Genomic and transcriptomic analysis of carbohydrate utilization by Paenibacillus sp. JDR-2: systems for bioprocessing plant polysaccharides

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.

Detailed transcriptome analysis of the plant growth promoting Paenibacillus riograndensis SBR5 by using RNA-seq technology

“…JDR-2 revealed a regulatory connection for the utilization of the polysaccharides β-glucan, starch and xylans, while transcription of genes coding for proteins involved in monosaccharide (e.g. arabinose and glucose) utilization was less apparent [ 13 ]. BLASTx analysis revealed 3 sporulation-related genes (P.riograndensis_final_4321, P.riograndensis_final_2316 and P.riograndensis_final_5601) among the most abundantly expressed genes (Table 5 ).…”

“…Recent research efforts on transcriptome characterization in paenibacilli focused on comparative transcriptomic analysis under different plant-related conditions [ 13 , 14 ]. Contrary to these differential transcriptomic analyses, comprehensive transcriptome analysis allows to chart the RNA landscape of a particular organism for improvement of the genome annotation, detection of novel transcripts and conserved sequence motifs such as transcription start sites (TSS), promoters and ribosomal biding sites (RBS) [ 15 , 16 ].…”

Paenibacillus sp. A59 GH10 and GH11 Extracellular Endoxylanases: Application in Biomass Bioconversion

“…The secreted enzymes on xylan hydrolysis had also been studied in other bacteria by proteomic analysis. Other Gram-positive strains secreted different endoxylanases as part of their hemicellulolytic secretome: the GH10-CBM9-CBM22-SLH previously mentioned from Paenibacillus JDR2 was described as the main endoxylanase involved in efficient xylan utilization [49], Bacillus subtilis secreted two endoxylanases (a GH11 and a GH30) after growth in glucuronoxylan [50], the t hermophilic anaerobe Caldicellulosiruptor kronotskyensis [51] secreted a GH10-CBM22 endoxylanase, and the hyperthermophile Thermotoga maritima presented a membrane bound multidomain GH10 endoxylanase as main component of its xylanolytic system [52]. Based on our findings and existing data, a possible hypothesis is that the modular GH10-CBM-SLH endoxylanase could remain adsorbed to the bacterial cell wall by the SLH domains while the CBMs would assist in binding to xylan [53].…”

Comparative genomic analysis of Paenibacillus sp. SSG-1 and its closely related strains reveals the effect of glycometabolism on environmental adaptation

“…For example, Paenibacillus sp. JDR-2 was isolated from the cut stems of sweet gum 35 , and it gained many xylose transport and metabolism related genes (Dataset S3). Seven strain were isolated from milk, and they gained many genes associated with lactose degradation (Dataset S1 and Dataset S3).…”