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Sporulation capability and amylosome conservation among diverse human colonic and rumen isolates of the keystone starch‐degrader Ruminococcus bromii

Ruminococcus bromii is a dominant member of the human colonic microbiota that plays a ‘keystone’ role in degrading dietary resistant starch. Recent evidence from one strain has uncovered a unique cell surface ‘amylosome’ complex that organizes starch‐degrading enzymes. New genome analysis presented...

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Autores principales: Mukhopadhya, Indrani, Moraïs, Sarah, Laverde‐Gomez, Jenny, Sheridan, Paul O., Walker, Alan W., Kelly, William, Klieve, Athol V., Ouwerkerk, Diane, Duncan, Sylvia H., Louis, Petra, Koropatkin, Nicole, Cockburn, Darrell, Kibler, Ryan, Cooper, Philip J., Sandoval, Carlos, Crost, Emmanuelle, Juge, Nathalie, Bayer, Edward A., Flint, Harry J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5814915/
https://www.ncbi.nlm.nih.gov/pubmed/29159997
http://dx.doi.org/10.1111/1462-2920.14000
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author Mukhopadhya, Indrani
Moraïs, Sarah
Laverde‐Gomez, Jenny
Sheridan, Paul O.
Walker, Alan W.
Kelly, William
Klieve, Athol V.
Ouwerkerk, Diane
Duncan, Sylvia H.
Louis, Petra
Koropatkin, Nicole
Cockburn, Darrell
Kibler, Ryan
Cooper, Philip J.
Sandoval, Carlos
Crost, Emmanuelle
Juge, Nathalie
Bayer, Edward A.
Flint, Harry J.
author_facet Mukhopadhya, Indrani
Moraïs, Sarah
Laverde‐Gomez, Jenny
Sheridan, Paul O.
Walker, Alan W.
Kelly, William
Klieve, Athol V.
Ouwerkerk, Diane
Duncan, Sylvia H.
Louis, Petra
Koropatkin, Nicole
Cockburn, Darrell
Kibler, Ryan
Cooper, Philip J.
Sandoval, Carlos
Crost, Emmanuelle
Juge, Nathalie
Bayer, Edward A.
Flint, Harry J.
author_sort Mukhopadhya, Indrani
collection PubMed
description Ruminococcus bromii is a dominant member of the human colonic microbiota that plays a ‘keystone’ role in degrading dietary resistant starch. Recent evidence from one strain has uncovered a unique cell surface ‘amylosome’ complex that organizes starch‐degrading enzymes. New genome analysis presented here reveals further features of this complex and shows remarkable conservation of amylosome components between human colonic strains from three different continents and a R. bromii strain from the rumen of Australian cattle. These R. bromii strains encode a narrow spectrum of carbohydrate active enzymes (CAZymes) that reflect extreme specialization in starch utilization. Starch hydrolysis products are taken up mainly as oligosaccharides, with only one strain able to grow on glucose. The human strains, but not the rumen strain, also possess transporters that allow growth on galactose and fructose. R. bromii strains possess a full complement of sporulation and spore germination genes and we demonstrate the ability to form spores that survive exposure to air. Spore formation is likely to be a critical factor in the ecology of this nutritionally highly specialized bacterium, which was previously regarded as ‘non‐sporing’, helping to explain its widespread occurrence in the gut microbiota through the ability to transmit between hosts.
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spelling pubmed-58149152018-02-27 Sporulation capability and amylosome conservation among diverse human colonic and rumen isolates of the keystone starch‐degrader Ruminococcus bromii Mukhopadhya, Indrani Moraïs, Sarah Laverde‐Gomez, Jenny Sheridan, Paul O. Walker, Alan W. Kelly, William Klieve, Athol V. Ouwerkerk, Diane Duncan, Sylvia H. Louis, Petra Koropatkin, Nicole Cockburn, Darrell Kibler, Ryan Cooper, Philip J. Sandoval, Carlos Crost, Emmanuelle Juge, Nathalie Bayer, Edward A. Flint, Harry J. Environ Microbiol Research Articles Ruminococcus bromii is a dominant member of the human colonic microbiota that plays a ‘keystone’ role in degrading dietary resistant starch. Recent evidence from one strain has uncovered a unique cell surface ‘amylosome’ complex that organizes starch‐degrading enzymes. New genome analysis presented here reveals further features of this complex and shows remarkable conservation of amylosome components between human colonic strains from three different continents and a R. bromii strain from the rumen of Australian cattle. These R. bromii strains encode a narrow spectrum of carbohydrate active enzymes (CAZymes) that reflect extreme specialization in starch utilization. Starch hydrolysis products are taken up mainly as oligosaccharides, with only one strain able to grow on glucose. The human strains, but not the rumen strain, also possess transporters that allow growth on galactose and fructose. R. bromii strains possess a full complement of sporulation and spore germination genes and we demonstrate the ability to form spores that survive exposure to air. Spore formation is likely to be a critical factor in the ecology of this nutritionally highly specialized bacterium, which was previously regarded as ‘non‐sporing’, helping to explain its widespread occurrence in the gut microbiota through the ability to transmit between hosts. John Wiley and Sons Inc. 2017-12-07 2018-01 /pmc/articles/PMC5814915/ /pubmed/29159997 http://dx.doi.org/10.1111/1462-2920.14000 Text en © 2017 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution (http://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Articles
Mukhopadhya, Indrani
Moraïs, Sarah
Laverde‐Gomez, Jenny
Sheridan, Paul O.
Walker, Alan W.
Kelly, William
Klieve, Athol V.
Ouwerkerk, Diane
Duncan, Sylvia H.
Louis, Petra
Koropatkin, Nicole
Cockburn, Darrell
Kibler, Ryan
Cooper, Philip J.
Sandoval, Carlos
Crost, Emmanuelle
Juge, Nathalie
Bayer, Edward A.
Flint, Harry J.
Sporulation capability and amylosome conservation among diverse human colonic and rumen isolates of the keystone starch‐degrader Ruminococcus bromii
title Sporulation capability and amylosome conservation among diverse human colonic and rumen isolates of the keystone starch‐degrader Ruminococcus bromii
title_full Sporulation capability and amylosome conservation among diverse human colonic and rumen isolates of the keystone starch‐degrader Ruminococcus bromii
title_fullStr Sporulation capability and amylosome conservation among diverse human colonic and rumen isolates of the keystone starch‐degrader Ruminococcus bromii
title_full_unstemmed Sporulation capability and amylosome conservation among diverse human colonic and rumen isolates of the keystone starch‐degrader Ruminococcus bromii
title_short Sporulation capability and amylosome conservation among diverse human colonic and rumen isolates of the keystone starch‐degrader Ruminococcus bromii
title_sort sporulation capability and amylosome conservation among diverse human colonic and rumen isolates of the keystone starch‐degrader ruminococcus bromii
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5814915/
https://www.ncbi.nlm.nih.gov/pubmed/29159997
http://dx.doi.org/10.1111/1462-2920.14000
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