Palaeoproterozoic ice houses and the evolution of oxygen-mediating enzymes: The case for a late origin of photosystem II

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 363, Issue 1504, 2008, Pages 2755-2765

  Kirschvink, Joseph L ^a   Kopp, Robert E ^b  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b PRINCETON UNIVERSITY   (United States)

Author keywords

Great Oxygenation Event; Makganyene Snowball Earth; Sterol biosynthesis

Indexed keywords

BIOMARKER; CYANOBACTERIUM; ENZYME; EVOLUTION; GLACIER; HYDROGEN PEROXIDE; LIPID; OXYGEN; PHOTOCHEMISTRY; PHOTOSYNTHESIS; PROTEROZOIC; REDOX POTENTIAL; STEROL; TOLERANCE;

CYANOBACTERIA;

EID: 47249131980     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2008.0024     Document Type: Conference Paper

References (83)

1. 2 by a new type of sulfate-reducing bacterium. Arch. Microbiol. 156, 5-14. (doi:10.1007/BF00418180)
2. Aeckersberg, F., Rainey, F. A. & Widdel, F. 1998 Growth, natural relationships, cellular fatty acids and metabolic adaptation of sulfate-reducing bacteria that utilize long-chain alkanes under anoxic conditions. Arch. Microbiol. 170, 361-369. (doi:10.1007/s002030050654)
3. Aitken, C. M., Jones, D. M. & Larter, S. R. 2004 Anaerobic hydrocarbon biodegradation in deep subsurface oil reservoirs. Nature 431, 291-294. (doi:10.1038/nature02922)
4. Anbar, A. D. et al. 2007 A whiff of oxygen before the Great Oxidation Event? Science 317, 1903-1906. (doi:10.1126/science. 1140325)
5. Andreasen, A. A. & Stier, T. J. B. 1953 Anaerobic nutrition of Saccharomyces cerevisiae. I. Ergosterol requirement for growth in a defined medium. J. Cell. Comp. Physiol. 41, 23-36. (doi:10.1002/jcp.1030410103)
6. 2: fundamental principles were enunciated by J. J. Ebelman in 1845. Geochim. Cosmochim. Acta 60, 1633-1637. (doi:10.1016/0016-7037(96)00104-4)
7. Berthe-Corti, L. & Fetzner, S. 2002 Bacterial metabolism of n-alkanes and ammonia under oxic, suboxic and anoxic conditions. Acta Biotechnol. 22, 299-336. (doi:10.1002/1521-3846(200207)22:3/ 4〈299::AID-ABIO299〉3.0.CO;2-F)
8. Bischof, K. G. 1854 Elements of chemical and physical geology. London, UK: Cavendish Society.
9. Blankenship, R. E. & Hartman, H. 1998 The origin and evolution of oxygenic photosynthesis. Trends Biochem. Sci. 23, 94-97. (doi:10.1016/S0968-0004(98)01186-4)
10. Boll, M., Fuchs, G. & Heider, J. 2002 Anaerobic oxidation of aromatic compounds and hydrocarbons. Curr. Opin. Chem. Biol. 6, 604-611. (doi:10.1016/S1367-5931(02)00375-7)
11. Bonin, P., Cravo-Laureau, C., Michotey, V. & Hirschler-Rea, A. 2004 The anaerobic hydrocarbon biodegrading bacteria: an overview. Ophelia 58, 243-254.
12. Brocks, J. J. 2005 The evolution of steroids and eukaryotes in the proterozoic. Eos Trans. AGU 86, B12A-5.
13. 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)
14. Brocks, J. J., Buick, R., Logan, G. A. & Summons, R. E. 2003a Composition and syngeneity of molecular fossils from the 2.78 to 2.45 billion-year-old Mount Bruce Supergroup, Pilbara Craton, Western Australia. Geochim. Cosmochim. Acta 67, 4289-4319. (doi:10.1016/S0016- 7037(03)00208-4)
15. Brocks, J. J., Buick, R., Summons, R. E. & Logan, G. A. 2003b A reconstruction of Archean biological diversity based on molecular fossils from the 2.78 to 2.45 billion-year-old Mount Bruce Supergroup, Hamersley Basin, Western Australia. Geochim. Cosmochim. Acta 67, 4321-4335. (doi:10.1016/S0016-7037(03)00209-6)
16. Cairncross, B., Beukes, N. J. & Gutzmer, J. 1997 The manganese adventure: the South African manganese fields. Johannesburg, Republic of South Africa: Associated Ore & Metal Corporation, Ltd.
17. Canfield, D. E. 2005 The early history of atmospheric oxygen: homage to Robert M. Garrels. Annu. Rev. Earth Planet. Sci. 33, 1-36. (doi:10.1146/annurev.earth.33.092203.122711)
18. Catling, D. C. & Claire, M. W. 2005 How Earth's atmosphere evolved to an oxic state: a status report. Earth Planet. Sci. Lett. 237, 1-20. (doi:10.1016/j.epsl.2005.06.013)
19. Clarke, F. W. 1924 The data of geochemistry. Bulletin 770. Washington, DC: US Geological Survey.
20. Cloud, P. E., Holland, H. D., Commoner, B., Davidson, C. F., Fischer, A. G., Berkner, L. V. & Marshall, L. C. 1965 Symposium on the evolution of the Earth's atmosphere. Proc. Natl Acad. Sci. USA 53, 1169-1226. (doi:10.1073/pnas.53.6.1169)
21. Darnet, S. & Rahier, A. 2003 Enzymological properties of sterol-C4-methyl-oxidase of yeast sterol biosynthesis. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1633, 106-117.
22. Dutkiewicz, A., Volk, H., George, S. C., Ridley, J. & Buick, R. 2006 Biomarkers from Huronian oil-bearing fluid inclusions: an uncontaminated record of life before the Great Oxidation Event. Geology 34, 437-440. (doi:10.1130/G22360.1)
23. Ebelman, J. J. 1845 Sur les produits de la décomposition des especes minérales de la familie des silicates. Ann. Mines 7, 3-66.
24. Evans, D. A. D. 2000 Stratigraphic, geochronological, and paleomagnetic constraints upon the Neoproterozoic climatic paradox. Am. J. Sci. 300, 347-433. (doi:10.2475/ajs.300.5.347)
25. Evans, D. A., Beukes, N. J. & Kirschvink, J. L. 1997 Low-latitude glaciation in the Paleoproterozoic. Nature 386, 262-266. (doi:10.1038/386262a0)
26. 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)
27. 2 photolysis: implications for the early atmosphere. J. Geophys. Res. 106, 32 829-32 839. (doi:10.1029/2000JE001437)
28. Fennel, K., Follows, M. & Falkowski, P. G. 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)
29. Fischer, W. W. & Pearson, A. 2007 Hypotheses for the origin and early evolution of triterpenoid cyclases. Geobiology 5, 19-34.
30. Fischer, W. W., Summons, R. E. & Pearson, A. 2005 Targeted genomic detection of biosynthetic pathways: anaerobic production of hopanoid biomarkers by a common sedimentary microbe. Geobiology 3, 33-40. (doi:10.1111/j.1472-4669.2005.00041.x)
31. Frey, M. M., Stewart, R. W., McConnell, J. R. & Bales, R. C. 2005 Atmospheric hydroperoxides in West Antarctica: links to stratospheric ozone and atmospheric oxidation capacity. J. Geophys. Res. 110, D23301. (doi:10.1029/2005JD006110)
32. 2) record preserved in 23 ice cores from West Antarctica. J. Geophys. Res. 111, D21301. (doi:10.1029/2005JD006816)
33. Fuerst, J. 2005 Intracellular compartmentation in planctomycetes. Annu. Rev. Microbiol. 59, 299-328. (doi:10.1146/annurev.micro.59. 030804.121258)
34. Gaidos, E. J., Nealson, K. H. & Kirschvink, J. L. 1999 Biogeochemistry - life in ice-covered oceans. Science 284, 1631-1633. (doi:10.1126/science.284.5420.1631)
35. Goldfine, H. 1965 Evolution of oxygen as a biosynthetic reagent. J. Gen. Physiol. 49, 253-268. (doi:10.1085/jgp.49.1.253)
36. Hayes, J. M., Kaplan, I. R. & Wedeking, K. W. 1983 Chemical fossils in Precambrian sediments. In Earth's earliest biosphere, its origin and evolution (ed. J. W. Schopf ), ch. 5-3-1, pp. 100-101. Princeton, NJ: Princeton University Press.
37. Hilburn, I. A., Kirschvink, J. L., Tajika, E., Tada, R., Hamano, Y. & Yamamoto, S. 2005 A negative fold test on the Lorrain Formation of the Huronian Supergroup: uncertainty on the paleolatitude of the Paleoproterozoic Gowganda glaciation and implications for the Great Oxygenation Event. Earth Planet. Sci. Lett. 232, 315-332. (doi:10.1016/j.epsl.2004.11.025)
38. Holland, H. D. 1962 Model for the evolution of the Earth's atmosphere. In Petrologic studies: a volume in honor of A.F. Buddington (eds A. E. J. Engel, H. I. James & B. F. Leonard), pp. 447-477. Boulder, CO: Geological Society of America.
39. Imlay, J. A. 2006 Iron-sulphur clusters and the problem with oxygen. Mol. Microbiol. 59, 1073-1082. (doi:10.1111/j.1365-2958.2006. 05028.x)
40. Jahnke, L. L. & Klein, H. P. 1983 Oxygen requirements for formation and activity of the squalene epoxidase in Saccharomyces cerevisiae. J. Bacteriol. 155, 488-492.
41. Jenney, F. E., Verhagen, M., Cui, X. Y. & Adams, M. W. W. 1999 Anaerobic microbes: oxygen detoxification without superoxide dismutase. Science 286, 306-309. (doi:10.1126/science.286.5438.306)
42. Kappler, A., Pasquero, C., Konhauser, K. O. & Newman, D. K. 2005 Deposition of banded iron formations by anoxygenic phototrophic Fe(II )-oxidizing bacteria. Geology 33, 865-868. (doi:10.1130/G21658.1)
43. Kaufman, A. J. et al. 2007 Late Archean biospheric oxygenation and atmospheric evolution. Science 317, 1900-1903. (doi:10.1126/science.1138700)
44. Kirschvink, J. L. & Weiss, B. P. 2002 Mars, panspermia, and the origin of life: where did it all begin? Palaeontol. Electron. 4, 8, editorial 2.
45. Kirschvink, J. L., Gaidos, E. J., Bertani, L. E., Beukes, N. J., Gutzmer, J., Maepa, L. N. & Steinberger, R. E. 2000 Paleoproterozoic Snowball Earth: extreme climatic and geochemical global change and its biological consequences. Proc. Natl Acad. Sci. USA 97, 1400-1405. (doi:10.1073/pnas.97.4. 1400)
46. Kniemeyer, O. & Heider, J. 2001 Ethylbenzene dehydrogenase, a novel hydrocarbon-oxidizing molybdenum/iron-sulfur/heme enzyme. J. Biol. Chem. 276, 21 381-21 386. (doi:10.1074/jbc.M101679200)
47. Knoll, A. H., Summons, R. E. & Waldbauer, J. E. 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. 133-163. Amsterdam, The Netherlands: Elsevier.
48. Koene, C. J. 1856/2004 An English translation of the chemical constitution of the atmosphere from Earth's origin to the present, and its implications for protection of industry and ensuring environmental quality. New York, NY: Mellen Press.
49. Kopp, R. E., Kirschvink, J. L., Hilburn, I. A. & Nash, C. Z. 2005 The Paleoproterozoic Snowball Earth: a climate disaster triggered by the evolution of oxygenic photosynthesis. Proc. Natl Acad. Sci. USA 102, 11 131-11 136. (doi:10.1073/pnas.0504878102)
50. Kump, L. R. & Barley, M. E. 2007 Increased subaerial volcanism and the rise of atmospheric oxygen 2.5 billion years ago. Nature 448, 1033-1036. (doi:10.1038/nature06058)
51. Lesburg, C. A., Caruthers, J. M., Paschall, C. M. & Christianson, D. W. 1998 Managing and manipulating carbocations in biology: terpenoid cyclase structure and mechanism. Curr. Opin. Struct. Biol. 8, 695-703. (doi:10.1016/S0959-440X(98)80088-2)
52. Liang, M. C., Hartman, H., Kopp, R. E., Kirschvink, J. L. & Yung, Y. L. 2006 Production of hydrogen peroxide in the atmosphere of a Snowball Earth and the origin of oxygenic photosynthesis. Proc. Natl Acad. Sci. USA 103, 18 896-18 899. (doi:10.1073/pnas.0608839103)
53. Lovelock, J. E. 1979 Gaia, a new look at life on Earth. Oxford, UK; New York, NY: Oxford University Press.
54. MacGregor, A. M. 1927 The problem of the Precambrian atmosphere. S. Afr. J. Sci. 24, 155-172.
55. McKay, C. P. & Hartman, H. 1991 Hydrogen-peroxide and the evolution of oxygenic photosynthesis. Orig. Life Evol. Biosph. 21, 157-163. (doi:10.1007/BF01809444)
56. Niyogi, K. K. 1999 Photoprotection revisited: genetic and molecular approaches. Annu. Rev. Plant Physiol. 50, 333-359. (doi:10.1146/annurev.arplant.50.1.333)
57. Orphan, V. J., House, C. H., Hinrichs, K. U., McKeegan, K. D. & DeLong, E. F. 2001 Methane-consuming archaea revealed by directly coupled isotopic and phylogenetic analysis. Science 293, 484-487. (doi:10.1126/science.1061338)
58. Orphan, V. J., House, C. H., Hinrichs, K. U., McKeegan, K. D. & DeLong, E. F. 2002 Multiple archaeal groups mediate methane oxidation in anoxic cold seep sediments. Proc. Natl Acad. Sci. USA 99, 7663-7668. (doi:10.1073/pnas.072210299)
59. 4 in the atmosphere of early Earth. J. Geophys. Res. 105, 11 981-11 990. (doi:10.1029/1999JE001134)
60. Pearson, A., Budin, M. & Brocks, J. J. 2003 Phylogenetic and biochemical evidence for sterol synthesis in the bacterium Gemmata obscuriglobus. Proc. Natl Acad. Sci. USA 100, 15 352-15 357. (doi:10.1073/pnas.2536559100)
61. Philippot, P., Van Zuilen, M., Lepot, K., Thomazo, C., Farquhar, J. & Van Kranendonk, M. J. 2007 Early Archaean microorganisms preferred elemental sulfur, not sulfate. Science 317, 1534-1537. (doi:10.1126/science. 1145861)
62. Rashby, S. E., Sessions, A. L., Summons, R. E. & Newman, D. K. 2007 Biosynthesis of 2-methylbacteriohopanepolyols by an anoxygenic phototroph. Proc. Natl Acad. Sci. USA 105, 15 099-15 104. (doi:10.1073/pnas. 0704912104)
63. Raymond, J. & Blankenship, R. E. 2004 Biosynthetic pathways, gene replacement, and the antiquity of life. Geobiology 2, 199-203. (doi:10.1111/j.1472-4677.2004.00037.x)
64. Raymond, J. & Segre, D. 2006 The effect of oxygen on biochemical networks and the evolution of complex life. Science 311, 1764-1767. (doi:10.1126/science.1118439)
65. Risley, J. M. 2002 Cholesterol biosynthesis: lanosterol to cholesterol. J. Chem. Educ. 79, 377-384.
66. Rosenfeld, E. & Beauvoit, B. 2003 Role of the nonrespiratory pathways in the utilization of molecular oxygen by Saccharomyces cerevisiae. Yeast 20, 1115-1144. (doi:10.1002/yea.1026)
67. Rosing, M. T. & Frei, R. 2004 U-rich Archaean 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)
68. Rueter, P., Rabus, R., Wilkes, H., Aeckersberg, F., Rainey, F. A., Jannasch, H. W. & Widdel, F. 1994 Anaerobic oxidation of hydrocarbons in crude-oil by new types of sulfate-reducing bacteria. Nature 372, 455-458. (doi:10.1038/372455a0)
69. So, C. M. & Young, L. Y. 1999 Initial reactions in anaerobic alkane degradation by a sulfate reducer, strain AK-01. Appl. Environ. Microbiol. 65, 5532-5540.
70. Stevenson, J. 1900 The chemical and geological history of the atmosphere. I. The history of free oxygen. Philos. Mag. 50, 312-323, 399-407.
71. Suflita, J. M., Davidova, I. A., Gieg, L. M., Nanny, M. & Prince, R. C. 2004 Anaerobic hydrocarbon biodegradation and the prospects for microbial enhanced energy production. In Petroleum biotechnology: developments and perspectives, vol. 151 (eds R. Vazquez-Duhalt & R. Quintero-Ramirez), pp. 283-305. Amsterdam, The Netherlands: Elsevier.
72. Summons, R. E., Jahnke, L. L., Hope, J. M. & Logan, G. A. 1999 2-Methylhopanoids as biomarkers for cyanobacterial oxygenic photosynthesis. Nature 400, 554-557. (doi:10.1038/23005)
73. Summons, R. E., Bradley, A. S., Jahnke, L. L. & Waldbauer, J. R. 2006 Steroids, triterpenoids and molecular oxygen. Phil. Trans. R. Soc. B 361, 951-968. (doi:10.1098/rstb.2006.1837)
74. Ueno, Y., Yamada, K., Yoshida, N., Maruyama, S. & Isozaki, Y. 2006 Evidence from fluid inclusions for microbial methanogenesis in the Early Archaean era. Nature 440, 516-519. (doi:10.1038/nature04584)
75. Urey, H. C. 1952 On the early chemical history of Earth and the origin of life. Proc. Natl Acad. Sci. USA 38, 351-363. (doi:10.1073/pnas. 38.4.351)
76. van Hise, C. 1904 A treatise on metamorphism. US Geological Survey Monograph. Washington, DC: US Geological Survey.
77. Walker, J. C. G. 1987 Was the Archean biosphere upside down? Nature 329, 710-712. (doi:10.1038/329710a0)
78. Wendt, K. U., Poralla, K. & Schulz, G. E. 1997 Structure and function of a squalene cyclase. Science 277, 1811-1815. (doi:10.1126/science.277.5333.1811)
79. Wendt, K. U., Schulz, G. E., Corey, E. J. & Liu, D. R. 2000 Enzyme mechanisms for polycyclic triterpene formation. Angew. Chem. 39, 2812-2833. (doi:10.1002/1521-3773(20000818)39:16〈2812::AID-ANIE2812〉3. 0.CO;2-)
80. Widdel, F. & Rabus, R. 2001 Anaerobic biodegradation of saturated and aromatic hydrocarbons. Curr. Opin. Biotechnol. 12, 259-276. (doi:10.1016/S0958-1669(00)00209-3)
81. Widdel, F., Schnell, S., Heising, S., Ehrenreich, A., Assmus, B. & Schink, B. 1993 Ferrous iron oxidation by anoxygenic phototrophic bacteria. Nature 362, 834-836. (doi:10.1038/362834a0)
82. Wolfe-Simon, F. 2005 The role and evolution of superoxide dismutases in algae. J. Phycol. 41, 453-465. (doi:10.1111/j.1529-8817.2005. 00086.x)
83. Young, G. M., Long, D. G. F., Fedo, C. M. & Nesbitt, H. W. 2001 Paleoproterozoic Huronian Basin: product of a Wilson cycle punctuated by glaciations and a meteorite impact. Sediment. Geol. 141, 233-254. (doi:10.1016/S0037-0738(01)00076-8)