Oxygen and animal evolution: Did a rise of atmospheric oxygen "trigger" the origin of animals?

BioEssays

Volumn 36, Issue 12, 2014, Pages 1145-1155

  Mills, Daniel B ^a   Canfield, Donald E ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

Eukaryotes; Geochemistry; Hypoxia; Marine oxygenation; Metazoans; Proterozoic

Indexed keywords

ANIMALIA; EUKARYOTA; METAZOA;

EID: 84920138326     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201400101     Document Type: Article

References (112)

1. Cloud PE. 1976. Beginnings of biospheric evolution and their biogeochemical consequences. Paleobiology 2: 351-87.
2. Knoll AH, Carroll SB. 1999. Early animal evolution: emerging views from comparative biology and geology. Science 284: 2129-37.
3. Runnegar B. 1982. The Cambrian explosion: animals or fossils? J Geol Soc Austral 29: 395-411.
4. Nursall JR. 1959. Oxygen as a prerequisite to the origin of the Metazoa. Nature 183: 1170-2.
5. Berkner LV, Marshall LC. 1965. On the origin and rise of oxygen concentration in the Earth's atmosphere. J Atmos Sci 22: 225-61.
6. Cloud PE. 1965. Significance of the Gunflint (Precambrian) Microflora. Science 148: 27-35.
7. Knoll AH. 1992. Biological and biogeochemical preludes to the ediacaran radiation. In Lipps JH, Signor PW, eds; Origin and Early Evolution of the Metazoa. New York: Plenum Press.
8. Cavalier-Smith T, Chao E. 1995. The opalozoan Apusomonas is related to the common ancestor of animals, fungi, and choanoflagellates. P Roy Soc Lond B Biol Sci 261: 1-6.
9. Wilkins AS. 2002. The evolution of developmental pathways. Sunderland, MA: Sinauer Associates Inc.
10. Richter DJ, King N. 2013. The genomic and cellular foundations of animal origins. Annu Rev Genet 47: 509-37.
11. Cloud PE. 1968. Atmospheric and hydrospheric evolution on the primitive Earth. Science 160: 729-36.
12. Knoll AH. 2011. The multiple origins of complex multicellularity. Annu Rev Earth Pl Sci 39: 217-39.
13. Sagan C. 1961. On the origin and planetary distribution of life. Radiation Res 15: 174-92.
14. Kasting JF, Catling D. 2003. Evolution of a habitable planet. Annu Rev Astron Astrophys 41: 429-63.
15. Madronich S, McKenzie RL, Björn LO, Caldwell MM. 1998. Changes in biologically active ultraviolet radiation reaching the Earth's surface. J Photochem Photobiol 46: 5-19.
16. Ratner MI, Walker JC. 1972. Atmospheric ozone and the history of life. J Atmos Sci 29: 803-8.
17. Sagan C, Chyba C. 1997. The early faint sun paradox: organic shielding of ultraviolet-labile greenhouse gases. Science 276: 1217-21.
18. Wolf E, Toon O. 2010. Fractal organic hazes provided an ultraviolet shield for early Earth. Science 328: 1266-8.
19. Rye R, Holland HD. 2000. Life associated with a 2.76Ga ephemeral pond? evidence from Mount Roe # 2 paleosol. Geology 28: 483-6.
20. Watanabe Y, Martini JE, Ohmoto H. 2000. Geochemical evidence for terrestrial ecosystems 2.6billion years ago. Nature 408: 574-8.
21. Stüeken EE, Catling DC, Buick R. 2012. Contributions to late Archaean sulphur cycling by life on land. Nat Geosci 5: 722-5.
22. Margulis L, Walker J, Rambler M. 1976. Reassessment of roles of oxygen and ultraviolet light in Precambrian evolution. Nature 264: 620-4.
23. Monty CL. 1973. Precambrian background and Phanerozoic history of stromatolitic communities, an overview. Ann Soc Geol Belg 96: 585-624.
24. Walker JJ, Pace NR. 2007. Endolithic microbial ecosystems. Annu Rev Microbiol 61: 331-47.
25. Garcia-Pichel F, Castenholz RW. 1993. Occurrence of UV-absorbing, mycosporine-like compounds among cyanobacterial isolates and an estimate of their screening capacity. Appl Environ Microbiol 59: 163-9.
26. Phoenix V, Konhauser K, Adams D, Bottrell S. 2001. Role of biomineralization as an ultraviolet shield: implications for Archean life. Geology 29: 823-6.
27. Rambler MB, Margulis L. 1980. Bacterial resistance to ultraviolet irradiation under anaerobiosis: implications for pre-Phanerozoic evolution. Science 210: 638-40.
28. Raff RA, Raff EC. 1970. Respiratory mechanisms and the metazoan fossil record. Nature 228: 1003-5.
29. Rhoads DC, Morse JW. 1971. Evolutionary and ecological significance of oxygen-deficient marine basins. Lethaia 4: 413-28.
30. Runnegar B. 1982. Oxygen requirements, biology and phylogenetic significance of the late Precambrian worm Dickinsonia, and the evolution of the burrowing habit. Alcheringa 6: 223-39.
31. Laflamme M, Darroch SAF, Tweedt SM, Peterson KJ, et al. 2013. The end of the Ediacara biota: extinction, biotic replacement, or Cheshire Cat? Gondwana Res 23: 558-73.
32. Alexander RM. 1971. Size and shape: Edward Arnold London.
33. Canfield DE. 2005. The early history of atmospheric oxygen: homage to Robert M. Garrels. Annu Rev Earth Pl Sci 33: 1-36.
34. Holland HD. 2002. Volcanic gases, black smokers, and the great oxidation event. Geochim Cosmochim Acta 66: 3811-26.
35. Bekker A, Holland HD. 2012. Oxygen overshoot and recovery during the early Paleoproterozoic. Earth Planet Sci Lett 317-318: 295-304.
36. Canfield DE, Ngombi-Pemba L, Hammarlund EU, Bengtson S, et al. 2013. Oxygen dynamics in the aftermath of the great oxidation of Earth's atmosphere. Proc Natl Acad Sci USA 110: 16736-41.
37. Canfield DE. 2014. Oxygen: A Four Billion Year History. Princeton, NJ: Princeton University Press.
38. Planavsky NJ, Bekker A, Hofmann A, Owens JD, et al. 2012. Sulfur record of rising and falling marine oxygen and sulfate levels during the Lomagundi event. Proc Natl Acad Sci USA 109: 18300-5.
39. Lyons TW, Reinhard CT, Planavsky NJ. 2014. The rise of oxygen in Earth's early ocean and atmosphere. Nature 506: 307-15.
40. Stolper DA, Revsbech NP, Canfield DE. 2010. Aerobic growth at nanomolar oxygen concentrations. Proc Natl Acad Sci USA 107: 18755-60.
41. Runnegar B. 1991. Precambrian oxygen levels estimated from the biochemistry and physiology of early eukaryotes. Palaeogeo Palaeoclimatol Palaeoecol 97: 97-111.
42. Erwin DH, Laflamme M, Tweedt SM, Sperling EA, et al. 2011. The Cambrian conundrum: early divergence and later ecological success in the early history of animals. Science 334: 1091-7.
43. Mills DB, Ward LM, Jones C, Sweeten B, et al. 2014. Oxygen requirements of the earliest animals. Proc Natl Acad Sci USA 111: 4168-72.
44. Sperling EA, Halverson GP, Knoll AH, Macdonald FA, et al. 2013. A basin redox transect at the dawn of animal life. Earth Planet Sci Lett 371-372: 143-55.
45. Hentschel U, Usher KM, Taylor MW. 2006. Marine sponges as microbial fermenters. FEMS Microbiol Ecol 55: 167-77.
46. Dohrmann M, Worheide G. 2013. Novel scenarios of early animal evolution - is it time to rewrite textbooks? Integr Comp Biol 53: 503-11.
47. Dunn CW, Hejnol A, Matus DQ, Pang K, et al. 2008. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452: 745-9.
48. Ryan JF, Pang K, Schnitzler CE, Nguyen A-D, et al. 2013. The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution. Science 342: 1242592.
49. Moroz LL, Kocot KM, Citarella MR, Dosung S, et al. 2014. The ctenophore genome and the evolutionary origins of neural systems. Nature 510: 109-14.
50. Pick K, Philippe H, Schreiber F, Erpenbeck D, et al. 2010. Improved phylogenomic taxon sampling noticeably affects nonbilaterian relationships. Mol Biol Evol 27: 1983-7.
51. Philippe H, Brinkmann H, Lavrov DV, Littlewood DTJ, et al. 2011. Resolving difficult phylogenetic questions: why more sequences are not enough. PLoS Biol 9: e1000602.
52. Nosenko T, Schreiber F, Adamska M, Adamski M, et al. 2013. Deep metazoan phylogeny: when different genes tell different stories. Mol Phylogenet Evol 67: 223-33.
53. Sperling EA, Pisani D, Peterson KJ. 2007. Poriferan paraphyly and its implications for Precambrian palaeobiology. Geol Soc Lond Special Publications 286: 355-68.
54. Wörheide G, Dohrmann M, Erpenbeck D, Larroux C, et al. 2012. 1 Deep phylogeny and evolution of Sponges (Phylum porifera). Adv Mar Biol 61: 1.
55. Nichols SA, Dayel MJ, King N. 2009. Genomic, phylogenetic, and cell biological insights into metazoan origins. In Telford MJ, Littlewood DTJ, eds; Animal Evolution: Genes, Genomes, Fossils and Trees. Oxford University Press. p. 24-32.
56. Hoffmann F, Larsen O, Thiel V, Rapp HT, et al. 2005. An anaerobic world in sponges. Geomicrobiol J 22: 1-10.
57. Hoffmann F, Røy H, Bayer K, Hentschel U, et al. 2008. Oxygen dynamics and transport in the Mediterranean sponge Aplysina aerophoba. Mar Biol 153: 1257-64.
58. Mentel M, Martin W. 2008. Energy metabolism among eukaryotic anaerobes in light of Proterozoic ocean chemistry. Philos Trans R Soc Lond B Biol Sci 363: 2717-29.
59. Mentel M, Martin W. 2010. Anaerobic animals from an ancient, anoxic ecological niche. BMC Biol 8: 32.
60. Muller M, Mentel M, van Hellemond JJ, Henze K, et al. 2012. Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol Mol Biol Rev 76: 444-95.
61. Martin W, Müller M. 1998. The hydrogen hypothesis for the first eukaryote. Nature 392: 37-41.
62. Embley TM, Martin W. 2006. Eukaryotic evolution, changes and challenges. Nature 440: 623-30.
63. Danovaro R, Dell'Anno A, Pusceddu A, Gambi C, et al. 2010. The first metazoa living in permanently anoxic conditions. BMC Biol 8: 30.
64. Olson SL, Kump LR, Kasting JF. 2013. Quantifying the areal extent and dissolved oxygen concentrations of Archean oxygen oases. Chem Geol 362: 35-43.
65. Budd GE, Jensen S. 2000. A critical reappraisal of the fossil record of the bilaterian phyla. Biol Rev 75: 253-95.
66. Budd GE. 2008. The earliest fossil record of the animals and its significance. Philos Trans R Soc Lond B Biol Sci 363: 1425-34.
67. Shoulders MD, Raines RT. 2009. Collagen structure and stability. Annu Rev Biochem 78: 929-58.
68. Garrone R. 1999. Collagen, a common thread in extracellular matrix evolution. Proc Indian Acad Sci Chem Sci Springer 111: 51-6.
69. Fujimoto D, Tamiya N. 1962. Incorporation of 18O from air into hydroxyproline by chick embryo. Biochem J 84: 333.
70. Prockop D, Kaplan A, Udenfriend S. 1963. Oxygen-18 studies on the conversion of proline to collagen hydroxyproline. Arch Biochem Biophys 101: 499-503.
71. Fujita Y, Gottlieb A, Peterkofsky B, Udenfriend S, et al. 1964. The preparation of cis-and trans-4-H3-l-prolines and their use in studying the mechanism of enzymatic hydroxylation in chick embryos. J Am Chem Soc 86: 4709-16.
72. Schierwater B, de Jong D, DeSalle R. 2009. Placozoa and the evolution of Metazoa and intrasomatic cell differentiation. Int J Biochem Cell Biol 41: 370-9.
73. 2 is required by complex life on habitable planets and the concept of planetary "oxygenation time". Astrobiology 5: 415-38.
74. Towe KM. 1970. Oxygen-collagen priority and the early metazoan fossil record. Proc Natl Acad Sci USA 65: 781-8.
75. Lyons TW, Reinhard CT, Love GD, Xiao S. 2012. Geobiology of the Proterozoic Eon. In Knoll AH, Canfield DE, Konhauser KO, eds; Fundamentals of Geobiology. Wiley-Blackwell. p. 371-402.
76. Erwin DH, Valentine J. 2013. The Cambrian explosion: the construction of animal biodiversity. West Sussex, UK.
77. Levin L, Gutiérrez D, Rathburn A, Neira C, et al. 2002. Benthic processes on the Peru margin: a transect across the oxygen minimum zone during the 1997-98 El Niño. Prog Oceanogr 53: 1-27.
78. Waldbauer JR, Newman DK, Summons RE. 2011. Microaerobic steroid biosynthesis and the molecular fossil record of Archean life. Proc Natl Acad Sci USA 108: 13409-14.
79. Och LM, Shields-Zhou GA. 2012. The Neoproterozoic oxygenation event: environmental perturbations and biogeochemical cycling. Earth Sci Rev 110: 26-57.
80. Canfield DE, Poulton SW, Narbonne GM. 2007. Late-Neoproterozoic deep-ocean oxygenation and the rise of animal life. Science 315: 92-5.
81. Canfield DE, Poulton SW, Knoll AH, Narbonne GM, et al. 2008. Ferruginous conditions dominated later neoproterozoic deep-water chemistry. Science 321: 949-52.
82. Scott C, Lyons TW, Bekker A, Shen Y, et al. 2008. Tracing the stepwise oxygenation of the Proterozoic ocean. Nature 452: 456-9.
83. Sahoo SK, Planavsky NJ, Kendall B, Wang X, et al. 2012. Ocean oxygenation in the wake of the Marinoan glaciation. Nature 489: 546-9.
84. Dahl TW, Hammarlund EU, Anbar AD, Bond DPG, et al. 2010. Devonian rise in atmospheric oxygen correlated to the radiations of terrestrial plants and large predatory fish. Proc Natl Acad Sci USA 107: 17911-5.
85. Frei R, Gaucher C, Poulton SW, Canfield DE. 2009. Fluctuations in Precambrian atmospheric oxygenation recorded by chromium isotopes. Nature 461: 250-3.
86. Canfield DE. 2014. Proterozoic atmospheric oxygen. In Holland HD, Turekian KK, eds; Treatise on Geochemistry (Second Ed.) Oxford: Elsevier. p. 197-216.
87. Shields-Zhou G, Och L. 2011. The case for a Neoproterozoic oxygenation event: geochemical evidence and biological consequences. GSA Today 21: 4-11.
88. Knoll AH, Holland HD. 1995. Oxygen and Proterozoic evolution: an update. Effects Past Global Change Life 21-33.
89. Cloud P. 1968. Pre-metazoan evolution and the origins of the Metazoa. in: Drake, ET, ed; Evolution and Environment. New Haven and London: Yale University Press, 72.
90. Love GD, Grosjean E, Stalvies C, Fike DA, et al. 2009. Fossil steroids record the appearance of Demospongiae during the Cryogenian period. Nature 457: 718-21.
91. Maloof AC, Rose CV, Beach R, Samuels BM, et al. 2010. Possible animal-body fossils in pre-Marinoan limestones from South Australia. Nat Geosci 3: 653-9.
92. Antcliffe JB, Callow RH, Brasier MD. 2014. Giving the early fossil record of sponges a squeeze. Biol Rev Camb Philos Soc, in press, doi: 10.1111/brv.12090.
93. Antcliffe JB. 2013. Questioning the evidence of organic compounds called sponge biomarkers. Palaeontology 56: 917-25.
94. Logan GA, Hayes JM, Hieshima GB, Summons RE. 1995. Terminal Proterozoic reorganization of biogeochemical cycles. Nature 376: 53-6.
95. Lenton TM, Boyle RA, Poulton SW, Shields-Zhou GA, et al. 2014. Co-evolution of eukaryotes and ocean oxygenation in the Neoproterozoic era. Nat Geosci 7: 257-65.
96. Butterfield NJ. 2009. Oxygen, animals and oceanic ventilation: an alternative view. Geobiol 7: 1-7.
97. Erwin DH, Tweedt S. 2012. Ecological drivers of the Ediacaran-Cambrian diversification of Metazoa. Evol Ecol 26: 417-33.
98. Gaidos E, Dubuc T, Dunford M, McAndrew P, et al. 2007. The Precambrian emergence of animal life: a geobiological perspective. Geobiol 5: 351-73.
99. de Goeij JM, van Oevelen D, Vermeij MJ, Osinga R, et al. 2013. Surviving in a marine desert: the sponge loop retains resources within coral reefs. Science 342: 108-10.
100. Maldonado M, Ribes M, van Duyl FC. 2012. Nutrient fluxes through sponges: biology, budgets, and ecological implications. Adv Mar Biol 62: 113-82.
101. Schwartzman D. 2002. Life, temperature, and the Earth: the self-organizing biosphere. Columbia University Press.
102. Payne JL, McClain CR, Boyer AG, Brown JH, et al. 2011. The evolutionary consequences of oxygenic photosynthesis: a body size perspective. Photosynthesis Res 107: 37-57.
103. Sperling EA, Frieder CA, Raman AV, Girguis PR, et al. 2013. Oxygen, ecology, and the Cambrian radiation of animals. Proc Natl Acad Sci USA 110: 13446-51.
104. Bergman NM, Lenton TM, Watson AJ. 2004. COPSE: a new model of biogeochemical cycling over Phanerozoic time. Am J Sci 304: 397-437.
105. Boyle RA, Lenton TM, Williams HT. 2007. Neoproterozoic 'snowball Earth' glaciations and the evolution of altruism. Geobiol 5: 337-49.
106. Planavsky NJ, Rouxel OJ, Bekker A, Lalonde SV, et al. 2010. The evolution of the marine phosphate reservoir. Nature 467: 1088-90.
107. Knauth LP. 2005. Temperature and salinity history of the Precambrian ocean: implications for the course of microbial evolution. Palaeogeogr Palaeoclimatol Palaeoecol 219: 53-69.
108. Lane N, Martin W. 2010. The energetics of genome complexity. Nature 467: 929-34.
109. Knoll AH, Sperling EA. 2014. Oxygen and animals in Earth history. Proc Natl Acad Sci USA 111: 3907-8.
110. Stanley SM. 1973. An ecological theory for the sudden origin of multicellular life in the late Precambrian. Proc Natl Acad Sci USA 70: 1486-9.
111. Alegado RA, Brown LW, Cao S, Dermenjian RK, et al. 2012. A bacterial sulfonolipid triggers multicellular development in the closest living relatives of animals. eLife 1: 1-16.
112. Boraas ME, Seale DB, Boxhorn JE. 1998. Phagotrophy by a flagellate selects for colonial prey: a possible origin of multicellularity. Evol Ecol 12: 153-64.