Characterization of Potential Polysaccharide Utilization Systems in the Marine Bacteroidetes Gramella Flava JLT2011 Using a Multi-Omics Approach

Abstract

Members of phylum <i>Bacteroidetes</i> are distributed across diverse marine niches and <i>Flavobacteria</i> is often the predominant bacterial class decomposing algae-derived polysaccharides. Here, we report the complete genome of <i>Gramella flava</i> JLT2011 (<i>Flavobacteria</i>) isolated from surface water of the southeastern Pacific. A remarkable genomic feature is that the number of glycoside hydrolase (GH) genes in the genome of <i>G. flava</i> JLT2011 is more than 2-fold higher than that of other <i>Gramella</i> species. The functional profiles of the GHs suggest extensive variation in <i>Gramella</i> species. Growth experiments revealed that <i>G. flava</i> JLT2011 has the ability to utilize a wide range of polysaccharides for growth such as xylan and homogalacturonan in pectin. Nearly half of all GH genes were located on the multi-gene polysaccharide utilization loci (PUL) or PUL-like systems in <i>G. flava</i> JLT2011. This species was also found to harbor the two xylan PULs and a pectin PUL, respectively. Gene expression data indicated that more GHs and sugar-specific outer-membrane <i>susC-susD</i> systems were found in the presence of xylan than in the presence of pectin, suggesting a different strategy for heteropolymeric xylan and homoglacturonan utilization. Multi-omics data (transcriptomics, proteomics, and metabolomics) indicated that xylan PULs and pectin PUL are respectively involved in the catabolism of their corresponding polysaccharides. This work presents a comparison of polysaccharide decomposition within a genus and expands current knowledge on the diversity and function of PULs in marine <i>Bacteroidetes</i>, thereby deepening our understanding of their ecological role in polysaccharide remineralization in the marine system.