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      Genome-Wide Functional Divergence after the Symbiosis of Proteobacteria with Insects Unraveled through a Novel Computational Approach

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      PLoS Computational Biology

      Public Library of Science

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          Abstract

          Symbiosis has been among the most important evolutionary steps to generate biological complexity. The establishment of symbiosis required an intimate metabolic link between biological systems with different complexity levels. The strict endo-cellular symbiotic bacteria of insects are beautiful examples of the metabolic coupling between organisms belonging to different kingdoms, a eukaryote and a prokaryote. The host (eukaryote) provides the endosymbiont (prokaryote) with a stable cellular environment while the endosymbiont supplements the host's diet with essential metabolites. For such communication to take place, endosymbionts' genomes have suffered dramatic modifications and reconfigurations of proteins' functions. Two of the main modifications, loss of genes redundant for endosymbiotic bacteria or the host and bacterial genome streamlining, have been extensively studied. However, no studies have accounted for possible functional shifts in the endosymbiotic proteomes. Here, we develop a simple method to screen genomes for evidence of functional divergence between two species clusters, and we apply it to identify functional shifts in the endosymbiotic proteomes. Despite the strong effects of genetic drift in the endosymbiotic systems, we unexpectedly identified genes to be under stronger selective constraints in endosymbionts of aphids and ants than in their free-living bacterial relatives. These genes are directly involved in supplementing the host's diet with essential metabolites. A test of functional divergence supports a strong relationship between the endosymbiosis and the functional shifts of proteins involved in the metabolic communication with the insect host. The correlation between functional divergence in the endosymbiotic bacterium and the ecological requirements of the host uncovers their intimate biochemical and metabolic communication and provides insights on the role of symbiosis in generating species diversity.

          Author Summary

          Biological complexity has emerged on earth by the combination of living forms. This combination, called symbiosis, had to overcome the problems caused by the uncoupled metabolisms of the organisms involved. One way to do so was through the loss of genes that were no longer needed for the endosymbiont in the protected cellular environment provided by the host. Another step necessary to adjust both metabolisms was through the change in the function of bacterial proteins to perform new roles in the symbiotic system. In this article, we test such events in symbiotic systems involving an insect and a bacterium by developing a new and simple method to identify proteome-wide functional shifts. Our results show that most of the functional changes occurred at genes involved in metabolic communication with the host and are correlated with the host's ecological traits.

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          Most cited references 70

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          Evolution by Gene Duplication.

           S. OHNO,  S Ohno,  Susumu Ohno (1970)
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            Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera.

            Most aphids possess intracellular bacteria of the genus Buchnera. The bacteria are transmitted vertically via the aphid ovary, and the association is obligate for both partners: Bacteria-free aphids grow poorly and produce few or no offspring, and Buchnera are both unknown apart from aphids and apparently unculturable. The symbiosis has a nutritional basis. Specifically, bacterial provisioning of essential amino acids has been demonstrated. Nitrogen recycling, however, is not quantitatively important to the nutrition of aphid species studied, and there is strong evidence against bacterial involvement in the lipid and sterol nutrition of aphids. Buchnera have been implicated in various non-nutritional functions. Of these, just one has strong experimental support: promotion of aphid transmission of circulative viruses. It is argued that strong parallels may exist between the nutritional interactions (including the underlying mechanisms) in the aphid-Buchnera association and other insect symbioses with intracellular microorganisms.
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              Is Open Access

              Why highly expressed proteins evolve slowly

              Much recent work has explored molecular and population-genetic constraints on the rate of protein sequence evolution. The best predictor of evolutionary rate is expression level, for reasons which have remained unexplained. Here, we hypothesize that selection to reduce the burden of protein misfolding will favor protein sequences with increased robustness to translational missense errors. Pressure for translational robustness increases with expression level and constrains sequence evolution. Using several sequenced yeast genomes, global expression and protein abundance data, and sets of paralogs traceable to an ancient whole-genome duplication in yeast, we rule out several confounding effects and show that expression level explains roughly half the variation in Saccharomyces cerevisiae protein evolutionary rates. We examine causes for expression's dominant role and find that genome-wide tests favor the translational robustness explanation over existing hypotheses that invoke constraints on function or translational efficiency. Our results suggest that proteins evolve at rates largely unrelated to their functions, and can explain why highly expressed proteins evolve slowly across the tree of life.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Comput Biol
                plos
                ploscomp
                PLoS Computational Biology
                Public Library of Science (San Francisco, USA )
                1553-734X
                1553-7358
                April 2009
                April 2009
                3 April 2009
                : 5
                : 4
                Affiliations
                Department of Genetics, Trinity College Dublin, University of Dublin, Dublin, Ireland
                University of Oxford, United Kingdom
                Author notes

                Conceived and designed the experiments: MAF. Analyzed the data: CT TAW MAF. Wrote the paper: MAF.

                Article
                08-PLCB-RA-1001R2
                10.1371/journal.pcbi.1000344
                2659769
                19343224
                Toft et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                Page count
                Pages: 10
                Categories
                Research Article
                Computational Biology/Genomics
                Genetics and Genomics/Bioinformatics
                Genetics and Genomics/Comparative Genomics

                Quantitative & Systems biology

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