Homologous recombination and gene-specific selection co-shape the vertical nucleotide diversity of mangrove sediment microbial populations.

Mangrove sediments host a diverse array of microbial populations and are characterized by high heterogeneity along their vertical depths. However, the genetic diversity within these populations is largely unknown, hindering our understanding of their adaptive evolution across the sediment depths. To elucidate their genetic diversity, we utilized metagenome sequencing to identify 16 high-frequency microbial populations comprised of two archaea and 14 bacteria from mangrove sediment cores (0-100 cm, with 10 depths) in Qi'ao Island, China. Our analysis of the genome-wide genetic variation revealed extensive nucleotide diversity in the microbial populations. The genes involved in the transport and the energy metabolism displayed a high nucleotide diversity (HND; 0.0045-0.0195; an indicator of shared minor alleles with the microbial populations). By tracking the processes of homologous recombination, we found that each microbial population was subjected to different purification selection levels at different depths (44.12% genes). This selection resulted in significant differences in synonymous/non-synonymous mutation ratio between 0-20 and 20-100 cm layers, indicating the adaptive evolutionary process of microbial populations. Furthermore, our assessment of differentiation in the allele frequencies between these two layers showed that the functional genes involved in the metabolic processes of amino acids or cofactors were highly differential in more than half of them. Together, we showed that the nucleotide diversity of microbial populations was shaped by homologous recombination and gene-specific selection, finally resulting in the stratified differentiation occurring between 0-20 and 20-100 cm. These results enhance our cognition of the microbial adaptation mechanisms to vertical environmental changes during the sedimentation process of coastal blue carbon ecosystems.