A Small Microbial Genome: The End of a Long Symbiotic Relationship?

Pérez‐Brocal, Vicente; Gil, Rosario; Ramos, Silvia; Lamelas, Araceli; Postigo, Marina; Michelena, José Manuel; Silva, Francisco J.; Moya, Andrés; Latorre, Amparo

doi:10.1126/science.1130441

Cited by 310 publications

(328 citation statements)

References 14 publications

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“…Our results show parallel evolution of these features in a symbiotic lineage outside the Gammaproteobacteria (Table 1). At Ϸ245 kb, the Sulcia genome is the second-smallest bacterial genome sequenced; correspondingly, its 22.4% GϩC content is one of the most biased base compositions among bacterial genomes (9,(22)(23)(24)(25)(26)(27)(28)(29). An increased rate of sequence evolution is also evident: phylogenetic analysis shows that Sulcia occurs on a long branch, indicating a higher rate of sequence evolution compared with its free-living relatives within the Bacteroidetes (Fig.…”

Section: Discussionmentioning

confidence: 91%

“…All of the previously sequenced genomes from insect symbionts have been from members of the Gammaproteobacteria division of Bacteria (9,(22)(23)(24)(25)(26)(27)(28)(29). These genomes share many features in common: small genome sizes, low GϩC contents, and increased substitution rates compared with their free-living relatives.…”

Section: Discussionmentioning

confidence: 99%

“…Extension of these results to include three recent small genomes [Buchnera aphidicola Cc (25), Carsonella ruddii (28), and Sulcia] reduces this number even further (Table 2): only gidA, the glucose-inhibited division protein, and dnaE, the ␣-subunit of DNA polymerase III (the subunit that contains the polymerase activity), are universally conserved in replication. In RNA transcription, only the RNA polymerase core enzyme (rpoA, the ␣ subunit; rpoB, the ␤ subunit; and rpoC, the ␤Ј subunit) and rpoD, the sigma 70 factor are universally conserved.…”

Section: Discussionmentioning

confidence: 99%

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Parallel genomic evolution and metabolic interdependence in an ancient symbiosis

McCutcheon

Moran

2007

Proc. Natl. Acad. Sci. U.S.A.

313

344

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Obligate symbioses with nutrient-provisioning bacteria have originated often during animal evolution and have been key to the ecological diversification of many invertebrate groups. To date, genome sequences of insect nutritional symbionts have been restricted to a related cluster within Gammaproteobacteria and have revealed distinctive features, including extreme reduction, rapid evolution, and biased nucleotide composition. Using recently developed sequencing technologies, we show that Sulcia muelleri, a member of the Bacteroidetes, underwent similar genomic changes during coevolution with its sap-feeding insect host (sharpshooters) and the coresident symbiont Baumannia cicadellinicola (Gammaproteobacteria). At 245 kilobases, Sulcia's genome is approximately one tenth of the smallest known Bacteroidetes genome and among the smallest for any cellular organism. Analysis of the coding capacities of Sulcia and Baumannia reveals striking complementarity in metabolic capabilities.Bacteroidetes ͉ insects ͉ pyrosequencing ͉ Sharpshooters ͉ genome reduction

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Section: Discussionmentioning

confidence: 91%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Parallel genomic evolution and metabolic interdependence in an ancient symbiosis

McCutcheon

Moran

2007

Proc. Natl. Acad. Sci. U.S.A.

313

344

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“…In particular, a highly simplified cell envelope and the absence of most transporter genes point towards dependency on the host machinery. In this, Westeberhardia resembles Buchnera aphidicola BCc, which also lacks the ability to synthesize cell surface components (Pérez-Brocal et al, 2006). Intracellularity allows the host to control endosymbiont populations (Vigneron et al, 2012), which together with the lack of dnaA suggests that Westeberhardia populations are controlled by C. obscurior.…”

Section: Westeberhardia As a Possible Source Of A Hgt Eventmentioning

confidence: 99%

A novel intracellular mutualistic bacterium in the invasive ant Cardiocondyla obscurior

et al. 2015

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The evolution of eukaryotic organisms is often strongly influenced by microbial symbionts that confer novel traits to their hosts. Here we describe the intracellular Enterobacteriaceae symbiont of the invasive ant Cardiocondyla obscurior, 'Candidatus Westeberhardia cardiocondylae'. Upon metamorphosis, Westeberhardia is found in gut-associated bacteriomes that deteriorate following eclosion. Only queens maintain Westeberhardia in the ovarian nurse cells from where the symbionts are transmitted to late-stage oocytes during nurse cell depletion. Functional analyses of the streamlined genome of Westeberhardia (533 kb, 23.41% GC content) indicate that neither vitamins nor essential amino acids are provided for the host. However, the genome encodes for an almost complete shikimate pathway leading to 4-hydroxyphenylpyruvate, which could be converted into tyrosine by the host. Taken together with increasing titers of Westeberhardia during pupal stage, this suggests a contribution of Westeberhardia to cuticle formation. Despite a widespread occurrence of Westeberhardia across host populations, one ant lineage was found to be naturally symbiont-free, pointing to the loss of an otherwise prevalent endosymbiont. This study yields insights into a novel intracellular mutualist that could play a role in the invasive success of C. obscurior.

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“…Examples of complex interdependent communities have been found in sharpshooters where two primary symbionts are present [108] and in some nematodes [109]. An interesting example is how the usually facultative symbiont S. symbiotica has become obligatory to the aphid Cinara cedri because it complements some functions that have been lost by the primary symbiont Buchnera [110,111]. Evolution of dependence will inevitably lead to a stabilization of the symbiont community, which should further facilitate the evolution of specific adaptation at the community level.…”

Section: Insects As Symbiotic Communitiesmentioning

confidence: 99%

Bacterial symbionts in insects or the story of communities affecting communities

Ferrari

Vavre

2011

Phil. Trans. R. Soc. B

289

264

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Bacterial symbionts are widespread in insects and other animals. Most of them are predominantly vertically transmitted, along with their hosts' genes, and thus extend the heritable genetic variation present in one species. These passengers have a variety of repercussions on the host's phenotypes: besides the cost imposed on the host for maintaining the symbiont population, they can provide fitness advantages to the host or manipulate the host's reproduction. We argue that insect symbioses are ideal model systems for community genetics. First, bacterial symbionts directly or indirectly affect the interactions with other species within a community. Examples include their involvement in modifying the use of host plants by phytophagous insects, in providing resistance to natural enemies, but also in reducing the global genetic diversity or gene flow between populations within some species. Second, one emerging picture in insect symbioses is that many species are simultaneously infected with more than one symbiont, which permits studying the factors that shape bacterial communities; for example, horizontal transmission, interactions between host genotype, symbiont genotype and the environment and interactions among symbionts. One conclusion is that insects' symbiotic complements are dynamic communities that affect and are affected by the communities in which they are embedded.

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A Small Microbial Genome: The End of a Long Symbiotic Relationship?

Cited by 310 publications

References 14 publications

Parallel genomic evolution and metabolic interdependence in an ancient symbiosis

Parallel genomic evolution and metabolic interdependence in an ancient symbiosis

A novel intracellular mutualistic bacterium in the invasive ant Cardiocondyla obscurior

Bacterial symbionts in insects or the story of communities affecting communities

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