The deep, dark energy biosphere: Intraterrestrial life on earth

Annual Review of Earth and Planetary Sciences

Volumn 40, Issue , 2012, Pages 551-568

  Edwards, Katrina J ^a   Becker, Keir ^b   Colwell, Frederick ^c  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF MIAMI   (United States)

^c OREGON STATE UNIVERSITY   (United States)

Author keywords

Continental subsurface; Extreme environments; Geochemistry; Geomicrobiology; Hydrogeology; Marine microbiology

Indexed keywords

BIOGEOCHEMICAL PROCESS; CONTINENTAL SUBSURFACE; DARK ENERGY; EXTREME ENVIRONMENT; GEOMICROBIOLOGY; IN-SITU; SOUTH AFRICA;

BIOSPHERICS; GEOCHEMISTRY; GROUNDWATER; HYDROGEOLOGY; MARINE BIOLOGY; RESEARCH;

ECOSYSTEMS;

BIOGEOCHEMISTRY; EXTREME EVENT; GEOMICROBIOLOGY; GYRE; HYDROGEOLOGY; MARINE SEDIMENT; MINE;

SOUTH AFRICA;

EID: 84860498769     PISSN: 00846597     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev-earth-042711-105500     Document Type: Article

References (91)

1. Amy PS, Haldeman DL. 1997. The Microbiology of the Terrestrial Deep Subsurface. New York: CRC
2. Anderson R, Chapelle F, Lovley D. 1998. Evidence against hydrogen-based microbial ecosystems in basalt aquifers. Science 281:976-77 (Pubitemid 28399243)
3. Bach W, Edwards KJ. 2003. Iron and sulfide oxidation within the basaltic ocean crust: implications for chemolithoautotrophic microbial biomass production. Geochim. Cosmochim. Acta 67:3871-87 (Pubitemid 37312329)
4. Bach W, Edwards KJ, Hayes JM, Sievert S, Huber JA, Sogin ML. 2006. Energy in the dark: fuel for life in the deep ocean and beyond. Eos Trans. AGU 87(7):73-78
5. Baker BJ, Tyson GW, Webb RI, Flanagan J, Hugenholtz P, et al. 2006. Lineages of acidophilic archaea revealed by community genomic analysis. Science 314(5807):1933-35 (Pubitemid 46026116)
6. Banerjee NR, Muehlenbachs K. 2003. Tuff life: bioalteration in volcaniclastic rocks from the Ontong Java Plateau. Geochem. Geophys. Geosyst. 4(4):1037
7. Becker K, Davis EE. 2005. A review of CORK designs and operations during the Ocean Drilling Program. Proc. Integr. Ocean Drill. Program, ed. AT Fisher, T Urabe, A Klaus, 301:MS 301-104. Washington, DC: Integr. Ocean Drill. Program Manag. Intl. doi:10. 2204/iodp. proc. 301. 104. 2005
8. Becker K, Langseth RP, Von Herzen RP, Erickson AJ, Jolivet J. 1983. Deep crustal geothermalmeasurements, Hole 504B, Costa Rica Rift. J. Geophys. Res. 88:3447-57
9. Becker K, Party LBS, Davis EE. 1998. Leg 174B revisits hole 395A: logging and long-term monitoring of off-axis hydrothermal processes in young oceanic crust. JOIDES J. 24:1-3
10. Bhartia R, Salas EC, Hug WF, Reid RD, Lane AL, et al. 2010. Label-free bacterial imaging with deep-UVlaser-induced native fluorescence. Appl. Environ. Microbiol. 76:7231-37
11. Borgonie G, Garcis-Moyano A, Litthauer D, Bert W, Bester A, et al. 2011. Nematoda from the terrestrial deep subsurface of South Africa. Nature 474:79-82
12. Brierley CL. 1978. Bacterial leaching. CRC Crit. Rev. Microbiol. 6(3):207-61
13. Chapelle FH, O'Neill K, Bradley PM, Meth́e BA, Ciufo SA, et al. 2002. Ahydrogen-based subsurface microbial community dominated by methanogens. Nature 415:312-15 (Pubitemid 34092297)
14. Chapelle FH, Zelibor J, Grimes D, Knobel L. 1987. Bacteria in deep coastal plain sediments of Maryland: a possible source of CO2 to groundwater. Water Resour. Res. 23:1625-32 (Pubitemid 17634267)
15. Chivian D, Brodie EL, Alm EJ, Culley DE, Dehal PS, et al. 2008. Environmental genomics reveals a singlespecies ecosystem deep within Earth. Science 322(5899):275-78
16. Cowen JP, Giovannoni SJ, Kenig F, Johnson HP, Butterfield D, et al. 2003. Fluids from aging ocean crust that support microbial life. Science 299:120-23 (Pubitemid 36042417)
17. D'Hondt S, Inagaki F, Zarikian CA. 2010. South Pacific Gyre microbiology. Integr. Ocean Drill. Program Sci. Prospectus 329, Integr. Ocean Drill. Program Manag. Intl., Wash., DC. doi:10. 2204/iodp. sp. 329. 2010
18. D'Hondt S, Jørgensen BB, Miller DJ, Batzke A, Blake R, et al. 2004. Distributions of microbial activities in deep subseafloor sediments. Science 306:2216-21 (Pubitemid 40024451)
19. D'Hondt S, Spivack AJ, Pockalny R, Ferdelman TG, Fisher JP, et al. 2009. Subseafloor sedimentary life in the South Pacific Gyre. Proc. Natl. Acad. Sci. USA 106:11651-56
20. Davis EE, Becker K, Pettigrew T, Carson B, MacDonald R. 1992a. CORK: a hydrological sea and downhole observatory for deep-ocean boreholes. Proc. Ocean Drill. Program Initial Rep., ed. EE Davis, MJ Mottl, AT Fisher, et al., 139:43-53. College Station, TX: Ocean Drill. Program (Pubitemid 23386854)
21. Davis EE, Chapman DS, Motti MJ, BentkowskiWJ, Dadey K, et al. 1992b. Flankflux: an experiment to study the nature of hydrothermal circulation in young oceanic crust. Can. J. Earth Sci. 29(5):925-52 (Pubitemid 23385485)
22. Deming JW, Baross JA. 1993. Deep-sea smokers: windows to a subsurface biosphere? Geochim. Cosmochim. Acta 57:3219-30 (Pubitemid 24418503)
23. Denef VJ, Kalnejais LH, Mueller RS, Wilmes P, Baker BJ, et al. 2010. Proteogenomic basis for ecological divergence of closely related bacteria in natural acidophilic microbial communities. Proc. Natl. Acad. Sci. USA 107(6):2383-90
24. Edwards KJ, Bach W, Klaus A. 2010. Mid-Atlantic ridge flank microbiology: initiation of long-term coupled microbiological, geochemical, and hydrological experimentation within the seafloor at North Pond, western flank of the Mid-Atlantic ridge. Integr. Ocean Drill. Program Sci. Prospectus 336, Integr. Ocean Drill. Program Manag. Intl., Wash., D. C.
25. Edwards KJ, Glazer BT, Rouxel OJ, Bach W, Emerson D, et al. 2011. Ultra-diffuse hydrothermal venting supports Fe-oxidizing bacteria and massive umber deposition at 5000m off Hawaii. ISME J. 5:1748-58
26. Engel AS, Stern LA, Bennett PC. 2004. Microbial contributions to cave formation: new insights into sulfuric acid speleogenesis. Geology 32:369-72 (Pubitemid 38616687)
27. Fisher AT, Wheat CG, Becker K, Cowen J, Orcutt B, et al. 2011. Design, deployment, and status of borehole observatory systems used for single-hole and cross-hole experiments, IODP Expedition 327, eastern flank of the Juan de Fuca Ridge. Proc. Integr. Ocean Drill. Program, ed. AT Fisher, T Tsuji, K Petronotis, Washington, DC: Integr. Ocean Drill. Program Manag. Intl. doi:10. 2204/iodp. proc. 327. 107. 2011
28. Fisher AT, Wheat CG, Becker K, Davis EE, Jannasch H, et al. 2005. Scientific and technical design and deployment of long-term subseafloor observatories for hydrogeologic and related experiments, IODP Expedition 301, eastern flank of Juan de Fuca Ridge. Proc Integr. Ocean Drill. Program, ed. AT Fisher, T Urabe, A Klaus, 301:MS 301-103. Washington, DC: Integr. Ocean Drill. Program Manag. Intl. doi:10. 2204/iodp. proc. 301. 103. 2005
29. Fisk MR, Giovannoni SJ, Thoreth IH. 1998. Alteration of oceanic volcanic glass: textural evidence ofmicrobial activity. Science 281:978-80 (Pubitemid 28399244)
30. Fredrickson JK, Balkwill DL. 2006. Geomicrobial processes and biodiversity in the deep terrestrial subsurface. Geomicrobiol. J. 23:345-56 (Pubitemid 44446541)
31. Fredrickson JK, Fletcher M. 2001. Subsurface Microbiology and Biogeochemistry. New York:Wiley-Liss. 329 pp.
32. Gold T. 1992. The deep, hot biosphere. Proc. Natl. Acad. Sci. USA 89:6045-49
33. Griffin WT, Phelps TJ, Colwell FS, Fredrickson JK. 1997. Sampling by drilling. See Amy & Haldeman 1997, pp. 23-44
34. Haldeman DL, Amy PS, RingelbergD, White DC. 1993. Characterization of the microbiology within a 21m3 section of rock from the deep subsurface. Microb. Ecol. 26:145-59
35. Harvey RW. 1997. Microorganisms as tracers in groundwater injection and recovery experiments: a review. FEMS Microbiol. Rev. 20:461-72
36. Harvey RW, Kinner NE, Bunn A, MacDonald D, Metge D. 1995. Transport behavior of groundwater protozoa and protozoan sized microspheres in sandy aquifer sediments. Appl. Environ. Microbiol. 61:209-17
37. Harvey RW, Smith RL, George L. 1984. Effect of organic contamination upon microbial distributions and heterotrophic uptake in a Cape Cod, Massachusetts, aquifer. Appl. Environ. Microbiol. 48:1197-202 (Pubitemid 15190693)
38. Head IM, Jones DM, Larter SR. 2003. Biological activity in the deep subsurface and the origin of heavy oil. Nature 426(6964):344-52 (Pubitemid 37463157)
39. Huber JA, Butterfield DA, Baross JA. 2002. Temporal changes in archaeal diversity and chemistry in a midocean ridge subseafloor habitat. Appl. Environ. Microbiol. 68(4):1585-94 (Pubitemid 34279962)
40. Huber JA, Butterfield DA, Baross JA. 2003. Bacterial diversity in a subseafloor habitat following a deep-sea volcanic eruption. FEMS Microbiol. Ecol. 43(3):393-409
41. Huber JA, Johnson HP, Butterfield DA, Baross JA. 2006. Microbial life in ridge flank crustal fluids. Environ. Microbiol. 8:88-99
42. Hyndman RD, Von Herzen RP, Erickson AJ, Jolivet J. 1976. Heat flow measurements in deep crustal holes on the Mid-Atlantic Ridge. J. Geophys. Res. 81:4053-60
43. Jannasch HW, Davis EE, KastnerM, Morris JD, Pettigrew TL, et al. 2003. CORK-II: long-term monitoring of fluid chemistry, fluxes, and hydrology in instrumented boreholes at the Costa Rica subduction zone. Proc. Ocean Drill. Program, ed. JD Morris, HWVillinger, A Klaus, 205:1-36. College Station, TX: Ocean Drill. Program
44. Kennedy CB, Scott JH, Ferris FG. 2003a. Characterization of bacteriogenic iron oxide deposits from Axial Volcano, Juan de Fuca Ridge, northeast Pacific Ocean. Geomicrobiol. J. 20:199-214 (Pubitemid 36971738)
45. Kennedy CB, Scott SD, Ferris FG. 2003b. Ultrastructure and potential sub-seafloor evidence of bacteriogenic iron oxides from Axial Volcano, Juan de Fuca Ridge, northeast Pacific Ocean. FEMS Microbiol. Ecol. 43:247-54 (Pubitemid 36197885)
46. Kinner NE, Harvey RW, Shay DM, Metge DW, Warren A. 2002. Field evidence for a protistan role in an organically-contaminated aquifer. Environ. Sci. Technol. 36(20):4312-18
47. Lin L-H, Wang P-L, Rumble D, Lippman-Pipke J, Boice E, et al. 2006. Long-term sustainability of a highenergy, low-diversity crustal biome. Science 314(5798):479-82
48. Mason OU, Nakagawa T, Rosner M, Van Nostrand JD, Zhou J, et al. 2010. First investigation of the microbiology of the deepest layer of ocean crust. PLoS ONE 5:e15399
49. Mikada H, Becker K, Moore JG, Klaus A, Party S. 2002. Volume 196 Initial Reports. College Station, TX: Ocean Drill. Program. http://www-odp. tamu. edu/publications/196-IR/196TOC. HTM
50. Morita RY. 2000. Is H2 the universal energy source for long-term survivaL̈ Microb. Ecol. 38:307-20 (Pubitemid 30231080)
51. Morita RY, ZoBell CE. 1955. Occurrence of bacteria in pelagic sediments collected during the Mid-Pacific Expedition. Deep-Sea Res. 3:66-73
52. Moses V. 1987. Microbes and oil recovery. Microbial. Sci. 4:306-9
53. Murphy EM, Schramke JA. 1998. Estimation of microbial respiration rates in groundwater by geochemical modeling constrained by stable isotopes. Geochim. Cosmochim. Acta 62:3395-406 (Pubitemid 29298543)
54. Murphy EM, Schramke JA, Frederickson JK, BledsoeHW, Francis AJ, et al. 1992. The influence of microbial activity and sedimentary organic carbon on the isotope geochemistry of the Middendorf Aquifer. Water Resour. Res. 28:723-40
55. 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(9):405-10 (Pubitemid 41207173)
56. Newby DT, Reed DW, Petzke LM, Igoe AL, DelwicheME, et al. 2004. Diversity of methanotroph communities in a basalt aquifer. FEMS Microbiol. Ecol. 48:333-44 (Pubitemid 38648921)
57. NielsenME, Fisk MR, Istok JD, Pedersen K. 2006. Microbial nitrate respiration of lactate at in situ conditions in ground water from a granitic aquifer situated 450 m underground. Geobiology 4:43-52
58. Northrup DE, Lavoie KH. 2001. Geomicrobiology of caves: a review. Geomicrobiol. J. 18:199-222 (Pubitemid 32901547)
59. Onstott TC. 2004. Impact of CO2 injections on deep subsurface microbial ecosystems and potential ramifications for the surface biosphere. In The CO2 Capture and Storage Project, Vol. II, ed. DC Thomas, SM Benson, pp. 1207-39. Berkeley, CA: Lawrence Berkeley Natl. Lab.
60. Onstott TC, McGown DJ, Bakermans C, Ruskeeniemi T, Ahonen L, et al. 2009. Microbial communities in subpermafrost saline fracture water at the Lupin Au Mine, Nunavut, Canada. Microb. Ecol. 58:786-807
61. Onstott TC, Moser DP, Pfiffner SM, Fredrickson JK, Brockman FJ, et al. 2003. Indigenous and contaminant microbes in ultradeep mines. Environ. Microbiol. 5(11):1168-91 (Pubitemid 37417788)
62. Orcutt BN, Bach W, Becker K, Fisher AT, Hentscher M, et al. 2011. Colonization of subsurface microbial observatories deployed in young ocean crust. ISME J. 5:692-703
63. Orcutt BN, Wheat CG, Edwards KJ. 2010. Subseafloor ocean crust microbial observatories: development of FLOCS (FLow-through Osmo Colonization System) and evaluation of borehole construction methods. Geomicrobiol. J. 27:143-57
64. Parkes RJ, Cragg BA, Wellsbury P. 2000. Recent studies on bacterial populations and processes in subseafloor sediments: a review. Hydrogeol. J. 8(1):11-28
65. Pedersen K. 1996. Investigations of subterranean bacteria in deep crystalline bedrock and their importance for the disposal of nuclear waste. Can. J. Microbiol. 42:382-91
66. Pedersen K. 1997. Microbial life in deep granitic rock. FEMS Microbiol. Rev. 20:399-414 (Pubitemid 27381912)
67. Pedersen K. 2000. Exploration of deep intraterrestrial microbial life: current perspectives. FEMS Microbiol. Lett. 185:9-16 (Pubitemid 30145600)
68. Phelps TJ, FliermansCB, GarlandTR, Pfiffner SM, WhiteDC. 1989. Methods for recovery of deep terrestrial subsurface sediments of microbiological studies. J. Microbiol. Methods 9:267-79
69. Phelps TJ, Murphy EM, Pfiffner SM, White DC. 1994. Comparison between geochemical and biological estimates of subsurface microbial activities. Microb. Ecol. 28:335-49
70. Rastogi G, Osman S, Kukkadapu R, EngelhardM, Vaishampayan PA, et al. 2010. Microbial andmineralogical characterizations of soils collected from the deep biosphere of the former Homestake gold mine, South Dakota. Microb. Ecol. 60:539-50
71. 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(4):371-84
72. Rebata-Landa V, Santamarina JC. 2006. Mechanical limits to microbial activity in deep sediments. Geochem. Geophys. Geosyst. 7:Q11006
73. Russell CE, Jacobson R, Haldeman DL, Amy PS. 1994. Heterogeneity of deep subsurface microorganisms and correlations to hydrogeological and geochemical parameters. Geomicrobiol. J. 12:37-51 (Pubitemid 2125645)
74. Santelli CM, Bach W, Banerjee NR, Edwards KJ. 2010. Tapping the subsurface ocean crust biosphere: Low biomass and drilling-related contamination calls for improved quality controls. Geomicrobiol. J. 27:158-69
75. Schrenk MO, Huber JA, Edwards KJ. 2009. Microbial provinces in the subseafloor. Oceanography 2:85-110
76. Shipboard Sci. Party. 2003. Leg 201 summary. Proc. Ocean Drill. Program Initial Rep., ed. S D'Hondt, BB Jørgensen, DJ Miller, et al., 201:1-81. College Station, TX: Ocean Drill. Program. doi: 10. 2973/odp. proc. ir. 201. 2003
77. Smith A, Popa R, Fisk MR, Nielsen M, Wheat CG, et al. 2011. In situ enrichment of ocean crust microbes on igneous minerals and glasses using an osmotic flow-through device. Geochem. Geophys. Geosyst. 12:Q06007
78. Smith DC, Spivack AJ, Fisk MR, Haveman SA, StaudigelH. 2000. Tracer-based estimates of drilling-induced microbial contamination of deep sea crust. Geomicrobiol. J. 17:207-17
79. Smith RL, Harvey RW, LeBlanc DR. 1991. Importance of closely spaced vertical sampling in delineating chemical and microbiological gradients in groundwater studies. J. Contam. Hydrol. 7:285-300
80. Spear JR, Walker JJ, McCollomTM, Pace NR. 2005. Hydrogen and bioenergetics in the Yellowstone geothermal ecosystem. Proc. Natl. Acad. Sci. USA 102(7):2555-60 (Pubitemid 40279415)
81. Stein CA, Stein S. 1994. Constraints on hydrothermal heat flux through the oceanic lithosphere from global heat flow. J. Geophys. Res. 99:3081-95 (Pubitemid 24425293)
82. Stevens TO. 1997. Subsurface microbiology and the evolution of the biosphere. See Amy & Haldeman 1997, pp. 205-23
83. Stevens TO, McKinley JP. 1995. Lithoautotrophic microbial ecosystems in deep basalt aquifers. Science 270:450-54 (Pubitemid 26449451)
84. Stevens TO, McKinley JP. 2000. Abiotic controls on hydrogen production from basalt-water reactions and implications for aquifer biogeochemistry. Environ. Sci. Technol. 34:826-31 (Pubitemid 30129826)
85. Takai K, Komatsu T, Inagaki F, Horikoshi K. 2001. Distribution of archaea in a black smoker chimney structure. Appl. Environ. Microbiol. 67:3618-29 (Pubitemid 33641234)
86. Tarafa ME, Whelan JK, Oremland RS, Smith RL. 1987. Evidence of the microbiological activity in leg 95 (New Jersey transect) sediments. Rep. Deep-Sea Drill. Proj. XCV, Texas A&M Univ. Coll. Geosci., Wash., DC
87. Walker A, Parkhill J. 2008. Single-cell genomics. Nat. Rev. Microbiol. 6:176-77 (Pubitemid 351256312)
88. Wanger G, Onstott TC, Southam G. 2008. Stars of the terrestrial deep subsurface: a novel 'star-shaped' bacterial morphotype from a South African platinum mine. Geobiology 6:325-30 (Pubitemid 351733138)
89. Whelan JJ, Oremland R, Tarafa M, Smith R, Howarth R, Lee C. 1986. Evidence for sulfate-reducing and methane-producing microorganisms in sediments from sites 618, 619, and 622. Rep. Deep-Sea Drill. Proj. XCVI, Texas A&M Univ. Coll. Geosci., Wash., DC
90. Whitman WB, Coleman DC, WiebeWJ. 1998. Prokaryotes: the unseen majority. Proc. Natl. Acad. Sci. USA 95:6578-83 (Pubitemid 28278022)
91. ZoBell CE, Anderson QA. 1936. Vertical distribution of bacteria in marine sediments. Bull. Am. Assoc. Petrol. Geol. 20(3):258-69