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.
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.
Access optionsAccess options
Subscribe to Journal
Get full journal access for 1 year
only $22.08 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Bak, A. L., Black, F. T., Christiansen, C. & Freundt, E. A. Genome size of mycoplasmal DNA. Nature 224, 1209–1210 (1969).
Maniloff, J. & Morowitz, H. J. Cell biology of the mycoplasmas. Bacteriol. Rev. 36, 263–290 (1972).
Wallace, D. C. & Morowitz, H. J. Genome size and evolution. Chromosoma 40, 121–126 (1973).
Woese, C. R., Maniloff, J. & Zablen, L. B. Phylogenetic analysis of the mycoplasmas. Proc. Natl Acad. Sci. USA 77, 494–498 (1980).
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).
Fraser, C. M. et al. The minimal gene complement of Mycoplasma genitalium. Science 270, 397–403 (1995).
Andersson, S. G. et al. The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396, 133–140 (1998).
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).
Fraser, C. M. et al. Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390, 580–586 (1997).
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).
Itaya, M. An estimation of minimal genome size required for life. FEBS Lett. 362, 257–260 (1995).
Mushegian, A. The minimal genome concept. Curr. Opin. Genet. Dev. 9, 709–714 (1999).
Koonin, E. V. Comparative genomics, minimal gene-sets and the last universal common ancestor. Nature Rev. Microbiol. 1, 127–136 (2003).
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).
Charlebois, R. L. & Doolittle, W. F. Computing prokaryotic gene ubiquity: rescuing the core from extinction. Genome Res. 14, 2469–2477 (2004).
Koonin, E. V. How many genes can make a cell: The minimal-gene-set concept. Annu. Rev. Genomics Hum. Genet. 1, 99–116 (2000).
Hutchison, C. A. et al. Global transposon mutagenesis and a minimal Mycoplasma genome. Science 286, 2165–2169 (1999).
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).
Kobayashi, K. et al. Essential Bacillus subtilis genes. Proc. Natl Acad. Sci. USA 100, 4678–4683 (2003).
Glass, J. I. et al. Essential genes of a minimal bacterium. Proc. Natl Acad. Sci. USA 103, 425–430 (2006).
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).
Moran, N. A., McCutcheon, J. P. & Nakabachi, A. Genomics and evolution of heritable bacterial symbionts. Annu. Rev. Genet. 42, 165–190 (2008).
Tamas, I. et al. 50 million years of genomic stasis in endosymbiotic bacteria. Science 296, 2376–2379 (2002).
van Ham, R. C. et al. Reductive genome evolution in Buchnera aphidicola. Proc. Natl Acad. Sci. USA 100, 581–586 (2003).
Akman, L. et al. Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nature Genet. 32, 402–407 (2002).
Gil, R. et al. The genome sequence of Blochmannia floridanus: comparative analysis of reduced genomes. Proc. Natl Acad. Sci. USA 100, 9388–9393 (2003).
Wu, D. et al. Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters. PLoS Biol. 4, e188 (2006).
Moran, N. A. Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc. Natl Acad. Sci. USA 93, 2873–2878 (1996).
Mira, A., Ochman, H. & Moran, N. A. Deletional bias and the evolution of bacterial genomes. Trends Genet. 17, 589–596 (2001).
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.
Kuo, C. H. & Ochman, H. Deletional bias across the three domains of life. Genome Biol. Evol. 1, 145–152 (2009).
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.
Fernandez, A. & Lynch, M. Non-adaptive origins of interactome complexity. Nature 474, 502–505 (2011).
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).
Ochman, H. & Davalos, L. M. The nature and dynamics of bacterial genomes. Science 311, 1730–1733 (2006).
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).
Cole, S. T. et al. Massive gene decay in the leprosy bacillus. Nature 409, 1007–1011 (2001).
Kuo, C. H., Moran, N. A. & Ochman, H. The consequences of genetic drift for bacterial genome complexity. Genome Res. 19, 1450–1454 (2009).
McCutcheon, J. P. The bacterial essence of tiny symbiont genomes. Curr. Opin. Microbiol. 13, 73–78 (2010).
Burger, G., Gray, M. W. & Lang, B. F. Mitochondrial genomes: anything goes. Trends Genet. 19, 709–716 (2003).
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).
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).
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.
Raoult, D. et al. The 1.2-megabase genome sequence of Mimivirus. Science 306, 1344–1350 (2004).
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).
Sueoka, N. On the genetic basis of variation and heterogeneity of DNA base composition. Proc. Natl Acad. Sci. USA 48, 582–592 (1962).
Muto, A. & Osawa, S. The guanine and cytosine content of genomic DNA and bacterial evolution. Proc. Natl Acad. Sci. USA 84, 166–169 (1987).
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).
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).
Hildebrand, F., Meyer, A. & Eyre-Walker, A. Evidence of selection upon genomic GC-content in bacteria. PLoS Genet. 6, e1001107 (2010).
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.
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).
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.
Rocha, E. P. & Danchin, A. Base composition bias might result from competition for metabolic resources. Trends Genet. 18, 291–294 (2002).
Bentley, S. D. & Parkhill, J. Comparative genomic structure of prokaryotes. Annu. Rev. Genet. 38, 771–792 (2004).
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.
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).
Knight, R. D., Freeland, S. J. & Landweber, L. F. Rewiring the keyboard: evolvability of the genetic code. Nature Rev. Genet. 2, 49–58 (2001).
Maniloff, J. in Molecular Biology and Pathogenicity of Mycoplasmas (eds Razin, S. & Herrmann, R.) 31–44 (Kluwer Academic Publishers, New York, 2002).
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.
Osawa, S. & Jukes, T. H. Evolution of the genetic code as affected by anticodon content. Trends Genet. 4, 191–198 (1988).
Osawa, S., Jukes, T. H., Watanabe, K. & Muto, A. Recent evidence for evolution of the genetic code. Microbiol. Rev. 56, 229–264 (1992).
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).
Andersson, S. G. & Kurland, C. G. Genomic evolution drives the evolution of the translation system. Biochem. Cell Biol. 73, 775–787 (1995).
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.
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).
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).
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).
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).
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.
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).
Dufresne, A., Garczarek, L. & Partensky, F. Accelerated evolution associated with genome reduction in a free-living prokaryote. Genome Biol. 6, R14 (2005).
Moran, N. A. Microbial minimalism: genome reduction in bacterial pathogens. Cell 108, 583–586 (2002).
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).
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).
Poliakov, A. et al. Large-scale label-free quantitative proteomics of the pea aphid-Buchnera symbiosis. Mol. Cell. Proteomics 10, M110.007039 (2011).
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).
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).
Tokuriki, N. & Tawfik, D. S. Chaperonin overexpression promotes genetic variation and enzyme evolution. Nature 459, 668–673 (2009).
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).
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).
Bjork, G. R. et al. Transfer RNA modification. Annu. Rev. Biochem. 56, 263–287 (1987).
Kessler, D. Enzymatic activation of sulfur for incorporation into biomolecules in prokaryotes. FEMS Microbiol. Rev. 30, 825–840 (2006).
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).
Gardner, M. J. et al. Genome sequence of Theileria parva, a bovine pathogen that transforms lymphocytes. Science 309, 134–137 (2005).
Gray, M. W., Burger, G. & Lang, B. F. Mitochondrial evolution. Science 283, 1476–1481 (1999).
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).
Palmer, J. D. Organelle genomes: going, going, gone! Science 275, 790–791 (1997).
Truscott, K. N., Brandner, K. & Pfanner, N. Mechanisms of protein import into mitochondria. Curr. Biol. 13, R326–R337 (2003).
Schleiff, E. & Soll, J. Travelling of proteins through membranes: translocation into chloroplasts. Planta 211, 449–456 (2000).
Andersson, J. O. Evolutionary genomics: is Buchnera a bacterium or an organelle? Curr. Biol. 10, R866–R868 (2000).
Consortium, T. I. A. G. Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biol. 8, e1000313 (2010).
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.
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.
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).
Hotopp, J. C. et al. Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317, 1753–1756 (2007).
Andersson, J. O. & Andersson, S. G. Genome degradation is an ongoing process in Rickettsia. Mol. Biol. Evol. 16, 1178–1191 (1999).
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).
Keeling, P. J. Endosymbiosis: bacteria sharing the load. Curr. Biol. 21, R623–R624 (2011).
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.
Theissen, U. & Martin, W. The difference between organelles and endosymbionts. Curr. Biol. 16, R1016–R1017 (2006).
Bhattacharya, D. & Archibald, J. M. The difference between organelles and endosymbionts: response to Theissen and Martin. Curr. Biol. 16, R1017–R1018 (2006).
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).
Buchner, P. Endosymbiosis of animals with plant microorganisms. (Interscience, New York, 1965).
Baumann, L. & Baumann, P. Cospeciation between the primary endosymbionts of mealybugs and their hosts. Curr. Microbiol. 50, 84–87 (2005).
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).
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).
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).
Stamatakis, A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690 (2006).
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).
Thao, M. L. & Baumann, P. Evolutionary relationships of primary prokaryotic endosymbionts of whiteflies and their hosts. Appl. Environ. Microbiol. 70, 3401–3406 (2004).
Stewart, G. C. Taking shape: control of bacterial cell wall biosynthesis. Mol. Microbiol. 57, 1177–1181 (2005).
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).
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).
Schroder, D. et al. Intracellular endosymbiotic bacteria of Camponotus species (carpenter ants): systematics, evolution and ultrastructural characterization. Mol. Microbiol. 21, 479–489 (1996).
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).
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).
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).
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).
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).
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.
The authors declare no competing financial interests.
- Axenic culture
A culture of a bacterium or other organism that is independent of any other living organism.
Symbionts that reside inside the cells of the host.
Specialized eukaryotic cells that contain symbionts within the cytosol.
A type of small insect that feeds on plant phloem sap.
About this article
BMC Genomics (2019)
Cicada Endosymbionts Have tRNAs That Are Correctly Processed Despite Having Genomes That Do Not Encode All of the tRNA Processing Machinery
A Tale of Three Species: Adaptation of Sodalis glossinidius to Tsetse Biology, Wigglesworthia Metabolism, and Host Diet
Symbionts of the ciliate Euplotes : diversity, patterns and potential as models for bacteria–eukaryote endosymbioses
Proceedings of the Royal Society B: Biological Sciences (2019)
An interspecies malate–pyruvate shuttle reconciles redox imbalance in an anaerobic microbial community
The ISME Journal (2019)