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Evolutionary fates within a microbial population highlight an essential role for protein folding during natural selection.

ABSTRACT: Systems biology can offer a great deal of insight into evolution by quantitatively linking complex properties such as protein structure, folding, and function to the fitness of an organism. Although the link between diseases such as Alzheimer's and misfolding is well appreciated, directly showing the importance of protein folding to success in evolution has been more difficult. We show here that predicting success during adaptation can depend critically on enzyme kinetic and folding models. We used a 'weak link' method to favor mutations to an essential, but maladapted, adenylate kinase gene within a microbial population that resulted in the identification of five mutants that arose nearly simultaneously and competed for success. Physicochemical characterization of these mutants showed that, although steady-state enzyme activity is important, success within the population is critically dependent on resistance to denaturation and aggregation. A fitness function based on in vitro measurements of enzyme activity, reversible and irreversible unfolding, and the physiological context reproduces in vivo evolutionary fates in the population linking organismal adaptation to its physical basis.

SUBMITTER: Pena MI

PROVIDER: S-EPMC2925523 | biostudies-literature | 2010 Jul

REPOSITORIES: biostudies-literature

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Evolutionary fates within a microbial population highlight an essential role for protein folding during natural selection.

Peña Matthew I MI Davlieva Milya M Bennett Matthew R MR Olson John S JS Shamoo Yousif Y

Molecular systems biology 20100701

Systems biology can offer a great deal of insight into evolution by quantitatively linking complex properties such as protein structure, folding, and function to the fitness of an organism. Although the link between diseases such as Alzheimer's and misfolding is well appreciated, directly showing the importance of protein folding to success in evolution has been more difficult. We show here that predicting success during adaptation can depend critically on enzyme kinetic and folding models. We u ...[more]

PMID: 20631681

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Project description:Host-associated microbes display remarkable convergence in genome repertoire resulting from selection to supplement missing host functions. Nutritional supplementation has been proposed in the verrucomicrobial endosymbiont Xiphinematobacter sp., which lives within a globally widespread group of plant-parasitic nematodes that vector damaging nepoviruses to plants. Only one genome sequence has been published from this symbiont, leaving unanswered questions about its diversity, host range, role, and selective pressures within its hosts. Because its hosts are exceptionally resistant to culturing, this symbiont is best studied through advanced genomic approaches. To analyze the role of Xiphinematobacter sp. in its host, sequencing was performed on nematode communities, and then genomes were extracted for comparative genomics, gene ontology enrichment tests, polymorphism analysis, de Bruijn-based genome-wide association studies, and tests of pathway- and site-specific selection on genes predicted play a role in the symbiosis. Results showed a closely clustered set of Xiphinematobacter isolates with reduced genomes of ∼917 kbp, for which a new species was proposed. Symbionts shared only 2.3% of genes with outgroup Verrucomicrobia, but comparative analyses showed high conservation of all 10 essential amino acid (EAA) biosynthesis pathways plus several vitamin pathways. These findings were supported by gene ontology enrichment tests and high polymorphisms in these pathways compared with background. Genome-wide association analysis confirmed high between-species fixation of alleles with significant functional enrichment for EAA and thiamine synthesis. Strong positive selection was detected on sites within these pathways, despite several being under increased purifying selection. Together, these results suggest that supplementation of EAAs missing in the host diet may drive this widespread symbiosis.IMPORTANCEXiphinematobacter spp. are distinctly evolved intracellular symbionts in the phylum Verrucomicrobia, which includes the important human gut-associated microbe Akkermansia muciniphila and many highly abundant free-living soil microbes. Like Akkermansia sp., Xiphinematobacter sp. is obligately associated with the gut of its hosts, which in this case consists of a group of plant-parasitic nematodes that are among the top 10 most destructive species to global agriculture, by vectoring plant viruses. This study examined the hypothesis that the key to this symbiont's stable evolutionary association with its host is through provisioning nutrients that its host cannot make that may be lacking in the nematode's plant phloem diet, such as essential amino acids and several vitamins. The significance of our research is in demonstrating, using population genomics, the signatures of selective pressure on these hypothesized roles to ultimately learn how this independently evolved symbiont functionally mirrors symbionts of phloem-feeding insects.

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Evolutionary fates within a microbial population highlight an essential role for protein folding during natural selection.

Publications

Evolutionary fates within a microbial population highlight an essential role for protein folding during natural selection.

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