Physiological and Molecular Understanding of Bacterial Polysaccharide Monooxygenases

Abstract

Bacteria have long been known to secrete enzymes that degrade cellulose and chitin. The degradation of these two polymers predominantly involves two enzyme families that work synergistically with one another: glycoside hydrolases (GHs) and polysaccharide monooxygenases (PMOs). Although bacterial PMOs are a relatively recent addition to the known biopolymer degradation machinery, there is an extensive amount of literature implicating PMO in numerous physiological roles. This review focuses on these diverse and physiological aspects of bacterial PMOs, including facilitating endosymbiosis, conferring a nutritional advantage, and enhancing virulence in pathogenic organisms. We also discuss the correlation between the presence of PMOs and bacterial lifestyle and speculate on the advantages conferred by PMOs under these conditions. In addition, the molecular aspects of bacterial PMOs, as well as the mechanisms regulating PMO expression and the function of additional domains associated with PMOs, are described. We anticipate that increasing research efforts in this field will continue to expand our understanding of the molecular and physiological roles of bacterial PMOs.

Keywords: Listeria monocytogenes; Pseudomonas; cellulolytic enzymes; cellulose; chitin; endosymbionts; infectious disease; monooxygenases; polysaccharides.

FIG 1

The reaction catalyzed by polysaccharide monooxygenases. Oxidation at the C-1 or C-4 position of the glycosidic linkage produces aldonolactones and 4-ketoaldoses, respectively (19, 152). Aldonolactone products are most commonly observed as aldonic acids, and 4-ketoaldoses are most commonly observed as gemdiols. For cellulose, R indicates Glc and R′ indicates OH; for chitin, R indicates GlcNAc, and R′ indicates NHCH₃CO.

FIG 2

Crystal structure of ScLPMO10B from Streptomyces coelicolor (PDB accession number 4OY6) (153). The histidine brace motif, consisting of the two copper-coordinating histidine residues, is shown in the inset. The surface of the protein is shown in light gray and illustrates the flat substrate binding surface.

FIG 3

Bacterial sensing of cellulose and chitin. Bacteria can sense cellulose and chitin through CebR and DasR, respectively. In turn, CebR and DasR regulate the expression of PMOs and other GHs. PMOs cleave cellulose and chitin chains, generating new chain ends more readily accessible by GHs for further degradation.

FIG 4

Putative functions of bacterial PMOs. Following secretion, bacterial PMOs can oxidize a range of polysaccharide substrates, resulting in PMOs being implicated as having various functions, including degrading biomass, being involved in endosymbiotic relationships, and serving as virulence factors of pathogenic bacteria and as antifungal agents, in addition to providing a nutritional source for bacteria.

FIG 5

Sequence alignment of conserved regions of bacterial PMOs. Green highlighting shows copper-coordinating residues, gray highlighting shows conserved residues on the putative substrate binding surface, and purple highlighting shows a conserved aromatic residue by the active site. Numbers indicate the residue of the reference sequence (italics). Shown are bacterial PMOs predicted to oxidize C-1 of cellulose (A), C-1/C-4 of cellulose (B), and chitin (C).