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Cellulosomics, a Gene-Centric Approach to Investigating the Intraspecific Diversity and Adaptation of Ruminococcus flavefaciens within the Rumen

BACKGROUND: The bovine rumen maintains a diverse microbial community that serves to break down indigestible plant substrates. However, those bacteria specifically adapted to degrade cellulose, the major structural component of plant biomass, represent a fraction of the rumen microbiome. Previously,...

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Autores principales: Brulc, Jennifer M., Yeoman, Carl J., Wilson, Melissa K., Berg Miller, Margret E., Jeraldo, Patricio, Jindou, Sadanari, Goldenfeld, Nigel, Flint, Harry J., Lamed, Raphael, Borovok, Ilya, Vodovnik, Maša, Nelson, Karen E., Bayer, Edward A., White, Bryan A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2011
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3197198/
https://www.ncbi.nlm.nih.gov/pubmed/22043282
http://dx.doi.org/10.1371/journal.pone.0025329
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author Brulc, Jennifer M.
Yeoman, Carl J.
Wilson, Melissa K.
Berg Miller, Margret E.
Jeraldo, Patricio
Jindou, Sadanari
Goldenfeld, Nigel
Flint, Harry J.
Lamed, Raphael
Borovok, Ilya
Vodovnik, Maša
Nelson, Karen E.
Bayer, Edward A.
White, Bryan A.
author_facet Brulc, Jennifer M.
Yeoman, Carl J.
Wilson, Melissa K.
Berg Miller, Margret E.
Jeraldo, Patricio
Jindou, Sadanari
Goldenfeld, Nigel
Flint, Harry J.
Lamed, Raphael
Borovok, Ilya
Vodovnik, Maša
Nelson, Karen E.
Bayer, Edward A.
White, Bryan A.
author_sort Brulc, Jennifer M.
collection PubMed
description BACKGROUND: The bovine rumen maintains a diverse microbial community that serves to break down indigestible plant substrates. However, those bacteria specifically adapted to degrade cellulose, the major structural component of plant biomass, represent a fraction of the rumen microbiome. Previously, we proposed scaC as a candidate for phylotyping Ruminococcus flavefaciens, one of three major cellulolytic bacterial species isolated from the rumen. In the present report we examine the dynamics and diversity of scaC-types both within and between cattle temporally, following a dietary switch from corn-silage to grass-legume hay. These results were placed in the context of the overall bacterial population dynamics measured using the 16S rRNA. PRINCIPAL FINDINGS: As many as 117 scaC-types were estimated, although just nineteen were detected in each of three rumens tested, and these collectively accounted for the majority of all types present. Variation in scaC populations was observed between cattle, between planktonic and fiber-associated fractions and temporally over the six-week survey, and appeared related to scaC phylogeny. However, by the sixth week no significant separation of scaC populations was seen between animals, suggesting enrichment of a constrained set of scaC-types. Comparing the amino-acid translation of each scaC-type revealed sequence variation within part of the predicted dockerin module but strong conservation in the N-terminus, where the cohesin module is located. CONCLUSIONS: The R. flavefaciens species comprises a multiplicity of scaC-types in-vivo. Enrichment of particular scaC-types temporally, following a dietary switch, and between fractions along with the phylogenetic congruence suggests that functional differences exist between types. Observed differences in dockerin modules suggest at least part of the functional heterogeneity may be conferred by scaC. The polymorphic nature of scaC enables the relative distribution of R. flavefaciens strains to be examined and represents a gene-centric approach to investigating the intraspecific adaptation of an important specialist population.
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spelling pubmed-31971982011-10-31 Cellulosomics, a Gene-Centric Approach to Investigating the Intraspecific Diversity and Adaptation of Ruminococcus flavefaciens within the Rumen Brulc, Jennifer M. Yeoman, Carl J. Wilson, Melissa K. Berg Miller, Margret E. Jeraldo, Patricio Jindou, Sadanari Goldenfeld, Nigel Flint, Harry J. Lamed, Raphael Borovok, Ilya Vodovnik, Maša Nelson, Karen E. Bayer, Edward A. White, Bryan A. PLoS One Research Article BACKGROUND: The bovine rumen maintains a diverse microbial community that serves to break down indigestible plant substrates. However, those bacteria specifically adapted to degrade cellulose, the major structural component of plant biomass, represent a fraction of the rumen microbiome. Previously, we proposed scaC as a candidate for phylotyping Ruminococcus flavefaciens, one of three major cellulolytic bacterial species isolated from the rumen. In the present report we examine the dynamics and diversity of scaC-types both within and between cattle temporally, following a dietary switch from corn-silage to grass-legume hay. These results were placed in the context of the overall bacterial population dynamics measured using the 16S rRNA. PRINCIPAL FINDINGS: As many as 117 scaC-types were estimated, although just nineteen were detected in each of three rumens tested, and these collectively accounted for the majority of all types present. Variation in scaC populations was observed between cattle, between planktonic and fiber-associated fractions and temporally over the six-week survey, and appeared related to scaC phylogeny. However, by the sixth week no significant separation of scaC populations was seen between animals, suggesting enrichment of a constrained set of scaC-types. Comparing the amino-acid translation of each scaC-type revealed sequence variation within part of the predicted dockerin module but strong conservation in the N-terminus, where the cohesin module is located. CONCLUSIONS: The R. flavefaciens species comprises a multiplicity of scaC-types in-vivo. Enrichment of particular scaC-types temporally, following a dietary switch, and between fractions along with the phylogenetic congruence suggests that functional differences exist between types. Observed differences in dockerin modules suggest at least part of the functional heterogeneity may be conferred by scaC. The polymorphic nature of scaC enables the relative distribution of R. flavefaciens strains to be examined and represents a gene-centric approach to investigating the intraspecific adaptation of an important specialist population. Public Library of Science 2011-10-17 /pmc/articles/PMC3197198/ /pubmed/22043282 http://dx.doi.org/10.1371/journal.pone.0025329 Text en Brulc et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Brulc, Jennifer M.
Yeoman, Carl J.
Wilson, Melissa K.
Berg Miller, Margret E.
Jeraldo, Patricio
Jindou, Sadanari
Goldenfeld, Nigel
Flint, Harry J.
Lamed, Raphael
Borovok, Ilya
Vodovnik, Maša
Nelson, Karen E.
Bayer, Edward A.
White, Bryan A.
Cellulosomics, a Gene-Centric Approach to Investigating the Intraspecific Diversity and Adaptation of Ruminococcus flavefaciens within the Rumen
title Cellulosomics, a Gene-Centric Approach to Investigating the Intraspecific Diversity and Adaptation of Ruminococcus flavefaciens within the Rumen
title_full Cellulosomics, a Gene-Centric Approach to Investigating the Intraspecific Diversity and Adaptation of Ruminococcus flavefaciens within the Rumen
title_fullStr Cellulosomics, a Gene-Centric Approach to Investigating the Intraspecific Diversity and Adaptation of Ruminococcus flavefaciens within the Rumen
title_full_unstemmed Cellulosomics, a Gene-Centric Approach to Investigating the Intraspecific Diversity and Adaptation of Ruminococcus flavefaciens within the Rumen
title_short Cellulosomics, a Gene-Centric Approach to Investigating the Intraspecific Diversity and Adaptation of Ruminococcus flavefaciens within the Rumen
title_sort cellulosomics, a gene-centric approach to investigating the intraspecific diversity and adaptation of ruminococcus flavefaciens within the rumen
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3197198/
https://www.ncbi.nlm.nih.gov/pubmed/22043282
http://dx.doi.org/10.1371/journal.pone.0025329
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