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

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.

SUBMITTER: Zheng Q

PROVIDER: S-EPMC5118931 | biostudies-literature | 2016 Dec

REPOSITORIES: biostudies-literature

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

Zheng Qiang Q Liu Yanting Y Jeanthon Christian C Zhang Rui R Lin Wenxin W Yao Jicheng J Jiao Nianzhi N

Applied and environmental microbiology 20161121 24

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 m ...[more]

PMID: 27736788

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Project description:BACKGROUND: Comparative genomics approaches help to shed light on evolutionary processes that shape differentiation between lineages. The nine-spined stickleback (Pungitius pungitius) is a closely related species of the ecological 'supermodel' three-spined stickleback (Gasterosteus aculeatus). It is an emerging model system for evolutionary biology research but has garnered less attention and lacks extensive genomic resources. To expand on these resources and aid the study of sticklebacks in a phylogenetic framework, we characterized nine-spined stickleback transcriptomes from brain and liver using deep sequencing. RESULTS: We obtained nearly eight thousand assembled transcripts, of which 3,091 were assigned as putative one-to-one orthologs to genes found in the three-spined stickleback. These sequences were used for evaluating overall differentiation and substitution rates between nine- and three-spined sticklebacks, and to identify genes that are putatively evolving under positive selection. The synonymous substitution rate was estimated to be 7.1 × 10(-9) per site per year between the two species, and a total of 165 genes showed patterns of adaptive evolution in one or both species. A few nine-spined stickleback contigs lacked an obvious ortholog in three-spined sticklebacks but were found to match genes in other fish species, suggesting several gene losses within 13 million years since the divergence of the two stickleback species. We identified 47 SNPs in 25 different genes that differentiate pond and marine ecotypes. We also identified 468 microsatellites that could be further developed as genetic markers in nine-spined sticklebacks. CONCLUSION: With deep sequencing of nine-spined stickleback cDNA libraries, our study provides a significant increase in the number of gene sequences and microsatellite markers for this species, and identifies a number of genes showing patterns of adaptive evolution between nine- and three-spined sticklebacks. We also report several candidate genes that might be involved in differential adaptation between marine and freshwater nine-spined sticklebacks. This study provides a valuable resource for future studies aiming to identify candidate genes underlying ecological adaptation in this and other stickleback species.

Dataset Information

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

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Publications

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

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