Evolution of multicellularity coincided with increased diversification of cyanobacteria and the Great Oxidation Event

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 5, 2013, Pages 1791-1796

  Schirrmeister, Bettina E ^a,c   De Vos, Jurriaan M ^a   Antonelli, Alexandre ^b   Bagheri, Homayoun C ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Early life; Major transitions; Molecular clock; Prokaryotic phylogenetics

Indexed keywords

OXYGEN; RNA 16S;

ARTICLE; BACTERIAL GENOME; CELL LINEAGE; CYANOBACTERIUM; MICROBIAL DIVERSITY; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION; PHYLOGENETIC TREE; PHYLUM; PRIORITY JOURNAL; RNA SEQUENCE; SEQUENCE ALIGNMENT;

ATMOSPHERE; BAYES THEOREM; BIODIVERSITY; BIOLOGICAL EVOLUTION; CYANOBACTERIA; GENETIC VARIATION; MARKOV CHAINS; MOLECULAR SEQUENCE DATA; MONTE CARLO METHOD; OXIDATION-REDUCTION; OXYGEN; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; TIME FACTORS;

EID: 84873157581     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1209927110     Document Type: Article

References (87)

1. Boone DR, Castenholz RW (2001) Bergey's Manual of Systematic Bacteriology: The Archaea and the Deeply Branching and Phototropic Bacteria: Cyanobacteria, ed Garrity GM (Springer, New York).
2. Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Genl MicrobioLogy 111:1-61. (Pubitemid 9142236)
3. Giovannoni SJ, et al. (1988) Evolutionary relationships among cyanobacteria and green chloroplasts. J Bacteriol 170(8):3584-3592.
4. Gugger MF, Hoffmann L (2004) Polyphyly of true branching cyanobacteria (Stigonematales). Int J Syst Evol Microbiol 54(Pt 2):349-357. (Pubitemid 38443725)
5. Schirrmeister BE, Antonelli A, Bagheri HC (2011) The origin of multicellularity in cyanobacteria. BMC Evol Biol 11:45.
6. Amard B, Bertrand-Sarfati J (1997) Microfossils in 2000 ma old cherty stromatolites of the Franceville group, Gabon. Precambrian Res 81(3-4):197-221.
7. Hofmann HJ (1976) Precambrian Microflora, Belcher islands, Canada-Significance and systematics. J Paleontol 50(6):1040-1073.
8. Blankenship RE (2002) Molecular Mechanisms of Photosynthesis (Blackwell Science, Oxford).
9. Bekker A, et al. (2004) Dating the rise of atmospheric oxygen. Nature 427(6970):117-120. (Pubitemid 38094946)
10. Kopp RE, Kirschvink JL, Hilburn IA, Nash CZ (2005) The Paleoproterozoic snowball Earth: A climate disaster triggered by the evolution of oxygenic photosynthesis. Proc Natl Acad Sci USA 102(32):11131-11136. (Pubitemid 41153787)
11. Allen JF, Martin W (2007) Evolutionary biology: Out of thin air. Nature 445(7128):610-612. (Pubitemid 46232875)
12. Frei R, Gaucher C, Poulton SW, Canfield DE (2009) Fluctuations in Precambrian atmospheric oxygenation recorded by chromium isotopes. Nature 461(7261):250-253.
13. Tomitani A, Knoll AH, Cavanaugh CM, Ohno T (2006) The evolutionary diversification of cyanobacteria: Molecular-phylogenetic and paleontological perspectives. Proc Natl Acad Sci USA 103(14):5442-5447.
14. Battistuzzi FU, Hedges SB (2009) A major clade of prokaryotes with ancient adaptations to life on land. Mol Biol Evol 26(2):335-343.
15. Blank CE, Sánchez-Baracaldo P (2010) Timing of morphological and ecological innovations in the cyanobacteria-A key to understanding the rise in atmospheric oxygen. Geobiology 8(1):1-23.
16. Larsson J, Nylander JAA, Bergman B (2011) Genome fluctuations in cyanobacteria reflect evolutionary, developmental and adaptive traits. BMC Evol Biol 11:187.
17. Schirrmeister BE, Anisimova M, Antonelli A, Bagheri HC (2011) Evolution of cyanobacterial morphotypes: Taxa required for improved phylogenomic approaches. Commun Integr Biol 4(4):424-427.
18. Wu DY, et al. (2009) A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea. Nature 462(7276):1056-1060.
19. Golubic S, Lee SJ (1999) Early cyanobacterial fossil record: Preservation, palaeoenvironments and identification. Eur J Phycol 34(4):339-348.
20. Sergeev VN, Gerasimenko LM, Zavarzin GA (2002) [Proterozoic history and present state of cyanobacteria]. Mikrobiologiia 71(6):725-740. (Pubitemid 44796468)
21. Benton MJ (2003) The quality of the fossil record. Telling the Evolutionary Time: Molecular Clocks and the Fossil Record, eds Donoghue PCJ, Smith MP (Tayler & Francis, London), pp 66-90.
22. Reisz RR, Müller J (2004) Molecular timescales and the fossil record: A paleontological perspective. Trends Genet 20(5):237-241. (Pubitemid 38510436)
23. Donoghue PCJ, Benton MJ (2007) Rocks and clocks: Calibrating the Tree of Life using fossils and molecules. Trends Ecol Evol 22(8):424-431. (Pubitemid 47058779)
24. Turner S, Pryer KM, Miao VPW, Palmer JD (1999) Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J Eukaryot Microbiol 46(4):327-338. (Pubitemid 29400753)
25. Honda D, Yokota A, Sugiyama J (1999) Detection of seven major evolutionary lineages in cyanobacteria based on the 16S rRNA gene sequence analysis with new sequences of five marine Synechococcus strains. J Mol Evol 48(6):723-739. (Pubitemid 29287963)
26. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4(5):e88.
27. Doolittle WF (1999) Phylogenetic classification and the universal tree. Science 284(5423):2124-2129.
28. Gogarten JP, Doolittle WF, Lawrence JG (2002) Prokaryotic evolution in light of gene transfer. Mol Biol Evol 19(12):2226-2238. (Pubitemid 35440456)
29. Andam CP, Gogarten JP (2011) Biased gene transfer in microbial evolution. Nat Rev Microbiol 9(7):543-555.
30. Suchard MA (2005) Stochastic models for horizontal gene transfer: Taking a random walk through tree space. Genetics 170(1):419-431. (Pubitemid 40800003)
31. Lapierre P, Lasek-Nesselquist E, Gogarten JP (2012) The impact of HGT on phylogenomic reconstruction methods. Brief Bioinform, 10.1093/bib/bbs050.
32. Yarza P, et al. (2008) The All-Species Living Tree project: A 16S rRNA-based phylogenetic tree of all sequenced type strains. Syst Appl Microbiol 31(4):241-250.
33. Woese CR (1987) Bacterial evolution. Microbiol Rev 51(2):221-271. (Pubitemid 17082512)
34. Olsen GJ, Woese CR (1993) Ribosomal RNA: A key to phylogeny. FASEB J 7(1):113-123. (Pubitemid 23034021)
35. Schirrmeister BE, Dalquen DA, Anisimova M, Bagheri HC (2012) Gene copy number variation and its significance in cyanobacterial phylogeny. BMC Microbiol 12(1):177.
36. Snel B, Bork P, Huynen MA (2002) Genomes in flux: The evolution of archaeal and proteobacterial gene content. Genome Res 12(1):17-25. (Pubitemid 34065586)
37. Kurland CG, Canback B, Berg OG (2003) Horizontal gene transfer: A critical view. Proc Natl Acad Sci USA 100(17):9658-9662. (Pubitemid 37086996)
38. Rokas A (2008) The molecular origins of multicellular transitions. Curr Opin Genet Dev 18(6):472-478.
39. Rossetti V, Filippini M, Svercel M, Barbour AD, Bagheri HC (2011) Emergent multicellular life cycles in filamentous bacteria owing to density-dependent population dynamics. J R Soc Interface 8(65):1772-1784.
40. Knoll AH, Javaux EJ, Hewitt D, Cohen P (2006) Eukaryotic organisms in Proterozoic oceans. Philos Trans R Soc Lond B Biol Sci 361(1470):1023-1038. (Pubitemid 44858913)
41. Giddings TH, Staehelin LA (1981) Observation of Microplasmodesmata in both heterocyst-forming and non-heterocyst forming filamentous Cyanobacteria by freezefracture electron microscopy. Arch Microbiol 129(4):295-298.
42. Flores E, Herrero A, Wolk CP, Maldener I (2006) Is the periplasm continuous in filamentous multicellular cyanobacteria? Trends Microbiol 14(10):439-443. (Pubitemid 44375022)
43. Flores E, Herrero A (2010) Compartmentalized function through cell differentiation in filamentous cyanobacteria. Nat Rev Microbiol 8(1):39-50.
44. Rossetti V, Schirrmeister BE, Bernasconi MV, Bagheri HC (2010) The evolutionary path to terminal differentiation and division of labor in cyanobacteria. J Theor Biol 262(1):23-34.
45. Ispolatov I, Ackermann M, Doebeli M (2012) Division of labour and the evolution of multicellularity. Proc Biol Sci 279(1734):1768-1776.
46. Rossetti V, Bagheri HC (2012) Advantages of the division of labour for the long-term population dynamics of cyanobacteria at different latitudes. Proc Biol Sci 279(1742):3457-3466.
47. Maynard Smith J, Szathmary E (1995) The Major Transitions in Evolution. (Oxford University Press, Oxford).
48. Bonner J (1998) The origin of multicellularity. Integr Biol 1(1):28-36.
49. Adams DG (1997) Cyanobacteria. Bacteria as Multicellular Organism, eds Shapiro JA, Dworkin M (Oxford Univ Press, New York), pp 109-148.
50. Ratcliff WC, Denison RF, Borrello M, Travisano M (2012) Experimental evolution of multicellularity. Proc Natl Acad Sci USA 109(5):1595-1600.
51. Koschwanez JH, Foster KR, Murray AW (2011) Sucrose utilization in budding yeast as a model for the origin of undifferentiated multicellularity. PLoS Biol 9(8):e1001122.
52. Nisbet EG, Sleep NH (2001) The habitat and nature of early life. Nature 409(6823):1083-1091. (Pubitemid 32206166)
53. Mojzsis SJ (2010) Early earth leftover lithosphere. Nat Geosci 3:148-149.
54. Sleep NH, Zahnle KJ, Kasting JF, Morowitz HJ (1989) Annihilation of ecosystems by large asteroid impacts on the early Earth. Nature 342(6246):139-142. (Pubitemid 20409866)
55. Westall F, et al. (2006) The 3.466 ga "Kitty's gap chert" an early Archean microbial ecosystem. Spec Pap Geol Soc Am 405:105-131.
56. Wacey D (2009) Early Life on Earth: A Practical Guide (Springer, New York).
57. Tice MM, Lowe DR (2004) Photosynthetic microbial mats in the 3, 416-Myr-old ocean. Nature 431(7008):549-552. (Pubitemid 39336331)
58. Sugitani K, et al. (2007) Diverse microstructures from Archaean chert from the mount Goldsworthy-mount grant area, Pilbara Craton, Western Australia: Microfossils, dubiofossils, or pseudofossils? Precambrian Res 158:228-262. (Pubitemid 47374911)
59. Glikson M, et al. (2008) Microbial remains in some earliest Earth rocks: Comparison with a potential modern analogue. Precambrian Res 164(3-4):187-200.
60. Wacey D, et al. (2008) Use of nanosims in the search for early life on Earth: Ambient inclusion trails in a c. 3400 ma sandstone. J Geol Soc London 165(1):43-53.
61. Knoll AH (1996) Palynology: Principles and Applications-Archean and Proterozoic Paleontology. (American Association of Stratigraphic Palynologists, Tulsa, OK), pp 51-80.
62. Altermann W, Schopf JW (1995) Microfossils from the Neoarchean Campbell Group, Griqualand west sequence of the Transvaal Supergroup, and their paleoenvironmental and evolutionary implications. Precambrian Res 75(1-2):65-90. (Pubitemid 26459239)
63. Kazmierczak J, Altermann W (2002) Neoarchean biomineralization by benthic cyanobacteria. Science 298(5602):2351.
64. Schopf JW (2009) Paleontology, microbial. Encyclopedia of Microbiology, eds Lederberg J, Schaechter M (Elsevier, Amsterdam), 3rd Ed, pp 390-400.
65. Brocks JJ, Logan GA, Buick R, Summons RE (1999) Archean molecular fossils and the early rise of eukaryotes. Science 285(5430):1033-1036.
66. Summons RE, Jahnke LL, Hope JM, Logan GA (1999) 2-Methylhopanoids as biomarkers for cyanobacterial oxygenic photosynthesis. Nature 400(6744):554-557. (Pubitemid 29381801)
67. Rasmussen B, Fletcher IR, Brocks JJ, Kilburn MR (2008) Reassessing the first appearance of eukaryotes and cyanobacteria. Nature 455(7216):1101-1104.
68. Lyons TW, Reinhard CT (2011) Earth science: Sea change for the rise of oxygen. Nature 478(7368):194-195.
69. Gaillard F, Scaillet B, Arndt NT (2011) Atmospheric oxygenation caused by a change in volcanic degassing pressure. Nature 478(7368):229-232.
70. Waldbauer JR, Sherman LS, Sumner DY, Summons RE (2009) Late Archean molecular fossils from the Transvaal Supergroup record the antiquity of microbial diversity and aerobiosis. Precambrian Res 169(1-4):28-47.
71. Stüeken EE, Catling DC, Buick R (2012) Contributions to late Archaean sulphur cycling by life on land. Nat Geosci 5(10):722-725.
72. Schopf JW (1993) Microfossils of the Early Archean Apex chert: New evidence of the antiquity of life. Science 260(5108):640-646. (Pubitemid 23392043)
73. Brasier M, McLoughlin N, Green O, Wacey D (2006) Afresh look at the fossil evidence for early Archaean cellular life. Philos Trans R Soc Lond B Biol Sci 361(1470):887-902. (Pubitemid 44858907)
74. Bilofsky HS, Burks C (1988) The GenBank genetic sequence data bank. Nucleic Acids Res 16(5):1861-1863.
75. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792-1797. (Pubitemid 38832724)
76. Akaike H (1974) New look at statistical-model identification. IEEE Trans Automat Contr AC 19(6):716-723.
77. Hurvich CM, Tsai CL (1989) Regression and time-series model selection in small samples. Biometrika 76(2):297-307.
78. Posada D (2008) jModelTest: Phylogenetic model averaging. Mol BiolEvol 25(7):1253-1256. (Pubitemid 351882013)
79. Lanave C, Preparata G, Saccone C, Serio G (1984) A new method for calculating evolutionary substitution rates. J Mol Evol 20(1):86-93. (Pubitemid 14116237)
80. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214.
81. Rippka R, Waterbury J, Cohenbazire G (1974) Cyanobacterium which lacks thylakoids. Arch Microbiol 100(1):419-436.
82. Nakamura Y, et al. (2003) Complete genome structure of Gloeobacter violaceus PCC 7421, a cyanobacterium that lacks thylakoids. DNA Res 10(4):137-145. (Pubitemid 37288299)
83. Ferris MJ, Ruff-Roberts AL, Kopczynski ED, Bateson MM, Ward DM (1996) Enrichment culture and microscopy conceal diverse thermophilic Synechococcus populations in a single hot spring microbial mat habitat. Appl Environ Microbiol 62(3):1045-1050.
84. Miller M, et al. (2009) The CIPRES portals. CIPRES. Available at. www.phyloorg/sub-sections/portal. Accessed February 2012.
85. Sukumaran J, Holder MT (2010) DendroPy: A Python library for phylogenetic computing. Bioinformatics 26(12):1569-1571.
86. Golubic S, Sergeev VN, Knoll AH (1995) Mesoproterozoic Archaeoellipsoides: Akinetes of heterocystous cyanobacteria. Lethaia 28:285-298. (Pubitemid 26460277)
87. Alfaro ME, et al. (2009) Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates. Proc Natl Acad Sci USA 106(32):13410-13414.