Electrons, life and the evolution of Earth's oxygen cycle

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 363, Issue 1504, 2008, Pages 2705-2716

  Falkowski, Paul G ^a   Godfrey, Linda V ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

Archaean ocean; Biogeochemical cycles; Nitrogen isotopes; Oxygenic photosynthesis; Wilson cycle

Indexed keywords

AMMONIUM; ARCHEAN; BIOGEOCHEMICAL CYCLE; CATALYSIS; COEVOLUTION; DENITRIFICATION; ELECTRON; EUKARYOTE; EVOLUTION; GENE TRANSFER; ISOTOPIC ANALYSIS; METABOLISM; NITRATE; NITROGEN; NITROGEN ISOTOPE; OXIDATION; OXYGEN; PHOTOSYNTHESIS; REDOX CONDITIONS; RESPIRATION; SEDIMENTARY ROCK; SOLAR SYSTEM;

ANIMALIA; EUKARYOTA; PROKARYOTA;

EID: 47249141583     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2008.0054     Document Type: Conference Paper

References (103)

1. Allen, J. F. & Martin, W. 2007 Out of thin air. Nature 445, 610-612. (doi:10.1038/445610a)
2. Aller, R. C. 1998 Mobile deltaic and continental shelf muds as fluidized bed reactors. Mar. Chem. 61, 143-155. (doi:10.1016/S0304-4203(98) 00024-3)
3. Altabet, M. 2006 Isotopic tracers of the marine nitrogen cycle: present and past. In Marine organic matter: biomarkers, isotopes and DNA, vol. 2N/2006 (ed. J. K. Volkman), pp. 251-293. Berlin, Germany: Springer.
4. Altabet, M. A., Murray, D. W. & Prell, W. L. 1999 Climatically linked oscillations in Arabian Sea denitrification over the past 1m.y.: implications for the marine N cycle. Paleoceanography 14, 732-743. (doi:10.1029/1999PA900035)
5. Anbar, A. D. & Knoll, A. H. 2002 Proterozoic ocean chemistry and evolution: a bioinorganic bridge? Science 297, 1137-1142. (doi:10.1126/science.1069651)
6. Barber, J. 2008 Photosynthetic generation of oxygen. Phil. Trans. R. Soc. B 363, 2665-2674. (doi:10.1098/rstb.2008.0047)
7. Behrenfeld, M. J. & Falkowski, P. G. 1997 Photosynthetic rates derived from satellite-based chlorophyll concentration. Limnol. Oceanogr. 42, 1-20.
8. Bekker, A., Holland, H. D., Wang, P.-L., Rumble III, D., Stein, H. J., Hannah, J. L., Coetze, L. L. & Beukes, J. 2004 Dating the rise of atmospheric oxygen. Nature 427, 117-120. (doi:10.1038/nature02260)
9. Bender, M. & Sowers, T. 1994 The Dole effect and its variations during the last 130,000 years as measured in the Vostok ice core. Global Biogeochem. Cycles 8, 363-376. (doi:10.1029/94GB00724)
10. Berman-Frank, I., Lundgren, P. & Falkowski, P. G. 2003 An anaerobic enzyme in an aerobic world: nitrogen fixation and photosynthetic oxygen evolution in cyanobacteria. Res. Microbiol. 154, 157-164. (doi:10.1016/S0923-2508(03)00029-9)
11. 2. Science 276, 544-546. (doi:10.1126/science.276.5312.544)
12. 2. New York, NY: Oxford University Press.
13. 2 over Phanerozoic time. Geology 34, 413-415. (doi:10.1130/G22470.1)
14. 2 evolution. Science 287, 1630-1633. (doi:10.1126/science.287.5458.1630)
15. Berry, J. A. 1992 Biosphere, atmosphere, ocean interactions: a plant physiologist's perspective. In Primary productivity and biogeochemical cycles in the sea (eds P. G. Falkowski & A. D. Woodhead), pp. 441-454. New York, NY: Plenum Press.
16. Blankenship, R. E. 2001 Molecular evidence for the evolution of photosynthesis. Trends Plant Sci. 6, 4-6. (doi:10.1016/S1360- 1385(00)01831-8)
17. Blankenship, R. E., Madigan, M. T. & Bauer, C. E. (eds) 1995 Anoxygenic photosynthetic bacteria. Dordrecht, The Netherlands: Kluwer Scientific.
18. Blankenship, R. E., Sadekar, S. & Raymond, J. 2007 The evolutionary transition from anoxygenic to oxygenic photosynthesis. In Evolution of primary producers in the sea (eds P. G. Falkowski & A. H. Knoll), pp. 21-35. San Diego, CA: Academic Press.
19. Brandes, J. A. & Devol, A. H. 2002 A global marine-fixed nitrogen isotopic budget: implications for Holocene nitrogen cycling. Global Biogeochem. Cycles 16, 1120. (doi:10.1029/2001GB001856)
20. Brandes, J. A., Boctor, N. Z., Cody, G. D., Cooper, B. A., Hazen, R. M. & Yoder Jr, H. S. 1998 Abiotic nitrogen reduction on the early Earth. Nature 395, 365-367. (doi:10.1038/26450)
21. Brocks, J. J., Logan, G. A., Buick, R. & Summons, R. E. 1999 Archean molecular fossils and the early rise of eukaryotes. Science 285, 1033-1036. (doi:10.1126/science.285.5430.1033)
22. Canfield, D. E. 2005 The early history of atmospheric oxygen: homage to Robert A. Garrels. Annu. Rev. Earth Planet. Sci. 33, 1-36. (doi:10.1146/annurev.earth.33.092203.122711)
23. Capone, D. G. & Carpenter, E. J. 1982 Nitrogen fixation in the marine environment. Science 217, 1140-1142. (doi:10.1126/science.217. 4565.1140)
24. Casciotti, K. L., Sigman, D. M. & Ward, B. B. 2003 Linking diversity and stable isotope fractionation in ammonia-oxidizing bacteria. Geomicrobiol. J. 20, 335-353.
25. Cline, J. D. & Kaplan, I. R. 1975 Isotopic fractionation of dissolved nitrate during denitrification in the eastern tropical North Pacific Ocean. Mar. Chem. 3, 271-299. (doi:10.1016/0304-4203(75)9009-2)
26. 2 concentrating mechanisms in cyanobacteria and microalgae. Plant Cell Environ. 14, 861-867. (doi:10.1111/j.1365-3040.1991.tb01449.x)
27. Condie, K. C. 2004 Precambrian superplume events. In The precambrain earth: tempos and events. (eds P. G. Eriksson, W. Altermann, D. R. Nelson, W. U. Mueller & O. Catuneau), pp. 163-173. Amsterdam: Elsevier.
28. Delwiche, C. F. 2000 Tracing the thread of plastid diversity through the tapestry of life. Am. Nat. 154, S164-S177. (doi:10.1086/303291)
29. Embley, T. M. & Martin, W. 2006 Eukaryotic evolution, changes and challenges. Nature 440, 623-630. (doi:10.1038/nature04546)
30. Eriksson, P. G., Mazumder, R., Catuneanu, O., Bumby, A. J. & Ilondo, B. O. 2006a Precambrian continental freeboard and geological evolution: a time perspective. Earth-Sci. Rev. 79, 165-204. (doi:10.1016/j.earscirev.2006.07.001)
31. Eriksson, P. G., Mazumder, R., Catuneau, O., Bumby, A. J. & Ilondo, B. O. 2006b Precambrian continental freeboard and geological evolution: a time perspective. Earth-Sci. Rev. 79, 156-204. (doi:10.1016/j.earscirev.2006.7.001)
32. Eriksson, P. G., Banerjee, S., Catuneanu, O., Sarkar, S., Bumby, A. J. & Mtimkulu, M. N. 2007 Prime controls on Archean-Paleoproterozoic sedimentation: change over time. Gondwana Res. 12, 550-559. (doi:10.1016/j.gr.2007.04.004)
33. 2 in the ocean. Nature 387, 272-275. (doi:10.1038/387272a0)
34. Falkowski, P. G. 2001 Biogeochemical cycles. Encyclopedia Biodivers. 1, 437-453. (doi:10.1006/rwbd.1999.0030)
35. Falkowski, P. G. 2006 Tracing oxygen's imprint on Earth's metabolic evolution. Science 311, 1724-1725. (doi:10.1126/science.1125937)
36. Falkowski, P. G. & Knoll, A. H. (eds) 2007 Evolution of primary producers in the sea. San Diego, CA: Academic Press.
37. Falkowski, P. G. & Raven, J. A. 2007 Aquatic photosynthesis. Princeton, NJ: Princeton University Press.
38. Falkowski, P. G., Dubinsky, Z., Muscatine, L. & McCloskey, L. 1993 Population control in symbiotic corals. BioScience 43, 606-611. (doi:10.2307/1312147)
39. Falkowski, P. G., Katz, M. E., Milligan, A. J., Fennel, K., Cramer, B. S., Aubry, M.-P., Berner, R. A., Novacek, M. J. & Zapol, W. M. 2005 The rise of oxygen over the past 205 million years and the evolution of large placental mammals. Science 309, 2202-2204. (doi:10.1126/science.1116047)
40. Falkowski, P. G., Fenchel, T. & DeLong, E. In press. The Microbial engines that drive Earth's biogeochemical cycles. Science.
41. Farquhar, J., Bao, H. & Thiemens, M. 2000 Atmospheric influence of Earth's earliest sulfur cycle. Science 289, 756-758. (doi:10.1126/science.289.5480.756)
42. Fenchel, T. & Finlay, B. 1995 Ecology and evolution in anoxic worlds. Oxford, UK: Oxford University Press.
43. Fennel, K., Follows, M. J. & Falkowski, P. 2005 The co-evolution of the nitrogen, carbon and oxygen cycles in the Proterozoic ocean. Am. J. Sci. 305, 526-545. (doi:10.2475/ajs.305.6-8.526)
44. Fisher, A. G. 1983 The two Phanerozoic supercycles. In Catastrophes and Earth history (eds W. A. Bergren & J. A. van Couvering), pp. 129-150. Princeton, NJ: Princeton University Press.
45. 2O by nitrifying bacteria at reduced concentrations of oxygen. Appl. Environ. Microbiol. 40, 526-532.
46. Hayes, J. M. & Waldbauer, J. R. 2006 The carbon cycle and associated redox processes through time. Phil. Trans. R. Soc. B 361, 931-950. (doi:10.1098/rstb.2006.1840)
47. Hayes, J. M., Kaplan, I. R. & Wedeking, K. W. 1983 Precambrian organic geochemistry, preservation of the record. In Earth's earliest biosphere: its origin and evolution (ed. J. W. Schopf ), pp. 93-135. Princeton, NJ: Princeton University Press.
48. Hedges, J. I. & Keil, R. G. 1995 Sedimentary organic matter preservation: an assessment and speculative synthesis. Mar. Chem. 49, 81-115. (doi:10.1016/0304-4203(95)00008-F)
49. Henderson-Sellers, A. & Schwartz, A. W. 1980 Chemical evolution and ammonia in the early earth's atmosphere. Nature 287, 526-528. (doi:10.1038/287526a0)
50. Holland, H. D. 2006 The oxygenation of the atmosphere and oceans. Phil. Trans. R. Soc. B 361, 903-915. (doi:10.1098/rstb.2006.1838)
51. Hu, G., Rumble, D. & Wang, P. 2003 An ultraviolet laser microprobe for the in situ analysis of multisulfur isotopes and its use in measuring Archean sulfur isotope mass-independent anomalies. Geochim. Cosmochim. Acta 67, 3101-3117. (doi:10.1016/S0016-7037(02)00929-8)
52. Jia, Y. F. & Kerrich, R. 2004 Nitrogen 15-enriched Precambrian kerogen and hydrothermal systems. Geochem. Geophys. Geosyst. 5, Q07005. (doi:10.1029/2004GC000716)
53. Jiang, Q. Q. & Bakken, L. R. 1999 Nitrous oxide production and methane oxidation by different ammonia-oxidizing bacteria. Appl. Environ. Microbiol. 65, 2679-2684.
54. Johnston, D. T., Farquhar, J., Wing, B. A., Lyons, T., Kah, L., Strauss, H. & Canfield, D. E. 2005 Using the multiple isotopes of sulfur to constrain microbial processes in the Proterozoic ocean. Geochim. Cosmochim. Acta 69, A548.
55. Kasting, J. F. 1993 Earth's early atmosphere. Science 259, 920-926. (doi:10.1126/science.11536547)
56. Katz, M. E., Finkel, Z. V., Grzebyk, D., Knoll, A. H. & Falkowski, P. G. 2004 Evolutionary trajectories and biogeochemical impacts of marine eukaryotic phytoplankton. Annu. Rev. Ecol. Evol. Syst. 35, 523-556. (doi:10.1146/annurev.ecolsys.35.112202.130137)
57. Kaufman, A. J., Corsetti, F. A. & Varni, M. A. 2007 The effect of rising atmospheric oxygen on carbon and sulfur isotope anomalies in the Neoproterozoic Johnnie formation, Death Valley, USA. Chem. Geol. 237, 47-63. (doi:10.1016/j.chemgeo.2006.06.023)
58. Keeling, R. F., Bender, M. L., Najjar, R. G. & Tans, P. P. 1993 What atmospheric oxygen measurements can tell us about the global carbon cycle. Global Biogeochem. Cycles 7, 37-67. (doi:10.1029/92GB02733)
59. Knoll, A. H. & Bauld, J. 1989 The evolution and ecological tolerance in prokaryotes. Trans. R. Soc. Edinb. 80, 209-233.
60. Knoll, A. H., Summons, R. E., Waldbauer, J. R. & Zumberge, J. 2007 The geological succession of primary producers in the oceans. In Evolution of primary producers in the sea (eds P. G. Falkowski & A. H. Knoll), pp. 134-163. San Diego, CA: Academic Press.
61. Koblížek, M., Béjà, O., Bidigare, R. R., Christensen, S., Benitez-Nelson, B., Vetriani, C., Kolber, M. K., Falkowski, P. G. & Kolber, Z. S. 2003 Isolation and characterization of Erythrobacter sp. strains from the upper ocean. Arch. Microbiol. 180, 327-338. (doi:10.1007/s00203-003-0596-6)
62. Kolber, Z., van Dover, C. L., Niederman, R. A. & Falkowski, P. G. 2000 Bacterial photosynthesis in surface waters of the open ocean. Nature 407, 177-179. (doi:10.1038/35025044)
63. Kolber, Z. S. et al. 2001 Contribution of aerobic photoheterotrophic bacteria to the carbon cycle in the ocean. Science 292, 2492-2495. (doi:10.1126/science.1059707)
64. Mariotti, A., Germon, J. C., Hubert, P., Kaiser, P., Letolle, R., Tardieux, A. & Tardieux, P. 1981 Experimental determination of nitrogen kinetic isotope fractionation: some principles; illustration for the denitrification nitrification processes. Plant Soil 62, 413-430. (doi:10.1007/BF02374138)
65. Martin, W., Stoebe, B., Goremykin, V., Hansmann, S., Hasegawa, M. & Kowallik, K. V. 1998 Gene transfer to the nucleus and the evolution of chloroplasts. Nature 393, 162-165. (doi:10.1038/30234)
66. Maynard Smith, J. & Szathmáry, E. 1997 The major transitions in evolution. Oxford, UK: Oxford University Press.
67. Milligan, A. J., Berman-Frank, I., Gerchman, Y., Dismukes, G. C. & Falkowski, P. G. 2007 Light-dependent oxygen consumption in nitrogen-fixing cyanobacteria plays a key role in nitrogenase protection. J. Phycol. 43, 845-852. (doi:10.1111/j.1529-8817.2007.00395.x)
68. Mortenson, L. E. 1964 Ferredoxin and ATP, requirements for nitrogen fixation in cell-free extracts of Clostridium pasteurianum. Proc. Natl Acad. Sci. USA 52, 272-279. (doi:10.1073/pnas.52.2.272)
69. Mojzsis, S. J., Coath, C. D., Greenwood, K. D., McKeegan, K. D. & Harrison, T. M. 2003 Mass-independent isotope effects in Archean (2.5 to 3.8 Ga) sedimentary sulfides determined by ion microprobe analysis. Geochim. Cosmochim. Acta 67, 1635-1658. (doi:10.1016/S0016-7037(03)00059-0)
70. Nealson, K. H. & Conrad, P. G. 1999 Life: past, present and future. Phil. Trans. R. Soc. B 354, 1923-1939. (doi:10.1098/rstb.1999. 0532)
71. Ohad, I., Koike, H., Kyle, D. J. & Inoue, Y. 1990 Mechanism of photoinhibition in vivo. J. Biol. Chem. 265, 1972-1979.
72. Ohmoto, H., Watanabe, Y., Ikemi, H., Poulson, S. R. & Taylor, B. E. 2006 Sulfur isotope evidence for an anoxic Archean atmosphere. Nature 442, 908-911. (doi:10.1038/nature05044)
73. Ono, S., Eigenbrode, J. L., Pavlov, A. A., Kharecha, P., Rumble, D., Kasting, J. F. & Freeman, K. H. 2003 New insights into Archean sulfur cycle from mass-independent sulfur isotope records from the Hamersley Basin, Australia. Earth Planet. Sci. Lett. 213, 15-30. (doi:10.1016/S0012-821X(03)00295-4)
74. Ono, S., Beukes, N. J., Rumble, D. & Fogel, M. L. 2006 Early evolution of atmospheric oxygen from multiple-sulfur and carbon isotope records of the 2.9 Ga Mozaan Group of the Pongola Supergroup, Southern Africa. South Afr. J. Geol. 109, 97-108. (doi:10.2113/gssajg.109.1-2.97)
75. Pace, N. R. 1997 A molecular view of microbial diversity and the biosphere. Science 276, 734-740. (doi:10.1126/science.276.5313. 734)
76. Palmer, J. D. 1997 Organelle genomes: going, going, gone!. Science 275, 790-791. (doi:10.1126/science.275.5301.790)
77. Palmer, J. D. & Delwiche, C. F. 1998 The origin and evolution of plastids and their genomes. In Molecular systematics of plants II. DNA sequencing (eds P. S. Soltis, D. E. Soltis & J. J. Doyle), pp. 375-409. Boston, MA: Kluwer Academic.
78. Papineau, D., Mojzsis, S. J., Karhu, J. A. & Marty, B. 2005 Nitrogen isotopic composition of ammoniated phyllosilicates: case studies from Precambrian metamorphosed sedimentary rocks. Chem. Geol. 216, 37-58. (doi:10.1016/j.chemgeo.2004.10.009)
79. Peters, J. W., Fisher, K. & Dean, D. R. 1995 Nitrogenase structure and function: a biochemical-genetic perspective. Annu. Rev. Microbiol. 49, 335-366. (doi:10.1146/annurev.mi.49.100195.002003)
80. Pinti, D. L. & Hashizume, K. 2001 Nitrogen and argon signatures in 3.8 to 2.8 Ga metasediments: clues on the chemical state of the archean ocean and the deep biosphere. Geochim. Cosmochim. Acta 65, 2301-2315. (doi:10.1016/S0016-7037(01)00590-7)
81. Postgate, J. R. 1998 Nitrogen fixation. Cambridge, UK: Cambridge University Press.
82. Prasil, O., Adir, N. & Ohad, I. 1992 Dynamics of photosystem II: mechanism of photoinhibtion and recovery processes. In The photosystems: stucture, function and molecular biology, vol. 11 (ed. J. R. Barber), pp. 295-348. New York, NY: Elsevier.
83. Quigg, A., Finkel, Z. V., Irwin, A. J., Rosenthal, Y., Ho, T.-Y., Reinfelder, J. R., Schofield, O., Morel, F. M. M. & Falkowski, P. G. 2003 The evolutionary inheritance of elemental stoichiometry in marine phytoplankton. Nature 425, 291-294. (doi:10.1038/nature01953)
84. Raven, J. A. & Allen, J. F. 2003 Genomics and chloroplast evolution: what did cyanobacteria do for plants? Genome Biol. 4, 209. (doi:10.1186/gb-2003-4-3-209)
85. Raven, J. A., Cockell, C. S. & De La Rocha, C. L. 2008 The evolution of inorganic carbon concentrating mechanisms in photosynthesis. Phil. Trans. R. Soc. B 363, 2641-2650. (doi:10.1098/rstb.2008.0020)
86. Raymond, J. & Segrè, D. 2006 The effect of oxygen on biochemical networks and the evolution of complex life. Science 311, 1764-1767. (doi:10.1126/science.1118439)
87. Raymond, J., Siefert, J. L., Staples, C. R. & Blankenship, R. E. 2004 The natural history of nitrogen fixation. Mol. Biol. Evol. 21, 541-554. (doi:10.1093/molbev/msh047)
88. 13C-depleted carbon microparticles in >3700-Ma sea-floor sedimentary rocks from West Greenland. Science 283, 674-676. (doi:10.1126/science.283.5402.674)
89. Rosing, M. T. & Frei, R. 2004 U-rich Archean sea-floor sediments from Greenland-indications of >3700 Ma oxygenic photosynthesis. Earth Planet. Sci. Lett. 217, 237-244. (doi:10.1016/S0012-821X(03)00609-5)
90. 15N value. Geochem. J. 24, 315-325.
91. Shi, T. & Falkowski, P. G. 2008 Genome evolution in cyanobacteria: the stable core and the variable shell. Proc. Natl Acad. Sci. USA 105, 2510-2515. (doi:10.1073/pnas.0711165105)
92. Shi, T., Bibby, T. S., Jiang, L., Irwin, A. J. & Falkowski, P. G. 2005 Protein interactions limit the rate of evolution of photosynthetic genes in cyanobacteria. Mol. Biol. Evol. 22, 2179-2189. (doi:10.1093/molbev/msi216)
93. Summers, D. P. & Chang, S. 1993 Prebiotic ammonia from reduction of nitrite by iron (II ) on the early earth. Nature 356, 630-633. (doi:10.1038/365630a0)
94. Summons, R. E., Jahnke, L. L., Hope, J. M. & Logan, G. A. 1999 2-Methylhopanoids as biomarkers for cyanobacterial oxygenic photosynthesis. Nature 400, 554-556. (doi:10.1038/23005)
95. Tabita, F. R., Hanson, T. E., Satagopan, S., Witte, B. H. & Kreel, N. E. 2008 Phylogenetic and evolutionary relationships of RubisCO and the RubisCO-like proteins and the functional lessons provided by diverse molecular forms. Phil. Trans. R. Soc. B 363, 2629-2640. (doi:10.1098/rstb. 2008.0023)
96. Tice, M. M. & Lowe, D. R. 2004 Photosynthetic microbial mats in the 3,416-Myr-old ocean. Nature 431, 549-552. (doi:10.1038/ nature02888)
97. Valentine, J. S., Foote, C. S., Greenberg, A. & Liebman, J. F. 1995 Active oxygen in biochemistry. London, UK: Chapman and Hall.
98. Voss, M., Dippner, J. W. & Montoya, J. P. 2001 Nitrogen isotope patterns in the oxygen-deficient waters of the Eastern Tropical North Pacific Ocean. Deep Sea Res. I 48, 1905-1921. (doi:10.1016/S0967-0637(00) 00110-2)
99. Williams, R. J. P. & Frausto da Silva, J. J. R. 1996 The natural selection of the chemical elements. Oxford, UK: Oxford University Press.
100. Wilson, J. T. 1965 A new class of faults and their bearing on continental drift. Nature 207, 343-347. (doi:10.1038/207343a0)
101. Worsley, T. R., Moody, J. B. & Damian, N. R. 1986 Tectonic cycles and the history of the Earth's biochemical and paleoceanographic record. Paleoceanography 1, 233-263. (doi:10.1029/PA001i003p00233)
102. Yang, D., Oyaizu, Y., Oyaizu, H., Olsen, G. J. & Woese, C. R. 1985 Mitochondrial origins. Proc. Natl Acad. Sci. USA 82, 4443-4447. (doi:10.1073/pnas.82.13.4443)
103. 2O as a product of nitrification. Nature 335, 528-529. (doi:10.1038/335528a0)