Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Anthropogenic impacts on the terrestrial subsurface biosphere

Abstract

The terrestrial subsurface is estimated to be the largest reservoir of microbial life on Earth. However, the subsurface also harbours economic, industrial and environmental resources, on which humans heavily rely, including diverse energy sources and formations for the storage of industrial waste and carbon dioxide for climate change mitigation. As a result of this anthropogenic activity, the subsurface landscape is transformed, including the subsurface biosphere. Through the creation of new environments and the introduction of substrates that fuel microbial life, the structure and function of subsurface microbiomes shift markedly. These microbial changes often have unintended effects on overall ecosystem function and are frequently challenging to manage from the surface of the Earth. In this Review, we highlight emerging research that investigates the impacts of anthropogenic activity on the terrestrial subsurface biosphere. We explore how humans alter the constraints on microbial life in the subsurface through drilling, mining, contamination and resource extraction, along with the resulting impacts of microorganisms on resource recovery and subsurface infrastructure.

This is a preview of subscription content, access via your institution

Access options

Buy this article

USD 39.95

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Physicochemical and microbial features of the subsurface biosphere.
Fig. 2: Impact of anthropogenic activity on the subsurface biosphere of the Earth.
Fig. 3: Microbial feedback and interactions in subsurface energy systems.
Fig. 4: Role of microorganisms in subsurface waste storage systems.
Fig. 5: Role of microorganisms in subsurface metal mobilization.

Similar content being viewed by others

References

  1. Whitman, W. B., Coleman, D. C. & Wiebe, W. J. Prokaryotes: the unseen majority. Proc. Natl Acad. Sci. USA 95, 6578–6583 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Gold, T. The deep, hot biosphere. Proc. Natl Acad. Sci. USA 89, 6045–6049 (1992). This study acknowledges the deep subsurface as an important biosphere on Earth.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Magnabosco, C. et al. The biomass and biodiversity of the continental subsurface. Nat. Geosci. 11, 707–717 (2018).

    Article  CAS  Google Scholar 

  4. Colman, D. R., Poudel, S., Stamps, B. W., Boyd, E. S. & Spear, J. R. The deep, hot biosphere: twenty-five years of retrospection. Proc. Natl Acad. Sci. USA 114, 6895–6903 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Onstott, T. C. et al. Indigenous and contaminant microbes in ultradeep mines. Environ. Microbiol. 5, 1168–1191 (2003).

    Article  CAS  PubMed  Google Scholar 

  6. Chivian, D. et al. Environmental genomics reveals a single-species ecosystem deep within Earth. Science 322, 275–278 (2008).

    Article  CAS  PubMed  Google Scholar 

  7. Lau, M. C. Y. et al. An oligotrophic deep-subsurface community dependent on syntrophy is dominated by sulfur-driven autotrophic denitrifiers. Proc. Natl Acad. Sci. USA 113, E7927–E7936 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Mouser, P. J., Borton, M., Darrah, T. H., Hartsock, A. & Wrighton, K. C. Hydraulic fracturing offers view of microbial life in the deep terrestrial subsurface. FEMS Microbiol. Ecol. https://doi.org/10.1093/femsec/fiw166 (2016).

    Article  PubMed  Google Scholar 

  9. Gieg, L. M., Jack, T. R. & Foght, J. M. Biological souring and mitigation in oil reservoirs. Appl. Microbiol. Biotechnol. 92, 263–282 (2011).

    Article  CAS  PubMed  Google Scholar 

  10. Procópio, L. Microbially induced corrosion impacts on the oil industry. Arch. Microbiol. 204, 138 (2022).

    Article  PubMed  Google Scholar 

  11. Colwell, F. S. & D’Hondt, S. Nature and extent of the deep biosphere. Rev. Mineral. Geochem. 75, 547–574 (2013).

    Article  CAS  Google Scholar 

  12. Kieft, T. L. in Their World: A Diversity of Microbial Environments (ed. Hurst, C. J.) 225–249 (Springer, 2016).

  13. Daly, R. A. et al. Microbial metabolisms in a 2.5-km-deep ecosystem created by hydraulic fracturing in shales. Nat. Microbiol. 1, 16146 (2016). This study reports the functional potential of metagenome-assembled genomes from hydraulic fracturing systems.

    Article  CAS  PubMed  Google Scholar 

  14. Oren, A. in The Prokaryotes: Prokaryotic Communities and Ecophysiology (eds Rosenberg, E. et al.) 421–440 (Springer, 2013).

  15. Flemming, H.-C. & Wuertz, S. Bacteria and archaea on Earth and their abundance in biofilms. Nat. Rev. Microbiol. 17, 247–260 (2019).

    Article  CAS  PubMed  Google Scholar 

  16. Skovhus, T. L., Eckert, R. B. & Rodrigues, E. Management and control of microbiologically influenced corrosion (MIC) in the oil and gas industry — overview and a North Sea case study. J. Biotech. 256, 31–45 (2017).

    Article  CAS  Google Scholar 

  17. Xu, D., Gu, T. & Lovley, D. R. Microbially mediated metal corrosion. Nat. Rev. Microbiol. 21, 705–718 (2023).

    Article  CAS  PubMed  Google Scholar 

  18. Vigneron, A., Head, I. M. & Tsesmetzis, N. Damage to offshore production facilities by corrosive microbial biofilms. Appl. Microbiol. Biotechnol. 102, 2525–2533 (2018).

    Article  CAS  PubMed  Google Scholar 

  19. Enning, D. & Garrelfs, J. Corrosion of iron by sulfate-reducing bacteria: new views of an old problem. Appl. Environ. Microbiol. 80, 1226–1236 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  20. Daniels, L., Belay, N., Rajagopal, B. S. & Weimer, P. J. Bacterial methanogenesis and growth from CO2 with elemental iron as the sole source of electrons. Science 237, 509–511 (1987).

    Article  CAS  PubMed  Google Scholar 

  21. Tang, H.-Y., Holmes, D. E., Ueki, T., Palacios, P. A. & Lovley, D. R. Iron corrosion via direct metal–microbe electron transfer. mBio 10, e00303–e00319 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Lovley, D. R. & Holmes, D. E. Electromicrobiology: the ecophysiology of phylogenetically diverse electroactive microorganisms. Nat. Rev. Microbiol. 20, 5–19 (2022).

    Article  CAS  PubMed  Google Scholar 

  23. Rajbongshi, A. & Gogoi, S. B. A review on anaerobic microorganisms isolated from oil reservoirs. World J. Microbiol. Biotechnol. 37, 111 (2021).

    Article  PubMed  Google Scholar 

  24. Olajire, A. A. A review of oilfield scale management technology for oil and gas production. J. Pet. Sci. 135, 723–737 (2015).

    Article  CAS  Google Scholar 

  25. Lerm, S. et al. Thermal effects on microbial composition and microbiologically induced corrosion and mineral precipitation affecting operation of a geothermal plant in a deep saline aquifer. Extremophiles 17, 311–327 (2013).

    Article  CAS  PubMed  Google Scholar 

  26. Reitenbach, V., Ganzer, L., Albrecht, D. & Hagemann, B. Influence of added hydrogen on underground gas storage: a review of key issues. Environ. Earth Sci. 73, 6927–6937 (2015).

    Article  CAS  Google Scholar 

  27. Cámara, M. et al. Economic significance of biofilms: a multidisciplinary and cross-sectoral challenge. NPJ Biofilms Microbiomes 8, 1–8 (2022).

    Article  Google Scholar 

  28. Kahrilas, G. A., Blotevogel, J., Corrin, E. R. & Borch, T. Downhole transformation of the hydraulic fracturing fluid biocide glutaraldehyde: implications for flowback and produced water quality. Environ. Sci. Technol. 50, 11414–11423 (2016).

    Article  CAS  PubMed  Google Scholar 

  29. Struchtemeyer, C. G., Morrison, M. D. & Elshahed, M. S. A critical assessment of the efficacy of biocides used during the hydraulic fracturing process in shale natural gas wells. Int. Biodeter. Biodegr. 71, 15–21 (2012).

    Article  CAS  Google Scholar 

  30. An, B. A., Shen, Y. & Voordouw, G. Control of sulfide production in high salinity bakken shale oil reservoirs by halophilic bacteria reducing nitrate to nitrite. Front. Microbiol. 8, 1164 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  31. Sharma, S. & Kumar, A. Recent advances in metallic corrosion inhibition: a review. J. Mol. Liq. 322, 114862 (2021).

    Article  CAS  Google Scholar 

  32. Youssef, N., Elshahed, M. S. & McInerney, M. J. in Advances in Applied Microbiology Vol. 66 (eds Laskin, A. I. et al.) 141–251 (Elsevier, 2009).

  33. Singh, A., Van Hamme, J. D., Kuhad, R. C., Parmar, N. & Ward, O. P. in Geomicrobiology and Biogeochemistry (eds Parmar, N. & Singh, A.) 153–173 (Springer, 2014).

  34. Wentzel, A., Lewin, A., Cervantes, F. J., Valla, S. & Kotlar, H. K. in Polyextremophiles: Life Under Multiple Forms of Stress (eds Seckbach, J. et al.) 439–466 (Springer, 2013).

  35. Wang, Q., Chen, X., Jha, A. N. & Rogers, H. Natural gas from shale formation — the evolution, evidences and challenges of shale gas revolution in United States. Renew. Sustain. Energy Rev. 30, 1–28 (2014).

    Article  Google Scholar 

  36. Tourtelot, H. A. Black shale — its deposition and diagenesis. Clays Clay Miner. 27, 313–321 (1979).

    Article  Google Scholar 

  37. Zhong, C. et al. Comparison of the hydraulic fracturing water cycle in China and North America: a critical review. Environ. Sci. Technol. 55, 7167–7185 (2021).

    Article  CAS  PubMed  Google Scholar 

  38. Hernandez-Becerra, N. et al. New microbiological insights from the Bowland shale highlight heterogeneity of the hydraulically fractured shale microbiome. Environ. Microbiome 18, 14 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  39. Amundson, K. K., Roux, S., Shelton, J. L. & Wilkins, M. J. Long-term CRISPR locus dynamics and stable host–virus co-existence in subsurface fractured shales. Curr. Biol. 33, 3125–3135 (2023).

    Article  CAS  PubMed  Google Scholar 

  40. Cluff, M. A., Hartsock, A., MacRae, J. D., Carter, K. & Mouser, P. J. Temporal changes in microbial ecology and geochemistry in produced water from hydraulically fractured Marcellus Shale gas wells. Environ. Sci. Technol. 48, 6508–6517 (2014).

    Article  CAS  PubMed  Google Scholar 

  41. Mohan, A. M., Bibby, K. J., Lipus, D., Hammack, R. W. & Gregory, K. B. The functional potential of microbial communities in hydraulic fracturing source water and produced water from natural gas extraction characterized by metagenomic sequencing. PLoS ONE 9, e107682 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  42. Murali Mohan, A. et al. Microbial community changes in hydraulic fracturing fluids and produced water from shale gas extraction. Environ. Sci. Technol. 47, 13141–13150 (2013).

    Article  CAS  PubMed  Google Scholar 

  43. Murali Mohan, A., Hartsock, A., Hammack, R. W., Vidic, R. D. & Gregory, K. B. Microbial communities in flowback water impoundments from hydraulic fracturing for recovery of shale gas. FEMS Microbiol. Ecol. 86, 567–580 (2013).

    Article  CAS  PubMed  Google Scholar 

  44. Nixon, S. L. et al. Genome-resolved metagenomics extends the environmental distribution of the Verrucomicrobia phylum to the deep terrestrial subsurface. mSphere 4, e00613–e00619 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Borton, M. A. et al. Comparative genomics and physiology of the genus Methanohalophilus, a prevalent methanogen in hydraulically fractured shale. Environ. Microbiol. 20, 4596–4611 (2018).

    Article  CAS  PubMed  Google Scholar 

  46. Booker, A. E. et al. Deep-subsurface pressure stimulates metabolic plasticity in shale-colonizing Halanaerobium spp. Appl. Environ. Microbiol. 85, e00018–e00019 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Booker, A. E. et al. Sulfide generation by dominant Halanaerobium microorganisms in hydraulically fractured shales. mSphere 2, e00257–e00317 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Daly, R. A. et al. Viruses control dominant bacteria colonizing the terrestrial deep biosphere after hydraulic fracturing. Nat. Microbiol. 4, 352–361 (2019).

    Article  CAS  PubMed  Google Scholar 

  49. Evans, M. V. et al. Members of Marinobacter and Arcobacter influence system biogeochemistry during early production of hydraulically fractured natural gas wells in the Appalachian basin. Front. Microbiol. 9, 2646 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  50. Borton, M. A. et al. Coupled laboratory and field investigations resolve microbial interactions that underpin persistence in hydraulically fractured shales. Proc. Natl Acad. Sci. USA 115, E6585–E6594 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Tinker, K., Lipus, D., Gardiner, J., Stuckman, M. & Gulliver, D. The microbial community and functional potential in the midland basin reveal a community dominated by both thiosulfate and sulfate-reducing microorganisms. Microbiol. Spectr. 10, e00049-22 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  52. Akob, D. M., Cozzarelli, I. M., Dunlap, D. S., Rowan, E. L. & Lorah, M. M. Organic and inorganic composition and microbiology of produced waters from Pennsylvania shale gas wells. J. Appl. Geochem. 60, 116–125 (2015).

    Article  CAS  Google Scholar 

  53. Liang, R. et al. Metabolic capability of a predominant Halanaerobium sp. in hydraulically fractured gas wells and its implication in pipeline corrosion. Front. Microbiol. 7, 988 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  54. Strong, L. C. et al. Biodegradation in waters from hydraulic fracturing: chemistry, microbiology, and engineering. J. Environ. Eng. 140, B4013001 (2014).

    Article  Google Scholar 

  55. Struchtemeyer, C. G. & Elshahed, M. S. Bacterial communities associated with hydraulic fracturing fluids in thermogenic natural gas wells in North Central Texas, USA. FEMS Microbiol. Ecol. 81, 13–25 (2012).

    Article  CAS  PubMed  Google Scholar 

  56. Shaffer, D. L. et al. Desalination and reuse of high-salinity shale gas produced water: drivers, technologies, and future directions. Environ. Sci. Technol. 47, 9569–9583 (2013).

    Article  CAS  PubMed  Google Scholar 

  57. Hull, N. M., Rosenblum, J. S., Robertson, C. E., Harris, J. K. & Linden, K. G. Succession of toxicity and microbiota in hydraulic fracturing flowback and produced water in the Denver–Julesburg Basin. Sci. Total. Environ. 644, 183–192 (2018).

    Article  CAS  PubMed  Google Scholar 

  58. Amundson, K. K. et al. Microbial colonization and persistence in deep fractured shales is guided by metabolic exchanges and viral predation. Microbiome 10, 5 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Oren, A. Thermodynamic limits to microbial life at high salt concentrations. Environ. Microbiol. 13, 1908–1923 (2011).

    Article  CAS  PubMed  Google Scholar 

  60. Kovač, A., Paranos, M. & Marciuš, D. Hydrogen in energy transition: a review. Int. J. Hydrog. Energy 46, 10016–10035 (2021).

    Article  Google Scholar 

  61. Milkov, A. V. Molecular hydrogen in surface and subsurface natural gases: abundance, origins and ideas for deliberate exploration. Earth-Sci. Rev. 230, 104063 (2022).

    Article  CAS  Google Scholar 

  62. Zivar, D., Kumar, S. & Foroozesh, J. Underground hydrogen storage: a comprehensive review. Int. J. Hydrog. Energy 46, 23436–23462 (2021).

    Article  CAS  Google Scholar 

  63. van der Roest, E., Snip, L., Fens, T. & van Wijk, A. Introducing power-to-H3: combining renewable electricity with heat, water and hydrogen production and storage in a neighbourhood. Appl. Energy 257, 114024 (2020).

    Article  Google Scholar 

  64. Götz, M. et al. Renewable power-to-gas: a technological and economic review. Renew. Energy 85, 1371–1390 (2016).

    Article  Google Scholar 

  65. Al-Shafi, M., Massarweh, O., Abushaikha, A. S. & Bicer, Y. A review on underground gas storage systems: natural gas, hydrogen and carbon sequestration. Energy Rep. 9, 6251–6266 (2023).

    Article  Google Scholar 

  66. Ranchou-Peyruse, M. et al. Microbial diversity under the influence of natural gas storage in a deep aquifer. Front. Microbiol. 12, 688929 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  67. Krevor, S. et al. Subsurface carbon dioxide and hydrogen storage for a sustainable energy future. Nat. Rev. Earth Environ. 4, 102–118 (2023).

    Article  CAS  Google Scholar 

  68. Dopffel, N., Jansen, S. & Gerritse, J. Microbial side effects of underground hydrogen storage — knowledge gaps, risks and opportunities for successful implementation. Int. J. Hydrog. Energy 46, 8594–8606 (2021).

    Article  CAS  Google Scholar 

  69. Greening, C. et al. Genomic and metagenomic surveys of hydrogenase distribution indicate H2 is a widely utilised energy source for microbial growth and survival. ISME J. 10, 761–777 (2016).

    Article  CAS  PubMed  Google Scholar 

  70. Li, S. et al. High diversity, abundance and expression of hydrogenases in groundwater. ISME Commun. 4, ycae023 (2024).

    Article  PubMed  PubMed Central  Google Scholar 

  71. Gregory, S., Barnett, M., Field, L. & Milodowski, A. Subsurface microbial hydrogen cycling: natural occurrence and implications for industry. Microorganisms 7, 53 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Dopffel, N. et al. Microbial hydrogen consumption leads to a significant pH increase under high-saline-conditions: implications for hydrogen storage in salt caverns. Sci. Rep. 13, 10564 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Heinemann, N. et al. Enabling large-scale hydrogen storage in porous media — the scientific challenges. Energy Environ. Sci. 14, 853–864 (2021).

    Article  CAS  Google Scholar 

  74. Heinemann, N. et al. Hydrogen storage in saline aquifers: the role of cushion gas for injection and production. Int. J. Hydrog. Energy 46, 39284–39296 (2021).

    Article  CAS  Google Scholar 

  75. Liu, N., Kovscek, A. R., Fernø, M. A. & Dopffel, N. Pore-scale study of microbial hydrogen consumption and wettability alteration during underground hydrogen storage. Front. Energy Res. https://doi.org/10.3389/fenrg.2023.1124621 (2023).

  76. Hellerschmied, C. et al. Hydrogen storage and geo-methanation in a depleted underground hydrocarbon reservoir. Nat. Energy 9, 333–344 (2024). This study reports a comprehensive field analysis of microbial communities in underground hydrogen storage and demonstrates the feasibility of this technology despite microbial interactions with hydrogen gas.

    Article  CAS  Google Scholar 

  77. Thaysen, E. M. et al. Estimating microbial growth and hydrogen consumption in hydrogen storage in porous media. Renew. Sustain. Energy Rev. 151, 111481 (2021).

    Article  CAS  Google Scholar 

  78. Buriánková, I. et al. Microbial communities in underground gas reservoirs offer promising biotechnological potential. Fermentation 8, 251 (2022).

    Article  Google Scholar 

  79. Yedinak, E. M. The curious case of geologic hydrogen: assessing its potential as a near-term clean energy source. Joule 6, 503–508 (2022).

    Article  Google Scholar 

  80. Chapelle, F. H. et al. A hydrogen-based subsurface microbial community dominated by methanogens. Nature 415, 312–315 (2002).

    Article  PubMed  Google Scholar 

  81. Strąpoć, D., Mastalerz, M., Eble, C. & Schimmelmann, A. Characterization of the origin of coalbed gases in southeastern Illinois Basin by compound-specific carbon and hydrogen stable isotope ratios. Org. Geochem. 38, 267–287 (2007).

    Article  Google Scholar 

  82. Strąpoć, D. et al. Biogeochemistry of microbial coal-bed methane. Annu. Rev. Earth Planet. Sci. 39, 617–656 (2011).

    Article  Google Scholar 

  83. Ritter, D. et al. Enhanced microbial coalbed methane generation: a review of research, commercial activity, and remaining challenges. Int. J. Coal Geol. 146, 28–41 (2015).

    Article  CAS  Google Scholar 

  84. McKay, L. J. et al. Activity-based, genome-resolved metagenomics uncovers key populations and pathways involved in subsurface conversions of coal to methane. ISME J. 16, 915–926 (2022). This study reports a cell sorting and activity labelling approach to identify active microbial populations that support methanogenesis within a coal seam.

    Article  CAS  PubMed  Google Scholar 

  85. Beckmann, S. et al. Long-term succession in a coal seam microbiome during in situ biostimulation of coalbed-methane generation. ISME J. 13, 632–650 (2019).

    Article  CAS  PubMed  Google Scholar 

  86. Mayumi, D. et al. Methane production from coal by a single methanogen. Science 354, 222–225 (2016).

    Article  CAS  PubMed  Google Scholar 

  87. Gniese, C. et al. in Geobiotechnology II: Energy Resources, Subsurface Technologies, Organic Pollutants and Mining Legal Principles (eds Schippers, A. et al.) 95–121 (Springer, 2014).

  88. Lund, J. W. & Toth, A. N. Direct utilization of geothermal energy 2020 worldwide review. Geothermics 90, 101915 (2021).

    Article  Google Scholar 

  89. Dinkel, E. et al. Groundwater circulation wells for geothermal use and their impact on groundwater quality. Geothermics 86, 101812 (2020).

    Article  Google Scholar 

  90. García-Gil, A. et al. Decreased waterborne pathogenic bacteria in an urban aquifer related to intense shallow geothermal exploitation. Sci. Total. Environ. 633, 765–775 (2018).

    Article  PubMed  Google Scholar 

  91. Bonte, M. et al. Impacts of shallow geothermal energy production on redox processes and microbial communities. Environ. Sci. Technol. 47, 14476–14484 (2013).

    Article  CAS  PubMed  Google Scholar 

  92. Lienen, T. et al. Effects of thermal energy storage on shallow aerobic aquifer systems: temporary increase in abundance and activity of sulfate-reducing and sulfur-oxidizing bacteria. Environ. Earth Sci. 76, 261 (2017). This study examines the effects of fluctuating temperature in geothermal systems on the microbial community, specifically sulfate-reducing and sulfur-oxidizing members.

    Article  Google Scholar 

  93. Griebler, C. et al. Potential impacts of geothermal energy use and storage of heat on groundwater quality, biodiversity, and ecosystem processes. Environ. Earth Sci. 75, 1391 (2016).

    Article  Google Scholar 

  94. Alawi, M. et al. Diversity of sulfate-reducing bacteria in a plant using deep geothermal energy. Grundwasser 16, 105–112 (2011).

    Article  Google Scholar 

  95. Matter, J. M. et al. Rapid carbon mineralization for permanent disposal of anthropogenic carbon dioxide emissions. Science 352, 1312–1314 (2016).

    Article  CAS  PubMed  Google Scholar 

  96. Gilfillan, S. M. V. et al. Solubility trapping in formation water as dominant CO2 sink in natural gas fields. Nature 458, 614–618 (2009).

    Article  CAS  PubMed  Google Scholar 

  97. Dillow, A. K., Dehghani, F., Hrkach, J. S., Foster, N. R. & Langer, R. Bacterial inactivation by using near- and supercritical carbon dioxide. Proc. Natl Acad. Sci. USA 96, 10344–10348 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Mitchell, A. C. et al. Resilience of planktonic and biofilm cultures to supercritical CO2. J. Supercrit. Fluids 47, 318–325 (2008).

    Article  CAS  Google Scholar 

  99. Mu, A., Boreham, C., Leong, H. X., Haese, R. & Moreau, J. W. Changes in the deep subsurface microbial biosphere resulting from a field-scale CO2 geosequestration experiment. Front. Microbiol. 5, 209 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  100. Mu, A., Thomas, B. C., Banfield, J. F. & Moreau, J. W. Subsurface carbon monoxide oxidation capacity revealed through genome-resolved metagenomics of a carboxydotroph. Environ. Microbiol. Rep. 12, 525–533 (2020).

    Article  CAS  PubMed  Google Scholar 

  101. Tyne, R. L. et al. Rapid microbial methanogenesis during CO2 storage in hydrocarbon reservoirs. Nature 600, 670–674 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Snæbjörnsdóttir, S. Ó. et al. Carbon dioxide storage through mineral carbonation. Nat. Rev. Earth Environ. 1, 90–102 (2020).

    Article  Google Scholar 

  103. Onstott, T. C. in Carbon Dioxide Capture for Storage in Deep Geologic Formations (ed. Thomas, D. C.) 1217–1249 (Elsevier Science, 2005).

  104. Trias, R. et al. High reactivity of deep biota under anthropogenic CO2 injection into basalt. Nat. Commun. 8, 1063 (2017). This study examines microbial responses to carbon dioxide injection into basalt formations, along with the biogeochemical processes that are likely to support microbial life in these engineered systems.

    Article  PubMed  PubMed Central  Google Scholar 

  105. Probst, A. J. et al. Differential depth distribution of microbial function and putative symbionts through sediment-hosted aquifers in the deep terrestrial subsurface. Nat. Microbiol. 3, 328–336 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. World Nuclear Association. Nuclear Power in the World Today. World Nuclear Association. https://world-nuclear.org/information-library/current-and-future-generation/nuclear-power-in-the-world-today.aspx (2024).

  107. Alwaeli, M. & Mannheim, V. Investigation into the current state of nuclear energy and nuclear waste management — a state-of-the-art review. Energies 15, 4275 (2022).

    Article  Google Scholar 

  108. Ruiz-Fresneda, M. A. et al. Impact of microbial processes on the safety of deep geological repositories for radioactive waste. Front. Microbiol. 14, 1134078 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  109. NEA. Management and Disposal of High-Level Radioactive Waste: Global Progress and Solutions. NEA No. 7532 (OECD, 2020).

  110. Hall, D. S., Behazin, M., Jeffrey Binns, W. & Keech, P. G. An evaluation of corrosion processes affecting copper-coated nuclear waste containers in a deep geological repository. Prog. Mater. Sci. 118, 100766 (2021).

    Article  CAS  Google Scholar 

  111. Bagnoud, A. et al. Reconstructing a hydrogen-driven microbial metabolic network in Opalinus clay rock. Nat. Commun. 7, 12770 (2016). This study of the Opalinus clay, a candidate for radioactive waste storage, used metagenomics and metaproteomics to reveal a hydrogen-driven microbial metabolic network.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Bagnoud, A. et al. A minimalistic microbial food web in an excavated deep subsurface clay rock. FEMS Microbiol. Ecol. https://doi.org/10.1093/femsec/fiv138 (2016).

    Article  PubMed  Google Scholar 

  113. Lopez-Fernandez, M., Matschiavelli, N. & Merroun, M. L. in The Microbiology of Nuclear Waste Disposal (eds Lloyd, J. R. & Cherkouk, A.) 137–155 (Elsevier, 2021).

  114. Burzan, N. et al. Growth and persistence of an aerobic microbial community in wyoming bentonite MX-80 despite anoxic in situ conditions. Front. Microbiol. 13, 858324 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  115. Haynes, H. M., Bailey, M. T. & Lloyd, J. R. Bentonite barrier materials and the control of microbial processes: safety case implications for the geological disposal of radioactive waste. Chem. Geol. 581, 120353 (2021).

    Article  CAS  Google Scholar 

  116. Lopez-Fernandez, M. et al. Bacterial diversity in bentonites, engineered barrier for deep geological disposal of radioactive wastes. Microb. Ecol. 70, 922–935 (2015).

    Article  CAS  PubMed  Google Scholar 

  117. Masurat, P., Eriksson, S. & Pedersen, K. Evidence of indigenous sulphate-reducing bacteria in commercial Wyoming bentonite MX-80. Appl. Clay Sci. 47, 51–57 (2010).

    Article  CAS  Google Scholar 

  118. Gregory, S. P., Mackie, J. R. M. & Barnett, M. J. Radioactive waste microbiology: predicting microbial survival and activity in changing extreme environments. FEMS Microbiol. Rev. https://doi.org/10.1093/femsre/fuae001 (2024).

    Article  PubMed  PubMed Central  Google Scholar 

  119. Jalique, D. R. et al. Culturability and diversity of microorganisms recovered from an eight-year old highly-compacted, saturated MX-80 Wyoming bentonite plug. Appl. Clay Sci. 126, 245–250 (2016).

    Article  CAS  Google Scholar 

  120. Stroes-Gascoyne, S., Hamon, C. J., Maak, P. & Russell, S. The effects of the physical properties of highly compacted smectitic clay (bentonite) on the culturability of indigenous microorganisms. Appl. Clay Sci. 47, 155–162 (2010).

    Article  CAS  Google Scholar 

  121. Ruiz-Fresneda, M. A. et al. Combined bioreduction and volatilization of SeVI by Stenotrophomonas bentonitica: formation of trigonal selenium nanorods and methylated species. Sci. Total. Environ. 858, 160030 (2023).

    Article  CAS  PubMed  Google Scholar 

  122. Ruiz-Fresneda, M. A. et al. Molecular binding of EuIII/CmIII by Stenotrophomonas bentonitica and its impact on the safety of future geodisposal of radioactive waste. Environ. Sci. Technol. 54, 15180–15190 (2020).

    Article  CAS  PubMed  Google Scholar 

  123. Pinel-Cabello, M. et al. Multisystem combined uranium resistance mechanisms and bioremediation potential of Stenotrophomonas bentonitica BII-R7: transcriptomics and microscopic study. J. Hazard. Mater. 403, 123858 (2021).

    Article  CAS  PubMed  Google Scholar 

  124. Kim, J. et al. Naturally occurring, microbially induced smectite-to-illite reaction. Geology 47, 535–539 (2019).

    Article  CAS  Google Scholar 

  125. Kim, J., Dong, H., Seabaugh, J., Newell, S. W. & Eberl, D. D. Role of microbes in the smectite-to-illite reaction. Science 303, 830–832 (2004).

    Article  CAS  PubMed  Google Scholar 

  126. Moll, H., Barkleit, A., Frost, L. & Raff, J. Curium(III) speciation in the presence of microbial cell wall components. Ecotoxicol. Environ. Saf. 227, 112887 (2021).

    Article  CAS  PubMed  Google Scholar 

  127. Moll, H. et al. Interactions of the Mont Terri opalinus clay isolate Sporomusa sp. MT-2.99 with curium(III) and europium(III). Geomicrobiol. J. 31, 682–696 (2014).

    Article  CAS  Google Scholar 

  128. Moll, H., Lütke, L., Barkleit, A. & Bernhard, G. Curium(III) speciation studies with cells of a groundwater strain of Pseudomonas fluorescens. Geomicrobiol. J. 30, 337–346 (2013).

    Article  CAS  Google Scholar 

  129. Rauschenbach, I. et al. Seleniivibrio woodruffii gen. nov., sp. nov., a selenate- and arsenate-respiring bacterium in the Deferribacteraceae. Int. J. Syst. Evol. Microbiol. 63, 3659–3665 (2013).

    Article  CAS  PubMed  Google Scholar 

  130. Rech, S. A. & Macy, J. M. The terminal reductases for selenate and nitrate respiration in Thauera selenatis are two distinct enzymes. J. Bacteriol. 174, 7316–7320 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Pinel-Cabello, M. et al. Delineation of cellular stages and identification of key proteins for reduction and biotransformation of Se(IV) by Stenotrophomonas bentonitica BII-R7. J. Hazard. Mater. 418, 126150 (2021).

    Article  CAS  PubMed  Google Scholar 

  132. Abascal, E., Gómez-Coma, L., Ortiz, I. & Ortiz, A. Global diagnosis of nitrate pollution in groundwater and review of removal technologies. Sci. Total. Environ. 810, 152233 (2022).

    Article  CAS  PubMed  Google Scholar 

  133. Burow, K. R., Nolan, B. T., Rupert, M. G. & Dubrovsky, N. M. Nitrate in groundwater of the United States, 1991−2003. Environ. Sci. Technol. 44, 4988–4997 (2010).

    Article  CAS  PubMed  Google Scholar 

  134. Nolan, J. & Weber, K. A. Natural uranium contamination in major U.S. aquifers linked to nitrate. Environ. Sci. Technol. Lett. 2, 215–220 (2015).

    Article  CAS  Google Scholar 

  135. van Berk, W. & Fu, Y. Redox roll-front mobilization of geogenic uranium by nitrate input into aquifers: risks for groundwater resources. Environ. Sci. Technol. 51, 337–345 (2017).

    Article  PubMed  Google Scholar 

  136. Westrop, J. P. et al. Nitrate-stimulated release of naturally occurring sedimentary uranium. Environ. Sci. Technol. 57, 4354–4366 (2023). This study uses genome-resolved analyses to describe the coupled microbiology and biogeochemistry behind uranium and nitrate co-occurrence.

    Article  CAS  PubMed  Google Scholar 

  137. Hansen, B., Thorling, L., Schullehner, J., Termansen, M. & Dalgaard, T. Groundwater nitrate response to sustainable nitrogen management. Sci. Rep. 7, 8566 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  138. Janot, N. et al. Reducing conditions influence U(IV) accumulation in sediments during in situ bioremediation. ACS Earth Space Chem. https://doi.org/10.1021/acsearthspacechem.3c00271 (2024).

  139. Pidchenko, I. N. et al. Deep anoxic aquifers could act as sinks for uranium through microbial-assisted mineral trapping. Commun. Earth Environ. 4, 1–11 (2023).

    Article  Google Scholar 

  140. Yunus, F. Md et al. A review of groundwater arsenic contamination in Bangladesh: the Millennium Development Goal era and beyond. Int. J. Environ. Res. Public. Health 13, 215 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  141. Smith, A. H., Lingas, E. O. & Rahman, M. Contamination of drinking-water by arsenic in Bangladesh: a public health emergency. Bull. World Health Organ. 78, 1093–1103 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  142. Lawson, M., Polya, D. A., Boyce, A. J., Bryant, C. & Ballentine, C. J. Tracing organic matter composition and distribution and its role on arsenic release in shallow Cambodian groundwaters. Geochim. Cosmochim. Acta 178, 160–177 (2016).

    Article  CAS  Google Scholar 

  143. Harvey, C. F. et al. Arsenic mobility and groundwater extraction in Bangladesh. Science 298, 1602–1606 (2002).

    Article  CAS  PubMed  Google Scholar 

  144. Islam, F. S. et al. Role of metal-reducing bacteria in arsenic release from Bengal delta sediments. Nature 430, 68–71 (2004).

    Article  CAS  PubMed  Google Scholar 

  145. Nickson, R. et al. Arsenic poisoning of Bangladesh groundwater. Nature 395, 338–338 (1998).

    Article  CAS  PubMed  Google Scholar 

  146. Mihajlov, I. et al. Arsenic contamination of Bangladesh aquifers exacerbated by clay layers. Nat. Commun. 11, 2244 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Xiu, W. et al. Genome-resolved metagenomic analysis of groundwater: insights into arsenic mobilization in biogeochemical interaction networks. Environ. Sci. Technol. 56, 10105–10119 (2022).

    Article  CAS  PubMed  Google Scholar 

  148. Parkes, R. J. et al. Deep bacterial biosphere in Pacific Ocean sediments. Nature 371, 410–413 (1994).

    Article  Google Scholar 

  149. Hallbeck, L. & Pedersen, K. Characterization of microbial processes in deep aquifers of the Fennoscandian Shield. Appl. Geochem. 23, 1796–1819 (2008).

    Article  CAS  Google Scholar 

  150. Moser, D. P. et al. Temporal shifts in the geochemistry and microbial community structure of an ultradeep mine borehole following isolation. Geomicrobiol. J. 20, 517–548 (2003).

    Article  CAS  Google Scholar 

  151. Heinken, A. et al. Genome-scale metabolic reconstruction of 7,302 human microorganisms for personalized medicine. Nat. Biotechnol. 41, 1320–1331 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Williams, K. H. et al. Geophysical monitoring of coupled microbial and geochemical processes during stimulated subsurface bioremediation. Environ. Sci. Technol. 43, 6717–6723 (2009).

    Article  CAS  PubMed  Google Scholar 

  153. Brantley, S. L., Goldhaber, M. B. & Ragnarsdottir, K. V. Crossing disciplines and scales to understand the critical zone. Elements 3, 307–314 (2007).

    Article  CAS  Google Scholar 

  154. Templeton, A. S. & Caro, T. A. The rock-hosted biosphere. Annu. Rev. Earth Planet. Sci. 51, 493–519 (2023).

    Article  CAS  Google Scholar 

  155. Onstott, T. C. et al. Does aspartic acid racemization constrain the depth limit of the subsurface biosphere? Geobiology 12, 1–19 (2014).

    Article  CAS  PubMed  Google Scholar 

  156. Lloyd, K. G. Time as a microbial resource. Environ. Microbiol. Rep. 13, 18–21 (2021).

    Article  PubMed  Google Scholar 

  157. Fredrickson, J. K. & Onstott, T. C. Microbes deep inside the Earth. Sci. Am. 275, 68–73 (1996).

    Article  CAS  PubMed  Google Scholar 

  158. Brown, C. T. et al. Unusual biology across a group comprising more than 15% of domain Bacteria. Nature 523, 208–211 (2015).

    Article  CAS  PubMed  Google Scholar 

  159. Stevens, T. O. & McKinley, J. P. Lithoautotrophic microbial ecosystems in deep basalt aquifers. Science 270, 450–455 (1995).

    Article  CAS  Google Scholar 

  160. Simkus, D. N. et al. Variations in microbial carbon sources and cycling in the deep continental subsurface. Geochim. Cosmochim. Acta 173, 264–283 (2016).

    Article  CAS  Google Scholar 

  161. Ringelberg, D. B., Sutton, S. & White, D. C. Biomass, bioactivity and biodiversity: microbial ecology of the deep subsurface: analysis of ester-linked phospholipid fatty acids. FEMS Microbiol. Rev. 20, 371–377 (1997).

    Article  CAS  Google Scholar 

  162. Hallmann, C., Schwark, L. & Grice, K. Community dynamics of anaerobic bacteria in deep petroleum reservoirs. Nat. Geosci. 1, 588–591 (2008).

    Article  CAS  Google Scholar 

  163. Borgonie, G. et al. Eukaryotic opportunists dominate the deep-subsurface biosphere in South Africa. Nat. Commun. 6, 8952 (2015).

    Article  CAS  PubMed  Google Scholar 

  164. Mehrshad, M. et al. Energy efficiency and biological interactions define the core microbiome of deep oligotrophic groundwater. Nat. Commun. 12, 4253 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  165. Paszczynski, A. J. et al. Proteomic and targeted qPCR analyses of subsurface microbial communities for presence of methane monooxygenase. Biodegradation 22, 1045–1059 (2011).

    Article  CAS  PubMed  Google Scholar 

  166. Schweitzer, H. D. et al. Subsurface hydrocarbon degradation strategies in low- and high-sulfate coal seam communities identified with activity-based metagenomics. NPJ Biofilms Microbiomes 8, 7 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  167. Conrad, M. E. et al. Field evidence for co-metabolism of trichloroethene stimulated by addition of electron donor to groundwater. Environ. Sci. Technol. 44, 4697–4704 (2010).

    Article  CAS  PubMed  Google Scholar 

  168. Wilkins, M. J. et al. Trends and future challenges in sampling the deep terrestrial biosphere. Front. Microbiol. 5, 481 (2014).

  169. Kieft, T. L. in Handbook of Hydrocarbon and Lipid Microbiology (ed Timmis, K. N.) 3427–3441 (Springer, 2010).

  170. Yanagawa, K. et al. 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, 327 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  171. Wu, Y. et al. Effects of different soil weights, storage times and extraction methods on soil phospholipid fatty acid analyses. Geoderma 150, 171–178 (2009).

    Article  CAS  Google Scholar 

  172. Herrera, A. & Cockell, C. S. Exploring microbial diversity in volcanic environments: a review of methods in DNA extraction. J. Microbiol. Methods 70, 1–12 (2007).

    Article  CAS  PubMed  Google Scholar 

  173. Direito, S. O. L., Marees, A. & Röling, W. F. M. Sensitive life detection strategies for low-biomass environments: optimizing extraction of nucleic acids adsorbing to terrestrial and Mars analogue minerals. FEMS Microbiol. Ecol. 81, 111–123 (2012).

    Article  CAS  PubMed  Google Scholar 

  174. Daly, R. A., Wrighton, K. C. & Wilkins, M. J. Characterizing the deep terrestrial subsurface microbiome. Methods Mol. Biol. 1849, 1–15 (2018).

    Article  CAS  PubMed  Google Scholar 

  175. Bell, E. et al. Active anaerobic methane oxidation and sulfur disproportionation in the deep terrestrial subsurface. ISME J. 16, 1583–1593 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by a grant (EAR-1847684) from the US National Science Foundation to M.J.W.

Author information

Authors and Affiliations

Authors

Contributions

The authors contributed equally to all aspects of the article.

Corresponding author

Correspondence to Michael J. Wilkins.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Reviews Microbiology thanks Frederick Colwell, Melody Lindsay, Beth Orcutt and Andreas Teske for their contribution to the peer review of this work.

Additional information

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

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

Amundson, K.K., Borton, M.A. & Wilkins, M.J. Anthropogenic impacts on the terrestrial subsurface biosphere. Nat Rev Microbiol 23, 147–161 (2025). https://doi.org/10.1038/s41579-024-01110-5

Download citation

  • Accepted:

  • Published:

  • Version of record:

  • Issue date:

  • DOI: https://doi.org/10.1038/s41579-024-01110-5

Search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Microbiology