Abstract
BackgroundPolysaccharides comprising plant biomass are potential resources for conversion to fuels and chemicals. These polysaccharides include xylans derived from the hemicellulose of hardwoods and grasses, soluble β-glucans from cereals and starch as the primary form of energy storage in plants. Paenibacillus sp. JDR-2 (Pjdr2) has evolved a system for bioprocessing xylans. The central component of this xylan utilization system is a multimodular glycoside hydrolase family 10 (GH10) endoxylanase with carbohydrate binding modules (CBM) for binding xylans and surface layer homology (SLH) domains for cell surface anchoring. These attributes allow efficient utilization of xylans by generating oligosaccharides proximal to the cell surface for rapid assimilation. Coordinate expression of genes in response to growth on xylans has identified regulons contributing to depolymerization, importation of oligosaccharides and intracellular processing to generate xylose as well as arabinose and methylglucuronate. The genome of Pjdr2 encodes several other putative surface anchored multimodular enzymes including those for utilization of β-1,3/1,4 mixed linkage soluble glucan and starch.ResultsTo further define polysaccharide utilization systems in Pjdr2, its transcriptome has been determined by RNA sequencing following growth on barley-derived soluble β-glucan, starch, cellobiose, maltose, glucose, xylose and arabinose. The putative function of genes encoding transcriptional regulators, ABC transporters, and glycoside hydrolases belonging to the corresponding substrate responsive regulon were deduced by their coordinate expression and locations in the genome. These results are compared to observations from the previously defined xylan utilization systems in Pjdr2. The findings from this study show that Pjdr2 efficiently utilizes these glucans in a manner similar to xylans. From transcriptomic and genomic analyses we infer a common strategy evolved by Pjdr2 for efficient bioprocessing of polysaccharides.ConclusionsThe barley β-glucan and starch utilization systems in Pjdr2 include extracellular glycoside hydrolases bearing CBM and SLH domains for depolymerization of these polysaccharides. Overlapping regulation observed during growth on these polysaccharides suggests they are preferentially utilized in the order of starch before xylan before barley β-glucan. These systems defined in Pjdr2 may serve as a paradigm for developing biocatalysts for efficient bioprocessing of plant biomass to targeted biofuels and chemicals.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2436-5) contains supplementary material, which is available to authorized users.
Highlights
Polysaccharides comprising plant biomass are potential resources for conversion to fuels and chemicals
The sample preparation and RNA sequencing (RNA-seq) data acquisition portions of this work overlap with a recently published xylan utilization transcriptome and the results presented here are compared with this earlier work to provide perspective, draw conclusions and identify themes which define the efficient manner in which Paenibacillus sp. JDR-2 (Pjdr2) utilizes polysaccharides [1]
The saccharides used in the study that provided the final comparative data set include barley βglucan (B) and cellobiose (C) representing β-configured glucans, starch (S) and maltose (M) representing αconfigured glucans, sweetgum glucuronoxylan (SG) and sorghum glucuronoarabinoxylan (SO) representing different xylan types and the constituent monosaccharides of these polysaccharides, including glucose (G), xylose (X) and arabinose (A)
Summary
Polysaccharides comprising plant biomass are potential resources for conversion to fuels and chemicals. The central component of this xylan utilization system is a multimodular glycoside hydrolase family 10 (GH10) endoxylanase with carbohydrate binding modules (CBM) for binding xylans and surface layer homology (SLH) domains for cell surface anchoring These attributes allow efficient utilization of xylans by generating oligosaccharides proximal to the cell surface for rapid assimilation. Previous studies showed that growth on minimal media supplemented with polymeric xylan was preferred to that on simple sugars such as xylose, glucose, or arabinose [1, 2] These studies indicated that efficient xylan utilization is attributable, in part, to a 157 kDa GH10 β-1,4-endoxylanase (Xyn10A1) containing carbohydrate binding modules (CBM) for binding to polysaccharides and surface layer homology (SLH) domains for cell-association. These early findings suggest that Pjdr utilizes glucuronoxylan in a vectorial manner with an unidentified mechanism for coupling surface localized polymer hydrolysis to rapid oligoxyloside transport into the cell
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