Genome beginnings: Rooting the tree of life

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 364, Issue 1527, 2009, Pages 2177-2185

  Lake, James A ^a,b   Skophammer, Ryan G ^a,b   Herbold, Craig W ^b   Servin, Jacqueline A ^b  

^a Cellular and Developmental Biology ^*  (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Archaebacteria; Eubacteria; Eukaryotes; Firmicutes; Indels; Root; Tree of life

Indexed keywords

CLADISTICS; COMMON ANCESTRY; ESTER; EVOLUTIONARY BIOLOGY; GENOME; LIPID; METABOLISM; PROKARYOTE; SPECIATION (BIOLOGY); THERMOPHILY;

ACTINOBACTERIA; ARCHAEA; BACTERIA (MICROORGANISMS); EUKARYOTA; FIRMICUTES; PROKARYOTA;

EID: 67651064683     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2009.0035     Document Type: Article

References (72)

1. Archibald, J. M. 2008 The eocyte hypothesis and the origin of eukaryotic cells. Proc. Natl Acad. Sci. USA 105, 20 049-20 050. (doi:10.1073/pnas.0811118106)
2. Bada, J. L. & Lazcano, A. 2002 Origin of life. Some like it hot, but not the first biomolecules. Science 296, 1982-1983. (doi:10.1126/science.1069487)
3. Baldauf, S. L. & Palmer, J. D. 1993 Animals and fungi are each other's closest relatives: congruent evidence from multiple proteins. Proc. Natl Acad. Sci. USA 90, 11 558-11 562. (doi:10.1073/pnas.90.24.11558)
4. Boone, D. & Castenholz, R. W. 2001 The Archaea and the deep branching and phototrophic Bacteria. New York, NY: Springer.
5. Boucher, Y., Douady, C. J., Papke, R. T., Walsch, D. A., Boudreau, M. E. R., Nesbo, C. L., Case, R. J. & Doolittle, W. F. 2003 Lateral gene transfer and the origins of prokaryotic groups. Annu. Rev. Genet. 37, 283-328. (doi:10.1146/annurev.genet.37.050503.084247)
6. Boucher, Y., Kamekura, M. & Doolittle, W. F. 2004 Origins and evolution of isoprenoid lipid biosynthesis in Archaea. Mol. Microbiol. 52, 515-527. (doi:10.1111/j.1365-2958. 2004.03992.x)
7. Brown, J. R. & Doolittle, W. F. 1995 Root of the universal tree of life based on ancient aminoacyl-transfer RNA synthetase gene duplications. Proc. Natl Acad. Sci. USA 92, 2441-2445. (doi:10.1073/pnas.92.7. 2441)
8. Cavalier-Smith, T. 2002 The neomuran origin of archaebac- teria, the negibacterial root of the universal tree and bacterial megaclassification. Int. J. Syst. Evol. Microbiol. 52, 7-76.
9. Cavalier-Smith, T. 2006 Rooting the tree of life by transition analyses. Biol. Direct 1, 1-135.
10. Champoux, J. J. 2001 DNA topoisomerases: structure, function, and mechanism. Annu. Rev. Biochem. 70, 369-413. (doi:10.1146/annurev. biochem.70.1.369)
11. Chistoserdova, L., Jenkins, C., Kalyuzhnaya, M. G., Marx, C. J., Lapidus, A., Vorholt, J. A., Staley, J. T. & Lidstrom, M. E. 2004 The enigmatic planctomycetes may hold a key to the origins of methanogenesis and methylotrophy. Mol. Biol. Evol. 21, 1234-1241. (doi:10.1093/molbev/ msh113)
12. Cox, C. J., Foster, P. G., Hirt, R. P., Harris, S. R. & Embley, T. M. 2008 The archaebacterial origin of eukaryotes. Proc. Natl Acad. Sci. USA 105, 20 356-20 361. (doi:10. 1073/pnas.0810647105)
13. Dagan, T. & Martin, W. 2006 The tree of one percent. Genome Biol. 7, 118. (doi:10.1186/gb-2006-7-10-118)
14. Daiyasu, H., Kuma, K.-I., Yokoi, T., Morii, H., Koga, Y. & Toh, H. 2005 A study of archaeal enzymes involved in polar lipid synthesis linking amino acid sequence information, genomic contexts and lipid composition. Archaea 1, 399-410.
15. Doolittle, W. F. 1999 Phylogenetic classification and the universal tree. Science 284, 2124-2128. (doi:10.1126/ science.284.5423.2124)
16. Embley, T. M. & Stackebrandt, E. 1994 The molecular phy- logeny and systematics of the actinomycetes. Annu. Rev. Microbiol. 48, 257-289.
17. Felsenstein, J. 1978 Cases in which parsimonyor compatibility methods will be positively misleading. Syst. Zool. 27, 401-410. (doi:10.2307/2412923)
18. Ferry, J. G. & House, C. H. 2006 The stepwise evolution of early life driven by energy conservation. Mol. Biol. Evol. 23, 1286-1292. (doi:10.1093/molbev/msk014)
19. Fitch, W. M. & Upper, K. 1987 The phylogeny of tRNA sequences provides evidence for ambiguity reduction in the origin of the genetic code. Cold Spring Harb. Symp. Quant. Biol. 52, 759 -767.
20. Galtier, N., Tourasse, N. & Gouy, M. 1999 A nonhyperther- mophilic common ancestor to extant life forms. Science 283, 220-221. (doi:10.1126/science.283.5399.220)
21. Gao, B. & Gupta, R. S. 2005 Conserved indels in protein sequences that are characteristic of the phylum Actino- bacteria. Int. J. Syst. Evol. Microbiol. 55, 2401 -2412. doi:10.1099/ijs.0.63785-0)
22. Garrity, G. & Holt, J. G. 2001 The road map to the manual. In Bergey's manual of systematic bacteriology (eds D. Boone & R. W. Castenholz). New York, NY: Springer.
23. Gogarten, J. P. et al. 1989 Evolution of the vacuolar H+- ATPase-implications for the origin of eukaryotes. Proc. Natl Acad.. Sci. USA 86, 6661-6665. (doi:10.1073/pnas.86.17.6661)
24. Gogarten, J. P., Murphey, R. D. & Olendzenski, L. 1999 Horizontal gene transfer: pitfalls and promises. Biol. Bull. 196, 359-361. (doi:10.2307/1542970)
25. Gogarten, J. P., Doolittle, W. F. & Lawrence, J. G. 2002 Prokaryotic evolution in light of gene transfer. Mol. Biol. Evol. 19, 2226-2238.
26. Gokhale, R. S., Saxena, P., Chopra, T. & Mohanty, D. 2007 Versatile polyketide enzymatic machinery for the biosynthesis of complex mycobacterial lipids. Nat. Prod. Rep. 24, 267-277. (doi:10.1039/b616817p)
27. Gouy, M. & Li, W. H. 1989 Phylogenetic analysis based on ribosomal-RNA sequences supports the archaebacterial rather than the eocyte tree. Nature 339, 145 -147. (doi:10.1038/339145a0)
28. Grassineau, N. V., Nisbet, E. G., Bickle, M. J., Fowler, C. M. R., Lowry, D., Mattey, D. P., Abell, P. & Martin, A. 2001 Antiquity of the biological sulphur cycle: evidence from sulphur and carbon isotopes in 2700 million-year- old rocks of the Belingwe Belt, Zimbabwe. Proc.R.Soc.B 268, 113-119. (doi:10.1098/rspb.2000.1338)
29. Gribaldo, S. & Brochier-Armanet, C. 2006 The origin and evolution of Archaea: a state of the art. Phil.Trans.R.Soc. B 361, 1077-1022. (doi:10.1098/rstb.2006.1841)
30. Gupta, R. S. 1998 Protein phylogenies and signature sequences: a reappraisal of evolutionary relationships among archaebacteria, eubacteria, and eukaryotes. Microbiol. Mol. Biol. Rev. 62, 1435-1491.
31. Gupta, R. S. & Singh, B. 1994 Phylogenetic analysis of 70- kD heat-shock protein sequences suggests a chimeric origin for the eukaryotic cell-nucleus. Curr. Biol. 4, 1104-1114. (doi:10.1016/S0960- 9822(00)00249-9)
32. Heinemann, J. A. & Sprague Jr, G. F. 1989 Bacterial conjugative plasmids mobilize DNA transfer between bacteria and yeast. Nature 340, 205-209. (doi:10.1038/ 340205a0)
33. Hendrix, R. W., Smith, M. C., Burns, R. N., Ford, M. E. & Hatfull, G. F. 1999 Evolutionary relationships among diverse bacteriophages and prophages: all the world's a phage. Proc. Natl Acad. Sci. USA 96, 2192-2197. (doi:10.1073/pnas.96.5.2192)
34. Hilario, E. & Gogarten, J. P. 1993 Horizontal transfer of ATPase genes-the tree of life becomes a net of life. Biosystems 31, 111-119. (doi:10.1016/0303-2647(93) 90038-E)
35. Iwabe, N., Kuma, K., Hasegawa, M., Osawa, S. & Miyata, T. 1989 Evolutionary relationship of archae- bacteria, eubacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes. Proc. Natl Acad. Sci. USA 86, 9355-9359. (doi:10.1073/pnas.86.23.9355)
36. Jain, R., Rivera, M. C. & Lake, J. A. 1999 Horizontal gene transfer among genomes: the complexity hypothesis. Proc. Natl Acad. Sci. USA 96, 3801 -3806. (doi:10. 1073/pnas.96.7.3801)
37. Jain, R., Rivera, M. C., Moore, J. E. & Lake, J. A. 2003 Horizontal gene transfer accelerates genome innovation and evolution. Mol. Biol. Evol. 20, 1598-1602. (doi:10. 1093/molbev/msg154)
38. Kelly, D. et al. 2005 A serpentinite-hosted ecosystem: the Lost City hydrothermal field. Science 307, 1428-1434. (doi:10.1126/science.1102556)
39. Konstantinidis, K. T. & Tiedje, J. M. 2005 Towards a genome- based taxonomy for prokaryotes. J. Bacteriol. 187, 6258-6264. (doi:10.1128/JB.187.18.6258-6264.2005)
40. Lake, J. A. 1988 Origin ofthe eukaryotic nucleus determined by rate-invariant analysis of ribosomal RNA sequences. Nature 331, 184-186. (doi:10.1038/331184a0)
41. Lake, J. A. 1991 Tracing origins with molecular sequences: metazoan and eukaryotic beginnings. Trends Biochem. Sci. 16, 46-50. (doi:10.1016/0968-0004(91)90020-V)
42. Lake, J. A. 2008 Reconstructing evolutionary graphs: 3D parsimony. Mol. Biol. Evol. 25, 1677 -1682. (doi:10. 1093/molbev/msn117)
43. Lake, J. A., Moore, J. E., Simonson, A. B. & Rivera, M. C. 2005 Fulfilling Darwin's dream. In Microbial evolution: concepts and controversies, (ed. J. Sapp), pp. 184-206. New York, NY: Oxford University Press.
44. Lake, J. A., Herbold, C. W., Rivera, M. C., Servin, J. A. & Skophammer, R. G. 2007 Rooting the tree of life using non-ubiquitous genes. Mol. Biol. Evol. 24, 130-136. (doi:10.1093/molbev/msl140)
45. Lake, J. A., Servin, J. A., Herbold, C. W. & Skophammer, R. G. 2008 Evidence for a new root of the tree of life. Syst. Biol. 57, 835-843. (doi:10.1080/10635150802555933)
46. Lange, B. M., Rujan, T., Martin, W. & Croteau, R. 2000 Isoprenoid biosynthesis: the evolution of two ancient and distinct pathways across genomes. Proc. Natl Acad. Sci. USA 97, 13 172-13 177. (doi:10.1073/pnas. 240454797)
47. Locher, K. P., Allen, T. L. & Rees, D. C. 2002 The E. coli BtuCD structure: a framework for ABC transporter architecture and mechanism. Science 296, 1091 -1097. (doi:10.1126/science.1071142)
48. Macnab, R. M. 2003 How bacteria assemble flagella. Annu. Rev. Microbiol. 57, 77-100. (doi:10.1146/annurev.micro. 57.030502.090832)
49. Martin, W. & Russell, M. J. 2003 On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. Phil. Trans. R. Soc. Lond. B 358, 59-85. (doi:10.1098/rstb.2002.1183)
50. McInerney, J. O. & Pisani, D. 2007 Paradigm for life. Science 318, 1390-1391. (doi:10.1126/science.1151657)
51. Miller, S. L. & Bada, J. L. 1988 Submarine hot springs and the origin of life. Nature 334, 609 -611. (doi:10.1038/ 334609a0)
52. Miller, S. L. & Lazcano, A. 1995 The origin of life-did it occur at high temperatures? J. Mol. Evol. 41, 689-692.
53. Ochman, H., Lawrence, J. G. & Groisman, E. A. 2000 Lateral gene transfer and the nature of bacterial innovation. Nature 405, 299-304. (doi:10.1038/35012500)
54. Ohno, M. et al. 2000 Symbiobacterium thermophilum gen. nov., sp. nov., a symbiotic thermophile that depends on co-culture with a Bacillus strain for growth. Int. J. Syst. Evol. Microbiol. 50, 1829-1832.
55. Philippe, H. & Forterre, P. 1999 The rooting ofthe universal tree of life is not reliable. J. Mol. Evol. 49, 509 -523. (doi:10.1007/PL00006573)
56. Philippe, H., Budin, K. & Moreira, D. 1999 Horizontal transfers confuse the prokaryotic phylogeny based on the HSP70 protein family. Mol. Microbiol. 31, 10071012. (doi:10.1046/j.1365-2958.1999.01185.x)
57. Purdy, K. J., Nedwell, D. B. & Embley, T. M. 2003 Analysis of the sulfate-reducing bacterial and methanogenic archaeal populations in contrasting Antarctic sediments. Appl. Environ. Microbiol. 69, 4501. (doi:10.1128/AEM. 69.6.3181-3191.2003)
58. Rivera, M. C. & Lake, J. A. 1992 Evidence that eukaryotes and eocyte prokaryotes are immediate relatives. Science 257, 74-76. (doi:10.1126/science.1621096)
59. Rivera, M. C. & Lake, J. A. 2004 The ring of life: evidence for a genome fusion origin of eukaryotes. Nature 431, 152-155. (doi:10.1038/nature02848)
60. Russell, M. J. & Hall, A. J. 1997 The emergence of life from iron monosulphide bubbles at a submarine hydrothermal redox and pH front. J. Geol. Soc. Lond. 154, 377 -402. (doi:10.1144/gsjgs.154.3.0377)
61. Russell, M. J. & Martin, W. 2004 The rocky roots of the acetyl-CoA pathway. Trends Biochem. Sci. 29, 358-363. (doi:10.1016/j.tibs. 2004.05.007)
62. Servin, J. A., Herbold, C. W., Skophammer, R. G. & Lake, J. A. 2008 Evidence excluding the root of the tree of life from the Actinobacteria. Mol. Biol. Evol. 25, 1-4. (doi:10.1093/molbev/msm249)
63. Skophammer, R. G., Herbold, C. W., Rivera, M., Servin, J. A. & Lake, J. A. 2006 Evidence that the root of the tree of life is not within the Archaea. Mol. Biol. Evol. 23, 1648-1651. (doi:10.1093/molbev/msl046)
64. Skophammer, R. G., Servin, J. A., Herbold, C. W. & Lake, J. A. 2007 Evidence for a Gram positive, eubacterial root of the tree of life. Mol. Biol. Evol. 24, 1761 -1768. (doi: 10.1093/molbev/msm096)
65. Smit, A. & Mushegian, A. R. 2000 Biosynthesis of isoprenoids via mevalonate in Archaea: the lost pathway. Genome Res. 10, 1468-1484. (doi:10.1101/gr 145600)
66. Sorek, R., Zhu, Y., Creevery, C. J., Francino, M. P., Bork, P. & Rubin, E. M. 2007 Genome-wide experimental determination of barriers to horizontal gene transfer. Science 318, 1449-1452. (doi:10.1126/science.1147112)
67. Syvanen, M. & Kado, C. I. (eds) 1998 Horizontal gene transfer. London, UK: Chapman & Hall.
68. Ueda, K., Yamashita, A., Ishikawa, J., Shimada, M., Watsuji, T., Morimura, K., Ikeda, H., Hattori, M. & Beppu, T. 2004 Genome sequence ofSymbiobacterium thermophilum, an uncultivable bacterium that depends on microbial commensalism. Nucleic Acids Res. 32, 4937-4944. (doi:10.1093/nar/gkh830)
69. Woese, C. R. 2002 On the evolution of cells. Proc. Natl Acad. Sci. USA 99, 2742-2747. (doi:10.1073/pnas.132266999)
70. Wu, M. et al. 2005 Life in hot carbon monoxide: the complete genome sequence of Carboxydothermus hydroge- noformans Z-2901. PLoS Genet. 1, 563 -574. (doi:10. 1371/journal.pgen.0010065)
71. Zhaxybayeva, O. & Gogarten, J. P. 2004 Cladogenesis, coalescence and the evolution of the three domains of life. Trends Genet. 20, 182-187. (doi:10.1016/j.tig.2004. 02.004)
72. Zhaxybayeva, O., Lapierre, P. & Gogarten, J. P. 2005 Ancient gene duplications and the root(s) of the tree of life. Protoplasma 227, 53-64. (doi:10.1007/s00709-005- 0135-1)