Abstract

The halophilic bacterium Salinibacter ruber is an abundant and ecologically important member of halophilic communities worldwide. Given its broad distribution and high intraspecific genetic diversity, S. ruber is considered one of the main models for ecological and evolutionary studies of bacterial adaptation to hypersaline environments. However, current insights on the genomic diversity of this species is limited to the comparison of the genomes of two co-isolated strains. Here, we present a comparative genomic analysis of eight S. ruber strains isolated at two different time points in each of two different Mediterranean solar salterns. Our results show an open pangenome with contrasting evolutionary patterns in the core and accessory genomes. We found that the core genome is shaped by extensive homologous recombination (HR), which results in limited sequence variation within population clusters. In contrast, the accessory genome is modulated by horizontal gene transfer (HGT), with genomic islands and plasmids acting as gateways to the rest of the genome. In addition, both types of genetic exchange are modulated by restriction and modification (RM) or CRISPR-Cas systems. Finally, genes differentially impacted by such processes reveal functional processes potentially relevant for environmental interactions and adaptation to extremophilic conditions. Altogether, our results support scenarios that conciliate “Neutral” and “Constant Diversity” models of bacterial evolution.

Highlights

  • The genomic and genetic diversification processes that act on prokaryotic species have been extensively studied (Thomas and Nielsen, 2005; Cohan, 2006; Fraser et al, 2007; Vos and Didelot, 2009; Didelot and Maiden, 2010; Polz, 2013)

  • The absence of a clear biogeographical structure, in terms of the genetic divergence between strains from the two sites, represented by clonal frame (CF) distributions, is in line with earlier results based on Pulse Field Gel Electrophoresis (PFGE) patterns (Peña et al, 2005), and MultiLocus Sequence Analysis (MLSA) (Rosselló-Mora et al, 2008)

  • Amongst Clusters of Otologous Groups (COG) involved in “cellular proceses and signaling” and “cellular metabolism” we found significant enrichments (P < 0.05, pFDR < 0.05, Fisher’s test) in functional terms related to glycosylation, “Cell wall/membrane/envelope biogenesis” (COG M) and “Carbohydrate transport and metabolism” (COG G) (Supplementary Table S8), which suggest a role of homologous recombination (HR) in the dynamics of envelope diversity

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Summary

Introduction

The genomic and genetic diversification processes that act on prokaryotic species have been extensively studied (Thomas and Nielsen, 2005; Cohan, 2006; Fraser et al, 2007; Vos and Didelot, 2009; Didelot and Maiden, 2010; Polz, 2013). Salinibacter ruber Genome Variation (Konstantinidis and DeLong, 2008) and hypersaline environments (Podell et al, 2013) Some of these latter studies have revealed that the genetic diversity of microbial species is often organized in the form of cohesive clusters, each composed of strains with genetic similarity above a given threshold, which are differentiated from other clusters by much larger genetic distances. This cluster structure has been suggested to result from the action of homologous recombination (HR), which would constrain levels of genomic sequence divergence within a population cluster. Under this model HR would constrain sequence divergence within a recombining population while increasing the number of transitory unique genetic entities (referred to as the metaclonal scenario)

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