A polysaccharide utilization locus from the gut bacterium dysgonomonas mossii encodes functionally distinct carbohydrate esterases
Journal article, 2021

The gut microbiota plays a central role in human health by enzymatically degrading dietary fiber and concomitantly excreting short chain fatty acids that are associated with manifold health benefits. The polysaccharide xylan is abundant in dietary fiber but noncarbohydrate decorations hinder efficient cleavage by glycoside hydrolases (GHs) and need to be addressed by carbohydrate esterases (CEs). Enzymes from carbohydrate esterase families 1 and 6 (CE1 and 6) perform key roles in xylan degradation by removing feruloyl and acetate decorations, yet little is known about these enzyme families especially with regard to their diversity in activity. Bacteroidetes bacteria are dominant members of the microbiota and often encode their carbohydrate-active enzymes in multigene polysaccharide utilization loci (PULs). Here we present the characterization of three CEs found in a PUL encoded by the gut Bacteroidete Dysgonomonas mossii. We demonstrate that the CEs are functionally distinct, with one highly efficient CE6 acetyl esterase and two CE1 enzymes with feruloyl esterase activities. One multidomain CE1 enzyme contains two CE1 domains: an N-terminal domain feruloyl esterase, and a C-terminal domain with minimal activity on model substrates. We present the structure of the C-terminal CE1 domain with the carbohydrate-binding module that bridges the two CE1 domains, as well as a complex of the same protein fragment with methyl ferulate. The investment of D. mossii in producing multiple CEs suggests that improved accessibility of xylan for GHs and cleavage of covalent polysaccharide-polysaccharide and lignin-polysaccharide bonds are important enzyme activities in the gut environment.

Author

Cathleen Kmezik

Chalmers, Biology and Biological Engineering, Industrial Biotechnology

Scott Mazurkewich

Chalmers, Biology and Biological Engineering, Industrial Biotechnology

Tomke Meents

Lauren S McKee

AlbaNova University Center

Wallenberg Wood Science Center (WWSC)

Alexander Idström

Chalmers, Chemistry and Chemical Engineering, Applied Chemistry, Lars Evenäs Group

Marina Armeni

Chalmers, Biology and Biological Engineering, Systems and Synthetic Biology, CMSI

Otto Savolainen

University of Eastern Finland

Chalmers, Biology and Biological Engineering, Systems and Synthetic Biology, CMSI

Gisela Brändén

University of Gothenburg

Johan Larsbrink

Chalmers, Biology and Biological Engineering, Industrial Biotechnology

Wallenberg Wood Science Center (WWSC)

Journal of Biological Chemistry

0021-9258 (ISSN) 1083-351X (eISSN)

Vol. 296 100500

Development of a consolidated bioprocess for conversion of plant biomass to versatile chemical building blocks

Swedish Research Council (VR) (2016-03931), 2017-01-01 -- 2020-12-31.

Novo Nordisk Foundation (NNF17OC0027648), 2018-01-01 -- 2020-12-31.

ÅForsk (17-345), 2017-07-01 -- 2018-05-31.

Subject Categories

Biochemistry and Molecular Biology

Structural Biology

Biocatalysis and Enzyme Technology

Areas of Advance

Materials Science

DOI

10.1016/j.jbc.2021.100500

PubMed

33667545

More information

Latest update

5/5/2021 2