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Deep biosphere

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The deep biosphere is the part of the biosphere that resides below the first few meters of the surface. It extends down at least 5 kilometers below the continental surface and 10.5 kilometers below the sea surface. It includes all three domains of life and the genetic diversity rivals that on the surface.

Definition

The deep biosphere is an ecosystem of organisms and their living space in the deep subsurface.[1] For the seafloor, an operational definition of deep subsurface is the region that is not penetrated by seawater or bioturbated by animals; this is generally about a meter or more below the surface.[2] On continents, it is below a few meters, not including soils.[3] The organisms in this zone are sometimes referred to as intraterrestrials.[4][5]

History

At the University of Chicago in the 1920s, geologist Edson Bastin enlisted the help of microbiologist Frank Greer in an effort to explain why water extracted from oil fields contained hydrogen sulfide and bicarbonates. These chemicals are normally created by bacteria, but the water came from a depth where the heat and pressure were considered too great to support life. They were able to culture anaerobic sulfate-reducing bacteria from the water, demonstrating that the chemicals had a bacterial origin.[6][7][8]

Also in the 1920s, Charles Lipman, a microbiologist at the University of California, Berkeley, noticed that bacteria that had been sealed in bottles for 40 years could be reanimated – a phenomenon now known as anhydrobiosis. He wondered whether the same was true of bacteria in coal seams. He sterilized samples of coal, wetted them, crushed them and then succeeded in culturing bacteria from the coal dust. One sterilization procedure, baking the coal at 160 degrees Celsius for up to 50 hours, actually encouraged their growth. He published the results in 1931.[4][8]

The first studies of subsurface life were conducted by Claude E. Zobell, the "father of marine microbiology",[9] in the late 1930s to the 1950s. Although the coring depth was limited, microbes were found wherever the sediments were sampled.[10][11] With increasing depth, aerobes gave way to anaerobes.[12]

Most biologists dismissed the subsurface microbes as contamination, especially after the submersible Alvin sank in 1968 and the scientists escaped, leaving their lunches behind. When Alvin was recovered, the lunches showed no sign of microbial decay.[9] This reinforced a view of the deep sea (and by extension the subsurface) as a lifeless desert. The study of the deep biosphere was dormant for decades, except for some Soviet microbiologists who began to refer to themselves as geomicrobiologists.[8]

Interest in subsurface life was renewed when the United States Department of Energy was looking for a safe way of burying nuclear waste, and Frank J. Wobber realized that microbes below the surface could either help by degrading the buried waste or hinder by breaching the sealed containers. He formed the Subsurface Science Program to study deep life. To address the problem of contamination, special equipment was designed to minimize contact between a core sample and the drilling fluid that lubricates the drill bit. In addition, tracers were added to the fluid to indicate whether it penetrated the core. In 1987, several boreholes were drilled near the Savannah River Site, and microorganisms were found to be plentiful and diverse at least 500 metres below the surface.[11]

From 1983 to 2003, microbiologists analyzed cell abundances in drill cores from the Ocean Drilling Program.[10] A group led by John Parkes of the University of Bristol reported concentrations of 104 to 108 cells per gram of sediment down to depths of 500 metres (agricultural soils contain about 109 cells per gram).[13] This was initially met with skepticism and it took them four years to publish their results.[9] In 1998, William Whitman and colleagues published a summary of twelve years of data in the Proceedings of the National Academy of Sciences.[13] They estimated that up to 95% of all prokaryotes (archaea and bacteria) live in the deep subsurface, with 55% in the marine subsurface and 39% in the terrestrial subsurface.[10] In 2002, ODP Leg 201 was the first to be motivated by a search for deep life. Most of the previous exploration was on continental margins, so the goal was to drill in the open ocean for comparison.[14][4]

Scientific methods

The present understanding of subsurface biology was made possible by numerous advances in technology for sample collection, field analysis, molecular science, cultivation, imaging and analysis.[12]

Sample collection

Chikyu 1 drilling ship

The ocean floor is sampled by drilling boreholes and collecting cores. The methods must be adapted to different types of rock, and the cost of drilling limits the number of holes that can be drilled.[15] Microbiologists have made use of scientific drilling programs: the Ocean Drilling Program (ODP), which used the JOIDES Resolution drilling platform, and the Integrated Ocean Drilling Program (IODP), which used the Japanese ship Chikyū.[12]

Deep underground mines, for example South African gold mines and the Pyhäsalmi copper and zinc mine in Finland, have provided opportunities to sample the deep biosphere.[16][17] Chosen or proposed nuclear waste repository sites (e.g. Yucca Mountain and the Waste Isolation Pilot Plant in the United States, Äspö and surrounding areas in Sweden, Onkalo and surrounding areas in Finland, Mont Terri in Switzerland) have also allowed sampling of the deep subsurface.[12] Scientific drilling of continental deep subsurface has been promoted by International Continental Scientific Drilling Program (ICDP).

To allow continuous underground sampling, various kinds of observatories have been developed. On the ocean floor, the Circulation Obviation Retrofit Kit (CORK) seals a borehole to cut off the influx of seawater.[18] An advanced version of CORK is able to seal off multiple regions using packers, rubber tubes that inflate to seal the space between the drill string and the wall of the borehole.[19][20] In sediments, the Simple Cabled Instrument for Measuring Parameters In-Situ (SCIMPI) is designed to remain and take measurements after a borehole has collapsed.[21]

Packers are also used in the continental subsurface,[22] along with devices such as the flow-through in situ reactor (FTISR). Various methods are used to extract fluids from these sites, including passive gas samplers, U-tube systems and osmotic gas samplers.[12] In narrow (less than 50 millimeter) holes, polyamide tubes with a back-pressure valve can be lowered to sample an entire column of fluid.[23][24]

Field analysis and manipulation

Some methods analyze microbes in situ rather than extract them. In biogeophysics, the effects of microbes on properties of geological materials are remotely probed using electrical signals. Microbes can be tagged using a stable isotope such as carbon-13 and then re-injected in the ground to see where they go.[12] A "push-pull" method involves injection of a fluid into an aquifer and extraction of a mixture of injected fluid with the ground water; the latter can then be analyzed to determine what chemical reactions occurred.[25]

Molecular methods and cultivation

Methods from modern molecular biology allow the extraction of nucleic acids, lipids and proteins from cells, DNA sequencing, and the physical and chemical analysis of molecules using mass spectrometry and flow cytometry. A lot can be learned about the microbial communities using these methods even when the individuals cannot be cultivated.[12] For example, at the Richmond Mine in California, scientists used shotgun sequencing to identify four new species of bacteria, three new species of archaea (known as the Archaeal Richmond Mine acidophilic nanoorganisms), and 572 proteins unique to the bacteria.[26][27]

Extent

Life has been found at depths of 5 km in continents and 10.5 km below the ocean surface.[28] In 1992, Thomas Gold calculated that if the estimated pore space of the terrestrial land mass down to 5 km depth was filled with water, and if 1% of this volume were microbial biomass, it would be enough living matter to cover Earth's land surface with a 1.5 m thick layer.[29] The estimated volume of the deep biosphere is 2–2.3 billion cubic kilometers, about twice the volume of the oceans.[30]

Diversity

"Ca. Desulforudis audaxviator" from a gold mine near Johannesburg[31]

The biomass of the subsurface life is about 15% of the total for the biosphere.[3] Life from all three domains of life (Archaea, Bacteria, and Eukarya) have been found in the deep subsurface. The genetic diversity is at least as great as that on the surface.[28] Bacteria are mainly Proteobacteria and Firmicutes while the Archaea are mainly Methanomicrobia and Thaumarchaeota.[32] The subsurface accounts for about 90% of all the biomass in Archaea and Bacteria.[3] One species of bacterium, "Candidatus Desulforudis audaxviator", is the first known to comprise a complete ecosystem by itself.[9]

The eukarya include some multicellular life. In 2009 a species of nematode, Halicephalobus mephisto, was discovered in rock fissures more than a kilometer down a South African gold mine. Nicknamed the "devil worm",[33] it may have been forced down along with pore water by earthquakes.[34] Other multicellular organisms have since been found, including fungi, Platyhelminthes (flatworms), Rotifera, Annelida (ringed worms) and Arthropoda.[35][36][37][38][39] However, their range may be limited because sterols, needed to construct membranes in eukarya, are not easily made in anaerobic conditions.[40]

See also

References

  1. ^ Hoehler, Tori M.; Jorgensen, Bo Barker (16 January 2013). "Microbial life under extreme energy limitation". Nature Reviews Microbiology. 11: 83–94. doi:10.1038/nrmicro2939.
  2. ^ Schippers, A. (2015). "Deep biosphere". In Harff, J.; Meschede, M.; Petersen, S.; Thiede, J. (eds.). Encyclopedia of Marine Geosciences. Dordrecht: Springer. ISBN 978-94-007-6644-0.
  3. ^ a b c Bar-On, Yinon M.; Phillips, Rob; Milo, Ron (19 June 2018). "The biomass distribution on Earth". Proceedings of the National Academy of Sciences. 115 (25): 6506–6511. doi:10.1073/pnas.1711842115. PMC 6016768.
  4. ^ a b c Edwards, Katrina (2 September 2011). "North Pond: Searching for Intraterrestrial Life". Scientific American Blog Network. Retrieved 18 January 2019.
  5. ^ Judson, Olivia (10 June 2008). "Meet the Intraterrestrials". Opinionator. Retrieved 18 January 2019.
  6. ^ Alley, William M. (1993). Regional Ground-Water Quality. John Wiley & Sons. p. 182. ISBN 9780471284536.
  7. ^ Ward, Peter D.; Brownlee, Donald (2006). Rare earth : why complex life is uncommon in the universe (Pbk. ed.). Copernicus. pp. 7–12. ISBN 9780387218489.
  8. ^ a b c Onstott 2016, Chapter 1
  9. ^ a b c d Leigh Mascarelli, Amanda (11 June 2009). "Low life". Nature. 459 (7248): 770–773. doi:10.1038/459770a.
  10. ^ a b c Edwards, Katrina J.; Becker, Keir; Colwell, Frederick (30 May 2012). "The Deep, Dark Energy Biosphere: Intraterrestrial Life on Earth". Annual Review of Earth and Planetary Sciences. 40 (1): 551–568. doi:10.1146/annurev-earth-042711-105500.
  11. ^ a b Fredrickson, James K.; Onstott, Tullis C. (1996). "Microbes Deep inside the Earth". Scientific American. 275 (4): 68–73. JSTOR 24993405.
  12. ^ a b c d e f g Colwell, F. S.; D'Hondt, S. (13 February 2013). "Nature and Extent of the Deep Biosphere". Reviews in Mineralogy and Geochemistry. 75 (1): 547–574. doi:10.2138/rmg.2013.75.17.
  13. ^ a b Onstott 2016, Chapter 6
  14. ^ "Leg 201: Controls on microbial communities in deeply buried sediments, eastern Equatorial Pacific and Peru Margin sites 1225-1231". Ocean Drilling Program. Retrieved 20 July 2019.
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  18. ^ "CORKs". Ocean Networks Canada. 15 October 2012. Retrieved 18 July 2019.
  19. ^ Becker, Keir; Davis, Earl E. (31 October 2005). "A review of CORK designs and operations during the Ocean Drilling Program". Proceedings of the Integrated Ocean Drilling Program. 301. doi:10.2204/iodp.proc.301.104.2005. Retrieved 23 August 2019.
  20. ^ "Packers and Flowmeters Tool Sheet". Overview of Ocean Drilling Program Engineering Tools and Hardware. Ocean Drilling Program. Retrieved 23 August 2019.
  21. ^ Kulin, Ian; Riedel, Michael; Klaus, Adam (2013). "Simple cabled instrument for measuring Parameters In situ (SCIMPI) and Hole 858G CORK replacement". IODP Scientific Prospectus. 341S. doi:10.2204/iodp.sp.341S.2013.
  22. ^ Purkamo, Lotta; Bomberg, Malin; Nyyssönen, Mari; Kukkonen, Ilmo; Ahonen, Lasse; Kietäväinen, Riikka; Itävaara, Merja (2013). "Dissecting the deep biosphere: retrieving authentic microbial communities from packer-isolated deep crystalline bedrock fracture zones". FEMS Microbiology Ecology. 85 (2): 324–337. doi:10.1111/1574-6941.12126. ISSN 1574-6941.
  23. ^ Nurmi, Pekka A.; Kukkonen, Ilmo T. (1986). "A new technique for sampling water and gas from deep drill holes". Canadian Journal of Earth Sciences. 23: 1540-1454.
  24. ^ Kietäväinen, Riikka; Ahonen, Lasse; Kukkonen, Ilmo T.; Hendriksson, Nina; Nyyssönen, Mari; Itävaara, Merja (2013-05-01). "Characterisation and isotopic evolution of saline waters of the Outokumpu Deep Drill Hole, Finland – Implications for water origin and deep terrestrial biosphere". Applied Geochemistry. Special Issue Devoted to the 9th International Symposium on Applied Isotope Geochemistry (AIG9), Tarragona, Spain, September 2011. 32: 37–51. doi:10.1016/j.apgeochem.2012.10.013. ISSN 0883-2927.
  25. ^ Haggerty, R.; Schroth, M.H.; Istok, J.D. (March 1998). "Simplified Method of "Push-Pull" Test Data Analysis for Determining In Situ Reaction Rate Coefficients". Ground Water. 36 (2): 314–324. doi:10.1111/j.1745-6584.1998.tb01097.x.
  26. ^ Sanders, Robert (5 May 2005). "Proteomics brings researchers closer to understanding microbes that produce acid mine drainage" (Press release). University of California Berkeley. Retrieved 2019-07-19.
  27. ^ Orell, Alvaro; Fröls, Sabrina; Albers, Sonja-Verena (8 September 2013). "Archaeal Biofilms: The Great Unexplored". Annual Review of Microbiology. 67 (1): 337–354. doi:10.1146/annurev-micro-092412-155616.
  28. ^ a b Collins, Terry; Pratt, Katie (10 December 2018). "Life in deep Earth totals 15 to 23 billion tonnes of carbon—hundreds of times more than humans" (Press release). Deep Carbon Observatory. Retrieved 2019-07-14.
  29. ^ Gold, T. (1992-07-01). "The deep, hot biosphere". Proceedings of the National Academy of Sciences. 89 (13): 6045–6049. doi:10.1073/pnas.89.13.6045. ISSN 0027-8424. PMID 1631089.
  30. ^ Amos, Jonathan (10 December 2018). "The vast scale of life beneath our feet". BBC News. Retrieved 14 July 2019.
  31. ^ Abe, Shige (10 October 2008). "Life without the Sun". Astrobiology at NASA. Retrieved 16 July 2019.
  32. ^ Magnabosco, C.; Lin, L.-H.; Dong, H.; Bomberg, M.; Ghiorse, W.; Stan-Lotter, H.; Pedersen, K.; Kieft, T. L.; van Heerden, E.; Onstott, T. C. (24 September 2018). "The biomass and biodiversity of the continental subsurface". Nature Geoscience. 11 (10): 707–717. doi:10.1038/s41561-018-0221-6.
  33. ^ Mosher, Dave (2 June 2011). "New "Devil Worm" Is Deepest-Living Animal". National Geographic News. Retrieved 2 July 2019.
  34. ^ "Deep life not limited to microbes: Earthquakes move surface animals to the deep" (Press release). Deep Carbon Observatory. 4 March 2019. Retrieved 2019-07-14.
  35. ^ Itävaara, Merja; Vikman, Minna; Salavirta, Heikki; Nyyssönen, Mari; Miettinen, Hanna; Bomberg, Malin; Sohlberg, Elina (2015). "Revealing the unexplored fungal communities in deep groundwater of crystalline bedrock fracture zones in Olkiluoto, Finland". Frontiers in Microbiology. 6. doi:10.3389/fmicb.2015.00573. ISSN 1664-302X.{{cite journal}}: CS1 maint: unflagged free DOI (link)
  36. ^ Bomberg, Malin; Itävaara, Merja; Kukkonen, Ilmo; Sohlberg, Elina; Miettinen, Hanna; Kietäväinen, Riikka; Purkamo, Lotta (2018-08-01). "Diversity and functionality of archaeal, bacterial and fungal communities in deep Archaean bedrock groundwater". FEMS Microbiology Ecology. 94 (8). doi:10.1093/femsec/fiy116. ISSN 0168-6496.
  37. ^ "Fungi are key players of the deep biosphere". ScienceDaily. Retrieved 2019-08-22.
  38. ^ Borgonie, G.; Linage-Alvarez, B.; Ojo, A. O.; Mundle, S.O.C.; Freese, L B.; Van Rooyen, C.; Kuloyo, O.; Albertyn, J.; Pohl, C.; Cason, E. D.; Vermeulen, J.; Pienaar, C.; Litthauer, D.; Van Niekerk, H.; Van Eeden, J.; Lollar, B. Sherwood.; Onstott, T. C.; Van Heerden, E. (24 November 2015). "Eukaryotic opportunists dominate the deep-subsurface biosphere in South Africa". Nature Communications. 6 (1). doi:10.1038/ncomms9952. PMC 4673884.
  39. ^ Ravindran, Sandeep (29 February 2016). "Inner Earth Is Teeming With Exotic Forms of Life". Smithsonian. Retrieved 14 July 2019.
  40. ^ Cite error: The named reference Colwell was invoked but never defined (see the help page).
  41. ^ "Guide to the Edson Sunderland Bastin Papers 1913–1922". The University of Chicago Library. Retrieved 4 July 2019.

Sources

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