Abstract
With the rapid increase in available bacterial whole-genome information, comparison of bacteria at the whole-genome level has proven to be highly useful in microbial phylogenetic research. Here we constructed a phylogenetic tree based on 15 whole genomes of Mycoplasma and the related bacteria. First, 143 orthologous gene families that are shared by all of the 15 bacteria were selected and 143 multiple alignments were generated. Next, a concatenated multiple alignment inferred from the 143 multiple alignments was generated. A total of 43,370 amino acid sites were considered in the neighbor-joining analysis. The phylogenetic tree based on the whole-genomic information indicated that the 15 bacteria were divided into four major groups with 100% bootstrap support, i.e., the M. hyopneumoniae (Mhy) group, the M. mycoides (Mmy) group, the M. pneumoniae (Mpn) group, and the Bacillus-Phytoplasma (BP) group. In the phylogenetic tree, the Mhy group was more closely related to the Mpn group than the Mmy group. The relationships among the Mhy, Mmy, Mpn, and BP groups were supported with 100% in bootstrap analysis. The phylogenetic tree based on the whole-genome comparison is different from the 16S rRNA tree. Thirty-nine of the 143 phylogenetic trees had the same type of the topology based on the whole-genome comparison. However, we could not identify a gene family contributing or solely belonging to the topology of the 39 proteins. In this study, we showed that some proteins, such as RpoA, RpoB, RpoC, and RpoD, are not suitable for evolutionary studies on relationships among major groups of mycoplasmas. We also showed that glycolysis-related genes of Ureaplasma have a higher substitution rate than the other bacteria. The phylogenetic approaches at the whole-genome level are very important and will be essential for microbial evolutionary studies.
Similar content being viewed by others
References
Brown JR, Douady CJ, Italia MJ, Marshall WE, Stanhope MJ (2001) Universal trees based on large combined protein sequence data sets. Nature Genet 28:281–285
Chambaud I, Heilig R, Ferris S, Barbe V, Samson D, Galisson F, Moszer I, Dybvig K, Wroblewski H, Viari A, Rocha EP, Blanchard A (2001) The complete genome sequence of the murine respiratory pathogen Mycoplasma pulmonis. Nucleic Acids Res 29:2145–2153
Doolittle WF (1999) Phylogenetic classification and the universal tree. Science 284:2124–2128
Falah M, Gupta RS (1997) Phylogenetic analysis of mycoplasmas based on Hsp70 sequences: cloning of the dnaK (hsp70) gene region of Mycoplasma capricolum. Int J Syst Bacteriol 47:38–45
Forterre P, Philippe H (1999) Where is the root or the universal tree of life? Bioessays 21:871–879
Fox GE, Wisotzkey JD, Jurtshuk P (1992) How close is close? 16S rRNA sequence identity may not be sufficient to guarantee species identity. Int J Syst Bacteriol 42:166–170
Fraser CM, Gocayne JD, White O, Adams MD, Clayton RA, Fleischmann RD, Bult CJ, Kerlavage AR, Sutton G, Kelley JM, Fritchman RD, Weidman JF, Small KV, Sandusky M, Fuhrmann J, Nguyen D, Utterback TR, Saudek DM, Phillips CA, Merrick JM, Tomb JF, Dougherty BA, Bott KF, Hu PC, Lucier TS, Peterson SN, Smith HO, Hutchison CA 3rd, Venter JC (1995) The minimal gene complement of Mycoplasma genitalium. Science 270:397–403
Ge F, Wang LS, Kim J (2005) The cobweb of life revealed by genome-scale estimates of horizontal gene transfer. PLoS Biol 3:1709–1718
Glass JI, Lefkowitz EJ, Glass JS, Heiner CR, Chen EY, Cassell GH (2000) The complete sequence of the mucosal pathogen Ureaplasma urealyticum. Nature 407:757–762
Gundersen DE, Lee IM, Rehner SA, Davis RE, Kingsbury DT (1994) Phylogeny of mycoplasmalike organisms (phytoplasmas) — a basis for their classification. J Bacteriol 176:5244–5254
Gundersen DE, Lee IM, Schaff DA, Harrison NA, Chang CJ, Davis RE, Kingsbury DT (1996) Genomic diversity and differentiation among phytoplasma strains in 16S rRNA groups I (aster yellows and related phytoplasmas) and III (X-disease and related phytoplasmas). Int J Syst Bacteriol 46:64–75
Hasegawa M, Kishino H, Yano TA (1989) Estimation of branching dates among primates by molecular clocks of nuclear DNA which slowed down in hominoidea. J Hum Evol 18:461–476
Himmelreich R, Hilbert H, Plagens H, Pirkl E, Li BC, Herrmann R (1997) Complete sequence analysis of the genome of the bacterium Mycoplasma pneumoniae. Nucleic Acids Res 24:4420–4449
Huynen MA, Bork P (1998) Measuring genome evolution. Proc Natl Acad Sci USA 95:5849–5856
Jaffe JD, Stange-Thomann N, Smith C, DeCaprio D, Fisher S, Butler J, Calvo S, Elkins T, FitzGerald MG, Hafez N, Kodira CD, Major J, Wang S, Wilkinson J, Nicol R, Nusbaum C, Birren B, Berg HC, Church GM (2004) The complete genome and proteome of Mycoplasma mobile. Genome Res 14:1447–1461
Jomantiene R, Davis RE, Maas J, Dally EL (1998) Classification of new phytoplasmas associated with diseases of strawberry in Florida, based on analysis of 16S rRNA and ribosomal protein gene operon sequences. Int J Syst Bacteriol 48:269–277
Kamla V, Henrich B, Hadding U (1996) Phylogeny based on elongation factor Tu reflects the phenotypic features of mycoplasmas better than that based on 16S rRNA. Gene 171:83–87
Kim BJ, Lee SH, Lyu MA, Kim SJ, Bai GH, Chae GT, Kim EC, Cha CY, Kook YH (1999) Identification of mycobacterial species by comparative sequence analysis of the RNA polymerase gene (rpoB). J Clin Microbiol 37:1714–1720
Kim KS, Ko KS, Chang MW, Hahn TW, Hong SK, Kook YH (2003) Use of rpoB sequences for phylogenetic study of Mycoplasma species. FEMS Microbiol Lett 226:299–305
Kumar S, Tamura K, Nei M (2004) MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163
Kunst F, Ogasawara N, Moszer I, Albertini AM, Alloni G, Azevedo V, Bertero MG, Bessieres P, Bolotin A, Borchert S, Borriss R, Boursier L, Brans A, Braun M, Brignell SC, Bron S, Brouillet S, Bruschi CV, Caldwell B, Capuano V, Carter NM, Choi SK, Codani JJ, Connerton IF, Cummings NJ, Daniel RA, Denizot F, Devine KM, Dusterhoft A, Ehrlich SD, Emmerson PT, Entian KD, Errington J, Fabret C, Ferrari E, Foulger D, Fritz C, Fujita M, Fujita Y, Fuma S, Galizzi A, Galleron N, Ghim SY, Glaser P, Goffeau A, Golightly EJ, Grandi G, Guiseppi G, Guy BJ, Haga K, Haiech J, Harwood CR, Henaut A, Hilbert H, Holsappel S, Hosono S, Hullo MF, Itaya M, Jones L, Joris B, Karamata D, Kasahara Y, KlaerrBlanchard M, Klein C, Kobayashi Y, Koetter P, Koningstein G, Krogh S, Kumano M, Kurita K, Lapidus A, Lardinois S, Lauber J, Lazarevic V, Lee SM, Levine A, Liu H, Masuda S, Mauel C, Medigue C, Medina N, Mellado RP, Mizuno M, Moestl D, Nakai S, Noback M, Noone D, OReilly M, Ogawa K, Ogiwara A, Oudega B, Park SH, Parro V, Pohl TM, Portetelle D, Porwollik S, Prescott AM, Presecan E, Pujic P, Purnelle B, Rapoport G, Rey M, Reynolds S, Rieger M, Rivolta C, Rocha E, Roche B, Rose M, Sadaie Y, Sato T, Scanlan E, Schleich S, Schroeter R, Scoffone F, Sekiguchi J, Sekowska A, Seror SJ, Serror P, Shin BS, Soldo B, Sorokin A, Tacconi E, Takagi T, Takahashi H, Takemaru K, Takeuchi M, Tamakoshi A, Tanaka T, Terpstra P, Tognoni A, Tosato V, Uchiyama S, Vandenbol M, Vannier F, Vassarotti A, Viari A, Wambutt R, Wedler E, Wedler H, Weitzenegger T, Winters P, Wipat A, Yamamoto H, Yamane K, Yasumoto K, Yata K, Yoshida K, Yoshikawa HF, Zumstein E, Yoshikawa H, Danchin A (1997) The complete genome sequence of the Gram-positive bacterium Bacillus subtilis. Nature 390:249–256
Lee IM, Davis RE, Gundersen-Rindal DE (2000) Phytoplasma: Phytopathogenic mollicutes. Annu Rev Microbiol 54:221–255
Lim PO, Sears BB (1992) Evolutionary relationships of a plant-pathogenic mycoplasmalike organism and Acholeplasma laidlawii deduced from 2 ribosomal protein gene sequences. J Bacteriol 174:2606–2611
Messier W, Stewart CB (1997) Episodic adaptive evolution of primate lysozymes. Nature 385:151–154
Minion FC, Lefkowitz EJ, Madsen ML, Cleary BJ, Swartzell SM, Mahairas GG (2004) The genome sequence of Mycoplasma hyopneumoniae strain 232, the agent of swine mycoplasmosis. J Bacteriol 186:7123–7133
Mollet C, Drancourt M, Raoult D (1997) rpoB sequence analysis as a novel basis for bacterial identification. Mol Microbiol 26:1005–1011
Nakamura Y, Itoh T, Matsuda H, Gojobori T (2004) Biased biological functions of horizontally transferred genes in prokaryotic genomes. Nature Genet 36:760–766
Nei M (1987) Molecular evolutionary genetics, Columbia University Press, New York
Oshima K, Kakizawa S, Nishigawa H, Jung HY, Wei W, Suzuki S, Arashida R, Nakata D, Miyata S, Ugaki M, Namba S (2004) Reductive evolution suggested from the complete genome sequence of a plant-pathogenic phytoplasma. Nature Genet 36:27–29
Papazisi L, Gorton TS, Kutish G, Markham PF, Browning GF, Nguyen DK, Swartzell S, Madan A, Mahairas G, Geary SJ (2003) The complete genome sequence of the avian pathogen Mycoplasma gallisepticum strain R-low. Microbiology 149:2307–2316
Razin S, Yogev D, Naot Y (1998) Molecular biology and pathogenicity of mycoplasmas. Microbiol Mol Biol Rev 62:1094–1156
Sasaki Y, Ishikawa J, Yamashita A, Oshima K, Kenri T, Furuya K, Yoshino C, Horino A, Shiba T, Sasaki T, Hattori M (2002) The complete genomic sequence of Mycoplasma penetrans, an intracellular bacterial pathogen in humans. Nucleic Acids Res 30:5293–5300
Thompson JD, Higgins DG, Gibson TJ (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 21:4673–4680
Vasconcelos AT, Ferreira HB, Bizarro CV, Bonatto SL, Carvalho MO, Pinto PM, Almeida DF, Almeida LG, Almeida R, Alves-Filho L, Assuncao EN, Azevedo VA, Bogo MR, Brigido MM, Brocchi M, Burity HA, Camargo AA, Camargo SS, Carepo MS, Carraro DM, de Mattos Cascardo JC, Castro LA, Cavalcanti G, Chemale G, Collevatti RG, Cunha CW, Dallagiovanna B, Dambros BP, Dellagostin OA, Falcao C, Fantinatti-Garboggini F, Felipe MS, Fiorentin L, Franco GR, Freitas NS, Frias D, Grangeiro TB, Grisard EC, Guimaraes CT, Hungria M, Jardim SN, Krieger MA, Laurino JP, Lima LF, Lopes MI, Loreto EL, Madeira HM, Manfio GP, Maranhao AQ, Martinkovics CT, Medeiros SR, Moreira MA, Neiva M, Ramalho-Neto CE, Nicolas MF, Oliveira SC, Paixao RF, Pedrosa FO, Pena SD, Pereira M, Pereira-Ferrari L, Piffer I, Pinto LS, Potrich DP, Salim AC, Santos FR, Schmitt R, Schneider MP, Schrank A, Schrank IS, Schuck AF, Seuanez HN, Silva DW, Silva R, Silva SC, Soares CM, Souza KR, Souza RC, Staats CC, Steffens MB, Teixeira SM, Urmenyi TP, Vainstein MH, Zuccherato LW, Simpson AJ, Zaha A (2005) Swine and poultry pathogens: the complete genome sequences of two strains of Mycoplasma hyopneumoniae and a strain of Mycoplasma synoviae. J Bacteriol 187:5568–5577
Westberg J, Persson A, Holmberg A, Goesmann A, Lundeberg J, Johansson KE, Pettersson B, Uhlen M (2004) The genome sequence of Mycoplasma mycoides subsp mycoides SC type strain PG1(T), the causative agent of contagious bovine pleuropneumonia (CBPP). Genome Res 14:221–227
Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms — proposal for the domains archaea, bacteria, and eucarya. Proc Natl Acad Sci USA 87:4576–4579
Wolf M, Muller T, Dandekar T, Pollack JD (2004) Phylogeny of Firmicutes with special reference to Mycoplasma (Mollicutes) as inferred from phosphoglycerate kinase amino acid sequence data. Int J Syst Evol Microbiol 54:871–875
Zhao Y, Davis RE, Lee IM (2005) Phylogenetic positions of ‘Candidatus Phytoplasma asteris’ and Spiroplasma kunkelii as inferred from multiple sets of concatenated core housekeeping proteins. Int J Syst Evol Microbiol 55:2131–2141
Acknowledgments
The authors thank Haruo Yamamoto for helpful advice in constructing phylogenetic trees and two anonymous reviewers for their valuable comments. The Agricultural Bioinformatics Research Unit is funded by the Japan Science and Technology Agency (JST).
Author information
Authors and Affiliations
Corresponding author
Additional information
Reviewing Editor: Dr. John Oakeshott
Electronic supplementary material
Electronic supplementary material
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Oshima, K., Nishida, H. Phylogenetic Relationships Among Mycoplasmas Based on the Whole Genomic Information. J Mol Evol 65, 249–258 (2007). https://doi.org/10.1007/s00239-007-9010-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00239-007-9010-3