Gut microbiome of the largest living rodent harbors unprecedented enzymatic systems to degrade plant polysaccharides

Lucelia Cabral, Gabriela F. Persinoti (), Douglas A. A. Paixão, Marcele P. Martins, Mariana A. B. Morais, Mariana Chinaglia, Mariane N. Domingues, Mauricio L. Sforca, Renan A. S. Pirolla, Wesley C. Generoso, Clelton A. Santos, Lucas F. Maciel, Nicolas Terrapon, Vincent Lombard, Bernard Henrissat and Mario T. Murakami ()
Additional contact information
Lucelia Cabral: Brazilian Center for Research in Energy and Materials
Gabriela F. Persinoti: Brazilian Center for Research in Energy and Materials
Douglas A. A. Paixão: Brazilian Center for Research in Energy and Materials
Marcele P. Martins: Brazilian Center for Research in Energy and Materials
Mariana A. B. Morais: Brazilian Center for Research in Energy and Materials
Mariana Chinaglia: Brazilian Center for Research in Energy and Materials
Mariane N. Domingues: Brazilian Center for Research in Energy and Materials
Mauricio L. Sforca: Brazilian Center for Research in Energy and Materials
Renan A. S. Pirolla: Brazilian Center for Research in Energy and Materials
Wesley C. Generoso: Brazilian Center for Research in Energy and Materials
Clelton A. Santos: Brazilian Center for Research in Energy and Materials
Lucas F. Maciel: Brazilian Center for Research in Energy and Materials
Nicolas Terrapon: The Institut National de la Recherche Agronomique, USC 1408 AFMB
Vincent Lombard: The Institut National de la Recherche Agronomique, USC 1408 AFMB
Bernard Henrissat: Technical University of Denmark
Mario T. Murakami: Brazilian Center for Research in Energy and Materials

Nature Communications, 2022, vol. 13, issue 1, 1-16

Abstract: Abstract The largest living rodent, capybara, can efficiently depolymerize and utilize lignocellulosic biomass through microbial symbiotic mechanisms yet elusive. Herein, we elucidate the microbial community composition, enzymatic systems and metabolic pathways involved in the conversion of dietary fibers into short-chain fatty acids, a main energy source for the host. In this microbiota, the unconventional enzymatic machinery from Fibrobacteres seems to drive cellulose degradation, whereas a diverse set of carbohydrate-active enzymes from Bacteroidetes, organized in polysaccharide utilization loci, are accounted to tackle complex hemicelluloses typically found in gramineous and aquatic plants. Exploring the genetic potential of this community, we discover a glycoside hydrolase family of β-galactosidases (named as GH173), and a carbohydrate-binding module family (named as CBM89) involved in xylan binding that establishes an unprecedented three-dimensional fold among associated modules to carbohydrate-active enzymes. Together, these results demonstrate how the capybara gut microbiota orchestrates the depolymerization and utilization of plant fibers, representing an untapped reservoir of enzymatic mechanisms to overcome the lignocellulose recalcitrance, a central challenge toward a sustainable and bio-based economy.

Date: 2022
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DOI: 10.1038/s41467-022-28310-y

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