Plant N -glycan breakdown by human gut Bacteroides

The major nutrients available to the human colonic microbiota are complex glycans derived from the diet. To degrade this highly variable mix of sugar structures, gut microbes have acquired a huge array of different carbohydrate-active enzymes (CAZymes), predominantly glycoside hydrolases, many of wh...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 119; no. 39; pp. 1 - e2208168119
Main Authors Crouch, Lucy I., Urbanowicz, Paulina A., Baslé, Arnaud, Cai, Zhi-Peng, Liu, Li, Voglmeir, Josef, Melo Diaz, Javier M., Benedict, Samuel T., Spencer, Daniel I. R., Bolam, David N.
Format Journal Article
LanguageEnglish
Published Washington National Academy of Sciences 27.09.2022
Subjects
Allergens
Bacteroides
Biological Sciences
Breakdown
Carbohydrates
Diet
Enzymes
Food allergies
Food plants
Genomes
Glycan
Glycosidases
Glycoside hydrolase
Insects
Intestinal microflora
Mannosidase
Microbiota
N-glycans
Nutrient availability
Nutrients
Plant-based foods
Pollen
Polysaccharides
Proteins
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Summary:The major nutrients available to the human colonic microbiota are complex glycans derived from the diet. To degrade this highly variable mix of sugar structures, gut microbes have acquired a huge array of different carbohydrate-active enzymes (CAZymes), predominantly glycoside hydrolases, many of which have specificities that can be exploited for a range of different applications. Plant N -glycans are prevalent on proteins produced by plants and thus components of the diet, but the breakdown of these complex molecules by the gut microbiota has not been explored. Plant N -glycans are also well characterized allergens in pollen and some plant-based foods, and when plants are used in heterologous protein production for medical applications, the N -glycans present can pose a risk to therapeutic function and stability. Here we use a novel genome association approach for enzyme discovery to identify a breakdown pathway for plant complex N -glycans encoded by a gut Bacteroides species and biochemically characterize five CAZymes involved, including structures of the PNGase and GH92 α-mannosidase. These enzymes provide a toolbox for the modification of plant N -glycans for a range of potential applications. Furthermore, the keystone PNGase also has activity against insect-type N -glycans, which we discuss from the perspective of insects as a nutrient source.
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Author contributions: L.I.C. and D.N.B. designed research; L.I.C., P.A.U., A.B., Z.-P.C., L.L., J.V., J.M.M.D., S.T.B., and D.I.R.S. performed research; L.I.C., P.A.U., A.B., J.V., J.M.M.D., D.I.R.S., and D.N.B. analyzed data; and L.I.C., A.B., D.I.R.S., and D.N.B. wrote the paper.
Edited by Natalie Ahn, University of Colorado Boulder, Boulder, CO; received May 16, 2022; accepted August 15, 2022
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.2208168119