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.
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ABSTRACT: Compared to our understanding of the taxonomic composition of the symbiotic microbes in marine sponges, the functional diversity of these symbionts is largely unknown. Furthermore, the application of genomic, transcriptomic, and proteomic techniques to functional questions on sponge host-symbiont interactions is in its infancy. In this study, we generated a transcriptome for the host and a metatranscriptome of its microbial symbionts for the giant barrel sponge, Xestospongia muta, from the Caribbean. In combination with a gene-specific approach, our goals were to 1) characterize genetic evidence for nitrogen cycling in X. muta, an important limiting nutrient on coral reefs 2) identify which prokaryotic symbiont lineages are metabolically active and, 3) characterize the metabolic potential of the prokaryotic community. Xestospongia muta expresses genes from multiple nitrogen transformation pathways that when combined with the abundance of this sponge, and previous data on dissolved inorganic nitrogen fluxes, shows that this sponge is an important contributor to nitrogen cycling on coral reefs. Additionally, we observed significant differences in gene expression of the archaeal amoA gene, which is involved in ammonia oxidation, between coral reef locations consistent with differences in the fluxes of dissolved inorganic nitrogen previously reported. In regards to symbiont metabolic potential, the genes in the biosynthetic pathways of several amino acids were present in the prokaryotic metatranscriptome dataset but in the host-derived transcripts only the catabolic reactions for these amino acids were present. A similar pattern was observed for the B vitamins (riboflavin, biotin, thiamin, cobalamin). These results expand our understanding of biogeochemical cycling in sponges, and the metabolic interchange highlighted here advances the field of symbiont physiology by elucidating specific metabolic pathways where there is high potential for host-prokaryote interactions.Frontiers in Microbiology 04/2015; 6. DOI:10.3389/fmicb.2015.00364 · 3.94 Impact Factor
The Open Evolution Journal 05/2010; 4(1):12-22. DOI:10.2174/1874404401004010012
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ABSTRACT: Genome data have created new opportunities to untangle evolutionary processes shaping microbial variation. Among bacteria, long-term mutualists of insects represent the smallest and (typically) most AT-rich genomes. Evolutionary theory provides a context to predict how an endosymbiotic lifestyle may alter fundamental evolutionary processes-mutation, selection, genetic drift, and recombination-and thus contribute to extreme genomic outcomes. These predictions can then be explored by comparing evolutionary rates, genome size and stability, and base compositional biases across endosymbiotic and free-living bacteria. Recent surprises from such comparisons include genome reduction among uncultured, free-living species. Some studies suggest that selection generally drives this streamlining, while drift drives genome reduction in endosymbionts; however, this remains an hypothesis requiring additional data. Unexpected evidence of selection acting on endosymbiont GC content hints that even weak selection may be effective in some long-term mutualists. Moving forward, intraspecific analysis offers a promising approach to distinguish underlying mechanisms, by testing the null hypothesis of neutrality and by quantifying mutational spectra. Such analyses may clarify whether endosymbionts and free-living bacteria occupy distinct evolutionary trajectories or, alternatively, represent varied outcomes of similar underlying forces. © 2015 New York Academy of Sciences.Annals of the New York Academy of Sciences 04/2015; DOI:10.1111/nyas.12740 · 4.31 Impact Factor