Fine-scale evolution: genomic, phenotypic and ecological differentiation in two coexisting Salinibacter ruber strains

Abstract

Genomic and metagenomic data indicate a high degree of genomic variation within microbial populations, although the ecological and evolutive meaning of this microdiversity remains unknown. Microevolution analyses, including genomic and experimental approaches, are so far very scarce for non-pathogenic bacteria. In this study, we compare the genomes, metabolomes and selected ecological traits of the strains M8 and M31 of the hyperhalophilic bacterium Salinibacter ruber that contain ribosomal RNA (rRNA) gene and intergenic regions that are identical in sequence and were simultaneously isolated from a Mediterranean solar saltern. Comparative analyses indicate that S. ruber genomes present a mosaic structure with conserved and hypervariable regions (HVRs). The HVRs or genomic islands, are enriched in transposases, genes related to surface properties, strain-specific genes and highly divergent orthologous. However, the many indels outside the HVRs indicate that genome plasticity extends beyond them. Overall, 10% of the genes encoded in the M8 genome are absent from M31 and could stem from recent acquisitions. S. ruber genomes also harbor 34 genes located outside HVRs that are transcribed during standard growth and probably derive from lateral gene transfers with Archaea preceding the M8/M31 divergence. Metabolomic analyses, phage susceptibility and competition experiments indicate that these genomic differences cannot be considered neutral from an ecological perspective. The results point to the avoidance of competition by micro-niche adaptation and response to viral predation as putative major forces that drive microevolution within these Salinibacter strains. In addition, this work highlights the extent of bacterial functional diversity and environmental adaptation, beyond the resolution of the 16S rRNA and internal transcribed spacers regions.

Phaeobacter gallaeciensis genomes from globally opposite locations reveal high similarity of adaptation to surface life

“…Only two loci at the start and end of the chromosomes are inverted. Highly similar gene order and orientation, as well as 94% similarity on the nucleotide and protein level, were also reported for two co-habitating strains of the halophilic bacterium Salinibacter ruber (Pena et al, 2010). In contrast, two strains of Alteromonas macleodii (Ivars-Martinez et al, 2008), isolated from either the Mediterranean Sea or close to Hawaii, revealed a low level of synteny, an average nucleotide identity of only 81.25% and 65% of shared genes.…”

“…Comparative analyses based on the (mostly unfinished) genomes of these isolates emphasized the heterogeneity of this bacterial clade and demonstrated the difficulty to classify and organize roseobacters in terms of ecological or biogeochemical functions (Newton et al, 2010). In contrast, comparative analyses encompassing more closely related organisms have proven to be a valuable approach to assess patterns of differentiation and adaptive strategies (Rocap et al, 2003;Pena et al, 2010;Kalhoefer et al, 2011). Our study thus focused on the genome comparison of two strains of the same species to gain insights into the genomic and phenotypic diversity below the species level (Schloter et al, 2000).…”

Culture-Independent Approaches for Studying Viruses from Hypersaline Environments

“…This has been indeed the case for some of the prokaryotes most frequently retrieved from salterns, such as the haloarchaeon Hqt. walsbyi (13,18,22,31) or the hyperhalophilic bacterium S. ruber (41,43,44). In both cases, in spite of the high degree of conservation of the ribosomal operon, variable areas have been detected in their genomes that very frequently code for proteins that could have a role in phage recognition and evasion.…”

“…However, beyond this low diversity of species compared to that of other aquatic habitats, a considerable level of microdiversity has been found in extremely halophilic prokaryotes (18,31,39,43,44). This microdiversity, i.e., diversity below the species level, is therefore not reflected at the 16S rRNA gene level, which is frequently used to describe prokaryotic diversity in nature.…”

“…However, in these last years, we have witnessed many changes regarding the well-established ideas about their microbiota: from the relatively high presence of active Bacteria (5), the distinctive characteristics of Hqt. walsbyi compared with the previously cultured haloarchaea (13), or the wide pangenome of the hyperhalophiles studied to date (31,39,41,43,44) to new lineages of haloarchaea present in salterns worldwide (37) and the just recently described widespread Nanohaloarchaea (24,35). (The recent description of Nanohaloarchaea raises the question of whether they had ever been counted as VLP, due to their small size).…”