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Parallel genomic evolution and metabolic interdependence in an ancient symbiosis.

ABSTRACT: 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.

SUBMITTER: McCutcheon JP

PROVIDER: S-EPMC2148300 | biostudies-literature | 2007 Dec

REPOSITORIES: biostudies-literature

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Parallel genomic evolution and metabolic interdependence in an ancient symbiosis.

McCutcheon John P JP Moran Nancy A NA

Proceedings of the National Academy of Sciences of the United States of America 20071128 49

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 ...[more]

PMID: 18048332

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Project description:Stable associations between bacterial endosymbionts and insect hosts provide opportunities to explore genome evolution in the context of established mutualisms and assess the roles of selection and genetic drift across host lineages and habitats. Blochmannia, obligate endosymbionts of ants of the tribe Camponotini, have coevolved with their ant hosts for ∼40 MY. To investigate early events in Blochmannia genome evolution across this ant host tribe, we sequenced Blochmannia from two divergent host lineages, Colobopsis obliquus and Polyrhachis turneri, and compared them with four published genomes from Blochmannia of Camponotus sensu stricto. Reconstructed gene content of the last common ancestor (LCA) of these six Blochmannia genomes is reduced (690 protein coding genes), consistent with rapid gene loss soon after establishment of the symbiosis. Differential gene loss among Blochmannia lineages has affected cellular functions and metabolic pathways, including DNA replication and repair, vitamin biosynthesis and membrane proteins. Blochmannia of P. turneri (i.e., B. turneri) encodes an intact DnaA chromosomal replication initiation protein, demonstrating that loss of dnaA was not essential for establishment of the symbiosis. Based on gene content, B. obliquus and B. turneri are unable to provision hosts with riboflavin. Of the six sequenced Blochmannia, B. obliquus is the earliest diverging lineage (i.e., the sister group of other Blochmannia sampled) and encodes the fewest protein-coding genes and the most pseudogenes. We identified 55 genes involved in parallel gene loss, including glutamine synthetase, which may participate in nitrogen recycling. Pathways for biosynthesis of coenzyme A, terpenoids and riboflavin were lost in multiple lineages, suggesting relaxed selection on the pathway after inactivation of one component. Analysis of Illumina read datasets did not detect evidence of plasmids encoding missing functions, nor the presence of coresident symbionts other than Wolbachia. Although gene order is strictly conserved in four Blochmannia of Camponotus sensu stricto, comparisons with deeply divergent lineages revealed inversions in eight genomic regions, indicating ongoing recombination despite ancestral loss of recA. In sum, the addition of two Blochmannia genomes of divergent host lineages enables reconstruction of early events in evolution of this symbiosis and suggests that Blochmannia lineages may experience distinct, host-associated selective pressures. Understanding how evolutionary forces shape genome reduction in this system may help to clarify forces driving gene loss in other bacteria, including intracellular pathogens.

Dataset Information

Parallel genomic evolution and metabolic interdependence in an ancient symbiosis.

Publications

Parallel genomic evolution and metabolic interdependence in an ancient symbiosis.

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