title: Xylan degradation by the human gut Bacteroides xylanisolvens XB1A(T) involves two distinct gene clusters that are linked at the transcriptional level.
abstract: Plant 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 XB1A(T).
  
  
  
  Transcriptomic analyses of B. xylanisolvens XB1A(T) 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.
  
  
  
  This study shows that xylan degradation by B. xylanisolvens XB1A(T) 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 XB1A(T) 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.
authors.affiliation: Institut National de la recherche Agronomique (INRA), UR454 Microbiologie, Centre de Clermont-Ferrand-Theix, 63122, Saint-Genès-Champanelle, France.
authors.forename: Jordane
authors.initials: J
authors.lastname: Despres
authors.affiliation: Institut National de la recherche Agronomique (INRA), UR454 Microbiologie, Centre de Clermont-Ferrand-Theix, 63122, Saint-Genès-Champanelle, France.
authors.forename: Evelyne
authors.initials: E
authors.lastname: Forano
authors.affiliation: Institut National de la recherche Agronomique (INRA), UR454 Microbiologie, Centre de Clermont-Ferrand-Theix, 63122, Saint-Genès-Champanelle, France.
authors.forename: Pascale
authors.initials: P
authors.lastname: Lepercq
authors.affiliation: Institut National de la recherche Agronomique (INRA), UR454 Microbiologie, Centre de Clermont-Ferrand-Theix, 63122, Saint-Genès-Champanelle, France.
authors.forename: Sophie
authors.initials: S
authors.lastname: Comtet-Marre
authors.affiliation: Institut National de la recherche Agronomique (INRA), UR454 Microbiologie, Centre de Clermont-Ferrand-Theix, 63122, Saint-Genès-Champanelle, France.
authors.forename: Gregory
authors.initials: G
authors.lastname: Jubelin
authors.affiliation: INRA, Plate-forme d'Exploration du Métabolisme, 63122, Saint-Genès Champanelle, France.
authors.forename: Christophe
authors.initials: C
authors.lastname: Chambon
authors.affiliation: Department of Animal and Range Sciences, Montana State University, Bozeman, MT, 59718, USA.
authors.forename: Carl J
authors.initials: CJ
authors.lastname: Yeoman
authors.affiliation: Department of Animal Sciences, University of Illinois at Urbana-Champaign, Urbana, IL, USA.
authors.forename: Margaret E
authors.initials: ME
authors.lastname: Berg Miller
authors.affiliation: Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA.
authors.forename: Christopher J
authors.initials: CJ
authors.lastname: Fields
authors.affiliation: Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor, MI, 48109, USA.
authors.forename: Eric
authors.initials: E
authors.lastname: Martens
authors.affiliation: Architecture et Fonction des Macromolécules Biologiques (AFMB), UMR 7257 CNRS, Université Aix-Marseille, 163 Avenue de Luminy, 13288, Marseille, France.|INRA, USC 1408 AFMB, 13288, Marseille, France.
authors.forename: Nicolas
authors.initials: N
authors.lastname: Terrapon
authors.affiliation: Architecture et Fonction des Macromolécules Biologiques (AFMB), UMR 7257 CNRS, Université Aix-Marseille, 163 Avenue de Luminy, 13288, Marseille, France.|INRA, USC 1408 AFMB, 13288, Marseille, France.|Department of Biological Sciences, King Abdulaziz University, Jeddah, Saudi Arabia.
authors.forename: Bernard
authors.initials: B
authors.lastname: Henrissat
authors.affiliation: Department of Animal Sciences, University of Illinois at Urbana-Champaign, Urbana, IL, USA.|Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA.
authors.forename: Bryan A
authors.initials: BA
authors.lastname: White
authors.affiliation: Institut National de la recherche Agronomique (INRA), UR454 Microbiologie, Centre de Clermont-Ferrand-Theix, 63122, Saint-Genès-Champanelle, France. pascale.mosoni@clermont.inra.fr.
authors.forename: Pascale
authors.initials: P
authors.lastname: Mosoni
mesh_terms: D001426:Bacterial Proteins / Q000235:genetics* / Q000378:metabolism; D001439:Bacteroides / Q000235:genetics / Q000254:growth & development* / Q000378:metabolism; D041981:Gastrointestinal Tract / Q000382:microbiology; D020869:Gene Expression Profiling / Q000379:methods*; D015964:Gene Expression Regulation, Bacterial; D006801:Humans; D005810:Multigene Family; D009876:Operon; D010940:Plant Proteins / Q000378:metabolism; D040901:Proteomics / Q000379:methods; D017423:Sequence Analysis, RNA / Q000379:methods*; D014990:Xylans / Q000378:metabolism*
chemical_list: D001426:Bacterial Proteins; D010940:Plant Proteins; D014990:Xylans
keywords: Bacteroides; CAZymes; Human gut; Mutagenesis; Polysaccharide-Utilization Locus; Proteomics; RNA-seq; Xylan degradation