Comparative genomic analysis of Chryseobacterium species: deep insights into plant-growth-promoting and halotolerant capacities

Members of the genus Chryseobacterium have attracted great interest as beneficial bacteria that can promote plant growth and biocontrol. Given the recent risks of climate change, it is important to develop tolerance strategies for efficient applications of plant-beneficial bacteria in saline environments. However, the genetic determinants of plant-growth-promoting and halotolerance effects in Chryseobacterium have not yet been investigated at the genomic level. Here, a comparative genomic analysis was conducted with seven Chryseobacterium species. Phylogenetic and phylogenomic analyses revealed niche-specific evolutionary distances between soil and freshwater Chryseobacterium species, consistent with differences in genomic statistics, indicating that the freshwater bacteria have smaller genome sizes and fewer genes than the soil bacteria. Phosphorus- and zinc-cycling genes (required for nutrient acquisition in plants) were universally present in all species, whereas nitrification and sulphite reduction genes (required for nitrogen- and sulphur-cycling, respectively) were distributed only in soil bacteria. A pan-genome containing 6842 gene clusters was constructed, which reflected the general features of the core, accessory and unique genomes. Halotolerant species with an accessory genome shared a Kdp potassium transporter and biosynthetic pathways for branched-chain amino acids and the carotenoid lycopene, which are associated with countermeasures against salt stress. Protein–protein interaction network analysis was used to define the genetic determinants of Chryseobacterium salivictor NBC122 that reduce salt damage in bacteria and plants. Sixteen hub genes comprised the aromatic compound degradation and Por secretion systems, which are required to cope with complex stresses associated with saline environments. Horizontal gene transfer and CRISPR–Cas analyses indicated that C. salivictor NBC122 underwent more evolutionary events when interacting with different environments. These findings provide deep insights into genomic adaptation to dynamic interactions between plant-growth-promoting Chryseobacterium and salt stress.