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The biomass and biodiversity of the continental subsurface

Abstract

Despite accounting for a significant portion of the Earth’s prokaryotic biomass, controls on the abundance and biodiversity of microorganisms residing in the continental subsurface are poorly understood. To redress this, we compiled cell concentration and microbial diversity data from continental subsurface localities around the globe. Based on considerations of global heat flow, surface temperature, depth and lithology, we estimated that the continental subsurface hosts 2 to 6 × 1029 cells and found that other variables such as total organic carbon and groundwater cellular abundances do not appear to be predictive of cell concentrations in the continental subsurface. Although we were unable to identify a reliable predictor of species richness in the continental subsurface, we found that bacteria are more abundant than archaea and that their community composition was correlated to sample lithology. Using our updated continental subsurface cellular estimate and existing literature, we estimate that the total global prokaryotic biomass is approximately 23 to 31 Pg of carbon C (PgC), roughly 4 to 10 times less than previous estimates.

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Fig. 1: The ~3,800 continental subsurface cell concentrations versus depth.
Fig. 2: Subsurface archaeal and bacterial communities.
Fig. 3: Continental subsurface diversity.

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Data availability:

Data are made available through GitHub (https://github.com/cmagnabosco), and an R markdown file with interactive Shiny app (https://caramagnabosco.shinyapps.io/subsufacebiomass/) is available for users to explore the data.

References

  1. Gold, T. The deep, hot biosphere. Proc. Natl Acad. Sci. USA 89, 6045–6049 (1992).

    Article  Google Scholar 

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

    Article  Google Scholar 

  3. Anantharaman, K. et al. Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system. Nat. Commun. 7, 13219 (2016).

    Article  Google Scholar 

  4. Rinke, C. et al. Insights into the phylogeny and coding potential of microbial dark matter. Nature 499, 431–437 (2013).

    Article  Google Scholar 

  5. Michalski, J. R. et al. The search for clues to abiogenesis on Mars. Nat. Geosci. 11, 21–26 (2017).

    Article  Google Scholar 

  6. Onstott, T. C. Deep Life (Princeton Univ. Press, Princeton, 2016).

  7. Kallmeyer, J., Pockalny, R., Adhikari, R. R., Smith, D. C. & D’Hondt, S. Global distribution of microbial abundance and biomass in subseafloor sediment. Proc. Natl Acad. Sci. USA 109, 16213–16216 (2012).

    Article  Google Scholar 

  8. Onstott, T. C. et al. in Enigmatic Microorganisms and Life in Extreme Environments (ed. Seckbach, J.) 489–499 (Kluwer Academic Publishers, ​Alphen aan den Rijn, 1998).

  9. Fredrickson, J. & Balkwill, D. Geomicrobiological processes and diversity in the deep terrestrial subsurface. Geomicrobiol. J. 23, 345–356 (2006).

    Article  Google Scholar 

  10. Parkes, R. J. et al. A review of prokaryotic populations and processes in sub-seafloor sediments, including biosphere:geosphere interactions. Mar. Geol. 352, 409–425 (2014).

    Article  Google Scholar 

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

    Article  Google Scholar 

  12. McMahon, S. & Parnell, J. Weighing the deep continental biosphere. FEMS Microbiol. Ecol. 87, 113–120 (2014).

    Article  Google Scholar 

  13. Bar-On, Y. M., Phillips, R. & Milo, R. The biomass distribution on Earth. Proc. Natl Acad. Sci. USA 115, 6506–6511 (2018).

    Article  Google Scholar 

  14. Heberling, C., Lowell, R. P., Liu, L. & Fisk, M. R. Extent of the microbial biosphere in the oceanic crust. Geochem. Geophys. Geosyst. 11, Q08003 (2010).

    Article  Google Scholar 

  15. Lipp, J. S., Morono, Y., Inagaki, F. & Hinrichs, K.-U. Significant contribution of Archaea to extant biomass in marine subsurface sediments. Nature 454, 991–994 (2008).

    Article  Google Scholar 

  16. D’Hondt, S. et al. Subseafloor sedimentary life in the South Pacific Gyre. Proc. Natl Acad. Sci. USA 106, 11651–11656 (2009).

    Article  Google Scholar 

  17. Pedersen, K. & Ekendahl, S. Distribution and activity of bacteria in deep granitic groundwaters of southeastern Sweden. Microb. Ecol. 20, 37–52 (1990).

    Article  Google Scholar 

  18. Hazen, T. C., Jimenez, L., López de Victoria, G. & Fliermans, C. B. Comparison of bacteria from deep subsurface sediment and adjacent groundwater. Microb. Ecol. 22, 293–304 (1991).

    Article  Google Scholar 

  19. Sinclair, J. & Ghiorse, W. Distribution of aerobic bacteria, protozoa, algae, and fungi in deep subsurface sediments. Geomicrobiol. J. 7, 15–31 (1989).

    Article  Google Scholar 

  20. Colwell, F. S. Microbiological comparison of a surface soil and unsaturated subsurface soil from a semiarid high desert. Appl. Environ. Microbiol. 55, 2420–2423 (1989).

    Google Scholar 

  21. Federle, T. W., Dobbins, D. C., Thornton-Manning, J. R. & Jones, D. D. Microbial biomass, activity, and community structure in subsurface soils. Groundwater 24, 365–374 (1986).

    Article  Google Scholar 

  22. Harvey, R. W., Smith, R. L. & George, L. Effect of organic contamination upon microbial distributions and heterotrophic uptake in a Cape Cod, Mass., aquifer. Appl. Environ. Microbiol. 48, 1197–1202 (1984).

    Google Scholar 

  23. Balkwill, D., Leach, F., Wilson, J., McNabb, J. & White, D. C. Equivalence of microbial biomass measures based on membrane lipid and cell wall components, adenosine triphosphate, and direct counts in subsurface sediments. Microb. Ecol. 16, 73–84 (1988).

    Article  Google Scholar 

  24. Beloin, R. M., Sinclair, J. L. & Ghiorse, W. C. Distribution and activity of microorganisms in subsurface sediments of a pristine study site in Oklahoma. Microb. Ecol. 16, 85–97 (1988).

    Article  Google Scholar 

  25. Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B Stat. Methodol. 57, 289–300 (1995).

    Google Scholar 

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

    Article  Google Scholar 

  27. Head, I. M., Gray, N. D. & Larter, S. R. Life in the slow lane; biogeochemistry of biodegraded petroleum containing reservoirs and implications for energy recovery and carbon management. Front. Microbiol. 5, 566 (2014).

    Article  Google Scholar 

  28. Miteva, V. I., Sheridan, P. P. & Brenchley, J. E. Phylogenetic and physiological diversity of microorganisms isolated from a deep Greenland glacier ice core. Appl. Environ. Microbiol. 70, 202–213 (2004).

    Article  Google Scholar 

  29. Telling, J. et al. Rock comminution as a source of hydrogen for subglacial ecosystems. Nat. Geosci. 8, 851–855 (2015).

    Article  Google Scholar 

  30. Boyd, E. S., Hamilton, T. L., Havig, J. R., Skidmore, M. L. & Shock, E. L. Chemolithotrophic primary production in a subglacial ecosystem. Appl. Environ. Microbiol. 80, 6146–6153 (2014).

    Article  Google Scholar 

  31. Chapelle, F. R. et al. A hydrogen-based subsurface microbial community dominated by methanogens. Nature 415, 312–314 (2002).

    Article  Google Scholar 

  32. Bomberg, M., Lamminmäki, T. & Itävaara, M. Microbial communities and their predicted metabolic characteristics in deep fracture groundwaters of the crystalline bedrock at Olkiluoto, Finland. Biogeosci. Discuss. 13, 6031–6047 (2016).

    Article  Google Scholar 

  33. Simkus, D. N. et al. Variations in microbial carbon sources and cycling in the deep continental subsurface. Geochim. Cosmochim. Acta. 173, 264–283 (2015).

    Article  Google Scholar 

  34. Bomberg, M., Nyyssönen, M., Pitkänen, P., Lehtinen, A. & Itävaara, M. Active microbial communities inhabit sulphate-methane interphase in deep bedrock fracture fluids in Olkiluoto, Finland. BioMed Res. Int. 2015, 979530 (2015).

    Article  Google Scholar 

  35. Knittel, K. & Boetius, A. Anaerobic oxidation of methane: progress with an unknown process. Annu. Rev. Microbiol. 63, 311–334 (2009).

    Article  Google Scholar 

  36. Crespo-Medina, M. et al. Insights into environmental controls on microbial communities in a continental serpentinite aquifer using a microcosm-based approach. Front. Microbiol. 5, 604 (2014).

    Article  Google Scholar 

  37. Tiago, I. & Veríssimo, A. Microbial and functional diversity of a subterrestrial high pH groundwater associated to serpentinization. Environ. Microbiol. 15, 1687–1706 (2013).

    Article  Google Scholar 

  38. Brazelton, W. J. et al. Metagenomic identification of active methanogens and methanotrophs in serpentinite springs of the Voltri Massif, Italy. PeerJ 5, e2945 (2017).

    Article  Google Scholar 

  39. Brazelton, W. J., Morrill, P. L., Szponar, N. & Schrenk, M. O. Bacterial communities associated with subsurface geochemical processes in continental serpentinite springs. Appl. Environ. Microbiol. 79, 3906–3916 (2013).

    Article  Google Scholar 

  40. Lavalleur, H. J. & Colwell, F. S. Microbial characterization of basalt formation waters targeted for geological carbon sequestration. FEMS Microbiol. Ecol. 85, 62–73 (2013).

    Article  Google Scholar 

  41. Nyyssönen, M. et al. Taxonomically and functionally diverse microbial communities in deep crystalline rocks of the Fennoscandian shield. ISME J. 8, 126–138 (2014).

    Article  Google Scholar 

  42. Pedersen, K., Bengtsson, A. F., Edlund, J. S. & Eriksson, L. C. Sulphate-controlled diversity of subterranean microbial communities over depth in deep groundwater with opposing gradients of sulphate and methane. Geomicrobiol. J. 31, 617–631 (2014).

    Article  Google Scholar 

  43. Osburn, M. R., LaRowe, D. E., Momper, L. M. & Amend, J. P. Chemolithotrophy in the continental deep subsurface: Sanford Underground Research Facility (SURF), USA. Front. Microbiol. 5, 610 (2014).

    Article  Google Scholar 

  44. Magnabosco, C. et al. Comparisons of the composition and biogeographic distribution of the bacterial communities occupying South African thermal springs with those inhabiting deep subsurface fracture water. Front. Microbiol. 5, 679–689 (2014).

    Article  Google Scholar 

  45. Magnabosco, C. et al. Fluctuations in populations of subsurface methane oxidizers in coordination with changes in electron acceptor availability. FEMS Microbiol. Ecol. 94, fiy089 (2018).

    Article  Google Scholar 

  46. Katayama, T. et al. Physicochemical impacts associated with natural gas development on methanogenesis in deep sand aquifers. ISME J. 9, 436–446 (2015).

    Article  Google Scholar 

  47. Dong, Y. et al. Halomonas sulfidaeris-dominated microbial community inhabits a 1.8 km-deep subsurface Cambrian Sandstone reservoir. Environ. Microbiol. 16, 1695–1708 (2014).

    Article  Google Scholar 

  48. 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  Google Scholar 

  49. Kryachko, Y., Dong, X., Sensen, C. W. & Voordouw, G. Compositions of microbial communities associated with oil and water in a mesothermic oil field. Antonie van Leeuwenhoek 101, 493–506 (2012).

    Article  Google Scholar 

  50. O’Mullan, G. et al. Microbial stimulation and succession following a test well injection simulating CO2 leakage into a shallow newark basin aquifer. PLoS ONE 10, e0117812 (2015).

    Article  Google Scholar 

  51. Marteinsson, V. T. et al. Microbial communities in the subglacial waters of the Vatnajokull ice cap, Iceland. ISME J. 7, 427–437 (2013).

    Article  Google Scholar 

  52. 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  Google Scholar 

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

    Article  Google Scholar 

  54. Magnabosco, C. et al. A metagenomic window into carbon metabolism at 3 km depth in Precambrian vontinental crust. ISME J. 10, 730–741 (2016).

    Article  Google Scholar 

  55. New, M. G., Hulme, M. & Jones, P. D. Representing twentieth-century space–time climate variability. Part I: development of a 1961–90 mean monthly terrestrial climatology. J. Climate 12, 829–856 (1999).

    Article  Google Scholar 

  56. Genthon, C. & Braun, A. ECMWF analyses and predictions of the surface climate of Greenland and Antarctica. J. Climate 8, 2324–2332 (1995).

    Article  Google Scholar 

  57. Davies, J. H. Global map of solid Earth surface heat flow. Geochem. Geophys. Geosyst. 14, 4608–4622 (2013).

    Article  Google Scholar 

  58. UNESCO-IHP-ISARM-Programme (United Nations Educational, Scientific and Cultural Organization, 2009).

  59. Laske, G., Masters, G., Ma, Z. & Pasyanos, M. Update on CRUST1. 0 — A 1‐degree global model of Earth’s crust. Geophys. Res. Abstracts 15, 2658 (2013).

    Google Scholar 

  60. Norland, S., Heldal, M. & Tumyr, O. On the relation between dry matter and volume of bacteria. Microb. Ecol. 13, 95–101 (1987).

    Article  Google Scholar 

  61. Griebler, C., Mindl, B., Slezak, D. & Geiger-Kaiser, M. Distribution patterns of attached and suspended bacteria in pristine and contaminated shallow aquifers studied with an in situ sediment exposure microcosm. Aquat. Microb. Ecol. 28, 117–129 (2002).

    Article  Google Scholar 

  62. Marxsen, J. Bacterial biomass and bacterial uptake of glucose in polluted and unpolluted groundwater of sandy and gravelly deposits. Verh. Int. Ver. Limnol. 21, 1371–1375 (1981).

    Google Scholar 

  63. Mason, O. U. et al. First investigation of the microbiology of the deepest layer of ocean crust. PLoS ONE 5, e15399 (2010).

    Article  Google Scholar 

  64. Locey, K. J. & Lennon, J. T. Scaling laws predict global microbial diversity. Proc. Natl Acad. Sci. USA 113, 5970–5975 (2015).

    Article  Google Scholar 

  65. Willis, A. Extrapolating abundance curves has no predictive power for estimating microbial biodiversity. Proc. Natl Acad. Sci. USA 113, E5096 (2016).

    Article  Google Scholar 

  66. Locey, K. J. & Lennon, J. T. Reply to Willis: powerful predictions of biodiversity from ecological models and scaling laws. Proc. Natl Acad. Sci. USA 113, E5097 (2016).

    Article  Google Scholar 

  67. Curtis, T. P., Sloan, W. T. & Scannell, J. W. Estimating prokaryotic diversity and its limits. Proc. Natl Acad. Sci. USA 99, 10494–10499 (2002).

    Article  Google Scholar 

  68. Rosenzweig, M. L. Species Diversity in Space and Time (Cambridge Univ. Press, Cambridge, 1995).

  69. Hanson, C. A., Fuhrman, J. A., Horner-Devine, M. C. & Martiny, J. B. H. Beyond biogeographic patterns: processes shaping the microbial landscape. Nat. Rev. Microbiol. 10, 497–506 (2012).

    Article  Google Scholar 

  70. Horner-Devine, M. C., Lage, M., Hughes, J. B. & Bohannan, B. J. M. A taxa–area relationship for bacteria. Nature 432, 750–753 (2004).

    Article  Google Scholar 

  71. Morlon, H. et al. A general framework for the distance–decay of similarity in ecological communities. Ecol. Lett. 11, 904–917 (2008).

    Article  Google Scholar 

  72. Sheik, C. S. et al. Identification and removal of contaminant sequences from ribosomal gene databases: lessons from the census of deep life. Front. Microbiol. 9, 840 (2018).

    Article  Google Scholar 

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

    Article  Google Scholar 

  74. Sohlberg, E. et al. Revealing the unexplored fungal communities in deep groundwater of crystalline bedrock fracture zones in Olkiluoto, Finland. Front. Microbiol. 6, 573 (2015).

    Article  Google Scholar 

  75. Pachiadaki, M. G., Rédou, V., Beaudoin, D. J., Burgaud, G. & Edgcomb, V. P. Fungal and prokaryotic activities in the marine subsurface biosphere at Peru Margin and Canterbury Basin inferred from RNA-based analyses and microscopy. Front. Microbiol. 7, 846 (2016).

    Article  Google Scholar 

  76. Bengtson, S. et al. Deep-biosphere consortium of fungi and prokaryotes in Eocene sub-seafloor basalts. Geobiology 12, 489–496 (2014).

    Article  Google Scholar 

  77. Anderson, R. E., Brazelton, W. J. & Baross, J. A. The deep viriosphere: assessing the viral impact on microbial community dynamics in the deep subsurface. Rev. Mineral. Geochem. 75, 649–675 (2013).

    Article  Google Scholar 

  78. Kyle, J. E., Eydal, H. S., Ferris, F. G. & Pedersen, K. Viruses in granitic groundwater from 69 to 450 m depth of the Äspö hard rock laboratory, Sweden. ISME J. 2, 571–574 (2008).

    Article  Google Scholar 

  79. Labonté, J. et al. Single cell genomics indicates horizontal gene transfer and viral infections in a deep subsurface Firmicutes population. Front. Microbiol. 6, 349 (2015).

    Google Scholar 

  80. Eydal, H., Jägevall, S., Hermansson, M. & Pedersen, K. Bacteriophage lytic to Desulfovibrio aespoeensis isolated from deep groundwater. ISME J. 3, 1139 (2009).

    Article  Google Scholar 

  81. Lloyd, K. G., May, M. K., Kevorkian, R. T. & Steen, A. D. Meta-analysis of quantification methods shows that Archaea and Bacteria have similar abundances in the subseafloor. Appl. Environ. Microbiol. 79, 7790–7799 (2013).

    Article  Google Scholar 

  82. Arístegui, J., Gasol, J. M., Duarte, C. M. & Herndl, G. J. Microbial oceanography of the dark ocean’s pelagic realm. Limnol. Oceanogr. 54, 1501–1529 (2009).

    Article  Google Scholar 

  83. Buitenhuis, E. et al. Global Distribution of Picoheterotrophs (Bacteria and Archaea) Abundance and Biomass-Gridded Data Product (NetCDF)-Contribution to the MAREDAT World Ocean Atlas of Plankton Functional Types (PANGEA, 2012); https://doi.org/10.1594/PANGAEA.779142

  84. Buitenhuis, E. T. et al. Picophytoplankton biomass distribution in the global ocean. Earth Syst. Sci. Data 4, 37–46 (2012b).

    Article  Google Scholar 

  85. Xu, X., Thornton, P. E. & Post, W. M. A global analysis of soil microbial biomass carbon, nitrogen and phosphorus in terrestrial ecosystems. Global Ecol. Biogeogr. 22, 737–749 (2013).

    Article  Google Scholar 

  86. Serna‐Chavez, H. M., Fierer, N. & Van Bodegom, P. M. Global drivers and patterns of microbial abundance in soil. Global Ecol. Biogeogr. 22, 1162–1172 (2013).

    Article  Google Scholar 

  87. Joergensen, R. G. & Wichern, F. Quantitative assessment of the fungal contribution to microbial tissue in soil. Soil Biol. Biochem. 40, 2977–2991 (2008).

    Article  Google Scholar 

  88. Kieft, T. L. & Simmons, K. A. Allometry of animal–microbe interactions and global census of animal-associated microbes. Proc. R. Soc. B 282, 20150702 (2015).

    Article  Google Scholar 

  89. Morisita, M. Measuring of interspecific association and similarity between communities. Mem. Fac. Sci. Kyushu Univ. Ser. 3, 65–80 (1959).

    Google Scholar 

  90. Turnbaugh, P. J. et al. The human microbiome project. Nature 449, 804–810 (2007).

    Article  Google Scholar 

  91. Dorofeeva, R. P. & Lysak, S. V. Heat Flow of Central Asia (Proc. World Geothermal Congress, 2010); https://www.geothermal-energy.org/pdf/IGAstandard/WGC/2010/1308.pdf

  92. Keller, C. B. & Schoene, B. Statistical geochemistry reveals disruption in secular lithospheric evolution about 2.5 Gyr ago. Nature 485, 490–493 (2012).

    Article  Google Scholar 

  93. Stevens, T. O., McKinley, J. P. & Fredrickson, J. K. Bacteria associated with deep, alkaline, anaerobic groundwaters in southeast Washington. Microb. Ecol. 25, 35–50 (1993).

    Article  Google Scholar 

  94. Takai, K. et al. Shifts in archaeal communities associated with lithological and geochemical variations in subsurface Cretaceous rock. Environ. Microbiol. 5, 309–320 (2003).

    Article  Google Scholar 

  95. Lloyd, K. G. in Microbial Life of the Deep Biosphere Vol. 1 (eds Kallmeyer, J. & Wagner, D.) 121–142 (DeGruyter, Berlin, 2014).

  96. Rajala, P. & Bomberg, M. Reactivation of deep subsurface microbial community in response to methane or methanol amendment. Front. Microbiol. 8, 431 (2017).

    Article  Google Scholar 

  97. Morono, Y. & Inagaki, F. in Advances in Applied Microbiology Vol. 95 (eds Gladd, G.M. & Sariaslani, S.) Ch. 3, 149–178 (Elsevier Inc., New York, 2016).

  98. White, D. C. in Microbes in Their Natural Environments: Thirty-fourth Symposium of the Society for General Microbiology (eds Slater, J. H., Whittenbury, R. & Wimpenny, J. W. T.) 37–66 (Cambridge Univ. Press, New York, 1983).

  99. Green, C. T. & Scow, K. M. Analysis of phospholipid fatty acids (PLFA) to characterize microbial communities in aquifers. Hydrogeol. J. 8, 126–141 (2000).

    Article  Google Scholar 

  100. Stouthamer, A. H. in Microbial Biochemistry Vol. 21 (ed Quayle, J. R.) Ch. 1, 1–47 (Univ. Park Press, 1979).

  101. Ringelberg, D., 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  Google Scholar 

  102. Lin, L. H. et al. Long term biosustainability in a high energy, low diversity crustal biome. Science 314, 479–482 (2006b).

    Article  Google Scholar 

  103. Byl, T. D. et al. Adaptations of indigenous bacteria to fuel contamination in karst aquifers in south-central Kentucky. J. Cave and Karst Studies 76, 104–113 (2014).

    Article  Google Scholar 

  104. Griebler, C., Mindl, B. & Slezak, D. Combining DAPI and SYBR Green II for the enumeration of total bacterial numbers in aquatic sediments. Internat. Rev. Hydrobiol. 86, 453–465 (2001).

    Article  Google Scholar 

  105. Webster, J., Hampton, G., Wilson, J., Ghiorose, W. & Leach, F. Determination of microbial cell numbers in subsurface samples. Ground Water 23, 17–25 (1985).

    Article  Google Scholar 

  106. Eydal, H. & Pedersen, K. Use of an ATP assay to determine viable microbial biomass in Fennoscandian Shield groundwater from depths of 3–1000 m. J. Microbiol. Methods 70, 363–373 (2007).

    Article  Google Scholar 

  107. Neidhardt, F. et al. Escherichia coli and Salmonella typhimurium (American Society for Microbiology, 1996).

  108. Lomstein, B. A., Langerhuus, A. T., D’Hondt, S., Jørgensen, B. B. & Spivack, A. J. Endospore abundance, microbial growth and necromass turnover in deep sub-seafloor sediment. Nature 484, 101–104 (2012).

    Article  Google Scholar 

  109. Kembe, S. W., Wu, M., Eisen, J. A. & Green, J. L. Incorporating 16S gene copy number information improves estimates of microbial diversity and abundance. PLoS Comput. Biol. 8, e1002743 (2012).

    Article  Google Scholar 

  110. Xiao, X., White, E. P., Hooten, M. B. & Durham, S. L. On the use of log-transformation vs. nonlinear regression for analyzing biological power laws. Ecology 92, 1887–1894 (2011).

    Article  Google Scholar 

  111. Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).

    Article  Google Scholar 

  112. Eren, A. M., Vineis, J. H., Morrison, H. G. & Sogin, M. L. A Filtering method to generate high quality short reads using Illumina paired-end technology. PLoS ONE 8, e66643 (2013).

    Article  Google Scholar 

  113. Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336 (2010).

    Article  Google Scholar 

  114. Willis, A. & Bunge, J. Estimating diversity via frequency ratios. Biometrics 71, 042–1049 (2015).

    Article  Google Scholar 

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Acknowledgements

We acknowledge the BGR/UNESCO for the use of their datasets on the global groundwater recharge rate. We thank J. T. Lennon and S. McMahon for helping to improve the quality and clarity of the manuscript. We also acknowledge the support to T.C.O. by NSF grants DEB-1442059 from the Dimensions of Biodiversity program and DEB-1441646 from the GoLife programme, the support to L.-H.L. by Taiwanese MOST and MOE (NTU-107L901002), and the support to H.D. by a grant from the Deep Carbon Observatory Sloan Grant G-2014-3-01. We are grateful to T. W. Shawa of the Map and Geospatial Information Center at Princeton University Libary for assistance with GIS analyses.

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T.C.O. was responsible for the biomass compilation and GIS calculations. C.M. was responsible for the 16S rRNA compilation and statistical analyses. T.C.O. and C.M. were responsible for writing the manuscript. L.-H.L., H.D., W.G., T.L.K., E.v.H and K.P. contributed previously unpublished biomass data, M.B. contributed previously unpublished amplicon data, and H.S.-L. contributed text on evaporite deposits.

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Correspondence to C. Magnabosco.

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Supplementary Information

Supplementary Description, Supplementary Tables 1–8, Supplementary Figures 1–25.

Supplementary Table 1

Summary of cell concentration database.

Supplementary Table 2

Cell concentration database.

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Magnabosco, C., Lin, LH., Dong, H. et al. The biomass and biodiversity of the continental subsurface. Nature Geosci 11, 707–717 (2018). https://doi.org/10.1038/s41561-018-0221-6

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