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Adaptations to energy stress dictate the ecology and evolution of the Archaea

Nature Reviews Microbiology volume 5, pages 316323 (2007) | Download Citation

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Abstract

The three domains of life on Earth include the two prokaryotic groups, Archaea and Bacteria. The Archaea are distinguished from Bacteriabased on phylogenetic and biochemical differences, but currently there is no unifying ecological principle to differentiate these groups. The ecology of the Archaea is reviewed here in terms of cellular bioenergetics. Adaptation to chronic energy stress is hypothesized to be the crucial factor that distinguishes the Archaea from Bacteria. The biochemical mechanisms that enable archaea to cope with chronic energy stress include low-permeability membranes and specific catabolic pathways. Based on the ecological unity and biochemical adaptations among archaea, I propose the hypothesis that chronic energy stress is the primary selective pressure governing the evolution of the Archaea.

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References

  1. 1.

    , & Archaebacteria. J. Mol. Evol. 11, 245–252 (1978).

  2. 2.

    & Archaeal genetics — the third way. Nature Rev. Gen. 6, 58–73 (2005).

  3. 3.

    Archaea in coastal marine environments. Proc. Natl Acad. Sci. USA 89, 5685–5689 (1992).

  4. 4.

    , & Novel major Archaebacterial group from marine plankton. Nature 356, 148–149 (1992).

  5. 5.

    , & Archaeal habitats — from the extreme to the ordinary. Can. J. Microbiol. 52, 73–116 (2006).

  6. 6.

    Biological energy requirements as quantitative boundary conditions for life in the subsurface. Geobiology 2, 205–215 (2004).

  7. 7.

    Bacteria in Oligotrophic Environments (Chapman and Hall, New York, 1997).

  8. 8.

    & Temperature dependence of metabolic rates for microbial growth, maintenance, and survival. Proc. Natl Acad. Sci. USA 101, 4631–4636 (2004).

  9. 9.

    et al. A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature 407, 623–626 (2000).

  10. 10.

    et al. Reverse methanogenesis: testing the hypothesis with environmental genomics. Science 305, 1457–1462 (2004).

  11. 11.

    , , , & Methane-consuming archaea revealed by directly coupled isotopic and phylogenetic analysis. Science 293, 484–487 (2001).

  12. 12.

    Biogeochemistry and microbial ecology of methane oxidation in anoxic environments: a review. Antonie Van Leeuwenhoek 81, 271–282 (2002).

  13. 13.

    Molecular ecology of extremely halophilic Archaea and Bacteria. FEMS Microbiol. Ecol. 39, 1–7 (2002).

  14. 14.

    The ecology of the extremely halophilic archaea. FEMS Microbiol. Rev. 13, 415–439 (1994).

  15. 15.

    , & Behavior of mixed populations of halophilic bacteria in continuous cultures. Can. J. Microbiol. 26, 1259–1263 (1980).

  16. 16.

    & Extending the upper temperature limit for life. Science 301, 934 (2003).

  17. 17.

    , & The essence of being extremophilic: the role of the unique archaeal membrane lipids. Extremophiles 2, 163–170 (1998).

  18. 18.

    , , , & Ion permeability of the cytoplasmic membrane limits the maximum growth temperature of bacteria and archaea. Mol. Microbiol. 18, 925–932 (1995).

  19. 19.

    , , & Bacterial and archaeal phylotypes associated with distinct mineralogical layers of a white smoker spire from a deep-sea hydrothermal vent site (9 degrees N, East Pacific Rise). Env. Microbiol. 8, 909–920 (2006).

  20. 20.

    , , & Incidence and diversity of microorganisms within the walls of an active deep-sea sulfide chimney. 69, 3580–3592 (2003).

  21. 21.

    , , & Hydrogen and bioenergetics in the Yellowstone geothermal ecosystem. 102, 2555–2560 (2005).

  22. 22.

    et al. Tetraether-linked membrane monolayers in Ferroplasma spp: a key to survival in acid. Extremophiles 8, 411–419 (2004).

  23. 23.

    , & Comparison of acid mine drainage microbial communities in physically and geochemically distinct ecosystems. Appl. Environ. Microbiol. 66, 4962–4971 (2000).

  24. 24.

    , , & Isolation and characterization of Acidicaldus organivorus, gen. nov., sp nov.: a novel sulfur-oxidizing, ferric iron-reducing thermo-acidophilic heterotrophic Proteobacterium. Arch. Microbiol. 185, 212–221 (2006).

  25. 25.

    , & Geochemical and biological diversity of acidic, hot springs in Lassen Volcanic National Park. Geomicrobiol. J. 23, 129–141 (2006).

  26. 26.

    et al. Archaeal nitrification in the ocean. Proc. Natl Acad. Sci. USA 103, 12317–12322 (2006).

  27. 27.

    , , , & Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc. Natl Acad. Sci. USA 102, 14683–14688 (2005).

  28. 28.

    et al. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442, 806–809 (2006).

  29. 29.

    et al. Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. Proc. Natl Acad. Sci. USA 103, 18296–18301 (2006).

  30. 30.

    et al. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437, 543–546 (2005).

  31. 31.

    , , , & Occurrence of ammonia-oxidizing archaea in wastewater treatment plant bioreactors. Appl. Environ. Microbiol. 72, 5643–5647 (2006).

  32. 32.

    et al. Quantifying archaeal community autotrophy in the mesopelagic ocean using natural radiocarbon. Proc. Natl Acad. Sci. USA 103, 6442–6447 (2006).

  33. 33.

    , & Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409, 507–510 (2001).

  34. 34.

    Biochemistry of methanogenesis: a tribute to Marjory Stephenson. Microbiology-UK 144, 2377–2406 (1998).

  35. 35.

    , , & Apparent minimum free energy requirements for methanogenic Archaea and sulfate-reducing bacteria in an anoxic marine sediment. FEMS Microbiol. Ecol. 38, 33–41 (2001).

  36. 36.

    Energetics of syntrophic cooperation in methanogenic degradation. Microbiol. Mol. Biol. Rev. 61, 262–280 (1997).

  37. 37.

    , , & Thermodynamic control on hydrogen concentrations in anoxic sediments. Geochim. Cosmochim. Acta 62, 1745–1756 (1998).

  38. 38.

    , & The capacity of hydrogenotrophic anaerobic bacteria to compete for traces of hydrogen depends on the redox potential of the terminal electron acceptor. Arch. Microbiol. 149, 350–357 (1988).

  39. 39.

    & Hydrogen concentrations as an indicator of the predominant terminal electron-accepting reactions in aquatic sediments. Geochim. Cosmochim. Acta 52, 2993–3003 (1988).

  40. 40.

    et al. A microbial consortium couples anaerobic methane oxidation to denitrification. Nature 440, 918–921 (2006).

  41. 41.

    , & Metabolic activity of subsurface life in deep-sea sediments. Science 295, 2067–2070 (2002).

  42. 42.

    , & Growth and population dynamics of anaerobic methane-oxidizing archaea and sulfate-reducing bacteria in a continuous-flow bioreactor. Appl. Environ. Microbiol. 71, 3725–3733 (2005).

  43. 43.

    , , & In vitro demonstration of anaerobic oxidation of methane coupled to sulphate reduction in sediment from a marine gas hydrate area. Environ. Microbiol. 4, 296–305 (2002).

  44. 44.

    & New perspectives on anaerobic methane oxidation. Environ. Microbiol. 2, 477–484 (2000).

  45. 45.

    , , & Field and laboratory studies of methane oxidation in an anoxic marine sediment — evidence for a methanogen–sulfate reducer consortium. Global Biogeochem. Cycles 8, 451–463 (1994).

  46. 46.

    et al. Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru. Proc. Natl Acad. Sci. USA 103, 3846–3851 (2006).

  47. 47.

    et al. Diversity of Archaea in marine sediments from Skan Bay, Alaska, including cultivation of methanogens and a description of Methanogenium boonei, sp. nov. Appl. Environ. Microbiol. 73, 407–414 (2007).

  48. 48.

    Microbial communities of deep marine subsurface sediments: molecular and cultivation surveys. Geomicrobiol. J. 23, 357–368 (2006).

  49. 49.

    Water transport across biological-membranes. FEBS Lett. 346, 115–122 (1994).

  50. 50.

    & Membranes and the setting of energy demand. J. Exp. Biol. 208, 1593–1599 (2005).

  51. 51.

    , , & Archaebacterial lipids — highly proton-impermeable membranes from 1, 2-diphytanyl-sn-glycero-3-phosphocholine. Biochim. Biophys. Acta 1146, 178–182 (1993).

  52. 52.

    , & Molecular mechanisms of water and solute transport across archaebacterial lipid membranes. J. Biol Chem. 276, 27266–27271 (2001).

  53. 53.

    , , & Bioenergetics and cytoplasmic membrane stability of the extremely acidophilic, thermophilic archaeon Picrophilus oshimae. Extremophiles 2, 67–74 (1998).

  54. 54.

    , , & Lipid membranes from halophilic and alkali-halophilic Archaea have a low H+ and Na+ permeability at high salt concentration. Extremophiles 3, 253–257 (1999).

  55. 55.

    Bacterial evolution. Microbiol. Rev. 51, 221–271 (1987).

  56. 56.

    et al. Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota. PLoS Biol. 4, e95 (2006).

  57. 57.

    , & A simple energy-conserving system: proton reduction coupled to proton translocation. Proc. Natl Acad. Sci. USA 100, 7545–7550 (2003).

  58. 58.

    in Methanogenesis: Ecology, Physiology, Biochemistry & Genetics (ed. Ferry, J. G.) 536 (Chapman & Hall, New York, 1993).

  59. 59.

    , , & Bioenergetics of the formyl-methanofuran dehydrogenase and heterodisulfide reductase reactions in Methanothermobacter thermautotrophicus. Eur. J. Biochem. 270, 66–75 (2003).

  60. 60.

    , & Environmental and molecular regulation of methanogenesis. Water Sci. Technol. 36, 1–6 (1997).

  61. 61.

    , , & Variation of carbon isotope fractionation in hydrogenotrophic methanogenic microbial cultures and environmental samples at different energy status. Global Change Biol. 11, 2103–2113 (2005).

  62. 62.

    , , , & Carbon and hydrogen isotope fractionation by moderately thermophilic methanogens. Geochim. Cosmochim. Acta 68, 1571–1590 (2004).

  63. 63.

    in Microbial Growth on C-1 Compounds (eds Lidstrom, M. E. & Tabita, R. F.) 335–342 (Kluwer Academic Publishers, 1996).

  64. 64.

    An exceptional variability in the motor of archaeal A1A0 ATPases: from multimeric to monomeric rotors comprising 6–13 ion binding sites. J. Bioenerg. Biomembr. 36, 115–125 (2004).

  65. 65.

    , , & ATP synthases with novel rotor subunits: new insights into structure, function and evolution of ATPases. J. Bioenerg. Biomembr. 37, 455–460 (2005).

  66. 66.

    List of bacterial names with standing in nomenclature: a folder available on the internet. Int. J. Syst. Bacteriol. 47, 590–592 (1997).

  67. 67.

    , & Lateral diffusion of the total polar lipids from Thermoplasma acidophilum in multilamellar liposomes. Biochim. Biophys. Acta 1369, 259–266 (1998).

  68. 68.

    , , & Hydration and molecular motions in synthetic phytanyl-chained glycolipid vesicle membranes. Biophys. J. 81, 3377–3386 (2001).

  69. 69.

    & Omega-3 fatty acids in cellular membranes: a unified concept. Prog. Lipid Res. 43, 383–402 (2004).

  70. 70.

    Do sterols reduce proton and sodium leaks through lipid bilayers? Prog. Lipid Res. 40, 299–324 (2001).

  71. 71.

    et al. Salinibacter ruber gen. nov., sp nov., a novel, extremely halophilic member of the Bacteria from saltern crystallizer ponds. Int. J. Syst. Evol. Microl. 52, 485–491 (2002).

  72. 72.

    et al. Aquifex pyrophilus gen. nov. sp. nov. represents a novel group of marine hyperthermophilic hydrogen-oxidizing Bacteria. Syst. Appl. Microbiol. 15, 340–351 (1992).

  73. 73.

    & Anaerobic microbial metabolism can proceed close to thermodynamic limits. Nature 415, 454–456 (2002).

  74. 74.

    , & Pure-culture growth of fermentative bacteria, facilitated by H2 removal: bioenergetics and H2 production. Appl. Environ. Microbiol. 72, 1079–1085 (2006).

  75. 75.

    , , & Energetics of syntrophic ethanol oxidation in defined chemostat cocultures. 1. Energy requirement for H2 production and H2 oxidation. Arch. Microbiol. 155, 82–88 (1990).

  76. 76.

    et al. Novel sulfonolipid in the extremely halophilic bacterium Salinibacter ruber. Appl. Environ. Microbiol. 70, 6678–6685 (2004).

  77. 77.

    et al. Prokaryotic cells of the deep sub-seafloor biosphere identified as living bacteria. Nature 433, 861–864 (2005).

  78. 78.

    , , & Direct in situ detection of cells in deep-sea sediment cores from the Peru Margin (ODP Leg 201, Site 1229). Geobiol. 2, 217–223 (2004).

  79. 79.

    et al. Massive expansion of marine archaea during a mid-Cretaceous oceanic anoxic event. Science 293, 92–94 (2001).

  80. 80.

    , , & Pathogenic archaea: do they exist? Bioessays 25, 1119–1128 (2003).

  81. 81.

    Archaebacteria then... archaes now (are there really no archaeal pathogens?). J. Bacteriol 181, 3613–3617 (1999).

  82. 82.

    , , & Acetogenesis from CO2 in an anoxic marine sediment. Limnol. Oceanogr. 44, 662–667 (1999).

  83. 83.

    , , & A psychrophilic crenarchaeon inhabits a marine sponge: Cenarchaeum symbiosum gen nov, sp, nov. Proc. Natl Acad. Sci. 93, 6241–6246 (1996).

  84. 84.

    & (eds) Bergey's manual of systematic bacteriology (Springer, New York, 2001).

  85. 85.

    , , & 2 Genetically distinct methyl-coenzyme M reductases in Methanobacterium thermoautotrophicum strain marburg and delta-H. Eur. J. Biochem. 194, 871–877 (1990).

  86. 86.

    & Influence of temperature on energetics of hydrogen metabolism in homoacetogenic, methanogenic, and other anaerobic bacteria. Arch. Microbiol. 155, 94–98 (1990).

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Acknowledgements

R.C. Valentine assisted in developing ideas about membrane function. C. Francis, J. Perona, M. Facciotti and C. Schleper provided useful comments on the manuscript. Support from the US National Science Foundation contributed to the formulation of this work.

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  1. David L. Valentine is at the Department of Earth Science and Marine Science Institute, University of California, Santa Barbara, California, 93106 USA.  valentine@geol.ucsb.edu

    • David L. Valentine

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The author declares no competing financial interests.

Glossary

Archaea

One of the three primary domains of life, inclusive of all organisms in the domain.

Archaeon

(archaea). An organism (organisms) belonging to the domain Archaea.

bacteria

A population or group of organisms belonging to the domain Bacteria.

Bacteria

One of the three primary domains of life, inclusive of all organisms within the domain.

Biological energy quantum

(BEQ). Finite minimum level of energy that an organism can conserve from catabolism.

Chemiosmotic

The use of an ion gradient across a membrane to generate ATP.

Clade

A hypothesis of evolutionary relatedness in which a group of organisms share a single common ancestor. In the context of microbial ecology this term is often used to indicate a group of organisms that have been shown to be monophyletic by comparative analysis of 16S rRNA or other conserved gene sequences.

Chronic energy stress

Condition in which cells are consistently faced with an insufficient supply of cellular energy. The stresses considered here to comprise chronic energy stress include the high rates of futile ion cycling driven by extreme temperature, acidity or salinity, as well as low rates of cellular energy generation due to limited substrate availability and/or unfavourable thermodynamic conditions.

Environmental exclusivity

The concept that some archaea are adapted to thrive in conditions that are inhospitable to bacteria.

Extremely halophilic

An organism that grows best in media that contains 2.5–5.2 M salt.

Maintenance energy

(ME). Minimum intake flux of energy (power) that is required to maintain molecular and cellular integrity as well as activity.

Metabolic exclusivity

The concept that dominance can be achieved by way of catabolic specialization.

Singularity of catabolism

Exclusive reliance on a single, highly specialized form of catabolism, such as methanogenesis.

Syntrophically

A syntrophic reaction is one in which two (or more) organisms interact metabolically to consume a substrate that neither can consume independently.

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https://doi.org/10.1038/nrmicro1619

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