Abstract
The rapidly increasing availability of complete bacterial genomes has created new opportunities for reconstructing bacterial evolution, but it has also highlighted the difficulty to fully understand the genomic and functional variations occurring among different lineages. Using the class Epsilonproteobacteria as a case study, we investigated the composition, flexibility, and function of its pan-genomes. Models were constructed to extrapolate the expansion of pan-genomes at three different taxonomic levels. The results show that, for Epsilonproteobacteria the seemingly large genome variations among strains of the same species are less noticeable when compared with groups at higher taxonomic ranks, indicating that genome stability is imposed by the potential existence of taxonomic boundaries. The analyses of pan-genomes has also defined a set of universally conserved core genes, based on which a phylogenetic tree was constructed to confirm that thermophilic species from deep-sea hydrothermal vents represent the most ancient lineages of Epsilonproteobacteria. Moreover, by comparing the flexible genome of a chemoautotrophic deep-sea vent species to (1) genomes of species belonging to the same genus, but inhabiting different environments, and (2) genomes of other vent species, but belonging to different genera, we were able to delineate the relative importance of lineage-specific versus niche-specific genes. This result not only emphasizes the overall importance of phylogenetic proximity in shaping the variable part of the genome, but also highlights the adaptive functions of niche-specific genes. Overall, by modeling the expansion of pan-genomes and analyzing core and flexible genes, this study provides snapshots on how the complex processes of gene acquisition, conservation, and removal affect the evolution of different species, and contribute to the metabolic diversity and versatility of Epsilonproteobacteria.
Highlights
The evolution of bacterial genomes is characterized by a massive amount of insertions, deletions, and rearrangements, permitting the differentiation and adaptation of evolutionarily related lineages into vastly diverse environments (Romero and Palacios, 1997; Cohan, 2001; Mira et al, 2002; Reams and Neidle, 2003)
In order to compare the pan-genomes of different taxonomic ranks, we constructed regression models for five groups of Epsilonproteobacteria that correspond to three different levels of taxonomy (Table S1): two groups representing strains of same species, two representing species of same genera, and one representing different species of the entire class
The recognition of bacterial pan-genomes has resulted in discussions regarding the bacterial species concept
Summary
The evolution of bacterial genomes is characterized by a massive amount of insertions, deletions, and rearrangements, permitting the differentiation and adaptation of evolutionarily related lineages into vastly diverse environments (Romero and Palacios, 1997; Cohan, 2001; Mira et al, 2002; Reams and Neidle, 2003). The fact that strains within a single species can have widely different repertoires of genes has highlighted the complexity in identifying bacterial species. The universally conserved 16S ribosomal RNA (rRNA) gene has been widely used to assess the phylogenetic diversity and, by inference, even the functional diversity of microbes in environmental samples. Various studies have demonstrated substantial genomic variations among strains that differ only slightly in 16S rRNA sequences (Coleman et al, 2006; Rasko et al, 2008; Tettelin et al, 2008). A genome-scale understanding of how genes evolve and what determines the acquisition and deletion of genes is essential for mapping the complete genetic variations of bacteria, while at the same time assisting in the classification and functional identification of bacterial species
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