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Comparative Genomics Uncovers Unique Gene Turnover and Evolutionary Rates in a Gene Family Involved in the Detection of Insect Cuticular Pheromones

ABSTRACT: Chemoreception is an essential process for the survival and reproduction of animals. Many of the proteins responsible for recognizing and transmitting chemical stimuli in insects are encoded by genes that are members of moderately sized multigene families. The members of the CheB family are specialized in gustatory-mediated detection of long-chain hydrocarbon pheromones in Drosophila melanogaster and play a central role in triggering and modulating mating behavior in this species. Here, we present a comprehensive comparative genomic analysis of the CheB family across 12 species of the Drosophila genus. We have identified a total of 102 new CheB genes in the genomes of these species, including a functionally divergent member previously uncharacterized in D. melanogaster. We found that, despite its relatively small repertory size, the CheB family has undergone multiple gain and loss events and various episodes of diversifying selection during the divergence of the surveyed species. Present estimates of gene turnover and coding sequence substitution rates show that this family is evolving faster than any known Drosophila chemosensory family. To date, only other insect gustatory-related genes among these families had shown evolutionary dynamics close to those observed in CheBs. Our findings reveal the high adaptive potential of molecular components of the gustatory system in insects and anticipate a key role of genes involved in this sensory modality in species adaptation and diversification.

SUBMITTER: Torres-Oliva M

PROVIDER: S-EPMC4943180 | biostudies-literature | 2016 Jun

REPOSITORIES: biostudies-literature

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Project description:Acidithiobacillus caldus is an extremely acidophilic sulfur-oxidizer with specialized characteristics, such as tolerance to low pH and heavy metal resistance. To gain novel insights into its genetic complexity, we chosen six A. caldus strains for comparative survey. All strains analyzed in this study differ in geographic origins as well as in ecological preferences. Based on phylogenomic analysis, we clustered the six A. caldus strains isolated from various ecological niches into two groups: group 1 strains with smaller genomes and group 2 strains with larger genomes. We found no obvious intraspecific divergence with respect to predicted genes that are related to central metabolism and stress management strategies between these two groups. Although numerous highly homogeneous genes were observed, high genetic diversity was also detected. Preliminary inspection provided a first glimpse of the potential correlation between intraspecific diversity at the genome level and environmental variation, especially geochemical conditions. Evolutionary genetic analyses further showed evidence that the difference in environmental conditions might be a crucial factor to drive the divergent evolution of A. caldus species. We identified a diverse pool of mobile genetic elements including insertion sequences and genomic islands, which suggests a high frequency of genetic exchange in these harsh habitats. Comprehensive analysis revealed that gene gains and losses were both dominant evolutionary forces that directed the genomic diversification of A. caldus species. For instance, horizontal gene transfer and gene duplication events in group 2 strains might contribute to an increase in microbial DNA content and novel functions. Moreover, genomes undergo extensive changes in group 1 strains such as removal of potential non-functional DNA, which results in the formation of compact and streamlined genomes. Taken together, the findings presented herein show highly frequent gene turnover of A. caldus species that inhabit extremely acidic environments, and shed new light on the contribution of gene turnover to the evolutionary adaptation of acidophiles.

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Comparative Genomics Uncovers Unique Gene Turnover and Evolutionary Rates in a Gene Family Involved in the Detection of Insect Cuticular Pheromones

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