Divergence in gene regulation contributes to sympatric speciation of Shewanella baltica strains.

Abstract

Niche partitioning and sequence evolution drive genomic and phenotypic divergence, which ultimately leads to bacterial diversification. This study investigated genomic composition of two Shewanella baltica clades previously identified through multi-locus sequencing typing and recovered from the redox transition zone in the central Baltic Sea. Comparative genomic analysis revealed significantly higher inter- than intra-clade genomic dissimilarity, and that a subset of genes present in Clade A were associated with potential adaptation to respiration of sulfur compounds present in the redox-transition zone. Transcriptomic divergence between two representative strains of Clades A and D, OS185 and OS195, was also characterized and revealed marked regulatory differences. We found that both transcriptional divergence of shared genes and expression of strain-specific genes lead to differences in regulatory patterns between strains that correlate with environmental redox niches. For instance, under anoxic conditions of respiratory nitrate ammonification, OS185 - the strain isolated from nitrate-rich environment, upregulated nearly twice the number of shared genes compared to OS195 - the strain isolated from H2S-containing anoxic environment. Conversely, OS195 showed stronger induction of strain-specific genes, especially those associated with sulfur compound respiration, under thiosulfate-reducing conditions. A positive association between the level of transcriptional divergence and sequence divergence for shared genes was also noted. Our results provide further support for the hypothesis that genomic changes impacting transcriptional regulation play an important role in the diversification of ecologically distinct populations.Importance This study examined potential mechanisms through which co-occurring Shewanella baltica strains diversified to form ecologically distinct populations. At the time of isolation, the strains studied composed the major fraction of culturable nitrate-reducing communities in the Baltica Sea. Analysis of genomic content of 13 S. baltica strains from two clades representing different ecotypes demonstrated that one clade specifically possesses a number of genes that could favor successful adaptation to respire sulfur compounds in the portion of the water column from which these strains were isolated. In addition, transcriptional profiling of fully-sequenced strains representative of these two clades, OS185 and OS195, under oxygen-, nitrate- and thiosulfate-respiring conditions demonstrated that the strains exhibit relatively similar transcriptional responses during aerobic growth, but more distinct transcriptional responses under nitrate and thiosulfate-respiring conditions. Results from this study provide insights into how genomic and gene regulatory diversification together impacted the redox specialization of the S. baltica strains.