Complex pectin metabolism by gut bacteria reveals novel catalytic functions.
The metabolism of carbohydrate polymers drives microbial diversity in the human gut microbiota. It is unclear, however, whether bacterial consortia or single organisms are required to depolymerize highly complex glycans. Here we show that the gut bacterium Bacteroides thetaiotaomicron uses the most structurally complex glycan known: the plant pectic polysaccharide rhamnogalacturonan-II, cleaving all but 1 of its 21 distinct glycosidic linkages. The deconstruction of rhamnogalacturonan-II side chains and backbone are coordinated to overcome steric constraints, and the degradation involves previously undiscovered enzyme families and catalytic activities. The degradation system informs revision of the current structural model of rhamnogalacturonan-II and highlights how individual gut bacteria orchestrate manifold enzymes to metabolize the most challenging glycan in the human diet.
Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle upon Tyne NE2 4HH, U.K.
Didier
D
Ndeh
Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle upon Tyne NE2 4HH, U.K.
Artur
A
Rogowski
Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle upon Tyne NE2 4HH, U.K.
Alan
A
Cartmell
Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle upon Tyne NE2 4HH, U.K.
Ana S
AS
Luis
Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle upon Tyne NE2 4HH, U.K.
Arnaud
A
Baslé
Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle upon Tyne NE2 4HH, U.K.
Joseph
J
Gray
Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle upon Tyne NE2 4HH, U.K.
Immacolata
I
Venditto
Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle upon Tyne NE2 4HH, U.K.
Jonathon
J
Briggs
Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle upon Tyne NE2 4HH, U.K.
Xiaoyang
X
Zhang
Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle upon Tyne NE2 4HH, U.K.
Aurore
A
Labourel
Architecture et Fonction des Macromolécules Biologiques, Centre National de la Recherche Scientifique (CNRS), Aix-Marseille University, F-13288 Marseille, France.
Nicolas
N
Terrapon
INRA, UR1268 Biopolymères Interactions Assemblages, 44300 Nantes, France.
Fanny
F
Buffetto
Department of Biological Chemistry, John Innes Centre Norwich Research Park, Norwich NR4 7UH, UK.
Sergey
S
Nepogodiev
Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor, MI, USA.
Yao
Y
Xiao
Department of Biological Chemistry, John Innes Centre Norwich Research Park, Norwich NR4 7UH, UK.
Robert A
RA
Field
Complex Carbohydrate Research Center, The University of Georgia, 315 Riverbend Road, Athens, GA 30602, USA.
Yanping
Y
Zhu
Complex Carbohydrate Research Center, The University of Georgia, 315 Riverbend Road, Athens, GA 30602, USA.
Malcolm A
MA
O'Neil
Complex Carbohydrate Research Center, The University of Georgia, 315 Riverbend Road, Athens, GA 30602, USA.
Breeana R
BR
Urbanowicz
Complex Carbohydrate Research Center, The University of Georgia, 315 Riverbend Road, Athens, GA 30602, USA.
William S
WS
York
Department of Chemistry, University of York, York YO10 5DD, U.K.
Gideon J
GJ
Davies
Lethbridge Research Centre, Lethbridge, AB, Canada.
D Wade
DW
Abbott
INRA, UR1268 Biopolymères Interactions Assemblages, 44300 Nantes, France.
Marie-Christine
MC
Ralet
Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor, MI, USA.
Eric C
EC
Martens
Architecture et Fonction des Macromolécules Biologiques, Centre National de la Recherche Scientifique (CNRS), Aix-Marseille University, F-13288 Marseille, France.|INRA, USC 1408 AFMB, F-13288 Marseille, France.|Department of Biological Sciences, King Abdulaziz University, Jeddah, Saudi Arabia.
Bernard
B
Henrissat
Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle upon Tyne NE2 4HH, U.K.
Harry J
HJ
Gilbert
D000070077:Bacteroides thetaiotaomicron / Q000201:enzymology* / Q000254:growth & development / Q000378:metabolism*; D055162:Biocatalysis; D001881:Borates / Q000737:chemistry / Q000378:metabolism; D020134:Catalytic Domain; D000069196:Gastrointestinal Microbiome; D041981:Gastrointestinal Tract / Q000382:microbiology*; D006026:Glycoside Hydrolases / Q000737:chemistry / Q000145:classification / Q000378:metabolism*; D006801:Humans; D008958:Models, Molecular; D010368:Pectins / Q000737:chemistry* / Q000378:metabolism*; D013379:Substrate Specificity
D001881:Borates; C042492:rhamnogalacturonan II; D010368:Pectins; D006026:Glycoside Hydrolases