Antonie van Leeuwenhoek

, Volume 101, Issue 1, pp 45–54 | Cite as

Microbial systematics in the post-genomics era



Microbial systematics and phylogeny should form the foundation and guiding light for a comprehensive understanding of different aspects of microbiology. However, there are many critical issues in microbial systematics that are currently not resolved. Some of these include: how to define and delimit a prokaryotic species; development of rationale criteria for the assignment of higher taxonomic ranks; understanding what unique properties distinguish species from different groups; and understanding the branching order and interrelationship among higher prokaryotic clades. The sequencing of genomes from large numbers of cultured as well as uncultured microbes covering prokaryotic diversity provides unique means to achieve these important objectives. Prokaryotic genomes are found to be very diverse and dynamic and horizontal gene transfers (HGTs) are indicated to have played important role in species/genome evolution. Although HGT adds a layer of complexity in terms of understanding the genomes and species evolution, it is contended that vast majority of genes and genetic characteristics that are distinctive characteristics of higher prokaryotic taxa are vertically inherited and based on them a solid foundation for microbial systematics can be developed. We describe two kinds of molecular markers consisting of conserved indels in protein sequences and whole proteins that are specific for different groups that are proving particularly valuable in defining different prokaryotic groups in clear molecular terms and in understanding their interrelationships. The genetic and biochemical studies on these taxa-specific molecular markers also open the way to discover novel biochemical and physiological characteristics that are unique properties of these groups.


Microbial phylogeny Bacterial systematics Molecular markers Conserved indels Conserved signature proteins Higher taxonomic clades Horizontal gene transfer 


  1. Abby S, Daubin V (2007) Comparative genomics and the evolution of prokaryotes. Trends Microbiol 15:135–141PubMedCrossRefGoogle Scholar
  2. Ahmod NZ, Gupta RS, Shah HN (2011) Identification of a Bacillus anthracis specific indel in the yeaC gene and development of a rapid pyrosequencing assay for distinguishing B. anthracis from the B. cereus group. J Microbiol Methods (in press)Google Scholar
  3. Alcaraz LD, Moreno-Hagelsieb G, Eguiarte LE, Souza V, Herrera-Estrella L, Olmedo G (2010) Understanding the evolutionary relationships and major traits of Bacillus through comparative genomics. BMC Genomics 11:332PubMedCrossRefGoogle Scholar
  4. Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial-cells without cultivation. Microbiol Rev 59:143–169PubMedGoogle Scholar
  5. Aris-Brosou S (2005) Determinants of adaptive evolution at the molecular level: the extended complexity hypothesis. Mol Biol Evol 22:200–209PubMedCrossRefGoogle Scholar
  6. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, Fernandes GR, Tap J, Bruls T, Batto JM, Bertalan M, Borruel N, Casellas F, Fernandez L, Gautier L, Hansen T, Hattori M, Hayashi T, Kleerebezem M, Kurokawa K, Leclerc M, Levenez F, Manichanh C, Nielsen HB, Nielsen T, Pons N, Poulain J, Qin JJ, Sicheritz-Ponten T, Tims S, Torrents D, Ugarte E, Zoetendal EG, Wang J, Guarner F, Pedersen O, de Vos WM, Brunak S, Dore J, Weissenbach J, Ehrlich SD, Bork P (2011) Enterotypes of the human gut microbiome. Nature 473:174–180PubMedCrossRefGoogle Scholar
  7. Beiko RG, Harlow TJ, Ragan MA (2005) Highways of gene sharing in prokaryotes. Proc Natl Acad Sci USA 102:14332–14337PubMedCrossRefGoogle Scholar
  8. Belda E, Moya A, Silva FJ (2005) Genome rearrangement distances and gene order phylogeny in gamma-proteobacteria. Mol Biol Evol 22:1456–1467PubMedCrossRefGoogle Scholar
  9. Brenner DJ, Staley JT, Krieg NR (2005) Classification of prokaryotic organisms and the concept of bacterial speciation. In: Brenner DJ, Krieg NR, Staley JT, Garrity GM (eds) Bergey’s manual of systematic bacteriology, 2nd edn. Springer, Berlin, pp 27–32CrossRefGoogle Scholar
  10. 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
  11. Coleman ML, Chisholm SW (2010) Ecosystem-specific selection pressures revealed through comparative population genomics. Proc Natl Acad Sci USA 107:18634–18639PubMedCrossRefGoogle Scholar
  12. Daubin V, Ochman H (2004) Bacterial genomes as new gene homes: the genealogy of ORFans in E.coli. Genome Res 14:1036–1042PubMedCrossRefGoogle Scholar
  13. Delong EF, Pace NR (2001) Environmental diversity of bacteria and archaea. Syst Biol 50:470–478PubMedCrossRefGoogle Scholar
  14. Delong EF, Preston CM, Mincer T, Rich V, Hallam SJ, Frigaard NU, Martinez A, Sullivan MB, Edwards R, Brito BR, Chisholm SW, Karl DM (2006) Community genomics among stratified microbial assemblages in the ocean’s interior. Science 311:496–503PubMedCrossRefGoogle Scholar
  15. Delsuc F, Brinkmann H, Philippe H (2005) Phylogenomics and the reconstruction of the tree of life. Nat Rev Genet 6:361–375PubMedCrossRefGoogle Scholar
  16. Ding GH, Yu ZH, Zhao J, Wang Z, Li Y, Xing XB, Wang CA, Liu L, Li YX (2008) Tree of life based on genome context networks. PLoS One 3(10):e3357PubMedCrossRefGoogle Scholar
  17. Dinsdale EA, Edwards RA, Hall D, Angly F, Breitbart M, Brulc JM, Furlan M, Desnues C, Haynes M, Li LL, McDaniel L, Moran MA, Nelson KE, Nilsson C, Olson R, Paul J, Brito BR, Ruan YJ, Swan BK, Stevens R, Valentine DL, Thurber RV, Wegley L, White BA, Rohwer F (2008) Functional metagenomic profiling of nine biomes. Nature 452:629–639PubMedCrossRefGoogle Scholar
  18. Donati C, Hiller NL, Tettelin H, Muzzi A, Croucher NJ, Angiuoli SV, Oggioni M, Hotopp JCD, Hu FZ, Riley DR, Covacci A, Mitchell TJ, Bentley SD, Kilian M, Ehrlich GD, Rappuoli R, Moxon ER, Masignani V (2010) Structure and dynamics of the pan-genome of Streptococcus pneumoniae and closely related species. Genome Biol 11(10):R107PubMedCrossRefGoogle Scholar
  19. Doolittle WF (1999) Phylogenetic classification and the universal tree. Science 284:2124–2128PubMedCrossRefGoogle Scholar
  20. Dutilh BE, Snel B, Ettema TJG, Huynen MA (2008) Signature genes as a phylogenomic tool. Mol Biol Evol 25:1659–1667PubMedCrossRefGoogle Scholar
  21. Fleischmann RD, Adams MD, White O, Clayton RA, Kirkness EF, Kerlavage AR, Bult CJ, Tomb JF, Dougherty BA, Merrick JM, Mckenney K, Sutton G, Fitzhugh W, Fields C, Gocayne JD, Scott J, Shirley R, Liu LI, Glodek A, Kelley JM, Weidman JF, Phillips CA, Spriggs T, Hedblom E, Cotton MD, Utterback TR, Hanna MC, Nguyen DT, Saudek DM, Brandon RC, Fine LD, Fritchman JL, Fuhrmann JL, Geoghagen NSM, Gnehm CL, Mcdonald LA, Small KV, Fraser CM, Smith HO, Venter JC (1995) Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269:496–512PubMedCrossRefGoogle Scholar
  22. Fraser C, Alm EJ, Polz MF, Spratt BG, Hanage WP (2009) The bacterial species challenge: making sense of genetic and ecological diversity. Science 323:741–746PubMedCrossRefGoogle Scholar
  23. Fraser-Liggett CM (2005) Insights on biology and evolution from microbial genome sequencing. Genome Res 15:1603–1610PubMedCrossRefGoogle Scholar
  24. 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
  25. Gao B, Gupta RS (2007) Phylogenomic analysis of proteins that are distinctive of archaea and its main subgroups and the origin of methanogenesis. BMC Genomics 8:86PubMedCrossRefGoogle Scholar
  26. Gao B, Paramanathan R, Gupta RS (2006) Signature proteins that are distinctive characteristics of actinobacteria and their subgroups. Antonie Van Leeuwenhoek 90:69–91PubMedCrossRefGoogle Scholar
  27. Gao B, Mohan R, Gupta RS (2009) Phylogenomics and protein signatures elucidating the evolutionary relationships among the gamma-proteobacteria. Int J Syst Evol Microbiol 59:234–247PubMedCrossRefGoogle Scholar
  28. Garrity GM, Bell JA, Lilburn T (2005) The revised road map to the manual. In: Brenner DJ, Krieg NR, Staley JT, Garrity GM (eds) Bergey’s manual of systematic bacteriology, 2nd edn. Springer, Berlin, pp 159–187CrossRefGoogle Scholar
  29. Gershon D (1997) Bioinformatics in a post-genomics age. Nature 389:417–418PubMedCrossRefGoogle Scholar
  30. Gevers D, Cohan FM, Lawrence JG, Spratt BG, Coenye T, Feil EJ, Stackebrandt E, Van de Peer Y, Vandamme P, Thompson FL, Swings J (2005) Re-evaluating prokaryotic species. Nat Rev Microbiol 3:733–739PubMedCrossRefGoogle Scholar
  31. Gianoulis TA, Raes J, Patel PV, Bjornson R, Korbel JO, Letunic I, Yamada T, Paccanaro A, Jensen LJ, Snyder M, Bork P, Gerstein MB (2009) Quantifying environmental adaptation of metabolic pathways in metagenomics. Proc Natl Acad Sci USA 106:1374–1379PubMedCrossRefGoogle Scholar
  32. Gogarten JP, Townsend JP (2005) Horizontal gene transfer, genome innovation and evolution. Nat Rev Microbiol 3:679–687PubMedCrossRefGoogle Scholar
  33. Gogarten JP, Doolittle WF, Lawrence JG (2002) Prokaryotic evolution in light of gene transfer. Mol Biol Evol 19:2226–2238PubMedGoogle Scholar
  34. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM (2007) DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57:81–91PubMedCrossRefGoogle Scholar
  35. Griffiths E, Gupta RS (2001) The use of signature sequences in different proteins to determine the relative branching order of bacterial divisions: evidence that fibrobacter diverged at a similar time to Chlamydia and the Cytophaga-Flavobacterium-Bacteroides division. Microbiology-Sgm 147:2611–2622Google Scholar
  36. Griffiths E, Gupta RS (2004a) Distinctive protein signatures provide molecular markers and evidence for the monophyletic nature of the Deinococcus-Thermus phylum. J Bacteriol 186:3097–3107PubMedCrossRefGoogle Scholar
  37. Griffiths E, Gupta RS (2004b) Signature sequences in diverse proteins provide evidence for the late divergence of the order Aquificales. Int Microbiol 7:41–52PubMedGoogle Scholar
  38. Griffiths E, Gupta RS (2006) Molecular signatures in protein sequences that are characteristics of the phylum Aquificae. Int J Syst Evol Microbiol 56:99–107PubMedCrossRefGoogle Scholar
  39. Griffiths E, Gupta RS (2007) Identification of signature proteins that are distinctive of the Deinococcus-Thermus phylum. Int Microbiol 10:201–208PubMedGoogle Scholar
  40. Griffiths E, Petrich AK, Gupta RS (2005) Conserved indels in essential proteins that are distinctive characteristics of Chlamydiales and provide novel means for their identification. Microbiology-Sgm 151:2647–2657CrossRefGoogle Scholar
  41. Griffiths E, Ventresca MS, Gupta RS (2006) BLAST screening of Chlamydial genomes to identify signature proteins that are unique for the Chlamydiales, Chlamydiaceae, Chlamydophila and Chlamydia groups of species. BMC Genomics 7:14PubMedCrossRefGoogle Scholar
  42. 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
  43. Gupta RS (2000a) The natural evolutionary relationships among prokaryotes. Crit Rev Microbiol 26:111–131PubMedCrossRefGoogle Scholar
  44. Gupta RS (2000b) The phylogeny of proteobacteria: relationships to other eubacterial phyla and eukaryotes. FEMS Microbiol Rev 24:367–402PubMedCrossRefGoogle Scholar
  45. 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
  46. Gupta RS (2003) Evolutionary relationships among photosynthetic bacteria. Photosynth Res 76:173–183PubMedCrossRefGoogle Scholar
  47. Gupta RS (2004) The phylogeny and signature sequences characteristics of fibrobacteres, chlorobi, and bacteroidetes. Crit Rev Microbiol 30:123–143PubMedCrossRefGoogle Scholar
  48. Gupta RS (2005) Protein signatures distinctive of alpha-proteobacteria and its subgroups and a model for alpha-proteobacterial evolution. Crit Rev Microbiol 31:101–135PubMedCrossRefGoogle Scholar
  49. Gupta RS (2006) Molecular signatures (unique proteins and conserved indels) that are specific for the epsilon-proteobacteria (Campylobacterales). BMC Genomics 7:167PubMedCrossRefGoogle Scholar
  50. Gupta RS (2009) Protein signatures (molecular synapomorphies) that are distinctive characteristics of the major cyanobacterial clades. Int J Syst Evol Microbiol 59 1:2510–2526CrossRefGoogle Scholar
  51. Gupta RS (2010) Molecular signatures for the main phyla of photosynthetic bacteria and their subgroups. Photosynth Res 104:357–372PubMedCrossRefGoogle Scholar
  52. Gupta RS (2011) Origin of diderm (gram-negative) bacteria: antibiotic selection pressure rather than endosymbiosis likely led to the evolution of bacterial cells with two membranes. Antonie Van Leeuwenhoek 100:171–182PubMedCrossRefGoogle Scholar
  53. Gupta RS, Bhandari V (2011) Phylogeny and molecular signatures for the phylum Thermotogae and its subgroups. Antonie Van Leeuwenhoek 100:1–34PubMedCrossRefGoogle Scholar
  54. Gupta RS, Gao B (2009) Phylogenomic analyses of clostridia and identification of novel protein signatures that are specific to the genus Clostridium sensu stricto (cluster I). Int J Syst Evol Microbiol 59:285–294PubMedCrossRefGoogle Scholar
  55. Gupta RS, Gao B (2010) Recent advances in understanding microbial systematics. In: Xu JP (ed) Microbial population genetics. Caister Academic Press, NorfolkGoogle Scholar
  56. Gupta RS, Griffiths E (2002) Critical issues in bacterial phylogeny. Theor Popul Biol 61:423–434PubMedCrossRefGoogle Scholar
  57. Gupta RS, Griffiths E (2006) Chlamydiae-specific proteins and indels: novel tools for studies. Trends Microbiol 14:527–535PubMedCrossRefGoogle Scholar
  58. Gupta RS, Lorenzini E (2007) Phylogeny and molecular signatures (conserved proteins and indels) that are specific for the bacteroidetes and chlorobi species. BMC Evol Biol 7:71PubMedCrossRefGoogle Scholar
  59. Gupta RS, Mathews DW (2010) Signature proteins for the major clades of cyanobacteria. BMC Evol Biol 10:24PubMedCrossRefGoogle Scholar
  60. Gupta RS, Mok A (2007) Phylogenomics and signature proteins for the alpha-proteobacteria and its main groups. BMC Microbiol 7:106PubMedCrossRefGoogle Scholar
  61. Gupta RS, Shami A (2011) Molecular signatures for the crenarchaeota and the thaumarchaeota. Antonie Van Leeuwenhoek 99:133–157PubMedCrossRefGoogle Scholar
  62. Gupta RS, Sneath PHA (2007) Application of the character compatibility approach to generalized molecular sequence data: branching order of the proteobacterial subdivisions. J Mol Evol 64:90–100PubMedCrossRefGoogle Scholar
  63. Horiike T, Miyata D, Hamada K, Saruhashi S, Shinozawa T, Kumar S, Chakraborty R, Komiyama T, Tateno Y (2009) Phylogenetic construction of 17 bacterial phyla by new method and carefully selected orthologs. Gene 429:59–64PubMedCrossRefGoogle Scholar
  64. Kainth P, Gupta RS (2005) Signature proteins that are distinctive of alpha-proteobacteria. BMC Genomics 6:94PubMedCrossRefGoogle Scholar
  65. Kersters K, Devos P, Gillis M, Swings J, Vandamme P, Stackebrandt E (2006) Introduction to the proteobacteria. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The prokaryotes: a handbook on the biology of bacteria, 3rd edition, Release 3.12 edn. Springer, New York, pp 3–37Google Scholar
  66. Klenk HP, Goker M (2010) En route to a genome-based classification of archaea and bacteria? Syst Appl Microbiol 33:175–182PubMedCrossRefGoogle Scholar
  67. Konstantinidis KT, Ramette A, Tiedje JM (2006) The bacterial species definition in the genomic era. Philos Trans R Soc Lond B Biol Sci 361:1929–1940PubMedCrossRefGoogle Scholar
  68. Koonin EV (2003) Comparative genomics, minimal gene-sets and the last universal common ancestor. Nat Rev Microbiol 1:127–136PubMedCrossRefGoogle Scholar
  69. Koonin EV (2009) Darwinian evolution in the light of genomics. Nucleic Acids Res 37:1011–1034PubMedCrossRefGoogle Scholar
  70. Koski LB, Morton RA, Golding GB (2001) Codon bias and base composition are poor indicators of horizontally transferred genes. Mol Biol Evol 18:404–412PubMedGoogle Scholar
  71. Kunin V, Ouzounis CA (2003) The balance of driving forces during genome evolution in prokaryotes. Genome Res 13:1589–1594PubMedCrossRefGoogle Scholar
  72. Kunin V, Goldovsky L, Darzentas N, Ouzounis CA (2005) The net of life: reconstructing the microbial phylogenetic network. Genome Res 15:954–959PubMedCrossRefGoogle Scholar
  73. Kuo CH, Ochman H (2009) The fate of new bacterial genes. FEMS Microbiol Rev 33:38–43PubMedCrossRefGoogle Scholar
  74. Lake JA, Herbold CW, Rivera MC, Servin JA, Skophammer RG (2007) Rooting the tree of life using non-ubiquitous genes. Mol Biol Evol 24:130–136PubMedCrossRefGoogle Scholar
  75. Lathe WC, Snel B, Bork P (2000) Gene context conservation of a higher order than operons. Trends Biochem Sci 25:474–479PubMedCrossRefGoogle Scholar
  76. Lawrence JG, Hendrickson H (2005) Genome evolution in bacteria: order beneath chaos. Curr Opin Microbiol 8:572–578PubMedCrossRefGoogle Scholar
  77. Lawrence JG, Ochman H (1997) Amelioration of bacterial genomes: rates of change and exchange. J Mol Evol 44:383–397PubMedCrossRefGoogle Scholar
  78. Lerat E, Daubin V, Ochman H, Moran NA (2005) Evolutionary origins of genomic repertoires in bacteria. PLoS Biol 3:807–814CrossRefGoogle Scholar
  79. Liu SL, Schryvers AB, Sanderson KE, Johnston RN (1999) Bacterial phylogenetic clusters revealed by genome structure. J Bacteriol 181:6747–6755PubMedGoogle Scholar
  80. Ludwig W, Klenk HP (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
  81. Lukjancenko O, Wassenaar TM, Ussery DW (2010) Comparison of 61 sequenced Escherichia coli genomes. Microb Ecol 60:708–720PubMedCrossRefGoogle Scholar
  82. Maidak BL, Cole JR, Lilburn TG, Parker CT, Saxman PR, Farris RJ, Garrity GM, Olsen GJ, Schmidt TM, Tiedje JM (2001) The RDP-II (ribosomal database project). Nucleic Acids Res 29:173–174PubMedCrossRefGoogle Scholar
  83. Marri PR, Golding GB (2008) Gene amelioration demonstrated: the journey of nascent genes in bacteria. Genome 51:164–168PubMedCrossRefGoogle Scholar
  84. Nakamura Y, Itoh T, Matsuda H, Gojobori T (2004) Biased biological functions of horizontally transferred genes in prokaryotic genomes. Nat Genet 36:760–766PubMedCrossRefGoogle Scholar
  85. Narra HP, Cordes MHJ, Ochman H (2008) Structural features and the persistence of acquired proteins. Proteomics 8:4772–4781PubMedCrossRefGoogle Scholar
  86. Naushad HS, Gupta RS (2011) Molecular signatures (conserved indels) in protein sequences that are specific for the order Pasteurellales and distinguish two of its main clades. Antonie Van Leeuwenhoek Epub ahead of print:Google Scholar
  87. NCBI database (2011) NCBI completed microbial genomes. Ref Type: Generic
  88. Novichkov PS, Omelchenko MV, Gelfand MS, Mironov AA, Wolf YI, Koonin EV (2004) Genome-wide molecular clock and horizontal gene transfer in bacterial evolution. J Bacteriol 186:6575–6585PubMedCrossRefGoogle Scholar
  89. Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405:299–304PubMedCrossRefGoogle Scholar
  90. Oren A (2010) Microbial systematics. In: Wang LK, Ivanov V, Jay JH (eds) Environmental biotechnology—handbook of environmental engineering. Springer, New York, pp 81–120Google Scholar
  91. Pallen MJ, Wren BW (2007) Bacterial pathogenomics. Nature 449:835–842PubMedCrossRefGoogle Scholar
  92. Philippe H, Delsuc F, Brinkmann H, Lartillot N (2005) Phylogenomics. Annu Rev Ecol Syst 36:541–562CrossRefGoogle Scholar
  93. Ragan MA (2001) Detection of lateral gene transfer among microbial genomes. Curr Opin Genet Dev 11:620–626PubMedCrossRefGoogle Scholar
  94. Ragan MA, Beiko RG (2009) Lateral genetic transfer: open issues. Philos Trans R Soc Lond B Biol Sci 364:2241–2251PubMedCrossRefGoogle Scholar
  95. Rokas A, Holland PWH (2000) Rare genomic changes as a tool for phylogenetics. Trends Ecol Evol 15:454–459PubMedCrossRefGoogle Scholar
  96. Singh B, Gupta RS (2009) Conserved inserts in Hsp60 (GroEL) and Hsp70 (DnaK) are essential for cellular growth. Mol Genet Genomics 281:361–373Google Scholar
  97. Snel B, Bork P, Huynen MA (1999) Genome phylogeny based on gene content. Nat Genet 21:108–110PubMedCrossRefGoogle Scholar
  98. Snel B, Huynen MA, Dutilh BE (2005) Genome trees and the nature of genome evolution. Annu Rev Microbiol 59:191–209PubMedCrossRefGoogle Scholar
  99. Stackebrandt E (2006) Defining taxonomic ranks. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The prokaryotes. Springer, New York, pp 29–57CrossRefGoogle Scholar
  100. Stackebrandt E, Frederiksen W, Garrity GM, Grimont PAD, Kampfer P, Maiden MCJ, Nesme X, Rossello-Mora R, Swings J, Truper HG, Vauterin L, Ward AC, Whitman WB (2002) Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int J Syst Evol Microbiol 52:1043–1047PubMedCrossRefGoogle Scholar
  101. Staley JT (2006) The bacterial species dilemma and the genomic-phylogenetic species concept. Philos Trans R Soc Lond B Biol Sci 361:1899–1909PubMedCrossRefGoogle Scholar
  102. Sutcliffe IC (2010) A phylum level perspective on bacterial cell envelope architecture. Trends Microbiol 18:464–470PubMedCrossRefGoogle Scholar
  103. Tettelin H, Masignani V, Cieslewicz MJ, Donati C, Medini D, Ward NL, Angiuoli SV, Crabtree J, Jones AL, Durkin AS, Deboy RT, Davidsen TM, Mora M, Scarselli M, Ros IMY, Peterson JD, Hauser CR, Sundaram JP, Nelson WC, Madupu R, Brinkac LM, Dodson RJ, Rosovitz MJ, Sullivan SA, Daugherty SC, Haft DH, Selengut J, Gwinn ML, Zhou LW, Zafar N, Khouri H, Radune D, Dimitrov G, Watkins K, O’Connor KJB, Smith S, Utterback TR, White O, Rubens CE, Grandi G, Madoff LC, Kasper DL, Telford JL, Wessels MR, Rappuoli R, Fraser CM (2005) Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial “pan-genome”. Proc Natl Acad Sci USA 102:13950–13955PubMedCrossRefGoogle Scholar
  104. Tettelin H, Riley D, Cattuto C, Medini D (2008) Comparative genomics: the bacterial pan-genome. Curr Opin Microbiol 11:472–477PubMedCrossRefGoogle Scholar
  105. Touchon M, Hoede C, Tenaillon O, Barbe V, Baeriswyl S, Bidet P, Bingen E, Bonacorsi S, Bouchier C, Bouvet O, Calteau A, Chiapello H, Clermont O, Cruveiller S, Danchin A, Diard M, Dossat C, El Karoui M, Frapy E, Garry L, Ghigo JM, Gilles AM, Johnson J, Le Bouguenec C, Lescat M, Mangenot S, Martinez-Jehanne V, Matic I, Nassif X, Oztas S, Petit MA, Pichon C, Rouy Z, Saint Ruf C, Schneider D, Tourret J, Vacherie B, Vallenet D, Medigue C, Rocha EPC, Denamur E (2009) Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet 5(1):e1000344PubMedCrossRefGoogle Scholar
  106. Tringe SG, von Mering C, Kobayashi A, Salamov AA, Chen K, Chang HW, Podar M, Short JM, Mathur EJ, Detter JC, Bork P, Hugenholtz P, Rubin EM (2005) Comparative metagenomics of microbial communities. Science 308:554–557PubMedCrossRefGoogle Scholar
  107. Turnbaugh PJ, Gordon JI (2008) An invitation to the marriage of metagenomics and metabolomics. Cell 134:708–713PubMedCrossRefGoogle Scholar
  108. Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, Wu DY, Paulsen I, Nelson KE, Nelson W, Fouts DE, Levy S, Knap AH, Lomas MW, Nealson K, White O, Peterson J, Hoffman J, Parsons R, Baden-Tillson H, Pfannkoch C, Rogers YH, Smith HO (2004) Environmental genome shotgun sequencing of the sargasso sea. Science 304:66–74PubMedCrossRefGoogle Scholar
  109. Wayne LG (1988) International committee on systematic bacteriology: announcement of the report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Syst Appl Microbiol 10:99–100Google Scholar
  110. Williams KP, Gillespie JJ, Sobral BWS, Nordberg EK, Snyder EE, Shallom JM, Dickerman AW (2010) Phylogeny of gammaproteobacteria. J Bacteriol 192:2305–2314PubMedCrossRefGoogle Scholar
  111. Woese CR (2006) How we do, don’t and should look at bacteria and bacteriology. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The Prokaryotes. Springer, New York, pp 3–23CrossRefGoogle Scholar
  112. Wu DY, Hugenholtz P, Mavromatis K, Pukall R, Dalin E, Ivanova NN, Kunin V, Goodwin L, Wu M, Tindall BJ, Hooper SD, Pati A, Lykidis A, Spring S, Anderson IJ, D’haeseleer P, Zemla A, Singer M, Lapidus A, Nolan M, Copeland A, Han C, Chen F, Cheng JF, Lucas S, Kerfeld C, Lang E, Gronow S, Chain P, Bruce D, Rubin EM, Kyrpides NC, Klenk HP, Eisen JA (2009) A phylogeny—driven genomic encyclopedia of bacteria and archaea. Nature 462:1056–1060PubMedCrossRefGoogle Scholar
  113. Xie W, Wang FP, Guo L, Chen ZL, Sievert SM, Meng J, Huang GR, Li YX, Yan QY, Wu S, Wang X, Chen SW, He GY, Xiao X, Xu AL (2011) Comparative metagenomics of microbial communities inhabiting deep-sea hydrothermal vent chimneys with contrasting chemistries. ISME J 5:414–426PubMedCrossRefGoogle Scholar
  114. Xu JP (2006) Microbial ecology in the age of genomics and metagenomics: concepts, tools, and recent advances. Mol Ecol 15:1713–1731PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Section of Microbial PathogenesisYale University School of MedicineNew HavenUSA
  2. 2.Department of Biochemistry and Biomedical SciencesMcMaster UniversityHamiltonCanada

Personalised recommendations