Insights into plant cell wall degradation from the genome sequence of the soil bacterium Cellvibrio japonicus

Abstract

The plant cell wall, which consists of a highly complex array of interconnecting polysaccharides, is the most abundant source of organic carbon in the biosphere. Microorganisms that degrade the plant cell wall synthesize an extensive portfolio of hydrolytic enzymes that display highly complex molecular architectures. To unravel the intricate repertoire of plant cell wall-degrading enzymes synthesized by the saprophytic soil bacterium Cellvibrio japonicus, we sequenced and analyzed its genome, which predicts that the bacterium contains the complete repertoire of enzymes required to degrade plant cell wall and storage polysaccharides. Approximately one-third of these putative proteins (57) are predicted to contain carbohydrate binding modules derived from 13 of the 49 known families. Sequence analysis reveals approximately 130 predicted glycoside hydrolases that target the major structural and storage plant polysaccharides. In common with that of the colonic prokaryote Bacteroides thetaiotaomicron, the genome of C. japonicus is predicted to encode a large number of GH43 enzymes, suggesting that the extensive arabinose decorations appended to pectins and xylans may represent a major nutrient source, not just for intestinal bacteria but also for microorganisms that occupy terrestrial ecosystems. The results presented here predict that C. japonicus possesses an extensive range of glycoside hydrolases, lyases, and esterases. Most importantly, the genome of C. japonicus is remarkably similar to that of the gram-negative marine bacterium, Saccharophagus degradans 2-40(T). Approximately 50% of the predicted C. japonicus plant-degradative apparatus appears to be shared with S. degradans, consistent with the utilization of plant-derived complex carbohydrates as a major substrate by both organisms.

FIG. 1.

Phylogenetic analysis and summary of BLAST results. (A) Consensus maximum-likelihood tree using 12 concatenated protein data sets. The numbers along the branches denote the percent occurrence of nodes among 100 bootstrap replicates. The scale bar represents the number of amino acid substitutions. (B) Distribution of protein percent similarities for the top 25 matching organisms in BLAST searches of the predicted C. japonicus proteome against a database of 382 completely sequenced bacterial genomes.

FIG. 2.

Whole-genome comparison of C. japonicus (A) and three related organisms (B to D). The Venn diagram shows the number of proteins shared (black) or unique (red) within a particular relationship. The large pie chart plots the number of gene sequences by main functional role category for C. japonicus. The small pie chart plots the distribution of predicted hydrolytic enzymes that target the plant cell wall and are shared by C. japonicus and S. degradans.

FIG. 3.

The plant cell wall-degrading apparatus of C. japonicus. The major enzymes that attack the plant cell wall and their sites of action are depicted with arrows. The values in parentheses refer to the predicted number of members that were identified for the corresponding enzyme family in the C. japonicus genome.