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Title: Comparative Genomics of Rumen Butyrivibrio spp. Uncovers a Continuum of Polysaccharide-Degrading Capabilities

Abstract

Plant polysaccharide breakdown by microbes in the rumen is fundamental to digestion in ruminant livestock. Bacterial species belonging to the rumen genera Butyrivibrio and Pseudobutyrivibrio are important degraders and utilizers of lignocellulosic plant material. These bacteria degrade polysaccharides and ferment the released monosaccharides to yield short-chain fatty acids that are used by the ruminant for growth and the production of meat, milk, and fiber products. Although rumen Butyrivibrio and Pseudobutyrivibrio species are regarded as common rumen inhabitants, their polysaccharide-degrading and carbohydrate-utilizing enzymes are not well understood. In this study, we analyzed the genomes of 40 Butyrivibrio and 6 Pseudobutyrivibrio strains isolated from the plant-adherent fraction of New Zealand dairy cows to explore the polysaccharide-degrading potential of these important rumen bacteria. Comparative genome analyses combined with phylogenetic analysis of their 16S rRNA genes and short-chain fatty acid production patterns provide insight into the genomic diversity and physiology of these bacteria and divide Butyrivibrio into 3 species clusters. Rumen Butyrivibrio bacteria were found to encode a large and diverse spectrum of degradative carbohydrate-active enzymes (CAZymes) and binding proteins. In total, 4,421 glycoside hydrolases (GHs), 1,283 carbohydrate esterases (CEs), 110 polysaccharide lyases (PLs), 3,605 glycosyltransferases (GTs), and 1,706 carbohydrate-binding protein modules (CBM) withmore » predicted activities involved in the depolymerization and transport of the insoluble plant polysaccharides were identified. Butyrivibrio genomes had similar patterns of CAZyme families but varied greatly in the number of genes within each category in the Carbohydrate-Active Enzymes database (CAZy), suggesting some level of functional redundancy. These results suggest that rumen Butyrivibrio species occupy similar niches but apply different degradation strategies to be able to coexist in the rumen.« less

Authors:
 [1];  [2];  [1];  [3];  [1]; ORCiD logo [4];  [1]
+ Show Author Affiliations
  1. AgResearch Limited, Palmerston North (New Zealand)
  2. Donvis Limited, Palmerston North (New Zealand)
  3. Agriculture and Food (CSIRO), St. Lucia, QLD (Australia)
  4. Massey Univ., Palmerston North (New Zealand)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); New Zealand Ministry of Business, Innovation and Employment New Economy Research Fund; New Zealand Government
OSTI Identifier:
1626066
Grant/Contract Number:  
AC02-05CH11231; C10X0803
Resource Type:
Accepted Manuscript
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Volume: 86; Journal Issue: 1; Journal ID: ISSN 0099-2240
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; biotechnology & applied microbiology; microbiology; rumen; bacteria; polysaccharide; butyrivibrio; pseudobutyrivibrio; genome; cazy; enolase

Citation Formats

Palevich, Nikola, Kelly, William J., Leahy, Sinead C., Denman, Stuart, Altermann, Eric, Rakonjac, Jasna, and Attwood, Graeme T. Comparative Genomics of Rumen Butyrivibrio spp. Uncovers a Continuum of Polysaccharide-Degrading Capabilities. United States: N. p., 2019. Web. doi:10.1128/aem.01993-19.
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Palevich, Nikola, Kelly, William J., Leahy, Sinead C., Denman, Stuart, Altermann, Eric, Rakonjac, Jasna, & Attwood, Graeme T. Comparative Genomics of Rumen Butyrivibrio spp. Uncovers a Continuum of Polysaccharide-Degrading Capabilities. United States. https://doi.org/10.1128/aem.01993-19
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Palevich, Nikola, Kelly, William J., Leahy, Sinead C., Denman, Stuart, Altermann, Eric, Rakonjac, Jasna, and Attwood, Graeme T. Fri . "Comparative Genomics of Rumen Butyrivibrio spp. Uncovers a Continuum of Polysaccharide-Degrading Capabilities". United States. https://doi.org/10.1128/aem.01993-19. https://www.osti.gov/servlets/purl/1626066.
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@article{osti_1626066,
title = {Comparative Genomics of Rumen Butyrivibrio spp. Uncovers a Continuum of Polysaccharide-Degrading Capabilities},
author = {Palevich, Nikola and Kelly, William J. and Leahy, Sinead C. and Denman, Stuart and Altermann, Eric and Rakonjac, Jasna and Attwood, Graeme T.},
abstractNote = {Plant polysaccharide breakdown by microbes in the rumen is fundamental to digestion in ruminant livestock. Bacterial species belonging to the rumen genera Butyrivibrio and Pseudobutyrivibrio are important degraders and utilizers of lignocellulosic plant material. These bacteria degrade polysaccharides and ferment the released monosaccharides to yield short-chain fatty acids that are used by the ruminant for growth and the production of meat, milk, and fiber products. Although rumen Butyrivibrio and Pseudobutyrivibrio species are regarded as common rumen inhabitants, their polysaccharide-degrading and carbohydrate-utilizing enzymes are not well understood. In this study, we analyzed the genomes of 40 Butyrivibrio and 6 Pseudobutyrivibrio strains isolated from the plant-adherent fraction of New Zealand dairy cows to explore the polysaccharide-degrading potential of these important rumen bacteria. Comparative genome analyses combined with phylogenetic analysis of their 16S rRNA genes and short-chain fatty acid production patterns provide insight into the genomic diversity and physiology of these bacteria and divide Butyrivibrio into 3 species clusters. Rumen Butyrivibrio bacteria were found to encode a large and diverse spectrum of degradative carbohydrate-active enzymes (CAZymes) and binding proteins. In total, 4,421 glycoside hydrolases (GHs), 1,283 carbohydrate esterases (CEs), 110 polysaccharide lyases (PLs), 3,605 glycosyltransferases (GTs), and 1,706 carbohydrate-binding protein modules (CBM) with predicted activities involved in the depolymerization and transport of the insoluble plant polysaccharides were identified. Butyrivibrio genomes had similar patterns of CAZyme families but varied greatly in the number of genes within each category in the Carbohydrate-Active Enzymes database (CAZy), suggesting some level of functional redundancy. These results suggest that rumen Butyrivibrio species occupy similar niches but apply different degradation strategies to be able to coexist in the rumen.},
doi = {10.1128/aem.01993-19},
journal = {Applied and Environmental Microbiology},
number = 1,
volume = 86,
place = {United States},
year = {2019},
month = {12}
}
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The Use of Semi-solid Agar for the Detection of Bacterial Motility
journal, June 1936

Molecular profiling of microbial community structure and their CAZymes via metagenomics, from Tsomgo lake in the Eastern Himalayas
journal, April 2021

Alcohol pretreatment of stools effect on culturomics
journal, March 2020

Hierarchical Grouping to Optimize an Objective Function
journal, March 1963

NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins
journal, January 2007

  • Pruitt, K. D.; Tatusova, T.; Maglott, D. R.
  • Nucleic Acids Research, Vol. 35, Issue Database
  • DOI: 10.1093/nar/gkl842

Fine-scale population structure and evidence for local adaptation in Australian giant black tiger shrimp (Penaeus monodon) using SNP analysis
journal, September 2020

R: A Language for Data Analysis and Graphics
journal, September 1996

Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes
journal, May 2014

  • Kim, M.; Oh, H. -S.; Park, S. -C.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 64, Issue Pt 5
  • DOI: 10.1099/ijs.0.064931-0
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