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Metabolic influence of core ciliates within the rumen microbiome
Protozoa comprise a major fraction of the microbial biomass in the rumen microbiome, of which the entodiniomorphs (order: Entodiniomorphida) and holotrichs (order: Vestibuliferida) are consistently observed to be dominant across a diverse genetic and geographical range of ruminant hosts. Despite the...
Autores principales: | , , , , , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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Nature Publishing Group UK
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10284877/ https://www.ncbi.nlm.nih.gov/pubmed/37169869 http://dx.doi.org/10.1038/s41396-023-01407-y |
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author | Andersen, Thea O. Altshuler, Ianina Vera-Ponce de León, Arturo Walter, Juline M. McGovern, Emily Keogh, Kate Martin, Cécile Bernard, Laurence Morgavi, Diego P. Park, Tansol Li, Zongjun Jiang, Yu Firkins, Jeffrey L. Yu, Zhongtang Hvidsten, Torgeir R. Waters, Sinead M. Popova, Milka Arntzen, Magnus Ø. Hagen, Live H. Pope, Phillip B. |
author_facet | Andersen, Thea O. Altshuler, Ianina Vera-Ponce de León, Arturo Walter, Juline M. McGovern, Emily Keogh, Kate Martin, Cécile Bernard, Laurence Morgavi, Diego P. Park, Tansol Li, Zongjun Jiang, Yu Firkins, Jeffrey L. Yu, Zhongtang Hvidsten, Torgeir R. Waters, Sinead M. Popova, Milka Arntzen, Magnus Ø. Hagen, Live H. Pope, Phillip B. |
author_sort | Andersen, Thea O. |
collection | PubMed |
description | Protozoa comprise a major fraction of the microbial biomass in the rumen microbiome, of which the entodiniomorphs (order: Entodiniomorphida) and holotrichs (order: Vestibuliferida) are consistently observed to be dominant across a diverse genetic and geographical range of ruminant hosts. Despite the apparent core role that protozoal species exert, their major biological and metabolic contributions to rumen function remain largely undescribed in vivo. Here, we have leveraged (meta)genome-centric metaproteomes from rumen fluid samples originating from both cattle and goats fed diets with varying inclusion levels of lipids and starch, to detail the specific metabolic niches that protozoa occupy in the context of their microbial co-habitants. Initial proteome estimations via total protein counts and label-free quantification highlight that entodiniomorph species Entodinium and Epidinium as well as the holotrichs Dasytricha and Isotricha comprise an extensive fraction of the total rumen metaproteome. Proteomic detection of protozoal metabolism such as hydrogenases (Dasytricha, Isotricha, Epidinium, Enoploplastron), carbohydrate-active enzymes (Epidinium, Diplodinium, Enoploplastron, Polyplastron), microbial predation (Entodinium) and volatile fatty acid production (Entodinium and Epidinium) was observed at increased levels in high methane-emitting animals. Despite certain protozoal species having well-established reputations for digesting starch, they were unexpectedly less detectable in low methane emitting-animals fed high starch diets, which were instead dominated by propionate/succinate-producing bacterial populations suspected of being resistant to predation irrespective of host. Finally, we reaffirmed our abovementioned observations in geographically independent datasets, thus illuminating the substantial metabolic influence that under-explored eukaryotic populations have in the rumen, with greater implications for both digestion and methane metabolism. |
format | Online Article Text |
id | pubmed-10284877 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Nature Publishing Group UK |
record_format | MEDLINE/PubMed |
spelling | pubmed-102848772023-06-23 Metabolic influence of core ciliates within the rumen microbiome Andersen, Thea O. Altshuler, Ianina Vera-Ponce de León, Arturo Walter, Juline M. McGovern, Emily Keogh, Kate Martin, Cécile Bernard, Laurence Morgavi, Diego P. Park, Tansol Li, Zongjun Jiang, Yu Firkins, Jeffrey L. Yu, Zhongtang Hvidsten, Torgeir R. Waters, Sinead M. Popova, Milka Arntzen, Magnus Ø. Hagen, Live H. Pope, Phillip B. ISME J Article Protozoa comprise a major fraction of the microbial biomass in the rumen microbiome, of which the entodiniomorphs (order: Entodiniomorphida) and holotrichs (order: Vestibuliferida) are consistently observed to be dominant across a diverse genetic and geographical range of ruminant hosts. Despite the apparent core role that protozoal species exert, their major biological and metabolic contributions to rumen function remain largely undescribed in vivo. Here, we have leveraged (meta)genome-centric metaproteomes from rumen fluid samples originating from both cattle and goats fed diets with varying inclusion levels of lipids and starch, to detail the specific metabolic niches that protozoa occupy in the context of their microbial co-habitants. Initial proteome estimations via total protein counts and label-free quantification highlight that entodiniomorph species Entodinium and Epidinium as well as the holotrichs Dasytricha and Isotricha comprise an extensive fraction of the total rumen metaproteome. Proteomic detection of protozoal metabolism such as hydrogenases (Dasytricha, Isotricha, Epidinium, Enoploplastron), carbohydrate-active enzymes (Epidinium, Diplodinium, Enoploplastron, Polyplastron), microbial predation (Entodinium) and volatile fatty acid production (Entodinium and Epidinium) was observed at increased levels in high methane-emitting animals. Despite certain protozoal species having well-established reputations for digesting starch, they were unexpectedly less detectable in low methane emitting-animals fed high starch diets, which were instead dominated by propionate/succinate-producing bacterial populations suspected of being resistant to predation irrespective of host. Finally, we reaffirmed our abovementioned observations in geographically independent datasets, thus illuminating the substantial metabolic influence that under-explored eukaryotic populations have in the rumen, with greater implications for both digestion and methane metabolism. Nature Publishing Group UK 2023-05-11 2023-07 /pmc/articles/PMC10284877/ /pubmed/37169869 http://dx.doi.org/10.1038/s41396-023-01407-y Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Article Andersen, Thea O. Altshuler, Ianina Vera-Ponce de León, Arturo Walter, Juline M. McGovern, Emily Keogh, Kate Martin, Cécile Bernard, Laurence Morgavi, Diego P. Park, Tansol Li, Zongjun Jiang, Yu Firkins, Jeffrey L. Yu, Zhongtang Hvidsten, Torgeir R. Waters, Sinead M. Popova, Milka Arntzen, Magnus Ø. Hagen, Live H. Pope, Phillip B. Metabolic influence of core ciliates within the rumen microbiome |
title | Metabolic influence of core ciliates within the rumen microbiome |
title_full | Metabolic influence of core ciliates within the rumen microbiome |
title_fullStr | Metabolic influence of core ciliates within the rumen microbiome |
title_full_unstemmed | Metabolic influence of core ciliates within the rumen microbiome |
title_short | Metabolic influence of core ciliates within the rumen microbiome |
title_sort | metabolic influence of core ciliates within the rumen microbiome |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10284877/ https://www.ncbi.nlm.nih.gov/pubmed/37169869 http://dx.doi.org/10.1038/s41396-023-01407-y |
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