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Evolutionary microbial genomics: insights into bacterial host adaptation

Nature Reviews Genetics volume 11, pages 465–475 (2010)Cite this article

Subjects

Key Points

  • The wealth of genome data for host-adapted bacteria have made it possible to re-examine and quantify the level of integration between bacteria and their hosts.

  • For genera with multiple hosts there seems to be a correlation between host range, host population size and the repertoire of bacterial outer surface proteins.

  • Shifts in bacterial lifestyle towards greater interaction with the host are mediated by mechanisms such as gain of new functions through horizontal gene transfer and duplication and functional divergence of existing genes.

  • Bacteria from many different phyla have established relationships with animals, plants and invertebrates. Mutualistic relationships are mostly seen in invertebrates, suggesting that plants and animals present barriers to obligate mutualism that are difficult to overcome.

  • Secretion systems in bacteria are essential for the interaction with their eukaryotic hosts. Horizontal gene transfer events, functional diversification and innovation through gene duplication of these systems have made it possible for bacteria to adapt to their host in various ways, giving rise to pathogenic or mutualistic relationships.

  • Obligate mutualistic bacteria with highly eroded genomes have survived owing to selective pressure on the essential function they contribute to eukaryotic fitness. This contribution has resulted in intimate relationships, in which some bacteria have transferred their genes to the host nuclear genome or established consortia with other co-habiting symbionts for the benefit of the host.

Abstract

Host-adapted bacteria include mutualists and pathogens of animals, plants and insects. Their study is therefore important for biotechnology, biodiversity and human health. The recent rapid expansion in bacterial genome data has provided insights into the adaptive, diversifying and reductive evolutionary processes that occur during host adaptation. The results have challenged many pre-existing concepts built from studies of laboratory bacterial strains. Furthermore, recent studies have revealed genetic changes associated with transitions from parasitism to mutualism and opened new research avenues to understand the functional reshaping of bacteria as they adapt to growth in the cytoplasm of a eukaryotic host.

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Figure 1: Global phylogeny of host-associated bacteria.
Figure 2: Stages of host adaptation.
Figure 3: Genome size in bacteria correlates with the intracellular stage.

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References

  1. McCutcheon, J. P., McDonald, B. R. & Moran, N. A. Origin of an alternative genetic code in the extremely small and GC-rich genome of a bacterial symbiont. PLoS Genet. 5, e1000565 (2009). This paper reports the most reduced bacterial genome identified to date. Like many mitochondrial genomes, the genetic code is altered, possibly owing to the loss of a reduced set of ribosome release factors.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Nakabachi, A. et al. The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science 314, 267 (2006).

    Article  CAS  PubMed  Google Scholar 

  3. Tamas, I. et al. 50 million years of genomic stasis in endosymbiotic bacteria. Science 296, 2376–2379 (2002).

    Article  CAS  PubMed  Google Scholar 

  4. Moran, N. A., McLaughlin, H. J. & Sorek, R. The dynamics and time scale of ongoing genomic erosion in symbiotic bacteria. Science 323, 379–382 (2009).

    Article  CAS  PubMed  Google Scholar 

  5. Fuxelius, H. H., Darby, A. C., Cho, N. H. & Andersson, S. G. Visualization of pseudogenes in intracellular bacteria reveals the different tracks to gene destruction. Genome Biol. 9, R42 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Cole, S. T. et al. Massive gene decay in the leprosy bacillus. Nature 409, 1007–1011 (2001).

    Article  CAS  PubMed  Google Scholar 

  7. Andersson, S. G. et al. The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396, 133–140 (1998).

    Article  CAS  PubMed  Google Scholar 

  8. Cho, N. H. et al. The Orientia tsutsugamushi genome reveals massive proliferation of conjugative type IV secretion system and host-cell interaction genes. Proc. Natl Acad. Sci. USA 104, 7981–7986 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Klasson, L. et al. The mosaic genome structure of the Wolbachia wRi strain infecting Drosophila simulans. Proc. Natl Acad. Sci. USA 106, 5725–5730 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Moya, A., Pereto, J., Gil, R. & Latorre, A. Learning how to live together: genomic insights into prokaryote–animal symbioses. Nature Rev. Genet. 9, 218–229 (2008).

    Article  CAS  PubMed  Google Scholar 

  11. Corsaro, D., Venditti, D., Padula, M. & Valassina, M. Intracellular life. Crit. Rev. Microbiol. 25, 39–79 (1999).

    Article  CAS  PubMed  Google Scholar 

  12. Boussau, B., Karlberg, E. O., Frank, A. C., Legault, B. A. & Andersson, S. G. Computational inference of scenarios for α-proteobacterial genome evolution. Proc. Natl Acad. Sci. USA 101, 9722–9727 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Snel, B., Bork, P. & Huynen, M. A. Genomes in flux: the evolution of archaeal and proteobacterial gene content. Genome Res. 12, 17–25 (2002).

    Article  CAS  PubMed  Google Scholar 

  14. Paulsen, I. T. et al. The Brucella suis genome reveals fundamental similarities between animal and plant pathogens and symbionts. Proc. Natl Acad. Sci. USA 99, 13148–13153 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Buchner, P. Endosymbiosis of Animals With Plant Microorganisms (Interscience New York, 1965).

    Google Scholar 

  16. Ley, R. E., Lozupone, C. A., Hamady, M., Knight, R. & Gordon, J. I. Worlds within worlds: evolution of the vertebrate gut microbiota. Nature Rev. Microbiol. 6, 776–788 (2008).

    Article  CAS  Google Scholar 

  17. Li, R. et al. The sequence and de novo assembly of the giant panda genome. Nature 463, 311–317 (2010).

    Article  CAS  PubMed  Google Scholar 

  18. Casadevall, A. Evolution of intracellular pathogens. Annu. Rev. Microbiol. 62, 19–33 (2008).

    Article  CAS  PubMed  Google Scholar 

  19. Albert-Weissenberger, C., Cazalet, C. & Buchrieser, C. Legionella pneumophila — a human pathogen that co-evolved with fresh water protozoa. Cell. Mol. Life Sci. 64, 432–448 (2007).

    Article  CAS  PubMed  Google Scholar 

  20. Thomas, V. & McDonnell, G. Relationship between mycobacteria and amoebae: ecological and epidemiological concerns. Lett. Appl. Microbiol. 45, 349–357 (2007).

    Article  CAS  PubMed  Google Scholar 

  21. Ogata, H. et al. Genome sequence of Rickettsia bellii illuminates the role of amoebae in gene exchanges between intracellular pathogens. PLoS Genet. 2, e76 (2006).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Salah, I. B., Ghigo, E. & Drancourt, M. Free-living amoebae, a training field for macrophage resistance of mycobacteria. Clin. Microbiol. Infect. 15, 894–905 (2009).

    Article  CAS  PubMed  Google Scholar 

  23. Schmitz-Esser, S. et al. The genome of the amoeba symbiont “Candidatus Amoebophilus asiaticus” reveals common mechanisms for host cell interaction among amoeba-associated bacteria. J. Bacteriol. 192, 1045–1057 (2010).

    Article  CAS  PubMed  Google Scholar 

  24. Birtles, R. J. et al. 'Candidatus Odyssella thessalonicensis' gen. nov., sp. nov., an obligate intracellular parasite of Acanthamoeba species. Int. J. Syst. Evol. Microbiol. 50, 63–72 (2000).

    Article  CAS  PubMed  Google Scholar 

  25. Fritsche, T. R. et al. In situ detection of novel bacterial endosymbionts of Acanthamoeba spp. phylogenetically related to members of the order Rickettsiales. Appl. Environ. Microbiol. 65, 206–212 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Horn, M., Fritsche, T. R., Gautom, R. K., Schleifer, K. H. & Wagner, M. Novel bacterial endosymbionts of Acanthamoeba spp. related to the Paramecium caudatum symbiont Caedibacter caryophilus. Environ. Microbiol. 1, 357–367 (1999).

    Article  CAS  PubMed  Google Scholar 

  27. Horn, M. et al. Obligate bacterial endosymbionts of Acanthamoeba spp. related to the β-Proteobacteria: proposal of 'Candidatus Procabacter acanthamoebae' gen. nov., sp. nov. Int. J. Syst. Evol. Microbiol. 52, 599–605 (2002).

    Article  PubMed  Google Scholar 

  28. Horn, M. et al. Members of the Cytophaga-Flavobacterium-Bacteroides phylum as intracellular bacteria of acanthamoebae: proposal of 'Candidatus Amoebophilus asiaticus'. Environ. Microbiol. 3, 440–449 (2001).

    Article  CAS  PubMed  Google Scholar 

  29. Amann, R. et al. Obligate intracellular bacterial parasites of acanthamoebae related to Chlamydia spp. Appl. Environ. Microbiol. 63, 115–121 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Birtles, R. J., Rowbotham, T. J., Storey, C., Marrie, T. J. & Raoult, D. Chlamydia-like obligate parasite of free-living amoebae. Lancet 349, 925–926 (1997).

    Article  CAS  PubMed  Google Scholar 

  31. Pine, L., George, J. R., Reeves, M. W. & Harrell, W. K. Development of a chemically defined liquid medium for growth of Legionella pneumophila. J. Clin. Microbiol. 9, 615–626 (1979).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Skrodzki, E. F. tularensis cultures on agar-peptone medium. Biul. Inst. Med. Morsk. Gdansk. 17, 471–478 (1966).

    CAS  PubMed  Google Scholar 

  33. Wong, M. T., Thornton, D. C., Kennedy, R. C. & Dolan, M. J. A chemically defined liquid medium that supports primary isolation of Rochalimaea (Bartonella) henselae from blood and tissue specimens. J. Clin. Microbiol. 33, 742–744 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Winkler, H. H. Rickettsia species (as organisms). Annu. Rev. Microbiol. 44, 131–153 (1990).

    Article  CAS  PubMed  Google Scholar 

  35. Stephens, R. S. Chlamydia: Intracellular Biology, Pathogenesis, and Immunity (Amer Society for Microbiology, Washington, D.C, 1999).

    Book  Google Scholar 

  36. Hybiske, K. & Stephens, R. S. Mechanisms of host cell exit by the intracellular bacterium Chlamydia. Proc. Natl Acad. Sci. USA 104, 11430–11435 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Baca, O. G. & Paretsky, D. Q fever and Coxiella burnetii: a model for host-parasite interactions. Microbiol. Rev. 47, 127–149 (1983).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Munson, M. A. et al. Evidence for the establishment of aphid-eubacterium endosymbiosis in an ancestor of four aphid families. J. Bacteriol. 173, 6321–6324 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Clark, M. A., Moran, N. A., Baumann, P. & Wernegreen, J. J. Cospeciation between bacterial endosymbionts (Buchnera) and a recent radiation of aphids (Uroleucon) and pitfalls of testing for phylogenetic congruence. Evolution 54, 517–525 (2000).

    Article  CAS  PubMed  Google Scholar 

  40. Moran, N. A. & Wernegreen, J. J. Lifestyle evolution in symbiotic bacteria: insights from genomics. Trends Ecol. Evol. 15, 321–326 (2000).

    Article  CAS  PubMed  Google Scholar 

  41. Mikkola, R. & Kurland, C. G. Selection of laboratory wild-type phenotype from natural isolates of Escherichia coli in chemostats. Mol. Biol. Evol. 9, 394–402 (1992).

    CAS  PubMed  Google Scholar 

  42. Zhu, P. et al. Fit genotypes and escape variants of subgroup III Neisseria meningitidis during three pandemics of epidemic meningitis. Proc. Natl Acad. Sci. USA 98, 5234–5239 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Falush, D. Toward the use of genomics to study microevolutionary change in bacteria. PLoS Genet. 5, e1000627 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  44. Risch, N. & Merikangas, K. The future of genetic studies of complex human diseases. Science 273, 1516–1517 (1996).

    Article  CAS  PubMed  Google Scholar 

  45. Barrick, J. E. et al. Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461, 1243–1247 (2009).

    Article  CAS  PubMed  Google Scholar 

  46. Zhong, S., Miller, S. P., Dykhuizen, D. E. & Dean, A. M. Transcription, translation, and the evolution of specialists and generalists. Mol. Biol. Evol. 26, 2661–2678 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Dethlefsen, L. & Schmidt, T. M. Performance of the translational apparatus varies with the ecological strategies of bacteria. J. Bacteriol. 189, 3237–3245 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Andersson, S. G. & Kurland, C. G. Reductive evolution of resident genomes. Trends Microbiol. 6, 263–268 (1998).

    Article  CAS  PubMed  Google Scholar 

  49. Moran, N. A. Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc. Natl Acad. Sci. USA 93, 2873–2878 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Funk, D. J., Wernegreen, J. J. & Moran, N. A. Intraspecific variation in symbiont genomes: bottlenecks and the aphid-buchnera association. Genetics 157, 477–489 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Bordenstein, S. R. & Reznikoff, W. S. Mobile DNA in obligate intracellular bacteria. Nature Rev. Microbiol. 3, 688–699 (2005).

    Article  CAS  Google Scholar 

  52. Williams, T. A., Codoner, F. M., Toft, C. & Fares, M. A. Two chaperonin systems in bacterial genomes with distinct ecological roles. Trends Genet. 26, 47–51 (2009).

    Article  PubMed  CAS  Google Scholar 

  53. McNally, D. & Fares, M. A. In silico identification of functional divergence between the multiple groEL gene paralogs in Chlamydiae. BMC Evol. Biol. 7, 81 (2007).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. Enninga, J. & Rosenshine, I. Imaging the assembly, structure and activity of type III secretion systems. Cell. Microbiol. 11, 1462–1470 (2009).

    Article  CAS  PubMed  Google Scholar 

  55. Fronzes, R., Christie, P. J. & Waksman, G. The structural biology of type IV secretion systems. Nature Rev. Microbiol. 7, 703–714 (2009).

    Article  CAS  Google Scholar 

  56. Ma, W., Dong, F. F., Stavrinides, J. & Guttman, D. S. Type III effector diversification via both pathoadaptation and horizontal transfer in response to a coevolutionary arms race. PLoS Genet. 2, e209 (2006).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  57. Frank, A. C., Alsmark, C. M., Thollesson, M. & Andersson, S. G. Functional divergence and horizontal transfer of type IV secretion systems. Mol. Biol. Evol. 22, 1325–1336 (2005).

    Article  CAS  PubMed  Google Scholar 

  58. Toft, C., Williams, T. A. & Fares, M. A. Genome-wide functional divergence after the symbiosis of proteobacteria with insects unraveled through a novel computational approach. PLoS Comput. Biol. 5, e1000344 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Maezawa, K. et al. Hundreds of flagellar basal bodies cover the cell surface of the endosymbiotic bacterium Buchnera aphidicola sp. strain APS. J. Bacteriol. 188, 6539–6543 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Toft, C. & Fares, M. A. The evolution of the flagellar assembly pathway in endosymbiotic bacterial genomes. Mol. Biol. Evol. 25, 2069–2076 (2008).

    Article  CAS  PubMed  Google Scholar 

  61. Quebatte, M. et al. The BatR/BatS two component regulatory system controls the adaptive response of Bartonella henselae during human endothelial cell infection. J. Bacteriol. 23 Apr 2010 (doi:10.1128/JB.01676-09).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Seubert, A., Hiestand, R., de la Cruz, F. & Dehio, C. A bacterial conjugation machinery recruited for pathogenesis. Mol. Microbiol. 49, 1253–1266 (2003).

    Article  CAS  PubMed  Google Scholar 

  63. Nystedt, B., Frank, A. C., Thollesson, M. & Andersson, S. G. Diversifying selection and concerted evolution of a type IV secretion system in Bartonella. Mol. Biol. Evol. 25, 287–300 (2008).

    Article  CAS  PubMed  Google Scholar 

  64. Dobrindt, U., Hochhut, B., Hentschel, U. & Hacker, J. Genomic islands in pathogenic and environmental microorganisms. Nature Rev. Microbiol. 2, 414–424 (2004).

    Article  CAS  Google Scholar 

  65. Dale, C. & Moran, N. A. Molecular interactions between bacterial symbionts and their hosts. Cell 126, 453–465 (2006).

    Article  CAS  PubMed  Google Scholar 

  66. Berglund, E. C. et al. Run-off replication of host-adaptability genes is associated with gene transfer agents in the genome of mouse-infecting Bartonella grahamii. PLoS Genet. 5, e1000546 (2009). This paper shows that a chromosomal segment of several hundred kilobases which contains gene clusters for various secretion systems is amplified and packaged into bacteriophage particles. The site covering the origin of the amplification process and the genes encoding the phage particles are conserved across strains, showing selection for mobility.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  67. Klasson, L. et al. Genome evolution of Wolbachia strain wPip from the Culex pipiens group. Mol. Biol. Evol. 25, 1877–1887 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Wu, M. et al. Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol. 2, E69 (2004).

    Article  PubMed  PubMed Central  Google Scholar 

  69. Nogueira, T. et al. Horizontal gene transfer of the secretome drives the evolution of bacterial cooperation and virulence. Curr. Biol. 19, 1683–1691 (2009). This paper shows that genes for secreted proteins tend to be located near mobile elements. It is thought that mobile elements enforce cooperation by reintroducing genes for secreted proteins into cheater cells in the populations that have lost these traits.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Mira, A., Ochman, H. & Moran, N. A. Deletional bias and the evolution of bacterial genomes. Trends Genet. 17, 589–596 (2001).

    Article  CAS  PubMed  Google Scholar 

  71. Hillesland, K. L. & Stahl, D. A. Rapid evolution of stability and productivity at the origin of a microbial mutualism. Proc. Natl Acad. Sci. USA 107, 2124–2129 (2010). The authors carried out a laboratory study of the evolution of a mutualistic relationship between sulphate-reducing and methanogenic microorganisms. The results contribute to the understanding of the evolutionary processes leading to the emergence and persistence of mutualistic associations.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Sachs, J. L., Mueller, U. G., Wilcox, T. P. & Bull., J. J. The evolution of cooperation. Q. Rev. Biol. 79, 135–160 (2004).

    Article  PubMed  Google Scholar 

  73. Frank, S. A. Host-symbiont conflict over the mixing of symbiotic lineages. Proc. Biol. Sci. 263, 339–344 (1996).

    Article  CAS  PubMed  Google Scholar 

  74. Sachs, J. L. & Simms, E. L. Pathways to mutualism breakdown. Trends Ecol. Evol. 21, 585–592 (2006).

    Article  PubMed  Google Scholar 

  75. Marchetti, M. et al. Experimental evolution of a plant pathogen into a legume symbiont. PLoS Biol. 8, e1000280 (2010). This paper shows that the transition from a pathogenic to a mutualistic relationship requires the acquisition of symbiotic genes and the modification of pre-existing functions through key mutations in regulatory and structural genes. The results reveal the role of adaptive changes in the recipient genome following horizontal transfers of symbiotic plasmids for the evolution of nodulation in Rhizobia.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  76. Sachs, J. L., Ehinger, M. O. & Simms, E. L. Origins of cheating and loss of symbiosis in wild Bradyrhizobium. J. Evol. Biol. 23, 1075–1089 (2010).

    Article  CAS  PubMed  Google Scholar 

  77. Werren, J. H., Baldo, L. & Clark, M. E. Wolbachia: master manipulators of invertebrate biology. Nature Rev. Microbiol. 6, 741–751 (2008).

    Article  CAS  Google Scholar 

  78. Stouthamer, R., Breeuwer, J. A. & Hurst, G. D. Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu. Rev. Microbiol. 53, 71–102 (1999).

    Article  CAS  PubMed  Google Scholar 

  79. Langworthy, N. G. et al. Macrofilaricidal activity of tetracycline against the filarial nematode Onchocerca ochengi: elimination of Wolbachia precedes worm death and suggests a dependent relationship. Proc. Biol. Sci. 267, 1063–1069 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Stevens, L., Giordano, R. & Fialho, R. F. Male-killing, nematode infections, bacteriophage infection, and virulence of cytoplasmic bacteria in the genus Wolbachia. Annu. Rev. Ecol. Syst. 32, 519–545 (2001).

    Article  Google Scholar 

  81. Foster, J. et al. The Wolbachia genome of Brugia malayi: endosymbiont evolution within a human pathogenic nematode. PLoS Biol. 3, e121 (2005).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  82. Hosokawa, T., Koga, R., Kikuchi, Y., Meng, X. Y. & Fukatsu, T. Wolbachia as a bacteriocyte-associated nutritional mutualist. Proc. Natl Acad. Sci. USA 107, 769–774 (2010). The first report of obligate bacteriocyte-associated nutritional mutualism in insect-infecting Wolbachia strains. As all previously described strains of Wolbachia associated with insects show commensal or parasitic relationships, the results reinforce the hypothesis that pathogens can evolve to mutualists, given the right conditions.

    Article  CAS  PubMed  Google Scholar 

  83. Perlman, S. J., Hunter, M. S. & Zchori-Fein, E. The emerging diversity of Rickettsia. Proc. Biol. Sci. 273, 2097–2106 (2006).

    PubMed  PubMed Central  Google Scholar 

  84. Perotti, M. A., Clarke, H. K., Turner, B. D. & Braig, H. R. Rickettsia as obligate and mycetomic bacteria. FASEB J. 20, 2372–2374 (2006).

    Article  CAS  PubMed  Google Scholar 

  85. Darby, A. C., Cho, N. H., Fuxelius, H. H., Westberg, J. & Andersson, S. G. Intracellular pathogens go extreme: genome evolution in the Rickettsiales. Trends Genet. 23, 511–520 (2007).

    Article  CAS  PubMed  Google Scholar 

  86. Perez-Brocal, V. et al. A small microbial genome: the end of a long symbiotic relationship? Science 314, 312–313 (2006).

    Article  CAS  PubMed  Google Scholar 

  87. Gosalbes, M. J., Lamelas, A., Moya, A. & Latorre, A. The striking case of tryptophan provision in the cedar aphid Cinara cedri. J. Bacteriol. 190, 6026–6029 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Toft, C. & Fares, M. A. Selection for translational robustness in Buchnera aphidicola, endosymbiotic bacteria of aphids. Mol. Biol. Evol. 26, 743–751 (2009).

    Article  CAS  PubMed  Google Scholar 

  89. Tamames, J. et al. The frontier between cell and organelle: genome analysis of Candidatus Carsonella ruddii. BMC Evol. Biol. 7, 181 (2007).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  90. Hotopp, J. C. et al. Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317, 1753–1756 (2007). Evidence for the presence of DNA inserts of Wolbachia spp. in the nuclear genomes of four insects and four nematode hosts. The results show that bacterial genes of endosymbiotic bacteria can be transferred to the nuclear genomes of their hosts.

    Article  CAS  Google Scholar 

  91. Timmis, J. N., Ayliffe, M. A., Huang, C. Y. & Martin, W. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nature Rev. Genet. 5, 123–135 (2004).

    Article  CAS  PubMed  Google Scholar 

  92. Nikoh, N. & Nakabachi, A. Aphids acquired symbiotic genes via lateral gene transfer. BMC Biol. 7, 12 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  93. Nikoh, N. et al. Bacterial genes in the aphid genome: absence of functional gene transfer from Buchnera to its host. PLoS Genet. 6, e1000827 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  94. Woyke, T. et al. One bacterial cell, one complete genome. PLoS One 5, e10314 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  95. Tang, F. et al. mRNA-Seq whole-transcriptome analysis of a single cell. Nature Methods 6, 377–382 (2009).

    Article  CAS  PubMed  Google Scholar 

  96. Bergelson, J., Dwyer, G. & Emerson, J. J. Models and data on plant–enemy coevolution. Annu. Rev. Genet. 35, 469–499 (2001).

    Article  CAS  PubMed  Google Scholar 

  97. Dawkins, R. & Krebs, J. R. Arms races between and within species. Proc. R. Soc. Lond. B. Biol. Sci. 205, 489–511 (1979).

    Article  CAS  PubMed  Google Scholar 

  98. Clay, K. & Kover, P. X. The Red Queen Hypothesis and plant/pathogen interactions. Annu. Rev. Phytopathol. 34, 29–50 (1996).

    Article  CAS  PubMed  Google Scholar 

  99. Stavrinides, J., Ma, W. & Guttman, D. S. Terminal reassortment drives the quantum evolution of type III effectors in bacterial pathogens. PLoS Pathog. 2, e104 (2006).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  100. Goldman, N. & Yang, Z. A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol. Biol. Evol. 11, 725–736 (1994).

    CAS  PubMed  Google Scholar 

  101. Crandall, K. A., Kelsey, C. R., Imamichi, H., Lane, H. C. & Salzman, N. P. Parallel evolution of drug resistance in HIV: failure of nonsynonymous/synonymous substitution rate ratio to detect selection. Mol. Biol. Evol. 16, 372–382 (1999).

    Article  CAS  PubMed  Google Scholar 

  102. Gu, X. Statistical methods for testing functional divergence after gene duplication. Mol. Biol. Evol. 16, 1664–1674 (1999).

    Article  CAS  PubMed  Google Scholar 

  103. Gu, X. Mathematical modeling for functional divergence after gene duplication. J. Comput. Biol. 8, 221–234 (2001).

    Article  CAS  PubMed  Google Scholar 

  104. Gu, X. Maximum-likelihood approach for gene family evolution under functional divergence. Mol. Biol. Evol. 18, 453–464 (2001).

    Article  CAS  PubMed  Google Scholar 

  105. Van der Goot, F. G. Pore-Forming Toxins (Springer Verlag, Berlin, 2001).

    Book  Google Scholar 

  106. Gonzalez, M. R., Bischofberger, M., Pernot, L., van der Goot, F. G. & Freche, B. Bacterial pore-forming toxins: the (w)hole story? Cell. Mol. Life Sci. 65, 493–507 (2008).

    Article  CAS  PubMed  Google Scholar 

  107. Galan, J. E. & Collmer, A. Type III secretion machines: bacterial devices for protein delivery into host cells. Science 284, 1322–1328 (1999).

    Article  CAS  PubMed  Google Scholar 

  108. Cornelis, G. R. The type III secretion injectisome. Nature Rev. Microbiol. 4, 811–825 (2006).

    Article  CAS  Google Scholar 

  109. Gophna, U., Ron, E. Z. & Graur, D. Bacterial type III secretion systems are ancient and evolved by multiple horizontal-transfer events. Gene 312, 151–163 (2003).

    Article  CAS  PubMed  Google Scholar 

  110. Alvarez-Martinez, C. E. & Christie, P. J. Biological diversity of prokaryotic type IV secretion systems. Microbiol. Mol. Biol. Rev. 73, 775–808 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Stebbins, C. E. & Galan, J. E. Structural mimicry in bacterial virulence. Nature 412, 701–705 (2001).

    Article  CAS  PubMed  Google Scholar 

  112. Galan, J. E. Common themes in the design and function of bacterial effectors. Cell Host Microbe 5, 571–579 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Price, C. T. et al. Molecular mimicry by an F-box effector of Legionella pneumophila hijacks a conserved polyubiquitination machinery within macrophages and protozoa. PLoS Pathog. 5, e1000704 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  114. Yarbrough, M. L. et al. AMPylation of Rho GTPases by Vibrio VopS disrupts effector binding and downstream signaling. Science 323, 269–272 (2009).

    Article  CAS  PubMed  Google Scholar 

  115. Ishoey, T., Woyke, T., Stepanauskas, R., Novotny, M. & Lasken, R. S. Genomic sequencing of single microbial cells from environmental samples. Curr. Opin. Microbiol. 11, 198–204 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Rodrigue, S. et al. Whole genome amplification and de novo assembly of single bacterial cells. PLoS One 4, e6864 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  117. Lasken, R. S. & Stockwell, T. B. Mechanism of chimera formation during the multiple displacement amplification reaction. BMC Biotechnol. 7, 19 (2007).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  118. Riesenfeld, C. S., Schloss, P. D. & Handelsman, J. Metagenomics: genomic analysis of microbial communities. Annu. Rev. Genet. 38, 525–552 (2004).

    Article  CAS  PubMed  Google Scholar 

  119. Wooley, J. C., Godzik, A. & Friedberg, I. A primer on metagenomics. PLoS Comput. Biol. 6, e1000667 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  120. Guell, M. et al. Transcriptome complexity in a genome-reduced bacterium. Science 326, 1268–1271 (2009).

    Article  PubMed  CAS  Google Scholar 

  121. Kuhner, S. et al. Proteome organization in a genome-reduced bacterium. Science 326, 1235–1240 (2009).

    Article  PubMed  CAS  Google Scholar 

  122. Yus, E. et al. Impact of genome reduction on bacterial metabolism and its regulation. Science 326, 1263–1268 (2009). In references 120–122, the metabolic, interactomic and transcriptomic maps are deciphered in the cell-surface parasite Mycoplasma pneumoniae . The authors show protein multi-functionality, explaining how cellular functions can be maintained despite a small gene set.

    Article  CAS  PubMed  Google Scholar 

  123. Gibson, D. G. et al. Complete chemical synthesis, assembly, and cloning of a Mycoplasma genitalium genome. Science 319, 1215–1220 (2008).

    Article  CAS  PubMed  Google Scholar 

  124. Gibson, D. G. et al. One-step assembly in yeast of 25 overlapping DNA fragments to form a complete synthetic Mycoplasma genitalium genome. Proc. Natl Acad. Sci. USA 105, 20404–20409 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Lartigue, C. et al. Creating bacterial strains from genomes that have been cloned and engineered in yeast. Science 325, 1693–1696 (2009).

    Article  CAS  PubMed  Google Scholar 

  126. Klasson, L. & Andersson, S. G. Research on small genomes: implications for synthetic biology. Bioessays 32, 288–295 (2010).

    Article  CAS  PubMed  Google Scholar 

  127. Pal, C. et al. Chance and necessity in the evolution of minimal metabolic networks. Nature 440, 667–670 (2006).

    Article  CAS  PubMed  Google Scholar 

  128. Wu, D. et al. A phylogeny-driven genomic encyclopaedia of bacteria and archaea. Nature 462, 1056–1060 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by grants to S.G.E.A. from the Swedish Research Council, the Göran Gustafsson Foundation, the Swedish Foundation for Strategic Research and the Knut and Alice Wallenberg Foundation.

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Authors and Affiliations

  1. Department of Molecular Evolution, Uppsala University, 752 36, Uppsala, Sweden

    Christina Toft & Siv G. E. Andersson

  2. Christina Toft & Siv G. E. Andersson

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Supplementary information

Supplementary Figure 1 (PDF 161 kb)

Supplementary Table 2

List of some of the main sequenced intracellular genomes (as of January 2010) indicating the genome size, GC contents, number of protein coding genes, RNAs, number of plasmids and the year of publishing as well as lifestyle. (PDF 265 kb)

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Glossary

Mutualistic relationship

A symbiosis in which both species increase their fitness.

Pathogenic relationship

A symbiosis in which one species increases its fitness while the fitness of the other species is adversely affected.

Commensal relationship

A symbiosis in which one partner increases its fitness without affecting the other species.

Endosymbiont

An intracellular organism that contributes to the survival of the host cell and depends on the host for its own persistence. The relationship can be either mutualistic or commensalistic.

Protozoan

A single-celled (usually microscopic) eukaryotic organism. The name originates from the Greek words 'proton' and 'zoa', meaning first and animals, respectively.

Horizontal gene transfer

The transfer of genetic material between the genomes of two organisms not through the normal parent–progeny transmission during cell division.

Pseudogenization

The process whereby changes in the coding region of a gene that disrupt the function of the gene lead to its inactivation.

Endosymbiotic bacterium

A non-pathogenic bacterium that lives inside host cells.

Bacteriocyte

A specialised host cell that houses obligate mutualistic bacteria.

Conjugation

The physical joining of two bacterial cells to transfer genetic material from the donor cell to the recipient cell through a pilus.

Coefficient of variation

A normalized measure of dispersion of a probability distribution.

Genomic island

A region of the genome that has been acquired through a horizontal event.

Bacteriophage

A virus that infects bacteria and can serve as a vector of novel genetic material.

Prophage

The genome of a bacteriophage when it is integrated into the chromosome of the host bacterium.

Secondary symbiont

A facultative bacterial symbiont that is not essential for host survival and reproduction.

tRNA isoacceptor

One of a group of tRNA species that can bind to different codons for the same amino acid residue.

Rhizobium

One of a group of nitrogen-fixing bacteria that have symbiotic associations with plants.

Virulence

The ability to cause disease by breaking down the protective mechanisms of the host.

Primary endosymbiont

An obligate mutualistic endosymbiont that is essential for host survival and reproduction. Primary endosymbionts are often located in bacteriocytes and are maternally transmitted between host generations.

Psyllids

Small sap-sucking insects, also known as 'jumping plant lice'.

Metagenomics

The functional and sequence-based analysis of the collective microbial genomes contained in an environmental sample.

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Toft, C., Andersson, S. Evolutionary microbial genomics: insights into bacterial host adaptation. Nat Rev Genet 11, 465–475 (2010). https://doi.org/10.1038/nrg2798

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