Xylan utilization in human gut commensal bacteria is orchestrated by unique modular organization of polysaccharide-degrading enzymes

Handle URI:
http://hdl.handle.net/10754/563707
Title:
Xylan utilization in human gut commensal bacteria is orchestrated by unique modular organization of polysaccharide-degrading enzymes
Authors:
Zhang, Meiling; Chekan, Jonathan R.; Dodd, Dylan; Hong, Pei-Ying ( 0000-0002-4474-6600 ) ; Radlinsk, Lauren; Revindran, Vanessa; Nair, Satish K.; Mackie, Roderick Ian; Cann, Isaac Ko O
Abstract:
Enzymes that degrade dietary and host-derived glycans represent the most abundant functional activities encoded by genes unique to the human gut microbiome. However, the biochemical activities of a vast majority of the glycan-degrading enzymes are poorly understood. Here, we use transcriptome sequencing to understand the diversity of genes expressed by the human gut bacteria Bacteroides intestinalis and Bacteroides ovatus grown in monoculture with the abundant dietary polysaccharide xylan. The most highly induced carbohydrate active genes encode a unique glycoside hydrolase (GH) family 10 endoxylanase (BiXyn10A or BACINT-04215 and BACOVA-04390) that is highly conserved in the Bacteroidetes xylan utilization system. The BiXyn10A modular architecture consists of a GH10 catalytic module disrupted by a 250 amino acid sequence of unknown function. Biochemical analysis of BiXyn10A demonstrated that such insertion sequences encode a new family of carbohydrate-binding modules (CBMs) that binds to xy-lose- configured oligosaccharide/polysaccharide ligands, the substrate of the BiXyn10A enzymatic activity. The crystal structures of CBM1 from BiXyn10A (1.8 Å), a cocomplex of BiXyn10A CBM1 with xylohexaose (1.14 Å), and the CBM fromits homolog in the Prevotella bryantii B 14 Xyn10C (1.68 Å) reveal an unanticipated mode for ligand binding. Aminimal enzyme mix, composed of the gene products of four of the most highly up-regulated genes during growth on wheat arabinoxylan, depolymerizes the polysaccharide into its component sugars. The combined biochemical and biophysical studies presented here provide a framework for understanding fiber metabolism by an important group within the commensal bacterial population known to influence human health.
KAUST Department:
Environmental Science and Engineering Program; Water Desalination and Reuse Research Center (WDRC); Biological and Environmental Sciences and Engineering (BESE) Division; Environmental Microbial Safety and Biotechnology Lab
Publisher:
Proceedings of the National Academy of Sciences
Journal:
Proceedings of the National Academy of Sciences
Issue Date:
18-Aug-2014
DOI:
10.1073/pnas.1406156111
PubMed ID:
25136124
PubMed Central ID:
PMC4156774
Type:
Article
ISSN:
00278424
Additional Links:
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4156774
Appears in Collections:
Articles; Environmental Science and Engineering Program; Water Desalination and Reuse Research Center (WDRC); Biological and Environmental Sciences and Engineering (BESE) Division

Full metadata record

DC FieldValue Language
dc.contributor.authorZhang, Meilingen
dc.contributor.authorChekan, Jonathan R.en
dc.contributor.authorDodd, Dylanen
dc.contributor.authorHong, Pei-Yingen
dc.contributor.authorRadlinsk, Laurenen
dc.contributor.authorRevindran, Vanessaen
dc.contributor.authorNair, Satish K.en
dc.contributor.authorMackie, Roderick Ianen
dc.contributor.authorCann, Isaac Ko Oen
dc.date.accessioned2015-08-03T12:07:12Zen
dc.date.available2015-08-03T12:07:12Zen
dc.date.issued2014-08-18en
dc.identifier.issn00278424en
dc.identifier.pmid25136124en
dc.identifier.doi10.1073/pnas.1406156111en
dc.identifier.urihttp://hdl.handle.net/10754/563707en
dc.description.abstractEnzymes that degrade dietary and host-derived glycans represent the most abundant functional activities encoded by genes unique to the human gut microbiome. However, the biochemical activities of a vast majority of the glycan-degrading enzymes are poorly understood. Here, we use transcriptome sequencing to understand the diversity of genes expressed by the human gut bacteria Bacteroides intestinalis and Bacteroides ovatus grown in monoculture with the abundant dietary polysaccharide xylan. The most highly induced carbohydrate active genes encode a unique glycoside hydrolase (GH) family 10 endoxylanase (BiXyn10A or BACINT-04215 and BACOVA-04390) that is highly conserved in the Bacteroidetes xylan utilization system. The BiXyn10A modular architecture consists of a GH10 catalytic module disrupted by a 250 amino acid sequence of unknown function. Biochemical analysis of BiXyn10A demonstrated that such insertion sequences encode a new family of carbohydrate-binding modules (CBMs) that binds to xy-lose- configured oligosaccharide/polysaccharide ligands, the substrate of the BiXyn10A enzymatic activity. The crystal structures of CBM1 from BiXyn10A (1.8 Å), a cocomplex of BiXyn10A CBM1 with xylohexaose (1.14 Å), and the CBM fromits homolog in the Prevotella bryantii B 14 Xyn10C (1.68 Å) reveal an unanticipated mode for ligand binding. Aminimal enzyme mix, composed of the gene products of four of the most highly up-regulated genes during growth on wheat arabinoxylan, depolymerizes the polysaccharide into its component sugars. The combined biochemical and biophysical studies presented here provide a framework for understanding fiber metabolism by an important group within the commensal bacterial population known to influence human health.en
dc.publisherProceedings of the National Academy of Sciencesen
dc.relation.urlhttp://www.ncbi.nlm.nih.gov/pmc/articles/PMC4156774en
dc.subjectGut microbiotaen
dc.subjectHemicelluloseen
dc.subjectHuman nutritionen
dc.subjectRNAseqen
dc.subjectXylanolytic bacteriaen
dc.titleXylan utilization in human gut commensal bacteria is orchestrated by unique modular organization of polysaccharide-degrading enzymesen
dc.typeArticleen
dc.contributor.departmentEnvironmental Science and Engineering Programen
dc.contributor.departmentWater Desalination and Reuse Research Center (WDRC)en
dc.contributor.departmentBiological and Environmental Sciences and Engineering (BESE) Divisionen
dc.contributor.departmentEnvironmental Microbial Safety and Biotechnology Laben
dc.identifier.journalProceedings of the National Academy of Sciencesen
dc.identifier.pmcidPMC4156774en
dc.contributor.institutionEnergy Biosciences Institute, University of Illinois at Urbana-Champaign, Urbana, IL 61801, United Statesen
dc.contributor.institutionInstitute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, United Statesen
dc.contributor.institutionDepartment of Animal Sciences, University of Illinois at Urbana-Champaign, Urbana, IL 61801, United Statesen
dc.contributor.institutionDepartment of Biochemistry, University of Illinois at Urbana-Champaign, Urbana, IL 61801, United Statesen
dc.contributor.institutionDepartment of Microbiology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, United Statesen
dc.contributor.institutionSchool of Life Sciences, East China Normal University, Shanghai 200241, Chinaen
dc.contributor.institutionDepartment of Pathology, Stanford University School of Medicine, Stanford, CA 94304, United Statesen
kaust.authorHong, Pei-Yingen

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