–239CrossRefGoogle Scholar
  65. Kallmeyer J, Pockalny R, Adhikari RR, Smith DC, D’Hondt S (2012) Global distribution of microbial abundance and biomass in subseafloor sediment. Proc Natl Acad Sci U S A 109:16213–16216PubMedPubMedCentralCrossRefGoogle Scholar
  66. Kelly LC, Cockell CS, Piceno YM, Andersen GL, Thorsteinsson T, Marteinsson V (2010) Bacterial diversity of weathered terrestrial Icelandic volcanic glasses. Microb Ecol 60:740–752PubMedCrossRefPubMedCentralGoogle Scholar
  67. Kelly LC, Cockell CS, Herrera-Belaroussi A, Piceno Y, Andersen G, DeSantis T, Brodie E, Thorsteinsson T, Marteinsson V, Poly F (2011) Bacterial diversity of terrestrial crystalline volcanic rocks, Iceland. Microb Ecol 62:69–79PubMedCrossRefPubMedCentralGoogle Scholar
  68. Kelly LC, Cockell CS, Thorsteinsson T, Marteinsson V, Stevenson J (2014) Pioneer microbial communities of the Fimmvörðuháls lava flow, Eyjafjallajökull, Iceland. Microb Ecol 68:504–518PubMedCrossRefPubMedCentralGoogle Scholar
  69. Kieft TL (2010) Sampling the deep sub-surface using drilling and coring techniques. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, Heidelberg, pp 3427–3441CrossRefGoogle Scholar
  70. Kieft TL (2016) Microbiology of the deep continental biosphere. In: Hurst CJ (ed) Their world: a diversity of microbial environments. Springer, Cham, pp 225–249CrossRefGoogle Scholar
  71. Kieft TL, McCuddy SM, Onstott TC, Davidson M, Lin L-H, Mislowack B, Pratt L, Boice E, Lollar BS, Lippmann-Pipke J (2005) Geochemically generated, energy-rich substrates and indigenous microorganisms in deep, ancient groundwater. Geomicrobiol J 22:325–335CrossRefGoogle Scholar
  72. Kieft TL, Phelps TJ, Fredrickson JK (2007) Drilling, coring, and sampling subsurface environments. In: Hurst CJ (ed) Manual of environmental microbiology, 3rd edn. ASM Press, Washington, DC, pp 799–817Google Scholar
  73. Knoll AH (2003a) The geological consequences of evolution. Geobiology 1:3–14CrossRefGoogle Scholar
  74. Knoll AH (2003b) Life on a young planet: the first three billion years of evolution on Earth. Princeton University Press, Princeton/Oxford, p 277Google Scholar
  75. Kotelnikova S, Pedersen K (1997) Evidence for methanogenic Archaea and homoacetogenic Bacteria in deep granitic rock aquifers. FEMS Microbiol Rev 20:339–349CrossRefGoogle Scholar
  76. Labonté JM, Lever MA, Edwards KJ, Orcutt BN (2017) Influence of igneous basement on deep sediment microbial diversity on the eastern Juan de Fuca ridge flank. Front Microbiol 8:1434PubMedPubMedCentralCrossRefGoogle Scholar
  77. Lau MCY, Cameron C, Magnabosco C, Brown CT, Schilkey F, Grim S, Hendrickson S, Pullin M, Sherwood Lollar B, van Heerden E (2014) Phylogeny and phylogeography of functional genes shared among seven terrestrial subsurface metagenomes reveal N-cycling and microbial evolutionary relationships. Front Microbiol 5:531PubMedPubMedCentralCrossRefGoogle Scholar
  78. Lau MCY, Kieft TL, Kuloyo O, Linage-Alvarez B, van Heerden E, Lindsay MR, Magnabosco C, Wang W, Wiggins JB, Guo L, Perlman DH, Kyin S, Shwe HH, Harris RL, Oh Y, Yi MJ, Purtschert R, Slater GF, Ono S, Wei S, Li L, Sherwood Lollar B, Onstott TC (2016) An oligotrophic deep-subsurface community dependent on syntrophy is dominated by sulfur-driven autotrophic denitrifiers. Proc Natl Acad Sci 113:E7927–E7936. CrossRefPubMedGoogle Scholar
  79. Lazar CS, Stoll W, Lehmann R, Herrmann M, Schwab VF, Akob DM, Nawaz A, Wubet T, Buscot F, Totsche K-U (2017) Archaeal diversity and CO2 fixers in carbonate-/siliciclastic-rock groundwater ecosystems. Archaea 2017: . CrossRefGoogle Scholar
  80. Leandro T, Rodriguez N, Rojas P, Sanz JL, da Costa MS, Amils R (2018) Study of methanogenic enrichment cultures of rock cores from the deep subsurface of the Iberian Pyritic Belt. Heliyon 4:e00605PubMedPubMedCentralCrossRefGoogle Scholar
  81. Lehman RM, Roberto FF, Earley D, Bruhn DF, Brink SE, O’Connell SP, Delwiche ME, Colwell FS (2001) Attached and unattached bacterial communities in a 120-meter corehole in an acidic, crystalline rock aquifer. Appl Environ Microbiol 67:2095–2106PubMedPubMedCentralCrossRefGoogle Scholar
  82. Lehman RM, O’Connell SP, Banta A, Fredrickson JK, Reysenbach AL, Kieft TL, Colwell FS (2004) Microbiological comparison of core and groundwater samples collected from a fractured basalt aquifer with that of dialysis chambers incubated in situ. Geomicrobiol J 21:169–182CrossRefGoogle Scholar
  83. Li S, Yang X, Yang S, Zhu M, Wang X (2012) Technology prospecting on enzymes: application, marketing and engineering. Comput Struct Biotechnol J 2:e201209017PubMedPubMedCentralCrossRefGoogle Scholar
  84. Lin LH, Wang PL, Rumble D, Lippmann-Pipke J, Boice E, Pratt LM, Lollar BS, Brodie EL, Hazen TC, Andersen GL, DeSantis T, Moser DP, Kershaw D, Onstott TC (2006) Long-term sustainability of a high-energy, low-diversity crustal biome. Science 314:479–482PubMedCrossRefGoogle Scholar
  85. Littlechild JA (2015) Archaeal enzymes and applications in industrial biocatalysts. Archaea 2015:1–7CrossRefGoogle Scholar
  86. Liu J, Hua JS, Chen LX, Kuang JL, Li SJ, Shu WS, Huang LN (2014) Correlating microbial diversity patterns with geochemistry in an extreme and heterogeneous environment of mine tailings. Appl Environ Microbiol 80:3677–3686PubMedPubMedCentralCrossRefGoogle Scholar
  87. Lundberg KS, Shoemaker DD, Adams MW, Short JM, Sorge JA, Mathur EJ (1991) High-fidelity amplification using a thermostable DNA polymerase isolated from Pyrococcus furiosus. Gene 108:1–6PubMedCrossRefGoogle Scholar
  88. Lysnes K, Thorseth IH, Steinsbu BO, Øvreås L, Torsvik T, Pedersen RB (2004) Microbial community diversity in seafloor basalt from the Arctic spreading ridges. FEMS Microbiol Ecol 50:213–230PubMedCrossRefGoogle Scholar
  89. Madigan MT, Martinko JM, Parker J (2006) Brock biology of microorganisms, 11th edn. Prentice Hall, LondonGoogle Scholar
  90. Madsen EL (2008) Microbial diversity: who is here and how do we know? In: Environmental microbiology from genomes to biogeochemistry. Blackwell Publishing, Hoboken, pp 150–207Google Scholar
  91. Magnabosco C, Ryan K, Lau MCY, Kuloyo O, Lollar BS, Kieft TL, Van Heerden E, Onstott TC (2016) A metagenomic window into carbon metabolism at 3 km depth in Precambrian continental crust. ISME J 10:730PubMedCrossRefGoogle Scholar
  92. Masui N, Morono Y, Inagaki F (2008) Microbiological assessment of circulation mud fluids during the first operation of riser drilling by the deep-earth research vessel Chikyu. Geomicrobiol J 25:274–282CrossRefGoogle Scholar
  93. Mattila P, Korpela J, Tenkanen T, Pitkämem K (1991) Fidelity of DNA synthesis by the Thermococcus littoralis DNA polymerase–an extremely heat stable enzyme with proofreading activity. Nucleic Acids Res 19:4967–4973PubMedPubMedCentralCrossRefGoogle Scholar
  94. McMahon S, Parnell J (2013) Weighing the deep continental biosphere. FEMS Microbiol Ecol 87:113–120PubMedCrossRefGoogle Scholar
  95. Ménez B, Dupraz S, Gérard E, Guyot F, Rommevaux Jestin C, Libert M, Jullien M, Michel C, Delorme F, Battaglia-Brunet F (2007) Impact of the deep biosphere on CO2 storage performance. Geotechnologien Sci Rep 9:150–163Google Scholar
  96. Miettinen H, Kietäväinen R, Sohlberg E, Numminen M, Ahonen L, Itävaara M (2015) Microbiome composition and geochemical characteristics of deep subsurface high-pressure environment, Pyhäsalmi mine Finland. Front Microbiol 6Google Scholar
  97. Miller HM, Matter JM, Kelemen P, Ellison ET, Conrad ME, Fierer N, Ruchala T, Tominaga M, Templeton AS (2016) Modern water/rock reactions in Oman hyperalkaline peridotite aquifers and implications for microbial habitability. Geochim Cosmochim Acta 179:217–241CrossRefGoogle Scholar
  98. Mills CT, Amano Y, Slater GF, Dias RF, Iwatsuki T, Mandernack KW (2010) Microbial carbon cycling in oligotrophic regional aquifers near the Tono Uranium Mine, Japan as inferred from δ13C and Δ14C values of in situ phospholipid fatty acids and carbon sources. Geochim Cosmochim Acta 74:3785–3805CrossRefGoogle Scholar
  99. Mishra M (2015) Microbial diversity: Its exploration and need of conservation. In: Kaushik G (eds.) Applied Environmental Biotechnology: Present Scenario and Future Trends. Springer, pp 43–58Google Scholar
  100. Miteva V, Burlingame C, Sowers T, Brenchley J (2014) Comparative evaluation of the indigenous microbial diversity vs. drilling fluid contaminants in the NEEM Greenland ice core. FEMS Microbiol Ecol 89:238–256PubMedCrossRefGoogle Scholar
  101. Momper L, Jungbluth SP, Lee MD, Amend JP (2017) Energy and carbon metabolisms in a deep terrestrial subsurface fluid microbial community. ISME J 11:2319PubMedPubMedCentralCrossRefGoogle Scholar
  102. Moser DP, Gihring TM, Brockman FJ, Fredrickson JK, Balkwill DL, Dollhopf ME, Lollar BS, Pratt LM, Boice E, Southam G, Wanger G, Baker BJ, Pfiffner SM, Lin L-H, Onstott TC (2005) Desulfotomaculum and Methanobacterium spp. dominate a 4-to 5- kilometer-deep fault. Appl Environ Microbiol 71:8773–8783PubMedPubMedCentralCrossRefGoogle Scholar
  103. Mu A, Boreham C, Leong HX, Haese R, Moreau JW (2014) Changes in the deep subsurface microbial biosphere resulting from a field-scale CO2 geosequestration experiment. Front Microbiol 5:209PubMedPubMedCentralCrossRefGoogle Scholar
  104. Nakagawa T, Hanada S, Maruyama A, Marumo K, Urabe T, Fukui M (2002) Distribution and diversity of thermophilic sulfate-reducing bacteria within a Cu-Pb-Zn mine (Toyoha, Japan). FEMS Microbiol Ecol 41:199–209PubMedCrossRefGoogle Scholar
  105. Nealson KH, Inagaki F, Takai K (2005) Hydrogen-driven subsurface lithoautotrophic microbial ecosystems (SLiMEs): do they exist and why should we care? Trends Microbiol 13:405–410PubMedCrossRefGoogle Scholar
  106. Newby DT, Reed DW, Petzke LM, Igoe AL, Delwiche ME, Roberto FF, McKinley JP, Whiticar MJ, Colwell FS (2004) Diversity of methanotroph communities in a basalt aquifer. FEMS Microbiol Ecol 48:333–344PubMedCrossRefGoogle Scholar
  107. Nyyssönen M, Bomberg M, Kapanen A, Nousiainen A, Pitkänen P, Itävaara M (2012) Methanogenic and sulphate-reducing microbial communities in deep groundwater of crystalline rock fractures in Olkiluoto, Finland. Geomicrobiol J 29:863–878CrossRefGoogle Scholar
  108. Nyyssönen M, Hultman J, Ahonen L, Kukkonen I, Paulin L, Laine P, Itävaara M, Auvinen P (2014) Taxonomically and functionally diverse microbial communities in deep crystalline rocks of the Fennoscandian shield. ISME J 8:126–138PubMedCrossRefGoogle Scholar
  109. O’Connell SP, Lehman RM, Snoeyenbos-West O, Winston VD, Cummings DE, Watwood ME, Colwell FS (2003) Detection of Euryarchaeota and Crenarchaeota in an oxic basalt aquifer. FEMS Microbiol Ecol 44:165–173PubMedCrossRefGoogle Scholar
  110. Onstott TC, Phelps TJ, Colwell FS, Ringelberg D, White DC, Boone DR (1998) Observations pertaining to the origin and ecology of microorganisms recovered from the deep subsurface of Taylorsville Bain, Virginia. Geomicrobiol J 15:353–385CrossRefGoogle Scholar
  111. Onstott TC, Moser DP, Pfiffner SM, Fredrickson JK, Brockman FJ, Phelps TJ, White DC, Peacock A, Balkwill D, Hoover R (2003) Indigenous and contaminant microbes in ultradeep mines. Environ Microbiol 5:1168–1191PubMedCrossRefGoogle Scholar
  112. Onstott TC, McGown DJ, Bakermans C, Ruskeeniemi T, Ahonen L, Telling J, Soffientino B, Pfiffner SM, Sherwood LB, Frape S, Stotler R, Johnson EJ, Vishnivetskaya TA, Rothmel R, Pratt LM (2009) Microbial communities in subpermafrost saline fracture water at the Lupin Au Mine, Nunavut, Canada. Microb Ecol 58:786–807PubMedCrossRefGoogle Scholar
  113. Osburn MR, LaRowe DE, Momper LM, Amend JP (2014) Chemolithotrophy in the continental deep subsurface: Sanford Underground Research Facility (SURF), USA. Front Microbiol 5:610PubMedPubMedCentralCrossRefGoogle Scholar
  114. Parkes RJ, Cragg BA, Bale SJ, Getlifff JM, Goodman K, Rochelle PA, Fry JC, Weightman AJ, Harvey SM (1994) Deep bacterial biosphere in Pacific Ocean sediments. Nature 371:410–413CrossRefGoogle Scholar
  115. Pedersen K (1999) Evidence for a hydrogen-driven, intraterrestrial biosphere in deep granitic rock aquifers. In: CR Bell, M Brylinsky & P Johnson-Green (eds.) Microb. Biosys.: New Frontiers. Proceedings of the 8th International Symposium on Microbial Ecology. Atlantic Canada Society for Microbial Ecology, Halifax, pp. 1–7Google Scholar
  116. Pedersen K, Ekendahl S (1990) Distribution and activity of bacteria in deep granitic groundwaters of southeastern Sweden. Microb Ecol 20:37–52PubMedCrossRefGoogle Scholar
  117. Pedersen H, Lomstein BA, Henry BT (1993) Evidence for bacterial urea production in marine sediments. FEMS Microbiol Ecol 12:51–59CrossRefGoogle Scholar
  118. Pedersen K, Hallbeck L, Arlinger J, Erlandson AC, Jahromi N (1997) Investigation of the potential for microbial contamination of deep granitic aquifers during drilling using 16S rRNA gene sequencing and culturing methods. J Microbiol Methods 30:179–192CrossRefGoogle Scholar
  119. Pedersen K, Arlinger J, Eriksson S, Hallbeck A, Hallbeck L, Johansson J (2008) Numbers, biomass and cultivable diversity of microbial populations relate to depth and borehole-specific conditions in groundwater from depths of 4–450 m in Olkiluoto, Finland. ISME J 2:760PubMedCrossRefGoogle Scholar
  120. Phelps TJ, Fliermans CB, Garland TR, Pfiffner SM, White DC (1989) Methods for recovery of deep terrestrial subsurface sediments for microbiological studies. J Microbiol Methods 9:267–279CrossRefGoogle Scholar
  121. Pikuta EV, Hoover RB, Tang J (2007) Microbial extremophiles at the limits of life. Crit Rev Microbiol 33:183–209PubMedCrossRefGoogle Scholar
  122. Podar M, Reysenbach AL (2006) New opportunities revealed by biotechnological explorations of extremophiles. Curr Opin Biotechnol 17:250–255PubMedCrossRefGoogle Scholar
  123. Prescott LM, Harley JP, Klein DA (2002) Microbial Nutrition. In: Microbiology, 5th edn. McGraw−Hill Companies, Boston, pp 96–111Google Scholar
  124. Purkamo L, Bomberg M, Nyyssönen M, Kukkonen I, Ahonen L, Kietäväinen R, Itävaara M (2013) Dissecting the deep biosphere: retrieving authentic microbial communities from packer-isolated deep crystalline bedrock fracture zones. FEMS Microbiol Ecol 85:324–337PubMedCrossRefGoogle Scholar
  125. Purkamo L, Bomberg M, Nyyssönen M, Kukkonen I, Ahonen L, Itävaara M (2015) Heterotrophic communities supplied by ancient organic carbon predominate in deep fennoscandian bedrock fluids. Microb Ecol 69:319–332. CrossRefPubMedGoogle Scholar
  126. Purkamo L, Bomberg M, Kietäväinen R, Salavirta H, Nyyssönen M, Nuppunen-Puputti M, Ahonen L, Kukkonen I, Itävaara M (2016) Microbial co-occurrence patterns in deep Precambrian bedrock fracture fluids. Biogeosciences 13:3091–3108. CrossRefGoogle Scholar
  127. Purkamo L, Bomberg M, Nyyssönen M, Ahonen L, Kukkonen I, Itävaara M (2017) Response of deep subsurface microbial community to different carbon sources and electron acceptors during ~2 months incubation in microcosms. Front Microbiol 8:232PubMedPubMedCentralCrossRefGoogle Scholar
  128. Purkamo L, Kietäväinen R, Miettinen H, Sohlberg E, Kukkonen I, Itävaara M, Bomberg M (2018) Diversity and functionality of archaeal, bacterial and fungal communities in deep Archaean bedrock groundwater. FEMS Microbiol Ecol 94. (In Press)Google Scholar
  129. Rajala P, Bomberg M (2017) Reactivation of deep subsurface microbial community in response to methane or methanol amendment. Front Microbiol 8:431PubMedPubMedCentralCrossRefGoogle Scholar
  130. Rajala P, Bomberg M, Kietäväinen R, Kukkonen I, Ahonen L, Nyyssönen M, Itävaara M (2015) Rapid reactivation of deep subsurface microbes in the presence of C-1 compounds. Microorganisms 3:17–33PubMedPubMedCentralCrossRefGoogle Scholar
  131. Ramette A, Tiedje JM (2007) Biogeography: an emerging cornerstone for understanding prokaryotic diversity, ecology, and evolution. Microb Ecol 53:197–207PubMedCrossRefPubMedCentralGoogle Scholar
  132. Rampelotto PH (2013) Extremophiles and extreme environments. Life 3:482–485PubMedPubMedCentralCrossRefGoogle Scholar
  133. Rastogi G, Stetler LD, Peyton BM, Sani RK (2009) Molecular analysis of prokaryotic diversity in the deep subsurface of the former Homestake gold mine, South Dakota, USA. J Microbiol 47:371–384PubMedCrossRefPubMedCentralGoogle Scholar
  134. Reese BK, Zinke LA, Sobol MS, LaRowe DE, Orcutt BN, Zhang X, Jaekel U, Wang F, Dittmar T, Defforey D, Tully B (2018) Nitrogen cycling of active bacteria within oligotrophic sediment of the Mid-Atlantic Ridge flank. Geomicrobiol J. Epub ahead of printCrossRefGoogle Scholar
  135. Reith F (2011) Life in the deep subsurface. Geology 39:287–288CrossRefGoogle Scholar
  136. Richards MA, Cassen V, Heavner BD, Ajami NE, Herrmann A, Simeonidis E, Price ND (2014) MediaDB: a database of microbial growth conditions in defined media. PLoS One 9:e103548PubMedPubMedCentralCrossRefGoogle Scholar
  137. Sahl JW, Schmidt R, Swanner ED, Mandernack KW, Templeton AS, Kieft TL, Smith RL, Sanford WE, Callaghan RL, Mitton JB, Spear JR (2008) Subsurface microbial diversity in deep-granitic fracture water in Colorado. Appl Environ Microbiol 74:143–152PubMedCrossRefGoogle Scholar
  138. Salter SJ, Cox MJ, Turek EM, Calus ST, Cookson WO, Moffatt MF, Turner P, Parkhill J, Loman NJ, Walker AW (2014) Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol 12:87PubMedPubMedCentralCrossRefGoogle Scholar
  139. Schütte UME, Abdo Z, Bent SJ, Shyu C, Williams CJ, Pierson JD, Forney LJ (2008) Advances in the use of terminal restriction fragment length polymorphism (T-RFLP) analysis of 16S rRNA genes to characterize microbial communities. Appl Microbiol Biotechnol 80:365–380PubMedCrossRefPubMedCentralGoogle Scholar
  140. Schwartz FW, Kim Y, Chae BG (2017) Deep borehole disposal of nuclear wastes: opportunities and challenges. J Nucl Fuel Cycle Waste Technol 15:301–312CrossRefGoogle Scholar
  141. Sheik CS, Reese BK, Twing KI, Sylvan JB, Grim SL, Schrenk MO, Sogin ML, Colwell F (2018) Identification and removal of contaminant sequences from ribosomal gene databases: lessons from the census of deep life. Front Microbiol 9:840PubMedPubMedCentralCrossRefGoogle Scholar
  142. Shimizu S, Akiyama M, Naganuma T, Fujioka M, Nako M, Ishijima Y (2007) Molecular characterization of microbial communities in deep coal seam groundwater of northern Japan. Geobiology 5:423–433CrossRefGoogle Scholar
  143. Smith DC, Spivack AJ, Fisk MR, Haveman SA, Staudigel H (2000) Tracer-based estimates of drilling-induced microbial contamination of deep sea crust. Geomicrobiol J 17:207–219CrossRefGoogle Scholar
  144. Spiegelman D, Whissell G, Greer CW (2005) A survey of the methods for the characterization of microbial consortia and communities. Can J Microbiol 51:355–386PubMedCrossRefPubMedCentralGoogle Scholar
  145. Staley JT, Konopka A (1985) Measurements of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats. Annu Rev Microbiol 39:321–346PubMedCrossRefPubMedCentralGoogle Scholar
  146. Stevens TO (1997) Lithoautotrophy in the subsurface. FEMS Microbiol Rev 20:327–337CrossRefGoogle Scholar
  147. Stevens TO, McKinley JP (1995) Lithoautotrophic microbial ecosystems in deep basalt aquifers. Science 270:450–455CrossRefGoogle Scholar
  148. Stevens TO, McKinley JP (2000) Abiotic controls on H2 production from Basalt – Water reactions and implications for aquifer biogeochemistry. Environ Sci Technol 34:826–831. CrossRefGoogle Scholar
  149. Stevens TO, McKinley JP, Fredrickson JK (1993) Bacteria associated with deep, alkaline, anaerobic groundwaters in Southeast Washington. Microb Ecol 25:35–50PubMedCrossRefPubMedCentralGoogle Scholar
  150. Stewart EJ (2012) Growing unculturable bacteria. J Bacteriol 194(16):4151–4160PubMedPubMedCentralCrossRefGoogle Scholar
  151. Struchtemeyer CG, Davis JP, Elshahed MS (2011) Influence of the drilling mud formulation process on the bacterial communities in thermogenic natural gas wells from the Barnett Shale. Appl Environ Microbiol 77:4744–4753PubMedPubMedCentralCrossRefGoogle Scholar
  152. Swanner E, Templeton A (2011) Potential for nitrogen fixation and nitrification in the granite-hosted subsurface at Henderson Mine, CO. Front Microbiol 2:254PubMedPubMedCentralCrossRefGoogle Scholar
  153. Takai KEN, Moser DP, DeFlaun M, Onstott TC, Fredrickson JK (2001) Archaeal diversity in waters from deep South African gold mines. Appl Environ Microbiol 67:5750–5760PubMedPubMedCentralCrossRefGoogle Scholar
  154. Templeton AS, Staudigel H, Tebo BM (2005) Diverse Mn (II)-oxidizing bacteria isolated from submarine basalts at Loihi Seamount. Geomicrobiol J 22:127–139CrossRefGoogle Scholar
  155. Thorseth IH, Torsvik T, Torsvik V, Daae FL, Pedersen RB (2001) Diversity of life in ocean floor basalt. Earth Planet Sci Lett 194:31–37CrossRefGoogle Scholar
  156. Timmers PHA, Welte CU, Koehorst JJ, Plugge CM, Jetten MSM, Stams AJM (2017) Reverse methanogenesis and respiration in methanotrophic archaea. Archaea 2017. CrossRefGoogle Scholar
  157. Tindall KR, Kunkel TA (1988) Fidelity of DNA synthesis by the Thermus aquaticus DNA polymerase. Biochemistry 27:6008–6013PubMedCrossRefGoogle Scholar
  158. Vanwonterghem I, Evans PN, Parks DH, Jensen PD, Woodcroft BJ, Hugenholtz P, Tyson GW (2016) Methylotrophic methanogenesis discovered in the archaeal phylum Verstraetearchaeota. Nat Microbiol 1:16170PubMedCrossRefGoogle Scholar
  159. Vartoukian SR, Palmer RM, Wade WG (2010) Strategies for culture of ‘unculturable’ bacteria. FEMS Microbiol Lett 309:1, 1–1, 7Google Scholar
  160. Vera M, Schippers A, Sand W (2013) Progress in bioleaching: fundamentals and mechanisms of bacterial metal sulfide oxidation–Part A. Appl Microbiol Biotechnol 97:7529–7541PubMedCrossRefGoogle Scholar
  161. Waldron PJ, Petsch ST, Martini AM, Nüsslein K (2007) Salinity constraints on subsurface archaeal diversity and methanogenesis in sedimentary rock rich in organic matter. Appl Environ Microbiol 73:4171–4179PubMedPubMedCentralCrossRefGoogle Scholar
  162. Whitman WB, Coleman DC, Wiebe WJ (1998) Prokaryotes: the unseen majority. Proc Natl Acad Sci U S A 95:6578–6583PubMedPubMedCentralCrossRefGoogle Scholar
  163. Wilkins MJ, Daly R, Mouser PJ, Trexler R, Wrighton KC, Sharma S, Cole DR, Biddle JF, Denis E, Fredrickson JK, Kieft TL (2014) Trends and future challenges in sampling the deep terrestrial biosphere. Front Microbiol 5:481PubMedPubMedCentralGoogle Scholar
  164. Wu X, Holmfeldt K, Hubalek V, Lundin D, Åström M, Bertilsson S, Dopson M (2015) Microbial metagenomes from three aquifers in the Fennoscandian shield terrestrial deep biosphere reveal metabolic partitioning among populations. ISME J 10:1192PubMedPubMedCentralCrossRefGoogle Scholar
  165. Yanagawa K, Nunoura T, McAllister S, Hirai M, Breuker A, Brandt L, House C, Moyer CL, Birrien JL, Aoike K, Sunamura M (2013) The first microbiological contamination assessment by deep-sea drilling and coring by the D/V Chikyu at the Iheya North hydrothermal field in the Mid-Okinawa Trough (IODP Expedition 331). Front Microbiol 4:327PubMedPubMedCentralCrossRefGoogle Scholar
  166. Zhang G, Dong H, Xu Z, Zhao D, Zhang C (2005) Microbial diversity in ultra-high-pressure rocks and fluids from the Chinese continental scientific drilling project in China. Appl Environ Microbiol 71:3213–3227PubMedPubMedCentralCrossRefGoogle Scholar
  167. Zhang G, Dong H, Jiang H, Xu Z, Eberl DD (2006) Unique microbial community in drilling fluids from Chinese continental scientific drilling. Geomicrobiol J 23:499–514CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Pinaki Sar
    • 1
  • Avishek Dutta
    • 1
  • Himadri Bose
    • 1
  • Sunanda Mandal
    • 2
  • Sufia K. Kazy
    • 2
  1. 1.Department of BiotechnologyIndian Institute of Technology KharagpurKharagpurIndia
  2. 2.Department of BiotechnologyNational Institute of Technology DurgapurDurgapurIndia

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