Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Extreme genome reduction in symbiotic bacteria

Nature Reviews Microbiology volume 10, pages 13–26 (2012)Cite this article

Subjects

Key Points

  • Prior to 2006, the smallest known cellular genomes, from several bacterial and archaeal phyla, reached a lower limit of about 500 kb, or approximately 500 genes.

  • Starting with 'Candidatus Carsonella ruddii' in 2006, several much smaller genomes have recently been reported, all from bacteria that are intracellular symbionts of insects. These represent independent lineages of symbiotic bacteria in the Gammaproteobacteria, Betaproteobacteria, Alphaproteobacteria and Bacteroidetes taxa and have genome sizes of 139–250 kb, encoding a total of only 121–227 proteins.

  • In addition to extreme genome reduction, these organisms show extreme biases in genomic GC content, massive acceleration in the rates of protein evolution and unusual, degenerate cell morphologies. They also exhibit constitutively elevated expression of chaperonin and other heat shock proteins.

  • Despite their small sizes, all of these genomes retain a set of genes encoding enzymes involved in biosynthetic pathways for the production of nutrients that are needed by the insect hosts.

  • Although none of these symbionts has been grown in pure culture outside of the host, these organisms, with the exception of 'Candidatus Tremblaya princeps', retain most of the core genes for DNA replication, transcription and translation. Thus, although their genome sizes approach those of organelles (mitochondria and plastids), their gene sets are much more 'cell like' than those of organelles.

  • Thus far, no evidence supports the importation of host-encoded proteins into the cytosol of symbionts, and no evidence supports the transfer of ancestral symbiont genes to the host nucleus.

  • In the exceptional case of 'Ca. Tremblaya princeps', with a genome of only 139 kb, the cell machinery has undergone a radical depletion; for example, all tRNA synthetases are absent, in striking contrast to the other tiny genomes described to date. This gene loss may reflect a dependence on the highly unusual presence of a second bacterial symbiont living within 'Ca. Tremblaya princeps'.

  • These symbionts with tiny genomes give insight into the nature of essential genes and the limits of cell and genome evolution.

Abstract

Since 2006, numerous cases of bacterial symbionts with extraordinarily small genomes have been reported. These organisms represent independent lineages from diverse bacterial groups. They have diminutive gene sets that rival some mitochondria and chloroplasts in terms of gene numbers and lack genes that are considered to be essential in other bacteria. These symbionts have numerous features in common, such as extraordinarily fast protein evolution and a high abundance of chaperones. Together, these features point to highly degenerate genomes that retain only the most essential functions, often including a considerable fraction of genes that serve the hosts. These discoveries have implications for the concept of minimal genomes, the origins of cellular organelles, and studies of symbiosis and host-associated microbiota.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Comparison of the smallest genomes for free-living and symbiotic organisms.
Figure 2: Extreme genomic features in symbionts with tiny genomes.
Figure 3: Stages of genome reduction in host-restricted bacteria for which small population sizes and an asexual life cycle result in mutation fixation.

Similar content being viewed by others

References

  1. Bak, A. L., Black, F. T., Christiansen, C. & Freundt, E. A. Genome size of mycoplasmal DNA. Nature 224, 1209–1210 (1969).

    Article  CAS  PubMed  Google Scholar 

  2. Maniloff, J. & Morowitz, H. J. Cell biology of the mycoplasmas. Bacteriol. Rev. 36, 263–290 (1972).

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Wallace, D. C. & Morowitz, H. J. Genome size and evolution. Chromosoma 40, 121–126 (1973).

    Article  CAS  PubMed  Google Scholar 

  4. Woese, C. R., Maniloff, J. & Zablen, L. B. Phylogenetic analysis of the mycoplasmas. Proc. Natl Acad. Sci. USA 77, 494–498 (1980).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Weisburg, W. G., Woese, C. R., Dobson, M. E. & Weiss, E. A common origin of rickettsiae and certain plant pathogens. Science 230, 556–558 (1985).

    Article  CAS  PubMed  Google Scholar 

  6. Fraser, C. M. et al. The minimal gene complement of Mycoplasma genitalium. Science 270, 397–403 (1995).

    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).

    CAS  PubMed  Google Scholar 

  8. Shigenobu, S., Watanabe, H., Hattori, M., Sakaki, Y. & Ishikawa, H. Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407, 81–86 (2000).

    Article  CAS  PubMed  Google Scholar 

  9. Fraser, C. M. et al. Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390, 580–586 (1997).

    Article  CAS  PubMed  Google Scholar 

  10. Mushegian, A. R. & Koonin, E. V. A minimal gene set for cellular life derived by comparison of complete bacterial genomes. Proc. Natl Acad. Sci. USA 93, 10268–10273 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Itaya, M. An estimation of minimal genome size required for life. FEBS Lett. 362, 257–260 (1995).

    Article  CAS  PubMed  Google Scholar 

  12. Mushegian, A. The minimal genome concept. Curr. Opin. Genet. Dev. 9, 709–714 (1999).

    Article  CAS  PubMed  Google Scholar 

  13. Koonin, E. V. Comparative genomics, minimal gene-sets and the last universal common ancestor. Nature Rev. Microbiol. 1, 127–136 (2003).

    Article  CAS  Google Scholar 

  14. Harris, J. K., Kelley, S. T., Spiegelman, G. B. & Pace, N. R. The genetic core of the universal ancestor. Genome Res. 13, 407–412 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Charlebois, R. L. & Doolittle, W. F. Computing prokaryotic gene ubiquity: rescuing the core from extinction. Genome Res. 14, 2469–2477 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Koonin, E. V. How many genes can make a cell: The minimal-gene-set concept. Annu. Rev. Genomics Hum. Genet. 1, 99–116 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Hutchison, C. A. et al. Global transposon mutagenesis and a minimal Mycoplasma genome. Science 286, 2165–2169 (1999).

    Article  CAS  PubMed  Google Scholar 

  18. Akerley, B. J. et al. A genome-scale analysis for identification of genes required for growth or survival of Haemophilus influenzae. Proc. Natl Acad. Sci. USA 99, 966–971 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Kobayashi, K. et al. Essential Bacillus subtilis genes. Proc. Natl Acad. Sci. USA 100, 4678–4683 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Glass, J. I. et al. Essential genes of a minimal bacterium. Proc. Natl Acad. Sci. USA 103, 425–430 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Curnow, A. W. et al. Glu-tRNAGln amidotransferase: a novel heterotrimeric enzyme required for correct decoding of glutamine codons during translation. Proc. Natl Acad. Sci. USA 94, 11819–11826 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Moran, N. A., McCutcheon, J. P. & Nakabachi, A. Genomics and evolution of heritable bacterial symbionts. Annu. Rev. Genet. 42, 165–190 (2008).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  24. van Ham, R. C. et al. Reductive genome evolution in Buchnera aphidicola. Proc. Natl Acad. Sci. USA 100, 581–586 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Akman, L. et al. Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nature Genet. 32, 402–407 (2002).

    Article  CAS  PubMed  Google Scholar 

  26. Gil, R. et al. The genome sequence of Blochmannia floridanus: comparative analysis of reduced genomes. Proc. Natl Acad. Sci. USA 100, 9388–9393 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Wu, D. et al. Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters. PLoS Biol. 4, e188 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. 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 

  29. 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 

  30. Nilsson, A. I. et al. Bacterial genome size reduction by experimental evolution. Proc. Natl Acad. Sci. USA 102, 12112–12116 (2005). Experimental support for the hypothesis that bacteria which are subject to frequent population bottlenecks can rapidly delete large amounts of DNA from their genomes.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Kuo, C. H. & Ochman, H. Deletional bias across the three domains of life. Genome Biol. Evol. 1, 145–152 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Fares, M. A., Ruiz-Gonzalez, M. X., Moya, A., Elena, S. F. & Barrio, E. Endosymbiotic bacteria: groEL buffers against deleterious mutations. Nature 417, 398 (2002). A study showing that high levels of chaperonin, as observed repeatedly in symbiotic bacteria, can ameliorate the effects of deleterious mutations, thus supporting the hypothesis that the rapid protein evolution which is characteristic of small genomes reflects largely deleterious evolution and that elevated expression of heat shock proteins represents a compensatory adaptation.

    Article  CAS  PubMed  Google Scholar 

  33. Fernandez, A. & Lynch, M. Non-adaptive origins of interactome complexity. Nature 474, 502–505 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Toh, H. et al. Massive genome erosion and functional adaptations provide insights into the symbiotic lifestyle of Sodalis glossinidius in the tsetse host. Genome Res. 16, 149–156 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Ochman, H. & Davalos, L. M. The nature and dynamics of bacterial genomes. Science 311, 1730–1733 (2006).

    Article  CAS  PubMed  Google Scholar 

  36. Burke, G. R. & Moran, N. A. Massive genomic decay in Serratia symbiotica, a recently evolved symbiont of aphids. Genome Biol. Evol. 3, 195–208 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  38. Kuo, C. H., Moran, N. A. & Ochman, H. The consequences of genetic drift for bacterial genome complexity. Genome Res. 19, 1450–1454 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. McCutcheon, J. P. The bacterial essence of tiny symbiont genomes. Curr. Opin. Microbiol. 13, 73–78 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Burger, G., Gray, M. W. & Lang, B. F. Mitochondrial genomes: anything goes. Trends Genet. 19, 709–716 (2003).

    Article  CAS  PubMed  Google Scholar 

  41. Brouard, J. S., Otis, C., Lemieux, C. & Turmel, M. The exceptionally large chloroplast genome of the green alga Floydiella terrestris illuminates the evolutionary history of the Chlorophyceae. Genome Biol. Evol. 2, 240–256 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Alverson, A. J. et al. Insights into the evolution of mitochondrial genome size from complete sequences of Citrullus lanatus and Cucurbita pepo (Cucurbitaceae). Mol. Biol. Evol. 27, 1436–1448 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. McCutcheon, J. P. & von Dohlen, C. D. An interdependent metabolic patchwork in the nested symbiosis of mealybugs. Curr. Biol. 21, 1366–1372 (2011). A description of the smallest reported bacterial genome, that of ' Ca. Tremblaya princeps', and of the unusually integrated metabolic complementarity of a bacteria-within-a-bacterium symbiosis.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Raoult, D. et al. The 1.2-megabase genome sequence of Mimivirus. Science 306, 1344–1350 (2004).

    Article  CAS  PubMed  Google Scholar 

  45. Fischer, M. G., Allen, M. J., Wilson, W. H. & Suttle, C. A. Giant virus with a remarkable complement of genes infects marine zooplankton. Proc. Natl Acad. Sci. USA 107, 19508–19513 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Sueoka, N. On the genetic basis of variation and heterogeneity of DNA base composition. Proc. Natl Acad. Sci. USA 48, 582–592 (1962).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Muto, A. & Osawa, S. The guanine and cytosine content of genomic DNA and bacterial evolution. Proc. Natl Acad. Sci. USA 84, 166–169 (1987).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Cox, E. C. & Yanofsky, C. Altered base ratios in the DNA of an Escherichia coli mutator strain. Proc. Natl Acad. Sci. USA 58, 1895–1902 (1967).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Rocha, E. P. & Feil, E. J. Mutational patterns cannot explain genome composition: Are there any neutral sites in the genomes of bacteria? PLoS Genet. 6, e1001104 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Hildebrand, F., Meyer, A. & Eyre-Walker, A. Evidence of selection upon genomic GC-content in bacteria. PLoS Genet. 6, e1001107 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Hershberg, R. & Petrov, D. A. Evidence that mutation is universally biased towards AT in bacteria. PLoS Genet. 6, e1001115 (2010). Along with reference 50, provides evidence of a universal (G or C)→(A or T) mutational bias in bacteria.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. McCutcheon, J. P. & Moran, N. A. Functional convergence in reduced genomes of bacterial symbionts spanning 200 My of evolution. Genome Biol. Evol. 2, 708–718 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  53. Nakabachi, A. et al. The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science 314, 267 (2006). A report of the first discovery of a tiny cellular genome that is only about one-third the size of the smallest previously reported bacterial genome but retains some genes that are devoted to nutrition of the host insect.

    Article  CAS  PubMed  Google Scholar 

  54. Rocha, E. P. & Danchin, A. Base composition bias might result from competition for metabolic resources. Trends Genet. 18, 291–294 (2002).

    Article  CAS  PubMed  Google Scholar 

  55. Bentley, S. D. & Parkhill, J. Comparative genomic structure of prokaryotes. Annu. Rev. Genet. 38, 771–792 (2004).

    Article  CAS  PubMed  Google Scholar 

  56. Lind, P. A. & Andersson, D. I. Whole-genome mutational biases in bacteria. Proc. Natl Acad. Sci. USA 105, 17878–17883 (2008). Experimental support for the role of DNA repair enzymes and small effective population sizes in the decreased GC content seen in most endosymbiont genomes.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Knight, R. D., Freeland, S. J. & Landweber, L. F. Rewiring the keyboard: evolvability of the genetic code. Nature Rev. Genet. 2, 49–58 (2001).

    Article  CAS  PubMed  Google Scholar 

  59. Maniloff, J. in Molecular Biology and Pathogenicity of Mycoplasmas (eds Razin, S. & Herrmann, R.) 31–44 (Kluwer Academic Publishers, New York, 2002).

    Book  Google Scholar 

  60. Knight, R. D., Landweber, L. F. & Yarus, M. How mitochondria redefine the code. J. Mol. Evol. 53, 299–313 (2001). A good overview of the many hypotheses to explain codon reassignments in mitochondria.

    Article  CAS  PubMed  Google Scholar 

  61. Osawa, S. & Jukes, T. H. Evolution of the genetic code as affected by anticodon content. Trends Genet. 4, 191–198 (1988).

    Article  CAS  PubMed  Google Scholar 

  62. Osawa, S., Jukes, T. H., Watanabe, K. & Muto, A. Recent evidence for evolution of the genetic code. Microbiol. Rev. 56, 229–264 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Santos, M. A., Moura, G., Massey, S. E. & Tuite, M. F. Driving change: the evolution of alternative genetic codes. Trends Genet. 20, 95–102 (2004).

    Article  CAS  PubMed  Google Scholar 

  64. Andersson, S. G. & Kurland, C. G. Genomic evolution drives the evolution of the translation system. Biochem. Cell Biol. 73, 775–787 (1995).

    Article  CAS  PubMed  Google Scholar 

  65. Hansen, A. K. & Moran, N. A. Aphid genome expression reveals host-symbiont cooperation in the production of amino acids. Proc. Natl Acad. Sci. USA 108, 2849–2854 (2011). Work showing a high level of coordination between gene expression in the aphid host and the B. aphidicola symbiont, and highlighting the types of host co-adaptations that allow genome reduction in mutualistic endosymbionts.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Daniel, R. A. & Errington, J. Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell. Cell 113, 767–776 (2003).

    Article  CAS  PubMed  Google Scholar 

  67. Wachi, M. et al. Mutant isolation and molecular cloning of mre genes, which determine cell shape, sensitivity to mecillinam, and amount of penicillin-binding proteins in Escherichia coli. J. Bacteriol. 169, 4935–4940 (1987).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Wachi, M., Doi, M., Okada, Y. & Matsuhashi, M. New mre genes mreC and mreD, responsible for formation of the rod shape of Escherichia coli cells. J. Bacteriol. 171, 6511–6516 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Henriques, A. O., Glaser, P., Piggot, P. J. & Moran, C. P., Jr. Control of cell shape and elongation by the rodA gene in Bacillus subtilis. Mol. Microbiol. 28, 235–247 (1998).

    Article  CAS  PubMed  Google Scholar 

  70. Leaver, M., Dominguez-Cuevas, P., Coxhead, J. M., Daniel, R. A. & Errington, J. Life without a wall or division machine in Bacillus subtilis. Nature 457, 849–853 (2009). The demonstration that few steps are required to form cell wall-less 'L-forms' of Bacillus subtilis , which become polymorphic spheres and divide by an unusual, FtsZ-independent extrusion–resolution mechanism. This work highlights the problem in defining a universal set of essential genes, as a single point mutation renders the 'essential' ftsZ gene non-essential.

    Article  CAS  PubMed  Google Scholar 

  71. Moran, N. A., Tran, P. & Gerardo, N. M. Symbiosis and insect diversification: an ancient symbiont of sap-feeding insects from the Bacterial phylum Bacteroidetes. Appl. Environ. Microbiol. 71, 8802–8810 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Dufresne, A., Garczarek, L. & Partensky, F. Accelerated evolution associated with genome reduction in a free-living prokaryote. Genome Biol. 6, R14 (2005).

    Article  PubMed  PubMed Central  Google Scholar 

  73. Moran, N. A. Microbial minimalism: genome reduction in bacterial pathogens. Cell 108, 583–586 (2002).

    Article  CAS  PubMed  Google Scholar 

  74. Hara, E. et al. The predominant protein in an aphid endosymbiont is homologous to an E. coli heat shock protein. Symbiosis 8, 271–283 (1990).

    CAS  Google Scholar 

  75. Baumann, P., Baumann, L. & Clark, M. A. Levels of Buchnera aphidicola chaperonin GroEL during growth of the Aphid Schizaphis graminum. Curr. Microbiol. 32, 279–285 (1996).

    Article  CAS  Google Scholar 

  76. Poliakov, A. et al. Large-scale label-free quantitative proteomics of the pea aphid-Buchnera symbiosis. Mol. Cell. Proteomics 10, M110.007039 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Haines, L. R., Haddow, J. D., Aksoy, S., Gooding, R. H. & Pearson, T. W. The major protein in the midgut of teneral Glossina morsitans morsitans is a molecular chaperone from the endosymbiotic bacterium Wigglesworthia glossinidia. Insect Biochem. Mol. Biol. 32, 1429–1438 (2002).

    Article  CAS  PubMed  Google Scholar 

  78. McCutcheon, J. P., McDonald, B. R. & Moran, N. A. Convergent evolution of metabolic roles in bacterial co-symbionts of insects. Proc. Natl Acad. Sci. USA 106, 15394–15399 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Tokuriki, N. & Tawfik, D. S. Chaperonin overexpression promotes genetic variation and enzyme evolution. Nature 459, 668–673 (2009).

    Article  CAS  PubMed  Google Scholar 

  80. Huang, C. Y., Lee, C. Y., Wu, H. C., Kuo, M. H. & Lai, C. Y. Interactions of chaperonin with a weakly active anthranilate synthase from the aphid endosymbiont Buchnera aphidicola. Microb. Ecol. 56, 696–703 (2008).

    Article  CAS  PubMed  Google Scholar 

  81. Tatusov, R. L., Galperin, M. Y., Natale, D. A. & Koonin, E. V. The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res. 28, 33–36 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Bjork, G. R. et al. Transfer RNA modification. Annu. Rev. Biochem. 56, 263–287 (1987).

    Article  CAS  PubMed  Google Scholar 

  83. Kessler, D. Enzymatic activation of sulfur for incorporation into biomolecules in prokaryotes. FEMS Microbiol. Rev. 30, 825–840 (2006).

    Article  CAS  PubMed  Google Scholar 

  84. Kambampati, R. & Lauhon, C. T. IscS is a sulfurtransferase for the in vitro biosynthesis of 4-thiouridine in Escherichia coli tRNA. Biochemistry 38, 16561–16568 (1999).

    Article  CAS  PubMed  Google Scholar 

  85. Gardner, M. J. et al. Genome sequence of Theileria parva, a bovine pathogen that transforms lymphocytes. Science 309, 134–137 (2005).

    Article  CAS  PubMed  Google Scholar 

  86. Gray, M. W., Burger, G. & Lang, B. F. Mitochondrial evolution. Science 283, 1476–1481 (1999).

    Article  CAS  PubMed  Google Scholar 

  87. 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 

  88. Palmer, J. D. Organelle genomes: going, going, gone! Science 275, 790–791 (1997).

    Article  CAS  PubMed  Google Scholar 

  89. Truscott, K. N., Brandner, K. & Pfanner, N. Mechanisms of protein import into mitochondria. Curr. Biol. 13, R326–R337 (2003).

    Article  CAS  PubMed  Google Scholar 

  90. Schleiff, E. & Soll, J. Travelling of proteins through membranes: translocation into chloroplasts. Planta 211, 449–456 (2000).

    Article  CAS  PubMed  Google Scholar 

  91. Andersson, J. O. Evolutionary genomics: is Buchnera a bacterium or an organelle? Curr. Biol. 10, R866–R868 (2000).

    Article  CAS  PubMed  Google Scholar 

  92. Consortium, T. I. A. G. Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biol. 8, e1000313 (2010).

    Article  CAS  Google Scholar 

  93. Kirkness, E. F. et al. Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle. Proc. Natl Acad. Sci. USA 107, 12168–12173 (2010). The complete louse and endosymbiont genomes reveal that no bacterial genes have been transferred to the insect genome and that genome reduction in ' Ca. Riesia pediculicola' has not been associated with gene transfer to the host, as is common in organelles.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. 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). An exhaustive search of the aphid genome for bacterial genes, showing that the endosymbiont B. aphidicola has not achieved its small genome via a process of transfer of functional genes to the nuclear genome of its hosts. In this case at least, this process of gene transfer can be ruled out, distinguishing B. aphidicola from organelles.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Kondo, N., Nikoh, N., Ijichi, N., Shimada, M. & Fukatsu, T. Genome fragment of Wolbachia endosymbiont transferred to X chromosome of host insect. Proc. Natl Acad. Sci. USA 99, 14280–14285 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Hotopp, J. C. et al. Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317, 1753–1756 (2007).

    Article  CAS  Google Scholar 

  97. Andersson, J. O. & Andersson, S. G. Genome degradation is an ongoing process in Rickettsia. Mol. Biol. Evol. 16, 1178–1191 (1999).

    Article  CAS  PubMed  Google Scholar 

  98. McCutcheon, J. P. & Moran, N. A. Parallel genomic evolution and metabolic interdependence in an ancient symbiosis. Proc. Natl Acad. Sci. USA 104, 19392–19397 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Keeling, P. J. Endosymbiosis: bacteria sharing the load. Curr. Biol. 21, R623–R624 (2011).

    Article  CAS  PubMed  Google Scholar 

  100. Keeling, P. J. & Archibald, J. M. Organelle evolution: what's in a name? Curr. Biol. 18, R345–R347 (2008). A good overview of the problems in classifying bacteria with reduced genomes as endosymbionts or organelles.

    Article  CAS  PubMed  Google Scholar 

  101. Theissen, U. & Martin, W. The difference between organelles and endosymbionts. Curr. Biol. 16, R1016–R1017 (2006).

    Article  CAS  PubMed  Google Scholar 

  102. Bhattacharya, D. & Archibald, J. M. The difference between organelles and endosymbionts: response to Theissen and Martin. Curr. Biol. 16, R1017–R1018 (2006).

    Article  CAS  Google Scholar 

  103. Bhattacharya, D., Archibald, J. M., Weber, A. P. M. & Reyes-Prieto, A. How do endosymbionts become organelles? Understanding early events in plastid evolution. Bioessays 29, 1239–1246 (2007).

    Article  CAS  PubMed  Google Scholar 

  104. Buchner, P. Endosymbiosis of animals with plant microorganisms. (Interscience, New York, 1965).

    Google Scholar 

  105. Baumann, L. & Baumann, P. Cospeciation between the primary endosymbionts of mealybugs and their hosts. Curr. Microbiol. 50, 84–87 (2005).

    Article  CAS  PubMed  Google Scholar 

  106. Baumann, L., Thao, M. L., Hess, J. M., Johnson, M. W. & Baumann, P. The genetic properties of the primary endosymbionts of mealybugs differ from those of other endosymbionts of plant sap-sucking insects. Appl. Environ. Microbiol. 68, 3198–3205 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Thao, M. L., Gullan, P. J. & Baumann, P. Secondary (gamma-Proteobacteria) endosymbionts infect the primary (beta-Proteobacteria) endosymbionts of mealybugs multiple times and coevolve with their hosts. Appl. Environ. Microbiol. 68, 3190–3197 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Kono, M., Koga, R., Shimada, M. & Fukatsu, T. Infection dynamics of coexisting beta- and gammaproteobacteria in the nested endosymbiotic system of mealybugs. Appl. Environ. Microbiol. 74, 4175–4184 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Stamatakis, A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690 (2006).

    Article  CAS  PubMed  Google Scholar 

  110. Katoh, K., Kuma, K., Toh, H. & Miyata, T. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 33, 511–518 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Thao, M. L. & Baumann, P. Evolutionary relationships of primary prokaryotic endosymbionts of whiteflies and their hosts. Appl. Environ. Microbiol. 70, 3401–3406 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Stewart, G. C. Taking shape: control of bacterial cell wall biosynthesis. Mol. Microbiol. 57, 1177–1181 (2005).

    Article  CAS  PubMed  Google Scholar 

  113. Silverman, D. J., Wisseman, C. L., Jr & Waddell, A. In vitro studies of Rickettsia-host cell interactions: ultrastructural study of Rickettsia prowazekii-infected chicken embryo fibroblasts. Infect. Immun. 29, 778–790 (1980).

    CAS  PubMed  PubMed Central  Google Scholar 

  114. Tully, J. G., Taylor-Robinson, D., Cole, R. M. & Rose, D. L. A newly discovered mycoplasma in the human urogenital tract. Lancet 1, 1288–1291 (1981).

    Article  CAS  PubMed  Google Scholar 

  115. Schroder, D. et al. Intracellular endosymbiotic bacteria of Camponotus species (carpenter ants): systematics, evolution and ultrastructural characterization. Mol. Microbiol. 21, 479–489 (1996).

    Article  CAS  PubMed  Google Scholar 

  116. Aksoy, S. Wigglesworthia gen. nov. and Wigglesworthia glossinidia sp. nov., taxa consisting of the mycetocyte-associated, primary endosymbionts of tsetse flies. Int. J. Syst. Bacteriol. 45, 848–851 (1995).

    Article  CAS  PubMed  Google Scholar 

  117. Moran, N. A., Dale, C., Dunbar, H., Smith, W. A. & Ochman, H. Intracellular symbionts of sharpshooters (Insecta: Hemiptera: Cicadellinae) form a distinct clade with a small genome. Environ. Microbiol. 5, 116–126 (2003).

    Article  CAS  PubMed  Google Scholar 

  118. Griffiths, G. W. & Beck, S. D. Effects of antibiotics on intracellular symbiotes in the pea aphid, Acyrthosiphon pisum. Cell Tissue Res. 148, 287–300 (1974).

    Article  CAS  PubMed  Google Scholar 

  119. von Dohlen, C. D., Kohler, S., Alsop, S. T. & McManus, W. R. Mealybug beta-proteobacterial endosymbionts contain gamma-proteobacterial symbionts. Nature 412, 433–436 (2001).

    Article  CAS  PubMed  Google Scholar 

  120. Gomez-Valero, L. et al. Coexistence of Wolbachia with Buchnera aphidicola and a secondary symbiont in the aphid Cinara cedri. J. Bacteriol. 186, 6626–6633 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Part of the work leading to this Review was supported by US National Science Foundation (NSF) awards 0626716 and 1062363 to N.A.M., and J.P.M. was supported by the NSF Montana Experimental Program to Stimulate Competitive Research grant EPS-0701906 during the writing of this Review.

Author information

Authors and Affiliations

  1. Division of Biological Sciences, University of Montana, 32 Campus Drive, HS104, Missoula, 59812, Montana, USA

    John P. McCutcheon

  2. Department of Ecology and Evolutionary Biology, Yale University, 300 Heffernan Drive, West Haven, 06516, Connecticut, USA

    Nancy A. Moran

Authors
  1. John P. McCutcheon
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nancy A. Moran
    View author publications

    You can also search for this author in PubMed Google Scholar

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Related links

Related links

FURTHER INFORMATION

John P. McCutcheon's homepage

Nancy A. Moran's homepage

Glossary

Axenic culture

A culture of a bacterium or other organism that is independent of any other living organism.

Endosymbionts

Symbionts that reside inside the cells of the host.

Bacteriocytes

Specialized eukaryotic cells that contain symbionts within the cytosol.

Psyllid

A type of small insect that feeds on plant phloem sap.

Rights and permissions

Reprints and permissions

About this article

Cite this article

McCutcheon, J., Moran, N. Extreme genome reduction in symbiotic bacteria. Nat Rev Microbiol 10, 13–26 (2012). https://doi.org/10.1038/nrmicro2670

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrmicro2670

This article is cited by

Search

Advanced search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Microbiology