A 1,3-1,4-β-Glucan Utilization Regulon in Paenibacillus sp Strain JDR-2

Paenibacillus sp. strain JDR-2 (Paenibacillus JDR-2) secretes a multimodular cell-associated glycoside hydrolase family 10 (GH10) endoxylanase (XynA10A(1)) that catalyzes the depolymerization of methylglucuronoxylan (MeGX(n)) and rapidly assimilates the products of depolymerization. Efficient utilization of MeGXn has been postulated to result from the coupling of the processes of exocellular depolymerization and assimilation of oligosaccharide products, followed by intracellular metabolism. Growth and substrate utilization patterns with barley glucan and laminarin similar to those observed with MeGXn as a substrate suggest similar processes for 1,3-1,4-beta-glucan and 1,3-beta-glucan depolymerization and product assimilation. The Paenibacillus JDR-2 genome includes a cluster of genes encoding a secreted multimodular GH16 beta-glucanase (Bgl16A(1)) containing surface layer homology (SLH) domains, a secreted GH16 beta-glucanase with only a catalytic domain (Bgl16A(2)), transporter proteins, and transcriptional regulators. Recombinant Bgl16A(1) and Bgl16A(2) catalyze the formation of trisaccharides, tetrasaccharides, and larger oligosaccharides from barley glucan and of mono-, di-, tri-, and tetrasaccharides and larger oligosaccharides from laminarin. The lack of accumulation of depolymerization products during growth and a marked preference for polymeric glucan over depolymerization products support a process coupling extracellular depolymerization, assimilation, and intracellular metabolism for beta-glucans similar to that ascribed to the GH10/GH67 xylan utilization system in Paenibacillus JDR-2. Coordinate expression of genes encoding GH16 beta-glucanases, transporters, and transcriptional regulators supports their role as a regulon for the utilization of soluble beta-glucans. As in the case of the xylan utilization regulons, this soluble beta-glucan regulon provides advantages in the growth rate and yields on polymeric substrates and may be exploited for the efficient conversion of plant-derived polysaccharides to targeted products.