Phylogenetic analyses of cyanobacterial genomes: Quantification of horizontal gene transfer events

Genome Research

Volumn 16, Issue 9, 2006, Pages 1099-1108

  Zhaxybayeva, Olga ^a,b   Gogarten, J Peter ^b   Charlebois, Robert L ^a   Doolittle, W Ford ^a   Papke, R Thane ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

^b UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL GENOME; COMPUTER SIMULATION; CYANOBACTERIUM; HORIZONTAL GENE TRANSFER; MOLECULAR EVOLUTION; MULTIGENE FAMILY; ORTHOLOGY; PHOTOSYNTHESIS; PHYLOGENETIC TREE; PHYLOGENY; PRIORITY JOURNAL; PROCHLOROCOCCUS; SEQUENCE HOMOLOGY; STRAIN DIFFERENCE; SYNECHOCOCCUS;

COMPUTATIONAL BIOLOGY; CYANOBACTERIA; EVOLUTION, MOLECULAR; GENE TRANSFER, HORIZONTAL; GENOME, BACTERIAL; PHYLOGENY; PROCHLOROCOCCUS; SYNECHOCOCCUS;

CYANOBACTERIA;

EID: 33748277982     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.5322306     Document Type: Article

References (75)

1. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402.
2. Andersson, J.O., Sarchfield, S.W., Roger, A.J., Sjogren, A.M., Davis, L.A., and Embley, T.M. 2005. Gene transfers from Nanoarchaeota to an ancestor of diplomonads and parabasalids - Phylogenetic analyses of diplomonad genes reveal frequent lateral gene transfers affecting eukaryotes. Mol. Biol. Evol. 22: 85-90.
3. Bapteste, E., Boucher, Y., Leigh, J., and Doolittle, W.F. 2004. Phylogenetic reconstruction and lateral gene transfer. Trends Microbiol. 12: 406-411.
4. Barker, G.L., Handley, B.A., Vacharapiyasophon, P., Stevens, J.R., and Hayes, P.K. 2000. Allele-specific PCR shows that genetic exchange occurs among genetically diverse Nodularia (cyanobacteria) filaments in the Baltic Sea. Microbiol. 146: 2865-2875.
5. Baum, B. 1992. Combining trees as a way of combining data sets for phylogenetic inference, and the desirability of combining gene trees. Taxon 41: 3-10.
6. Beiko, R.G., Harlow, T.J., and Ragan, M.A. 2005. Highways of gene sharing in prokaryotes. Proc. Natl. Acad. Sci. 102: 14332-14337.
7. Boucher, Y., Douady, C.J., Papke, R.T., Walsh, D.A., Boudreau, M.E., Nesbo, C.L., Case, R.J., and Doolittle, W.F. 2003. Lateral gene transfer and the origins of prokaryotic groups. Annu. Rev. Genet. 37: 283-328.
8. Boucher, Y., Douady, C.J., Sharma, A.K., Kamekura, M., and Doolittle, W.F. 2004. Intragenomic heterogeneity and intergenomic recombination among haloarchaeal rRNA genes. J. Bacteriol. 186: 3980-3990.
9. Charlebois, R.L. and Doolittle, W.F. 2004. Computing prokaryotic gene ubiquity: Rescuing the core from extinction. Genome Res. 14: 2469-2477.
10. Chase, P. 1970. Algorithm 382: Combinations of M out of N objects [G6]. Commun. ACM 13: 368.
11. Chisholm, S.W., Olson, R.J., Zettler, E.R., Goericke, R., Waterbury, J.B., and Welschmeyer, N.A. 1988. A novel free-living prochlorophyte abundant in the oceanic euphotic zone. Nature 334: 340-343.
12. Creevey, C.J. and McInerney, J.O. 2005. Clann: Investigating phylogenetic information through supertree analyses. Bioinformatics 21: 390-392.
13. Drummond, A. and Strimmer, K. 2001. PAL: An object-oriented programming library for molecular evolution and phylogenetics. Bioinformatics 17: 662-663.
14. Dufresne, A., Garczarek, L., and Partensky, F. 2005. Accelerated evolution associated with genome reduction in a free-living prokaryote. Genome Biol. 6: R14.
15. Felsenstein, J. 1978. Cases in which parsimony and compatibility methods will be positively misleading. Syst. Zool. 27: 401-410.
16. _. 1993. PHYLIP (Phylogeny Inference Package). Distributed by the author. Department of Genetics, University of Washington, Seattle.
17. _. 2004. Inferring phylogenies. Sinauer, Sunderland, MA.
18. Ge, F., Wang, L.-S., and Kim, J. 2005. The cobweb of life revealed by genome-scale estimates of horizontal gene transfer. PLoS Biol. 3: e316.
19. Giovannoni, S.J., Turner, S., Olsen, G.J., Barns, S., Lane, D.J., and Pace, N.R. 1988. Evolutionary relationships among cyanobacteria and green chloroplasts. J. Bacteriol. 170: 3584-3592.
20. Gogarten, J.P. and Townsend, J.P. 2005. Horizontal gene transfer, genome innovation and evolution. Nat. Rev. Microbiol. 3: 679-687.
21. Gogarten, J.P., Doolittle, W.F., and Lawrence, J.G. 2002. Prokaryotic evolution in light of gene transfer. Mol. Biol. Evol. 19: 2226-2238.
22. Grant, P.R., Grant, B.R., Markert, J.A., Keller, L.F., and Petren, K. 2004. Convergent evolution of Darwin's finches caused by introgressive hybridization and selection. Evolution Int. J. Org. Evolution 58: 1588-1599.
23. Guindon, S. and Gascuel, O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52: 696-704.
24. Gupta, R.S., Pereira, M., Chandrasekera, C., and Johari, V. 2003. Molecular signatures in protein sequences that are characteristic of cyanobacteria and plastid homologues. Int. J. Syst. Evol. Microbiol. 53: 1833-1842.
25. Hagen, K.D. and Meeks, J.C. 2001. The unique cyanobacterial protein OpcA is an allosteric effector of glucose-6-phosphate dehydrogenase in Nostoc punctiforme ATCC 29133. J. Biol. Chem. 276: 11477-11486.
26. Harlow, T.J., Gogarten, J.P., and Ragan, M.A. 2004. A hybrid clustering approach to recognition of protein families in 114 microbial genomes. BMC Bioinformatics 5: 45.
27. Hendy, M. and Penny, M. 1993. Spectral analysis of phylogenetic data. J. Classif. 10: 5-24.
28. Honda, D., Yokota, A., and 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: 723-739.
29. Huang, J., Xu, Y., and Gogarten, J.P. 2005. The presence of a haloarchaeal type tyrosyl tRNA synthetase marks the opisthokonts as monophyletic. Mol. Biol. Evol. 22: 2142-2146.
30. Ikeuchi, M. and Tabata, S. 2001. Synechocystis sp. PCC 6803 - A useful tool in the study of the genetics of cyanobacteria. Photosynth. Res. 70: 73-83.
31. Iwai, M., Katoh, H., Katayama, M., and Ikeuchi, M. 2004. Improved genetic transformation of the thermophilic cyanobacterium, Thermosynechococcus elongatus BP-1. Plant Cell Physiol. 45: 171-175.
32. Jain, R., Rivera, M.C., and Lake, J.A. 1999. Horizontal gene transfer among genomes: The complexity hypothesis. Proc. Natl. Acad. Sci. 96: 3801-3806.
33. Koonin, E.V., Makarova, K.S., and Aravind, L. 2001. Horizontal gene transfer in prokaryotes: Quantification and classification. Annu. Rev. Microbiol. 55: 709-742.
34. Kunin, V., Goldovsky, L., Darzentas, N., and Ouzounis, C.A. 2005. The net of life: Reconstructing the microbial phylogenetic network. Genome Res. 15: 954-959.
35. Lawrence, J.G. 2002. Gene transfer in bacteria: Speciation without species? Theor. Popul. Biol. 61: 449-460.
36. Lawrence, J.G. and Hendrickson, H. 2005. Genome evolution in bacteria: Order beneath chaos. Curr. Opin. Microbiol. 8: 572-578.
37. Lento, G.M., Hickson, R.E., Chambers, G.K., and Penny, D. 1995. Use of spectral analysis to test hypotheses on the origin of pinnipeds. Mol. Biol. Evol. 12: 28-52.
38. Lerat, E., Daubin, V., and Moran, N.A. 2003. From gene trees to organismal phylogeny in prokaryotes: The case of the γ-Proteobacteria. PLoS Biol. 1: E19.
39. Lindell, D., Sullivan, M.B., Johnson, Z.I., Tolonen, A.C., Rohwer, F., and Chisholm, S.W. 2004. Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc. Natl. Acad. Sci. 101: 11013-11018.
40. Lodders, N., Stackebrandt, E., and Nubel, U. 2005. Frequent genetic recombination in natural populations of the marine cyanobacterium Microcoleus chthonoplastes. Environ. Microbiol. 7: 434-442.
41. Mann, N.H., Cook, A., Millard, A., Bailey, S., and Clokie, M. 2003. Marine ecosystems: Bacterial photosynthesis genes in a virus. Nature 424: 741.
42. Millard, A., Clokie, M.R., Shub, D.A., and Mann, N.H. 2004. Genetic organization of the psbAD region in phages infecting marine Synechococcus strains. Proc. Natl. Acad. Sci. 101: 11007-11012.
43. Miller, S.R., Augustine, S., Olson, T.L., Blankenship, R.E., Selker, J., and Wood, A.M. 2005. Discovery of a free-living chlorophyll d-producing cyanobacterium with a hybrid proteobacterial/cyanobacterial small-subunit rRNA gene. Proc. Natl. Acad. Sci. 102: 850-855.
44. Mirkin, B.G., Fenner, T.I., Galperin, M.Y., and Koonin, E.V. 2003. Algorithms for computing parsimonious evolutionary scenarios for genome evolution, the last universal common ancestor and dominance of horizontal gene transfer in the evolution of prokaryotes. BMC Evol. Biol. 3: 2.
45. Mitreva, M., Blaxter, M.L., Bird, D.M., and McCarter, J.P. 2005. Comparative genomics of nematodes. Trends Genet. 21: 573-581.
46. Morandi, A., Zhaxybayeva, O., Gogarten, J.P., and Graf, J. 2005. Evolutionary and diagnostic implications of intragenomic heterogeneity in the 16S rRNA gene in Aeromonas strains. J. Bacteriol. 187: 6561-6564.
47. Nagai, T., Ru, S., Katoh, A., Dong, S., and Kuwabara, T. 2001. An extracellular hemolysin homolog from cyanobacterium Synechocystis sp. PCC6803. In Proceedings of 12th International Congress on Photosynthesis, pp. S36-S10. CSIRO Publishing, Melbourne, Australia.
48. Nakamura, Y., Itoh, T., Matsuda, H., and Gojobori, T. 2004. Biased biological functions of horizontally transferred genes in prokaryotic genomes. Nat. Genet. 36: 760-766.
49. Ochman, H., Lawrence, J.G., and Groisman, E.A. 2000. Lateral gene transfer and the nature of bacterial innovation. Nature 405: 299-304.
50. Olendzenski, L., Zhaxybayeva, O., and Gogarten, J.P. 2002. Horizontal gene transfer: A new taxonomic principle? In Horizontal gene transfer (eds. M. Syvanen and C. Kado), pp. 427-435. Academic Press, New York.
51. Otero, A. and Vincenzini, M. 2004. Nostoc (Cyanophyceae) goes nude: Extracellular polysaccharides serve as a sink for reducing power under unbalanced C/N metabolism. J. Phycol. 40: 74-81.
52. Partensky, F., Hess, W.R., and Vaulot, D. 1999. Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol. Mol. Biol. Rev. 63: 106-127.
53. Ragan, M.A. 1992. Phylogenetic inference based on matrix representation of trees. Mol. Phylogenet. Evol. 1: 53-58.
54. _. 2001. Detection of lateral gene transfer among microbial genomes. Curr. Opin. Genet. Dev. 11: 620-626.
55. Rippka, R., Deruelles, J., Waterbury, J.B., Herdman, M., and Stanier, R.Y. 1979. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J. Gen. Microbiol. 111: 1-61.
56. Rocap, G., Larimer, F.W., Lamerdin, J., Malfatti, S., Chain, P., Ahlgren, N.A., Arellano, A., Coleman, M., Hauser, L., Hess, W.R., et al. 2003. Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424: 1042-1047.
57. Rudi, K., Skulberg, O.M., and Jakobsen, K.S. 1998. Evolution of cyanobacteria by exchange of genetic material among phyletically related strains. J. Bacteriol. 180: 3453-3461.
58. Schmidt, H.A., Strimmer, K., Vingron, M., and von Haeseler, A. 2002. TREE-PUZZLE: Maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18: 502-504.
59. Seo, P.S. and Yokota, A. 2003. The phylogenetic relationships of cyanobacteria inferred from 16S rRNA, gyrB, rpoC1 and rpoD1 gene sequences. J. Gen. Appl. Microbiol. 49: 191-203.
60. Snel, B., Bork, P., and Huynen, M.A. 2002. Genomes in flux: The evolution of archaeal and proteobacterial gene content. Genome Res. 12: 17-25.
61. Sullivan, M.B., Coleman, M.L., Weigele, P., Rohwer, F., and Chisholm, S.W. 2005. Three Prochlorococcus cyanophage genomes: Signature features and ecological interpretations. PLoS Biol. 3: e144.
62. Swofford, D. 1998. PAUP* 4.0 beta version, phylogenetic analysis using parsimony (and other methods). Sinauer Associates, Inc., Sunderland, MA.
63. Tatusov, R.L., Fedorova, N.D., Jackson, J.D., Jacobs, A.R., Kiryutin, B., Koonin, E.V., Krylov, D.M., Mazumder, R., Mekhedov, S.L., Nikolskaya, A.N., et al. 2003. The COG database: An updated version includes eukaryotes. BMC Bioinformatics 4: 41.
64. Thompson, J.D., Higgins, D.G., and Gibson, T.J. 1994. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680.
65. Ting, C.S., Rocap, G., King, J., and Chisholm, S.W. 2002. Cyanobacterial photosynthesis in the oceans: The origins and significance of divergent light-harvesting strategies. Trends Microbiol. 10: 134-142.
66. Turner, S. 1997. Molecular systematics of oxygenic photosynthetic bacteria. Plant Syst. Evol. Suppl. 11: 13-52.
67. Turner, S., Pryer, K.M., Miao, V.P., and Palmer, J.D. 1999. Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J. Eukaryot. Microbiol. 46: 327-338.
68. Wilmotte, A. and Herdman, M. 2001. Phylogenetic relationships among the cyanobacteria based on 16S rRNA sequences. In Bergey's manual of systematic bacteriology (ed. G.M. Garrity), pp. 487-493. Springer, New York.
69. Wolf, Y.I., Aravind, L., Grishin, N.V., and Koonin, E.V. 1999. Evolution of aminoacyl-tRNA synthetases - Analysis of unique domain architectures and phylogenetic trees reveals a complex history of horizontal gene transfer events. Genome Res. 9: 689-710.
70. Yang, Z. 1994. Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: Approximate methods. J. Mol. Evol. 39: 306-314.
71. Yap, W.H., Zhang, Z., and Wang, Y. 1999. Distinct types of rRNA operons exist in the genome of the actinomycete Thermomonospora chromogena and evidence for horizontal transfer of an entire rRNA operon. J. Bacteriol. 181: 5201-5209.
72. Zeidner, G., Bielawski, J.P., Shmoish, M., Scanlan, D.J., Sabehi, G., and Beja, O. 2005. Potential photosynthesis gene recombination between Prochlorococcus and Synechococcus via viral intermediates. Environ. Microbiol. 7: 1505-1513.
73. Zhaxybayeva, O. and Gogarten, J. 2002. Bootstrap, Bayesian probability and maximum likelihood mapping: Exploring new tools for comparative genome analyses. BMC Genomics 3: 4.
74. _. 2003. An improved probability mapping approach to assess genome mosaicism. BMC Genomics 4: 37.
75. Zhaxybayeva, O., Lapierre, P., and Gogarten, J.P. 2004. Genome mosaicism and organismal lineages. Trends Genet. 20: 254-260.