Phylogeny and molecular signatures for the phylum Thermotogae and its subgroups

Review Paper

Abstract

Thermotogae species are currently identified mainly on the basis of their unique toga and distinct branching in the rRNA and other phylogenetic trees. No biochemical or molecular markers are known that clearly distinguish the species from this phylum from all other bacteria. The taxonomic/evolutionary relationships within this phylum, which consists of a single family, are also unclear. We report detailed phylogenetic analyses on Thermotogae species based on concatenated sequences for many ribosomal as well as other conserved proteins that identify a number of distinct clades within this phylum. Additionally, comprehensive analyses of protein sequences from Thermotogae genomes have identified >60 Conserved Signature Indels (CSI) that are specific for the Thermotogae phylum or its different subgroups. Eighteen CSIs in important proteins such as PolI, RecA, TrpRS and ribosomal proteins L4, L7/L12, S8, S9, etc. are uniquely present in various Thermotogae species and provide molecular markers for the phylum. Many CSIs were specific for a number of Thermotogae subgroups. Twelve of these CSIs were specific for a clade consisting of various Thermotoga species except Tt. lettingae, which was separated from other Thermotoga species by a long branch in phylogenetic trees; Fourteen CSIs were specific for a clade consisting of the Fervidobacterium and Thermosipho genera and eight additional CSIs were specific for the genus Thermosipho. In addition, the existence of a clade consisting of the deep branching species Petrotoga mobilis,Kosmotoga olearia and Thermotogales bacterium mesG1 was supported by seven CSIs. The deep branching of this clade was also supported by a number of CSIs that were present in various Thermotogae species, but absent in this clade and all other bacteria. Most of these clades were strongly supported by phylogenetic analyses based on two datasets of protein sequences and they identify potential higher taxonomic grouping (viz. families) within this phylum. We also report 16 CSIs that are shared by either some or all Thermotogae species and some species from other taxa such as Archaea, Aquificae, Firmicutes, Proteobacteria, Deinococcus, Fusobacteria, Dictyoglomus, Chloroflexi and eukaryotes. The shared presence of some of these CSIs could be due to lateral gene transfers between these groups. However, no clear preference for any particular group was observed in this regard. The molecular probes based on different genes/proteins, which contain these Thermotogae-specific CSIs, provide novel and highly specific means for identification of both known as well as previously unknown Thermotogae species in different environments. Additionally, these CSIs also provide valuable tools for genetic and biochemical studies that could lead to discovery of novel properties that are unique to these bacteria.

Keywords

Conserved indels Thermotogae taxonomy FervidobacteriumThermosipho clade KosmotogaPetrotoga clade Branching order Thermotoga lettingae Protein structures Lateral gene transfers 

Supplementary material

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Supplementary material 1 (PDF 1668 kb)

References

  1. Akiva E, Itzhaki Z, Margalit H (2008) Built-in loops allow versatility in domain–domain interactions: lessons from self-interacting domains. Proc Natl Acad Sci USA 105:13292–13297PubMedCrossRefGoogle Scholar
  2. Alain K, Marteinsson VT, Miroshnichenko ML, Bonch-Osmolovskaya EA, Prieur D, Birrien JL (2002) Marinitoga piezophila sp. nov., a rod-shaped, thermo-piezophilic bacterium isolated under high hydrostatic pressure from a deep-sea hydrothermal vent. Int J Syst Evol Microbiol 52:1331–1339PubMedCrossRefGoogle Scholar
  3. Antoine E, Cilia V, Meunier JR, Guezennec J, Lesongeur F, Barbier G (1997) Thermosipho melanesiensis sp. nov., a new thermophilic anaerobic bacterium belonging to the order Thermotogales, isolated from deep-sea hydrothermal vents in the southwestern Pacific Ocean. Int J Syst Bacteriol 47:1118–1123PubMedCrossRefGoogle Scholar
  4. Baldauf SL, Palmer JD (1993) Animals and fungi are each other’s closest relatives: congruent evidence from multiple proteins. Proc Natl Acad Sci USA 90:11558–11562PubMedCrossRefGoogle Scholar
  5. Balk M, Weijma J, Stams AJ (2002) Thermotoga lettingae sp. nov., a novel thermophilic, methanol-degrading bacterium isolated from a thermophilic anaerobic reactor. Int J Syst Evol Microbiol 52:1361–1368PubMedCrossRefGoogle Scholar
  6. Bocchetta M, Gribaldo S, Sanangelantoni A, Cammarano P (2000) Phylogenetic depth of the bacterial genera Aquifex and Thermotoga inferred from analysis of ribosomal protein, elongation factor, and RNA polymerase subunit sequences. J Mol Evol 50:366–380PubMedGoogle Scholar
  7. Boucher Y, Douady CJ, Papke RT et al (2003) Lateral gene transfer and the origins of prokaryotic groups. Annu Rev Genet 37:283–328PubMedCrossRefGoogle Scholar
  8. Boussau B, Gueguen L, Gouy M (2008) Accounting for horizontal gene transfers explains conflicting hypotheses regarding the position of aquificales in the phylogeny of Bacteria. BMC Evol Biol 8:272PubMedCrossRefGoogle Scholar
  9. Brocchieri L, Karlin S (2000) Conservation among HSP60 sequences in relation to structure, function, and evolution. Protein Sci 9:476–486PubMedCrossRefGoogle Scholar
  10. Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552PubMedGoogle Scholar
  11. Chlenov M, Masuda S, Murakami KS, Nikiforov V, Darst SA, Mustaev A (2005) Structure and function of lineage-specific sequence insertions in the bacterial RNA polymerase beta′ subunit. J Mol Biol 353:138–154PubMedCrossRefGoogle Scholar
  12. Ciccarelli FD, Doerks T, von Mering C, Creevey CJ, Snel B, Bork P (2006) Toward automatic reconstruction of a highly resolved tree of life. Science 311:1283–1287PubMedCrossRefGoogle Scholar
  13. Cole JR, Wang Q, Cardenas E et al (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141–D145PubMedCrossRefGoogle Scholar
  14. Conners SB, Mongodin EF, Johnson MR, Montero CI, Nelson KE, Kelly RM (2006) Microbial biochemistry, physiology, and biotechnology of hyperthermophilic Thermotoga species. FEMS Microbiol Rev 30:872–905PubMedCrossRefGoogle Scholar
  15. Delano WL (2002) The Pymol user’s manual. Delano Scientific, Palo AltoGoogle Scholar
  16. Di Giulio M (2003) The universal ancestor was a thermophile or a hyperthermophile: tests and further evidence. J Theor Biol 221:425–436PubMedCrossRefGoogle Scholar
  17. Dipippo JL, Nesbo CL, Dahle H, Doolittle WF, Birkland NK, Noll KM (2009) Kosmotoga olearia gen. nov., sp. nov., a thermophilic, anaerobic heterotroph isolated from an oil production fluid. Int J Syst Evol Microbiol 59:2991–3000PubMedCrossRefGoogle Scholar
  18. Dunkle JA, Xiong L, Mankin AS, Cate JH (2010) Structures of the Escherichia coli ribosome with antibiotics bound near the peptidyl transferase center explain spectra of drug action. Proc Natl Acad Sci USA 107:17152–17157PubMedCrossRefGoogle Scholar
  19. Eisen JA (1995) The RecA protein as a model molecule for molecular systematic studies of bacteria: comparison of trees of RecAs and 16S rRNAs from the same species. J Mol Evol 41:1105–1123PubMedCrossRefGoogle Scholar
  20. Eriksen NT, Riis ML, Holm NK, Iversen N (2010) H(2) synthesis from pentoses and biomass in Thermotoga spp. Biotechnol Lett 33:293–300PubMedCrossRefGoogle Scholar
  21. Fardeau ML, Ollivier B, Patel BK et al (1997) Thermotoga hypogea sp. nov., a xylanolytic, thermophilic bacterium from an oil-producing well. Int J Syst Bacteriol 47:1013–1019PubMedCrossRefGoogle Scholar
  22. Feng Y, Cheng L, Zhang X, Li X, Deng Y, Zhang H (2010) Thermococcoides shengliensis gen. nov., sp. nov., a new member of the order Thermotogales isolated from oil-production fluid. Int J Syst Evol Microbiol 60:932–937PubMedCrossRefGoogle Scholar
  23. Frock AD, Notey JS, Kelly RM (2010) The genus Thermotoga: recent developments. Environ Technol 31:1169–1181PubMedCrossRefGoogle Scholar
  24. Gaget V, Gribaldo S, Tandeau dM (2011) An rpoB signature sequence provides unique resolution for the molecular typing of Cyanobacteria. Int J Syst Evol Microbiol 61:170–183PubMedCrossRefGoogle Scholar
  25. Galley KA, Singh B, Gupta RS (1992) Cloning of HSP70 (dnaK) gene from Clostridium perfringens using a general polymerase chain reaction based approach. Biochem Biophys Acta 1130:203–208PubMedGoogle Scholar
  26. Gao B, Gupta RS (2005) Conserved indels in protein sequences that are characteristic of the phylum Actinobacteria. Int J Syst Evol Microbiol 55:2401–2412PubMedCrossRefGoogle Scholar
  27. Gao B, Mohan R, Gupta RS (2009) Phylogenomics and protein signatures elucidating the evolutionary relationships among the Gammaproteobacteria. Int J Syst Evol Microbiol 59:234–247PubMedCrossRefGoogle Scholar
  28. Griffiths E, Gupta RS (2002) Protein signatures distinctive of chlamydial species: horizontal transfer of cell wall biosynthesis genes glmU from Archaebacteria to Chlamydiae, and murA between Chlamydiae and Streptomyces. Microbiology 148:2541–2549PubMedGoogle Scholar
  29. Griffiths E, Gupta RS (2004) Signature sequences in diverse proteins provide evidence for the late divergence of the order Aquificales. Int Microbiol 7:41–52PubMedGoogle Scholar
  30. Griffiths E, Gupta RS (2006a) Lateral transfers of serine hydroxymethyl transferase (glyA) and UDP-N-acetylglucosamine enolpyruvyl transferase (murA) genes from free-living Actinobacteria to the parasitic chlamydiae. J Mol Evol 63:283–296PubMedCrossRefGoogle Scholar
  31. Griffiths E, Gupta RS (2006b) Molecular signatures in protein sequences that are characteristics of the phylum Aquificales. Int J Syst Evol Microbiol 56:99–107PubMedCrossRefGoogle Scholar
  32. Griffiths E, Gupta RS (2007) Phylogeny and shared conserved inserts in proteins provide evidence that Verrucomicrobia are the closest known free-living relatives of chlamydiae. Microbiology 153:2648–2654PubMedCrossRefGoogle Scholar
  33. Gudkov AT (1997) The L7/L12 ribosomal domain of the ribosome: structural and functional studies. FEBS Lett 407:253–256PubMedCrossRefGoogle Scholar
  34. Gupta RS (1995) Evolution of the chaperonin families (Hsp60, Hsp10 and Tcp-1) of proteins and the origin of eukaryotic cells. Mol Microbiol 15:1–11PubMedCrossRefGoogle Scholar
  35. Gupta RS (1997) Protein phylogenies and signature sequences: evolutionary relationships within prokaryotes and between prokaryotes and eukaryotes. Antonie van Leeuwenhoek 72:49–61PubMedCrossRefGoogle Scholar
  36. Gupta RS (1998) Protein phylogenies and signature sequences: a reappraisal of evolutionary relationships among Archaebacteria, Eubacteria, and Eukaryotes. Microbiol Mol Biol Rev 62:1435–1491PubMedGoogle Scholar
  37. Gupta RS (2000) The phylogeny of Proteobacteria: relationships to other eubacterial phyla and eukaryotes. FEMS Microbiol Rev 24:367–402PubMedCrossRefGoogle Scholar
  38. Gupta RS (2001) The branching order and phylogenetic placement of species from completed bacterial genomes, based on conserved indels found in various proteins. Int Microbiol 4:187–202PubMedCrossRefGoogle Scholar
  39. Gupta RS (2003) Evolutionary relationships among photosynthetic bacteria. Photosynth Res 76:173–183PubMedCrossRefGoogle Scholar
  40. Gupta RS (2004) The phylogeny and signature sequences characteristics of Fibrobacters, Chlorobi and Bacteroidetes. Crit Rev Microbiol 30:123–143PubMedCrossRefGoogle Scholar
  41. Gupta RS (2009) Protein signatures (molecular synapomorphies) that are distinctive characteristics of the major cyanobacterial clades. Int J Syst Evol Microbiol 59:2510–2526PubMedCrossRefGoogle Scholar
  42. Gupta RS (2010) Molecular signatures for the main phyla of photosynthetic bacteria and their subgroups. Photosynth Res 104:357–372PubMedCrossRefGoogle Scholar
  43. Gupta RS, Golding GB (1993) Evolution of HSP70 gene and its implications regarding relationships between archaebacteria, eubacteria, and eukaryotes. J Mol Evol 37:573–582PubMedCrossRefGoogle Scholar
  44. Gupta RS, Griffiths E (2002) Critical issues in bacterial phylogenies. Theor Popul Biol 61:423–434PubMedCrossRefGoogle Scholar
  45. Gupta RS, Griffiths E (2006) Chlamydiae-specific proteins and indels: novel tools for studies. Trends Microbiol 14:527–535PubMedCrossRefGoogle Scholar
  46. Gupta RS, Mathews DW (2010) Signature proteins for the major clades of Cyanobacteria. BMC Evol Biol 10:24PubMedCrossRefGoogle Scholar
  47. Gupta RS, Shami A (2011) Molecular signatures for the Crenarchaeota and the Thaumarchaeota. Antonie van Leeuwenhoek 99:133–157PubMedCrossRefGoogle Scholar
  48. Gupta RS, Mukhtar T, Singh B (1999) Evolutionary relationships among photosynthetic prokaryotes (Heliobacterium chlorum, Chloroflexus aurantiacus, cyanobacteria, Chlorobium tepidum and proteobacteria): implications regarding the origin of photosynthesis. Mol Microbiol 32:893–906PubMedCrossRefGoogle Scholar
  49. Harris JK, Kelley ST, Spiegelman GB, Pace NR (2003) The genetic core of the universal ancestor. Genome Res 13:407–412PubMedCrossRefGoogle Scholar
  50. Hormozdiari F, Salari R, Hsing M et al (2009) The effect of insertions and deletions on wirings in protein–protein interaction networks: a large-scale study. J Comput Biol 16:159–167PubMedCrossRefGoogle Scholar
  51. Huber R, Hannig M (2006) Thermotogales. Prokaryotes 7:899–922CrossRefGoogle Scholar
  52. Huber R, Langworthy TA, Konig H et al (1986) Thermotoga maritima sp. nov. represents a new genus of unique extremely thermophilic eubacteria growing up to 90°C. Arch Microbiol 144:324–333CrossRefGoogle Scholar
  53. Itzhaki Z, Akiva E, Altuvia Y, Margalit H (2006) Evolutionary conservation of domain–domain interactions. Genome Biol 7:R125PubMedCrossRefGoogle Scholar
  54. Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ (1998) Multiple sequence alignment with Clustal X. Trends Biochem Sci 23:403–405PubMedCrossRefGoogle Scholar
  55. Karlin S, Brocchieri L (1998) Heat shock protein 70 family: multiple sequence comparisons, function, and evolution. J Mol Evol 47:565–577PubMedCrossRefGoogle Scholar
  56. Karlin S, Weinstock GM, Brendel V (1995) Bacterial classifications derived from recA protein sequence comparisons. J Bacteriol 177:6881–6893PubMedGoogle Scholar
  57. Kim JY, Kavas M, Fouad WM, Nong G, Preston JF, Altpeter F (2010) Production of hyperthermostable GH10 xylanase Xyl10B from Thermotoga maritima in transplastomic plants enables complete hydrolysis of methylglucuronoxylan to fermentable sugars for biofuel production. Plant Mol BiolGoogle Scholar
  58. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120PubMedCrossRefGoogle Scholar
  59. Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, CambridgeGoogle Scholar
  60. Klenk HP, Meier TD, Durovic P et al (1999) RNA polymerase of Aquifex pyrophilus: Implications for the evolution of the bacterial rpoBC operon and extremely thermophilic bacteria. J Mol Evol 48:528–541PubMedCrossRefGoogle Scholar
  61. Koski LB, Golding GB (2001) The closest BLAST hit is often not the nearest neighbor. J Mol Evol 52:540–542PubMedGoogle Scholar
  62. Kunisawa T (2005) Dichotomy of major bacterial phyla inferred from gene arrangement comparisons. J Theor Biol 234:1–5PubMedCrossRefGoogle Scholar
  63. Lee D, Seo H, Park, C, Park K (2009) WeGAS: a web-based microbial genome annotation system. Biosci Biotechnol Biochem 73:213–216Google Scholar
  64. Leijonmarck M, Liljas A (1987) Structure of the C-terminal domain of the ribosomal protein L7/L12 from Escherichia coli at 1.7 A. J Mol Biol 195:555–579Google Scholar
  65. Ludwig W, Klenk H-P (2005) Overview: a phylogenetic backbone and taxonomic framework for prokaryotic systematics. In: Brenner DJ, Krieg NR, Staley JT, Garrity GM (eds) Bergey’s manual of systematic bacteriology. Springer, Berlin, pp 49–65CrossRefGoogle Scholar
  66. Mongodin EF, Hance IR, DeBoy RT et al (2005) Gene transfer and genome plasticity in Thermotoga maritima, a model hyperthermophilic species. J Bacteriol 187:4935–4944PubMedCrossRefGoogle Scholar
  67. NCBI Completed microbial genomes (2011) http://www.ncbi.nlm.nih.gov/PMGifs/Genomes/micr.html
  68. Nelson KE, Clayton R, Gill S et al (1999) Evidence for lateral gene transfer between Archaea and Bacteria from genome sequence of Thermotoga maritima. Nature 399:323–329PubMedCrossRefGoogle Scholar
  69. Nesbo CL, L’Haridon S, Stetter KO, Doolittle WF (2001) Phylogenetic analyses of two “Archaeal” genes in Thermotoga maritima reveal multiple transfers between Archaea and Bacteria. Mol Biol Evol 18:362–375PubMedGoogle Scholar
  70. Nesbo CL, Dlutek M, Doolittle WF (2006) Recombination in Thermotoga: implications for species concepts and biogeography. Genetics 172:759–769PubMedCrossRefGoogle Scholar
  71. Nesbo CL, Bapteste E, Curtis B et al (2009) The genome of Thermosipho africanus TCF52B: lateral genetic connections to the Firmicutes and Archaea. J Bacteriol 191:1974–1978PubMedCrossRefGoogle Scholar
  72. Nesbo CL, Kumaraswamy R, Dlutek M, Doolittle WF, Foght J (2010) Searching for mesophilic Thermotogales bacteria: “mesotogas” in the wild. Appl Environ Microbiol 76:4896–4900PubMedCrossRefGoogle Scholar
  73. Olsen GJ, Woese CR (1993) Ribosomal RNA: a key to phylogeny. FASEB J 7:113–123PubMedGoogle Scholar
  74. Olsen GJ, Woese CR, Overbeek R (1994) The winds of (evolutionary) change: breathing new life into microbiology. J Bacteriol 176:1–6PubMedGoogle Scholar
  75. Osborne AR, Clemons WM Jr, Rapoport TA (2004) A large conformational change of the translocation ATPase SecA. Proc Natl Acad Sci USA 101:10937–10942PubMedCrossRefGoogle Scholar
  76. Patel BKC, Morgan HW, Daniel RM (1985) Fervidobacterium nodosum gen. nov. and spec. nov., a novel chemoorganotrophic, caldoactive, anaerobic bacterium. Arch Microbiol 141:63–69CrossRefGoogle Scholar
  77. Podell S, Gaasterland T (2007) DarkHorse: a method for genome-wide prediction of horizontal gene transfer. Genome Biol 8:R16PubMedCrossRefGoogle Scholar
  78. Reysenbach A-L (2001) Phylum BII. Thermotogae phy. nov. In: Boone DR, Castenholz RW (eds) Bergey’s manual of systematic bacteriology. Springer, Berlin, pp 369–387Google Scholar
  79. Rivera MC, Lake JA (1992) Evidence that eukaryotes and eocyte prokaryotes are immediate relatives. Science 257:74–76PubMedCrossRefGoogle Scholar
  80. Rodnina MV, Pape T, Fricke R, Wintermeyer W (1995) Elongation factor Tu, a GTPase triggered by codon recognition on the ribosome: mechanism and GTP consumption. Biochem Cell Biol 73:1221–1227PubMedCrossRefGoogle Scholar
  81. Rokas A, Holland PW (2000) Rare genomic changes as a tool for phylogenetics. Trends Ecol Evol 15:454–459PubMedCrossRefGoogle Scholar
  82. Rokas A, Williams BL, King N, Carroll SB (2003) Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature 425:798–804PubMedCrossRefGoogle Scholar
  83. Schmidt HA, Strimmer K, Vingron M, von Haeseler A (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18:502–504PubMedCrossRefGoogle Scholar
  84. Schoeffler AJ, May AP, Berger JM (2010) A domain insertion in Escherichia coli GyrB adopts a novel fold that plays a critical role in gyrase function. Nucleic Acids Res 38:7830–7844PubMedCrossRefGoogle Scholar
  85. Seo PS, Yokota A (2003) The phylogenetic relationships of cyanobacteria inferred from 16S rRNA, gyrB, rpoC1 and rpoD1 gene sequences. J Gen Appl Microbiol 49:191–203PubMedCrossRefGoogle Scholar
  86. Singh B, Gupta RS (2009) Conserved inserts in the Hsp60 (GroEL) and Hsp70 (DnaK) proteins are essential for cellular growth. Mol Genet Genomics 281:361–373PubMedCrossRefGoogle Scholar
  87. Urios L, Cueff-Gauchard V, Pignet P et al (2004) Thermosipho atlanticus sp. nov., a novel member of the Thermotogales isolated from a Mid-Atlantic Ridge hydrothermal vent. Int J Syst Evol Microbiol 54:1953–1957PubMedCrossRefGoogle Scholar
  88. Van de Peer Y, De Wachter R (1997) Construction of evolutionary distance trees with TREECON for Windows: accounting for variation in nucleotide substitution rate among sites. Comput Appl Biosci 13:227–230PubMedGoogle Scholar
  89. Wahl MC, Bourenkov GP, Bartunik HD, Huber R (2000) Flexibility, conformational diversity and two dimerization modes in complexes of ribosomal protein L12. EMBO J 19:174–186PubMedCrossRefGoogle Scholar
  90. Watanabe K, Nelson J, Harayama S, Kasai H (2001) ICB database: the gyrB database for identification and classification of bacteria. Nucleic Acids Res 29:344–345PubMedCrossRefGoogle Scholar
  91. Woese CR (1987) Bacterial evolution. Microbiol Rev 51:221–271PubMedGoogle Scholar
  92. Wong JT, Chen J, Mat WK, Ng SK, Xue H (2007) Polyphasic evidence delineating the root of life and roots of biological domains. Gene 403:39–52PubMedCrossRefGoogle Scholar
  93. Worbs M, Huber R, Wahl MC (2000) Crystal structure of ribosomal protein L4 shows RNA-binding sites for ribosome incorporation and feedback control of the S10 operon. EMBO J 19:807–818PubMedCrossRefGoogle Scholar
  94. Worning P, Jensen LJ, Nelson KE, Brunak S, Ussery DW (2000) Structural analysis of DNA sequence: evidence for lateral gene transfer in Thermotoga maritima. Nucleic Acids Res 28:706–709PubMedCrossRefGoogle Scholar
  95. Wu H, Jiang L, Zimmermann RA (1994) The binding site for ribosomal protein S8 in 16S rRNA and spc mRNA from Escherichia coli: minimum structural requirements and the effects of single bulged bases on S8–RNA interaction. Nucleic Acids Res 22:1687–1695PubMedCrossRefGoogle Scholar
  96. Wu D, Hugenholtz P, Mavromatis K et al (2009) A phylogeny-driven genomic encyclopaedia of bacteria and archaea. Nature 462:1056–1060PubMedCrossRefGoogle Scholar
  97. Zhaxybayeva O, Gogarten JP, Charlebois RL, Doolittle WF, Papke RT (2006) Phylogenetic analyses of cyanobacterial genomes: quantification of horizontal gene transfer events. Genome Res 16:1099–1108PubMedCrossRefGoogle Scholar
  98. Zhaxybayeva O, Swithers KS, Lapierre P et al (2009) On the chimeric nature, thermophilic origin, and phylogenetic placement of the Thermotogales. Proc Natl Acad Sci USA 106:5865–5870PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Department of Biochemistry and Biomedical SciencesMcMaster UniversityHamiltonCanada

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