Early anaerobic metabolisms

Before the advent of oxygenic photosynthesis, the biosphere was driven by anaerobic metabolisms. We catalogue and quantify the source strengths of the most probable electron donors and electron acceptors that would have been available to fuel early-Earth ecosystems. The most active ecosystems were probably driven by the cycling of H2 and Fe2+ through primary production conducted by anoxygenic phototrophs. Interesting and dynamic ecosystems would have also been driven by the microbial cycling of sulphur and nitrogen species, but their activity levels were probably not so great. Despite the diversity of potential early ecosystems, rates of primary production in the early-Earth anaerobic biosphere were probably well below those rates observed in the marine environment. We shift our attention to the Earth environment at 3.8 Gyr ago, where the earliest marine sediments are preserved. We calculate, consistent with the carbon isotope record and other considerations of the carbon cycle, that marine rates of primary production at this time were probably an order of magnitude (or more) less than today. We conclude that the flux of reduced species to the Earth surface at this time may have been sufficient to drive anaerobic ecosystems of sufficient activity to be consistent with the carbon isotope record. Conversely, an ecosystem based on oxygenic photosynthesis was also possible with complete removal of the oxygen by reaction with reduced species from the mantle.

[1]  W. Peltier.  The Phanerozoic Carbon Cycle: CO2 and O2 by Robert A. Berner , 2006 .

[2]  W. Horwath.  The Phanerozoic Carbon Cycle , 2006 .

[3]  H. Paulick,et al.  Unraveling the sequence of serpentinization reactions: petrography, mineral chemistry, and petrophysics of serpentinites from MAR 15°N (ODP Leg 209, Site 1274) , 2006 .

[4]  J. Hayes,et al.  The carbon cycle and associated redox processes through time , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[5]  Keita Yamada,et al.  Evidence from fluid inclusions for microbial methanogenesis in the early Archaean era , 2006, Nature.

[6]  J. Olson.  Photosynthesis in the Archean Era , 2006, Photosynthesis Research.

[7]  D. Newman,et al.  Deposition of banded iron formations by anoxygenic phototrophic Fe(II)-oxidizing bacteria , 2005 .

[8]  D. Catling,et al.  How Earth's atmosphere evolved to an oxic state: A status report , 2005 .

[9]  D. Newman,et al.  Isolation and Characterization of a Genetically Tractable Photoautotrophic Fe(II)-Oxidizing Bacterium, Rhodopseudomonas palustris Strain TIE-1 , 2005, Applied and Environmental Microbiology.

[10]  S. Wilde,et al.  Magmatic δ18O in 4400–3900 Ma detrital zircons: A record of the alteration and recycling of crust in the Early Archean , 2005 .

[11]  W. Seyfried,et al.  Hydrothermal Fe fluxes during the Precambrian: Effect of low oceanic sulfate concentrations and low hydrostatic pressure on the composition of black smokers [rapid communication] , 2005 .

[12]  D. Canfield.  THE EARLY HISTORY OF ATMOSPHERIC OXYGEN: Homage to Robert M. Garrels , 2005 .

[13]  Alexander A. Pavlov,et al.  A Hydrogen-Rich Early Earth Atmosphere , 2005, Science.

[14]  R. Amann,et al.  Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[15]  D. Canfield,et al.  Anaerobic ammonium oxidation (anammox) in the marine environment. , 2005, Research in microbiology.

[16]  James F. Kasting,et al.  A coupled atmosphere–ecosystem model of the early Archean Earth , 2005 .

[17]  N. Pfennig.  The phototrophic bacteria and their role in the sulfur cycle , 1975, Plant and Soil.

[18]  S. A. Wildeb,et al.  Magmatic y 18 O in 4400 – 3900 Ma detrital zircons : A record of the alteration and recycling of crust in the Early Archean , 2005 .

[19]  D. Canfield,et al.  Aquatic geomicrobiology. , 2005, Advances in marine biology.

[20]  D. Canfield,et al.  THE EARLY HISTORY OF ATMOSPHERIC OXYGEN , 2005 .

[21]  C. McKay,et al.  The evolution of nitrogen cycling , 2005, Origins of life and evolution of the biosphere.

[22]  D. Canfield.  The evolution of the Earth surface sulfur reservoir , 2004 .

[23]  Ole Leth,et al.  A mechanism for enhanced upwelling off central Chile: Eddy advection , 2004 .

[24]  Kentaro Nakamura,et al.  Carbonatization of oceanic crust by the seafloor hydrothermal activity and its significance as a CO2 sink in the Early Archean , 2004 .

[25]  S. Hedges,et al.  A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land , 2004, BMC Evolutionary Biology.

[26]  D. Canfield,et al.  New insights into the burial history of organic carbon on the early Earth , 2004 .

[27]  M. Rosing,et al.  U-rich Archaean sea-floor sediments from Greenland – indications of >3700 Ma oxygenic photosynthesis , 2004 .

[28]  John W. Delano,et al.  Redox History of the Earth's Interior since ∼3900 Ma: Implications for Prebiotic Molecules , 2001, Origins of life and evolution of the biosphere.

[29]  J. Olson,et al.  Thinking About the Evolution of Photosynthesis , 2004, Photosynthesis Research.

[30]  R. Berner.  The phanerozoic carbon cycle : CO[2] and O[2] , 2004 .

[31]  Robert Eugene Blankenship.  Origin and early evolution of photosynthesis , 2004, Photosynthesis Research.

[32]  J. Kasting,et al.  New insights into Archean sulfur cycle from mass-independent sulfur isotope records from the Hamersley Basin, Australia , 2003 .

[33]  D. Canfield,et al.  N2 production by the anammox reaction in the anoxic water column of Golfo Dulce, Costa Rica , 2003, Nature.

[34]  J. G. Kuenen,et al.  Anaerobic ammonium oxidation by anammox bacteria in the Black Sea , 2003, Nature.

[35]  A. Knoll.  Life on a Young Planet: The First Three Billion Years of Evolution on Earth , 2003 .

[36]  W. Shanks,et al.  Serpentinization of abyssal peridotites from the MARK area, Mid-Atlantic Ridge: Sulfur geochemistry and reaction modeling , 2003 .

[37]  Heinrich D. Holland,et al.  Volcanic gases, black smokers, and the great oxidation event , 2002 .

[38]  Hans-F. Graf,et al.  The annual volcanic gas input into the atmosphere, in particular into the stratosphere: a global data set for the past 100 years , 2002 .

[39]  Donald E. Canfield,et al.  Ocean productivity before about 1.9 Gyr ago limited by phosphorus adsorption onto iron oxides , 2002, Nature.

[40]  D. Canil.  Vanadium in peridotites, mantle redox and tectonic environments: Archean to present , 2002 .

[41]  J. Kasting,et al.  Mass-independent fractionation of sulfur isotopes in Archean sediments: strong evidence for an anoxic Archean atmosphere. , 2002, Astrobiology.

[42]  S. Airieau,et al.  Observation of wavelength‐sensitive mass‐independent sulfur isotope effects during SO2 photolysis: Implications for the early atmosphere , 2001 .

[43]  J. Kasting,et al.  UV shielding of NH3 and O2 by organic hazes in the Archean atmosphere , 2001 .

[44]  K. Zahnle,et al.  Biogenic Methane, Hydrogen Escape, and the Irreversible Oxidation of Early Earth , 2001, Science.

[45]  Christopher P. McKay,et al.  A possible nitrogen crisis for Archaean life due to reduced nitrogen fixation by lightning , 2001, Nature.

[46]  Donald E. Canfield,et al.  Isotopic evidence for microbial sulphate reduction in the early Archaean era , 2001, Nature.

[47]  N. Sleep,et al.  The habitat and nature of early life , 2001, Nature.

[48]  N. Sleep,et al.  Carbon dioxide cycling and implications for climate on ancient Earth , 2001 .

[49]  Simon A. Wilde,et al.  Evidence from detrital zircons for the existence of continental crust and oceans on the Earth 4.4 Gyr ago , 2001, Nature.

[50]  J. Kasting,et al.  Rise of atmospheric oxygen and the “upside‐down” Archean mantle , 2001 .

[51]  R. Castenholz,et al.  Phylum BVI. Chloroflexi phy. nov. , 2001 .

[52]  Robert Eugene Blankenship.  Molecular evidence for the evolution of photosynthesis. , 2001, Trends in plant science.

[53]  Stirred, Not Shaken , 2000, Science.

[54]  D. D. Marais,et al.  When Did Photosynthesis Emerge on Earth? , 2000, Science.

[55]  C. Bauer,et al.  Molecular evidence for the early evolution of photosynthesis. , 2000, Science.

[56]  M. Thiemens,et al.  Atmospheric influence of Earth's earliest sulfur cycle , 2000, Science.

[57]  J. Veizer,et al.  Tectonic control of chemical and isotopic composition of ancient oceans; the impact of continental growth , 2000 .

[58]  D. J. De Marais,et al.  Evolution. When did photosynthesis emerge on Earth? , 2000, Science.

[59]  D. Canfield,et al.  The evolution of the sulfur cycle , 1999 .

[60]  A. J. Kaufman,et al.  THE ABUNDANCE OF 13C IN MARINE ORGANIC MATTER AND ISOTOPIC FRACTIONATION IN THE GLOBAL BIOGEOCHEMICAL CYCLE OF CARBON DURING THE PAST 800 MA , 1999 .

[61]  W. Ludwig,et al.  Chlorobium ferrooxidans sp. nov., a phototrophic green sulfur bacterium that oxidizes ferrous iron in coculture with a “Geospirillum” sp. strain , 1999, Archives of Microbiology.

[62]  Doolittle Wf.  Phylogenetic Classification and the Universal Tree , 1999 .

[63]  J. Lake,et al.  Horizontal gene transfer among genomes: the complexity hypothesis. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[64]  M. Rosing,et al.  13C-Depleted carbon microparticles in >3700-Ma sea-floor sedimentary rocks from west greenland , 1999, Science.

[65]  L. Orgel,et al.  Phylogenetic Classification and the Universal Tree , 1999 .

[66]  D. Canfield.  A new model for Proterozoic ocean chemistry , 1998, Nature.

[67]  T. Yoshinari,et al.  Isotopic composition of nitrate in the central Arabian Sea and eastern tropical North Pacific: A tracer for mixing and nitrogen cycles , 1998 .

[68]  G. Cody,et al.  Abiotic nitrogen reduction on the early Earth , 1998, Nature.

[69]  W. Dean,et al.  Organic‐matter production and preservation and evolution of anoxia in the Holocene Black Sea , 1998 .

[70]  J. Randerson,et al.  Primary production of the biosphere: integrating terrestrial and oceanic components , 1998, Science.

[71]  J F Nunn,et al.  Evolution of the atmosphere. , 1998, Proceedings of the Geologists' Association. Geologists' Association.

[72]  James R. Brown,et al.  Archaea and the prokaryote-to-eukaryote transition. , 1997, Microbiology and molecular biology reviews : MMBR.

[73]  B. Schink.  Energetics of syntrophic cooperation in methanogenic degradation , 1997, Microbiology and molecular biology reviews : MMBR.

[74]  K. Stetter.  Hyperthermophiles in the history of life. , 2007, Ciba Foundation symposium.

[75]  M. Rosing,et al.  Earliest part of Earth's stratigraphic record: A reappraisal of the >3.7 Ga Isua (Greenland) supracrustal sequence , 1996 .

[76]  William I. Rose,et al.  Chapter 1. VOLCANIC-GAS STUDIES: METHODS, RESULTS, AND APPLICATIONS , 1994 .

[77]  F. Widdel,et al.  Anaerobic oxidation of ferrous iron by purple bacteria, a new type of phototrophic metabolism , 1994, Applied and environmental microbiology.

[78]  D. Canfield,et al.  Factors influencing organic carbon preservation in marine sediments. , 1994, Chemical geology.

[79]  William I. Rose,et al.  Volcanic-gas studies: Methods, results, and applications , 1994 .

[80]  F. Widdel,et al.  Phototrophic oxidation of ferrous minerals — a new aspect in the redox microbiology of iron , 1994 .

[81]  F. Widdel,et al.  Ferrous iron oxidation by anoxygenic phototrophic bacteria , 1993, Nature.

[82]  K. Finster,et al.  Bacterial Disproportionation of Elemental Sulfur Coupled to Chemical Reduction of Iron or Manganese , 1993, Applied and environmental microbiology.

[83]  J. Gogarten,et al.  Horizontal transfer of ATPase genes--the tree of life becomes a net of life. , 1993, Bio Systems.

[84]  H. Strauss,et al.  Carbon isotope evidence for the stepwise oxidation of the Proterozoic environment , 1992, Nature.

[85]  A. Knoll,et al.  The evolution of ecological tolerance in prokaryotes , 1989, Earth and Environmental Science Transactions of the Royal Society of Edinburgh.

[86]  W. Reeburgh,et al.  Carbon and hydrogen isotope fractionation resulting from anaerobic methane oxidation , 1988 .

[87]  C. Klein,et al.  Chemistry, petrology and origin of banded iron-formation lithologies from the 3800 MA isua supracrustal belt, West Greenland , 1988 .

[88]  M. Schidlowski.  A 3,800-million-year isotopic record of life from carbon in sedimentary rocks , 1988, Nature.

[89]  C. Woese,et al.  Bacterial evolution , 1987, Microbiological reviews.

[90]  M. Arthur.  The Chemical Evolution of the Atmospheres and Oceans , 1986 .

[91]  T. D. Brock.  Life at High Temperatures , 1985, Science.

[92]  M. Gaffey,et al.  The Chemical Evolution of the Atmosphere and Oceans , 1984 .

[93]  J.-F. Minster,et al.  Tracers in the Sea , 1982 .

[94]  R. Garrels,et al.  Phanerozoic cycles of sedimentary carbon and sulfur. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[95]  J. Kasting,et al.  Limits on oxygen concentration in the prebiological atmosphere and the rate of abiotic fixation of nitrogen , 1981 .

[96]  W. Reeburgh.  Anaerobic methane oxidation: Rate depth distributions in Skan Bay sediments , 1980 .

[97]  M. McElroy,et al.  Fixation of Nitrogen in the Prebiotic Atmosphere , 1979, Science.

[98]  H. D. Holland.  The chemistry of the atmosphere and oceans , 1978 .

[99]  D. Hunten.  The Escape of Light Gases from Planetary Atmospheres , 1973 .

[100]  P. Cloud.  A working model of the primitive Earth , 1972 .

[101]  Harry Marlin Tinkcom,et al.  I. Early Life , 1940 .

[102]  L. Baas-Becking.  Studies on the Sulphur Bacteria , 1925 .

[103]  J. M. Pratt.  The Fixation of Nitrogen , 1924, Science.

[104]  F. Hauff,et al.  N 2 production by the anammox reaction in the anoxic water column of Golfo Dulce , Costa Rica , 2022 .