Homologous Recombination in Core Genomes Facilitates Marine Bacterial Adaptation

Abstract

Acquisition of ecologically relevant genes is common among ocean bacteria, but whether it has a major impact on genome evolution in marine environments remains unknown. Here, we analyzed the core genomes of 16 phylogenetically diverse and ecologically relevant bacterioplankton lineages, each consisting of up to five genomes varying at the strain level. Statistical approaches identified from each lineage up to ∼50 loci showing anomalously high divergence at synonymous sites, which is best explained by recombination with distantly related organisms. The enriched gene categories in these outlier loci match well with the characteristics previously identified as the key phenotypes of these lineages. Examples are antibiotic synthesis and detoxification in , exopolysaccharide production in, hydrocarbon degradation in , and cold adaptation in Intriguingly, the outlier loci feature polysaccharide catabolism in but not in, consistent with their primary habitat preferences in macroalga and beach sands respectively. Likewise, analysis of showed that photosynthesis related genes listed in the outlier loci are only found in high-light adapted ecotype but not in the low-light adapted ecotype. These observations strongly suggest that recombination with distant relatives is a key mechanism driving the ecological diversification among marine bacterial lineages. Acquisition of new metabolic genes has been known as an important mechanism driving bacterial evolution and adaptation in the ocean, but acquisition of novel alleles of existing genes and its potential ecological role has not been examined. Guided by population genetic theories, our genomic analysis showed that divergent allele acquisition is prevalent in phylogenetically diverse marine bacterial lineages and that the affected loci often encode metabolic functions that underlies the known ecological roles of the lineages under study.

Comparative Genomics Reveals Broad Genetic Diversity, Extensive Recombination and Nascent Ecological Adaptation in Micrococcus luteus

“…The results above are consistent with the high proportion of admixture inferred from population assignment and numerous insertion sequences and transposases detected in the genomes, which could allow frequent gene exchange between M. luteus strains and other organisms. Recombination has been proved as an important driver of the evolution of most prokaryotes, and acquisition of novel alleles of existing genes will also accelerate ecological adaptation of bacterial populations [72][73][74].…”

Unexpectedly high mutation rate of a deep-sea hyperthermophilic anaerobic archaeon

“…The S of each gene family was obtained by averaging all pairwise ds values, and then the median S across all single-copy gene families together with μ were used to calculate the Ne. We used the median S instead of the mean value, because loci showing unusually large dS as a result of allelic replacement via homologous recombination with divergent lineages are common in bacterial species 54 , which are expected to bias the mean value but have a limited effect on the median value across gene loci.…”

A hydrogen‐oxidizing bacterium enriched from the open ocean resembling a symbiont

“…Recombination with distant relatives is a crucial mechanism for the adaptation to different environments and the emergence of diverse marine bacteria. In similar genomic core regions of various marine bacterial lineages, very contrastive recombination patterns have been detected, presumably due to recombination with distantly related organisms (Sun and Luo, 2018). These identified gene sections encode for functions that are beneficial for the bacterium's survival in a given habitat (e.g., antibiotic synthesis or cold adaptation) (Sun and Luo, 2018).…”

“…In similar genomic core regions of various marine bacterial lineages, very contrastive recombination patterns have been detected, presumably due to recombination with distantly related organisms (Sun and Luo, 2018). These identified gene sections encode for functions that are beneficial for the bacterium's survival in a given habitat (e.g., antibiotic synthesis or cold adaptation) (Sun and Luo, 2018). Another important mechanism for horizontal gene transfer in the marine environment that can affect bacterial community diversity is bacteriophage-mediated horizontal transduction (Jiang and Paul, 1998).…”