1. In Vivo Competitions between Fibrobacter succinogenes , Ruminococcus flavefaciens , and Ruminoccus albus in a Gnotobiotic Sheep Model Revealed by Multi-Omic Analyses
- Author
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Pascale Lepercq, Bryan A. White, Philippe Ruiz, Pascale Mosoni, Evelyne Forano, Carl J. Yeoman, Christopher J. Fields, Montana State University (MSU), Eastern Illinois University, Toulouse Biotechnology Institute (TBI), Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Institut National des Sciences Appliquées (INSA)-Université Fédérale Toulouse Midi-Pyrénées-Institut National des Sciences Appliquées (INSA)-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Microbiologie Environnement Digestif Santé (MEDIS), Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Clermont Auvergne (UCA), MEDIS laboratory (INRAE France) Roy J. Carver Biotechnology Center Montana Agricultural Experiment Station MONB00113National Institute of General Medical Sciences of the National Institutes of Health (NIH-NIGMS) P20GM103474U.S. Beef W4177MONB00195, University of Illinois at Urbana-Champaign [Urbana], University of Illinois System, Institut National des Sciences Appliquées (INSA)-Université de Toulouse (UT)-Institut National des Sciences Appliquées (INSA)-Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Carl R. Woese Institute of Genomic Biology, University of Illinois System-University of Illinois System, University of Illinois College of Medicine, MEDIS laboratory (INRAE France) Roy J. Carver Biotechnology Center Montana Agricultural Experiment Station MONB00113 National Institute of General Medical Sciences of the National Institutes of Health (NIH-NIGMS) P20GM103474 U.S. Beef W4177 MONB00195, and Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)
- Subjects
animal structures ,[SDV]Life Sciences [q-bio] ,Population ,Cellulase ,Microbiology ,03 medical and health sciences ,Rumen ,fluids and secretions ,cellulose degradation ,Virology ,Metabolome ,Food science ,education ,gnotobiotic animal model ,030304 developmental biology ,2. Zero hunger ,0303 health sciences ,education.field_of_study ,rumen ,Fibrobacter succinogenes ,biology ,030306 microbiology ,food and beverages ,biology.organism_classification ,QR1-502 ,[SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology ,pili IV ,biology.protein ,Xylanase ,Fermentation ,Bacteria ,CAZymes ,outer membrane vesicles ,Research Article - Abstract
Ruminant animals, including cattle and sheep, depend on their rumen microbiota to digest plant biomass and convert it into absorbable energy. Considering that the extent of meat and milk production depends on the efficiency of the microbiota to deconstruct plant cell walls, the functionality of predominant rumen cellulolytic bacteria, Fibrobacter succinogenes, Ruminococcus albus, and Ruminococcus flavefaciens, has been extensively studied in vitro to obtain a better knowledge of how they operate to hydrolyze polysaccharides and ultimately find ways to enhance animal production., Fibrobacter succinogenes, Ruminococcus albus, and Ruminococcus flavefaciens are the three predominant cellulolytic bacterial species found in the rumen. In vitro studies have shown that these species compete for adherence to, and growth upon, cellulosic biomass. Yet their molecular interactions in vivo have not heretofore been examined. Gnotobiotically raised lambs harboring a 17-h-old immature microbiota devoid of culturable cellulolytic bacteria and methanogens were inoculated first with F. succinogenes S85 and Methanobrevibacter sp. strain 87.7, and 5 months later, the lambs were inoculated with R. albus 8 and R. flavefaciens FD-1. Longitudinal samples were collected and profiled for population dynamics, gene expression, fibrolytic enzyme activity, in sacco fibrolysis, and metabolite profiling. Quantitative PCR, metagenome and metatranscriptome data show that F. succinogenes establishes at high levels initially but is gradually outcompeted following the introduction of the ruminococci. This shift resulted in an increase in carboxymethyl cellulase (CMCase) and xylanase activities but not in greater fibrolysis, suggesting that F. succinogenes and ruminococci deploy different but equally effective means to degrade plant cell walls. Expression profiles showed that F. succinogenes relied upon outer membrane vesicles and a diverse repertoire of CAZymes, while R. albus and R. flavefaciens preferred type IV pili and either CBM37-harboring or cellulosomal carbohydrate-active enzymes (CAZymes), respectively. The changes in cellulolytics also affected the rumen metabolome, including an increase in acetate and butyrate at the expense of propionate. In conclusion, this study provides the first demonstration of in vivo competition between the three predominant cellulolytic bacteria and provides insight on the influence of these ecological interactions on rumen fibrolytic function and metabolomic response.
- Published
- 2021