Xylan degradation by the human gut Bacteroides xylanisolvens XB1AT involves two distinct gene clusters that are linked at the transcriptional level

Abstract

BackgroundPlant cell wall (PCW) polysaccharides and especially xylans constitute an important part of human diet. Xylans are not degraded by human digestive enzymes in the upper digestive tract and therefore reach the colon where they are subjected to extensive degradation by some members of the symbiotic microbiota. Xylanolytic bacteria are the first degraders of these complex polysaccharides and they release breakdown products that can have beneficial effects on human health. In order to understand better how these bacteria metabolize xylans in the colon, this study was undertaken to investigate xylan breakdown by the prominent human gut symbiont Bacteroides xylanisolvens XB1AT.ResultsTranscriptomic analyses of B. xylanisolvens XB1AT grown on insoluble oat-spelt xylan (OSX) at mid- and late-log phases highlighted genes in a polysaccharide utilization locus (PUL), hereafter called PUL 43, and genes in a fragmentary remnant of another PUL, hereafter referred to as rPUL 70, which were highly overexpressed on OSX relative to glucose. Proteomic analyses supported the up-regulation of several genes belonging to PUL 43 and showed the important over-production of a CBM4-containing GH10 endo-xylanase. We also show that PUL 43 is organized in two operons and that the knockout of the PUL 43 sensor/regulator HTCS gene blocked the growth of the mutant on insoluble OSX and soluble wheat arabinoxylan (WAX). The mutation not only repressed gene expression in the PUL 43 operons but also repressed gene expression in rPUL 70.ConclusionThis study shows that xylan degradation by B. xylanisolvens XB1AT is orchestrated by one PUL and one PUL remnant that are linked at the transcriptional level. Coupled to studies on other xylanolytic Bacteroides species, our data emphasize the importance of one peculiar CBM4-containing GH10 endo-xylanase in xylan breakdown and that this modular enzyme may be used as a functional marker of xylan degradation in the human gut. Our results also suggest that B. xylanisolvens XB1AT has specialized in the degradation of xylans of low complexity. This functional feature may provide a niche to all xylanolytic bacteria harboring similar PULs. Further functional and ecological studies on fibrolytic Bacteroides species are needed to better understand their role in dietary fiber degradation and their impact on intestinal health.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2680-8) contains supplementary material, which is available to authorized users.

Polysaccharide niche partitioning of distinct Polaribacter clades during North Sea spring algal blooms

“…This PUL comprised a GH3 (e.g., xylosidase), a GH10 (e.g., β-xylanase) and two sulfatase genes, together with an adjacent putative PUL containing a GH128 (β-glucanase) and four sulfatases genes. A similar PUL with GH3 and GH10 was shown to be upregulated with xylan in the human gut bacterium Bacteroides xylanisolvens [62]. Xylans are also components of marine phytoplankton [63], and high xylanase activities have been reported for many ocean provinces [64].…”

Polysaccharide Utilization Loci: Fueling Microbial Communities

“…100 PULs; however, strikingly few homologous PULs are shared between them, suggesting that these two symbionts have distinct glycan niches (39). Similarly, recent transcrip-tomic analyses indicated that B. xylanisolvens dynamically responds to discrete structures of pectins and xylans through several differentially regulated PULs (91,92). Such studies reflect the exquisite nutrient adaptation of individual Bacteroidetes bacteria.…”

PULDB: the expanded database of Polysaccharide Utilization Loci

“…Attempts to define PUL boundaries in the absence of expression data were also reported in the genome publication of Capnocytophaga canimorsus Cc5 ( 10 ). Moreover, several specific analyses have focused on the degradation of defined polysaccharides by their corresponding PULs, including plant (fructan ( 11 ), pectin ( 12 ), xylan ( 13 , 14 ), xyloglucan ( 15 ) and type II rhamnogalacturonan (RGII) ( 16 )) and non-plant (α-mannan ( 17 ), galactomannan ( 18 ), 1,6-β-glucan ( 19 ), mucin ( 20 ), sialoglycoconjugates ( 21 ), N-glycan ( 17 , 22 – 24 ), heparin and heparan sulfate ( 25 ), chitin ( 26 ), alginate and laminarin ( 27 )) polysaccharides. To facilitate the retrieval of characterized PULs by their cognate substrate, a new field appears in the PULDB homepage, to search for a given character substring within the PUL substrate labels.…”