Geographic Impact on Genomic Divergence as Revealed by Comparison of Nine Citromicrobial Genomes

Abstract

ABSTRACT Aerobic anoxygenic phototrophic bacteria (AAPB) are thought to be important players in oceanic carbon and energy cycling in the euphotic zone of the ocean. The genus Citromicrobium , widely found in oligotrophic oceans, is a member of marine alphaproteobacterial AAPB. Nine Citromicrobium strains isolated from the South China Sea, the Mediterranean Sea, or the tropical South Atlantic Ocean were found to harbor identical 16S rRNA sequences. The sequencing of their genomes revealed high synteny in major regions. Nine genetic islands (GIs) involved mainly in type IV secretion systems, flagellar biosynthesis, prophage, and integrative conjugative elements, were identified by a fine-scale comparative genomics analysis. These GIs played significant roles in genomic evolution and divergence. Interestingly, the coexistence of two different photosynthetic gene clusters (PGCs) was not only found in the analyzed genomes but also confirmed, for the first time, to our knowledge, in environmental samples. The prevalence of the coexistence of two different PGCs may suggest an adaptation mechanism for Citromicrobium members to survive in the oceans. Comparison of genomic characteristics (e.g., GIs, average nucleotide identity [ANI], single-nucleotide polymorphisms [SNPs], and phylogeny) revealed that strains within a marine region shared a similar evolutionary history that was distinct from that of strains isolated from other regions (South China Sea versus Mediterranean Sea). Geographic differences are partly responsible for driving the observed genomic divergences and allow microbes to evolve through local adaptation. Three Citromicrobium strains isolated from the Mediterranean Sea diverged millions of years ago from other strains and evolved into a novel group. IMPORTANCE Aerobic anoxygenic phototrophic bacteria are a widespread functional group in the upper ocean, and their abundance could be up to 15% of the total heterotrophic bacteria. To date, a great number of studies display AAPB biogeographic distribution patterns in the ocean; however, little is understood about the geographic isolation impact on the genome divergence of marine AAPB. In this study, we compare nine Citromicrobium genomes of strains that have identical 16S rRNA sequences but different ocean origins. Our results reveal that strains isolated from the same marine region share a similar evolutionary history that is distinct from that of strains isolated from other regions. These Citromicrobium strains diverged millions of years ago. In addition, the coexistence of two different PGCs is prevalent in the analyzed genomes and in environmental samples.