Chance and necessity in the genome evolution of endosymbiotic bacteria of insects.
An open question in evolutionary biology is how does the selection-drift balance determine the fates of biological interactions. We searched for signatures of selection and drift in genomes of five endosymbiotic bacterial groups known to evolve under strong genetic drift. Although most genes in endosymbiotic bacteria showed evidence of relaxed purifying selection, many genes in these bacteria exhibited stronger selective constraints than their orthologs in free-living bacterial relatives. Remarkably, most of these highly constrained genes had no role in the host-symbiont interactions but were involved in either buffering the deleterious consequences of drift or other host-unrelated functions, suggesting that they have either acquired new roles or their role became more central in endosymbiotic bacteria. Experimental evolution of Escherichia coli under strong genetic drift revealed remarkable similarities in the mutational spectrum, genome reduction patterns and gene losses to endosymbiotic bacteria of insects. Interestingly, the transcriptome of the experimentally evolved lines showed a generalized deregulation of the genome that affected genes encoding proteins involved in mutational buffering, regulation and amino acid biosynthesis, patterns identical to those found in endosymbiotic bacteria. Our results indicate that drift has shaped endosymbiotic associations through a change in the functional landscape of bacterial genes and that the host had only a small role in such a shift.
Instituto de Biología Molecular y Celular de Plantas, Consejo Superior de Investigaciones Científicas (CSIC)-Universidad Politécnica de Valencia (UPV), Valencia, Spain.|Systems Biology of Molecular Interactions and Regulation, Institute for Integrative Systems Biology (I2SysBio), Consejo Superior de Investigaciones Científicas (CSIC) - Universidad de Valencia (UV), Valencia, Spain.|Department of Genetics, Smurfit Institute of Genetics, University of Dublin, Trinity College, Dublin, Ireland.
Beatriz
B
Sabater-Muñoz
Department of Genetics, Universidad de Valencia, Valencia, Spain.|Instituto de Agroquímica y Tecnología de los Alimentos, Consejo Superior de Investigaciones Científicas (CSIC), Valencia, Spain.
Christina
C
Toft
Department of Biology, University of Nevada, Reno, NV, USA.
David
D
Alvarez-Ponce
Instituto de Biología Molecular y Celular de Plantas, Consejo Superior de Investigaciones Científicas (CSIC)-Universidad Politécnica de Valencia (UPV), Valencia, Spain.|Systems Biology of Molecular Interactions and Regulation, Institute for Integrative Systems Biology (I2SysBio), Consejo Superior de Investigaciones Científicas (CSIC) - Universidad de Valencia (UV), Valencia, Spain.|Department of Genetics, Smurfit Institute of Genetics, University of Dublin, Trinity College, Dublin, Ireland.
Mario A
0000-0002-4345-3013
MA
Fares
D000818:Animals; D001419:Bacteria / Q000235:genetics*; D019143:Evolution, Molecular; D040961:Genetic Drift; D016680:Genome, Bacterial; D007313:Insecta / Q000382:microbiology*; D009154:Mutation; D012641:Selection, Genetic; D013559:Symbiosis / Q000235:genetics*