Characterization of two novel species of the genus Flagellimonas reveals the key role of vertical inheritance in the evolution of alginate utilization loci

ABSTRACT Flavobacteriaceae is the major participant in the degradation of algal polysaccharides. With diverse polysaccharide utilization loci (PULs) and specific carbohydrate-active enzymes (CAZymes), Flavobacteriaceae strains appear to have different abilities in algal polysaccharide degradation and therefore change their roles in the bacterial community. Here, we identified two novel isolates as two novel species of genus Flagellimonas with the names Flagellimonas alginolytica sp. nov. and Flagellimonas cixiensis sp. nov. Furthermore, the comprehensive genomic comparison of 41 Flagellimonas genomes revealed that Flagellimonas strains were diverse in the CAZymes and PUL profiles and exhibited a preference for polysaccharides derived from brown algae. The evolutionary analysis of alginate utilization loci (AUL) in this genus illuminated that the function genes in AULs, that is, PL7 and PL17, were more reliant on the stable inheritance from ancestors associated with gene duplication and loss rather than horizontal gene transfer (HGT) from outside, and the AUL structures exhibited a trend of simplification which resulted in the incidental decrease in alginate degradation ability. This study highlights the important role of vertical inheritance in the evolution of AULs and proves that the discrepancy in AUL structure can arouse phenotypic differences, providing a new perspective on the evolution of AUL and the niche adaptation mechanism of Flavobacteriaceae strains.IMPORTANCEFlavobacteriaceae play an important role in the marine carbon cycle with their noteworthy ability in algal polysaccharides degradation, which is primarily reliant on diverse polysaccharide utilization loci (PULs). Our study highlights the crucial role of vertical inheritance in the evolution of alginate utilization loci (AUL) in Flagellimonas strains and reveals the AUL structural simplification found in Flagellimonas strains that will lead to the reduction of alginate degradation ability. These insights advance understanding of niche adaptation strategy and related evolutionary mechanisms of Flavobacteriaceae strains.