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Effect of the macroalgae Asparagopsis taxiformis on methane production and rumen microbiome assemblage

BACKGROUND: Recent studies using batch-fermentation suggest that the red macroalgae Asparagopsis taxiformis has the potential to reduce methane (CH(4)) production from beef cattle by up to ~ 99% when added to Rhodes grass hay; a common feed in the Australian beef industry. These experiments have sho...

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Autores principales: Roque, Breanna Michell, Brooke, Charles Garrett, Ladau, Joshua, Polley, Tamsen, Marsh, Lyndsey Jean, Najafi, Negeen, Pandey, Pramod, Singh, Latika, Kinley, Robert, Salwen, Joan King, Eloe-Fadrosh, Emiley, Kebreab, Ermias, Hess, Matthias
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7803124/
https://www.ncbi.nlm.nih.gov/pubmed/33499933
http://dx.doi.org/10.1186/s42523-019-0004-4
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author Roque, Breanna Michell
Brooke, Charles Garrett
Ladau, Joshua
Polley, Tamsen
Marsh, Lyndsey Jean
Najafi, Negeen
Pandey, Pramod
Singh, Latika
Kinley, Robert
Salwen, Joan King
Eloe-Fadrosh, Emiley
Kebreab, Ermias
Hess, Matthias
author_facet Roque, Breanna Michell
Brooke, Charles Garrett
Ladau, Joshua
Polley, Tamsen
Marsh, Lyndsey Jean
Najafi, Negeen
Pandey, Pramod
Singh, Latika
Kinley, Robert
Salwen, Joan King
Eloe-Fadrosh, Emiley
Kebreab, Ermias
Hess, Matthias
author_sort Roque, Breanna Michell
collection PubMed
description BACKGROUND: Recent studies using batch-fermentation suggest that the red macroalgae Asparagopsis taxiformis has the potential to reduce methane (CH(4)) production from beef cattle by up to ~ 99% when added to Rhodes grass hay; a common feed in the Australian beef industry. These experiments have shown significant reductions in CH(4) without compromising other fermentation parameters (i.e. volatile fatty acid production) with A. taxiformis organic matter (OM) inclusion rates of up to 5%. In the study presented here, A. taxiformis was evaluated for its ability to reduce methane production from dairy cattle fed a mixed ration widely utilized in California, the largest milk producing state in the US. RESULTS: Fermentation in a semi-continuous in-vitro rumen system suggests that A. taxiformis can reduce methane production from enteric fermentation in dairy cattle by 95% when added at a 5% OM inclusion rate without any obvious negative impacts on volatile fatty acid production. High-throughput 16S ribosomal RNA (rRNA) gene amplicon sequencing showed that seaweed amendment effects rumen microbiome consistent with the Anna Karenina hypothesis, with increased β-diversity, over time scales of approximately 3 days. The relative abundance of methanogens in the fermentation vessels amended with A. taxiformis decreased significantly compared to control vessels, but this reduction in methanogen abundance was only significant when averaged over the course of the experiment. Alternatively, significant reductions of CH(4) in the A. taxiformis amended vessels was measured in the early stages of the experiment. This suggests that A. taxiformis has an immediate effect on the metabolic functionality of rumen methanogens whereas its impact on microbiome assemblage, specifically methanogen abundance, is delayed. CONCLUSIONS: The methane reducing effect of A. taxiformis during rumen fermentation makes this macroalgae a promising candidate as a biotic methane mitigation strategy for dairy cattle. But its effect in-vivo (i.e. in dairy cattle) remains to be investigated in animal trials. Furthermore, to obtain a holistic understanding of the biochemistry responsible for the significant reduction of methane, gene expression profiles of the rumen microbiome and the host animal are warranted. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s42523-019-0004-4) contains supplementary material, which is available to authorized users.
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spelling pubmed-78031242021-01-19 Effect of the macroalgae Asparagopsis taxiformis on methane production and rumen microbiome assemblage Roque, Breanna Michell Brooke, Charles Garrett Ladau, Joshua Polley, Tamsen Marsh, Lyndsey Jean Najafi, Negeen Pandey, Pramod Singh, Latika Kinley, Robert Salwen, Joan King Eloe-Fadrosh, Emiley Kebreab, Ermias Hess, Matthias Anim Microbiome Research Article BACKGROUND: Recent studies using batch-fermentation suggest that the red macroalgae Asparagopsis taxiformis has the potential to reduce methane (CH(4)) production from beef cattle by up to ~ 99% when added to Rhodes grass hay; a common feed in the Australian beef industry. These experiments have shown significant reductions in CH(4) without compromising other fermentation parameters (i.e. volatile fatty acid production) with A. taxiformis organic matter (OM) inclusion rates of up to 5%. In the study presented here, A. taxiformis was evaluated for its ability to reduce methane production from dairy cattle fed a mixed ration widely utilized in California, the largest milk producing state in the US. RESULTS: Fermentation in a semi-continuous in-vitro rumen system suggests that A. taxiformis can reduce methane production from enteric fermentation in dairy cattle by 95% when added at a 5% OM inclusion rate without any obvious negative impacts on volatile fatty acid production. High-throughput 16S ribosomal RNA (rRNA) gene amplicon sequencing showed that seaweed amendment effects rumen microbiome consistent with the Anna Karenina hypothesis, with increased β-diversity, over time scales of approximately 3 days. The relative abundance of methanogens in the fermentation vessels amended with A. taxiformis decreased significantly compared to control vessels, but this reduction in methanogen abundance was only significant when averaged over the course of the experiment. Alternatively, significant reductions of CH(4) in the A. taxiformis amended vessels was measured in the early stages of the experiment. This suggests that A. taxiformis has an immediate effect on the metabolic functionality of rumen methanogens whereas its impact on microbiome assemblage, specifically methanogen abundance, is delayed. CONCLUSIONS: The methane reducing effect of A. taxiformis during rumen fermentation makes this macroalgae a promising candidate as a biotic methane mitigation strategy for dairy cattle. But its effect in-vivo (i.e. in dairy cattle) remains to be investigated in animal trials. Furthermore, to obtain a holistic understanding of the biochemistry responsible for the significant reduction of methane, gene expression profiles of the rumen microbiome and the host animal are warranted. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s42523-019-0004-4) contains supplementary material, which is available to authorized users. BioMed Central 2019-02-12 /pmc/articles/PMC7803124/ /pubmed/33499933 http://dx.doi.org/10.1186/s42523-019-0004-4 Text en © The Author(s) 2019, corrected publication March 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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 Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Roque, Breanna Michell
Brooke, Charles Garrett
Ladau, Joshua
Polley, Tamsen
Marsh, Lyndsey Jean
Najafi, Negeen
Pandey, Pramod
Singh, Latika
Kinley, Robert
Salwen, Joan King
Eloe-Fadrosh, Emiley
Kebreab, Ermias
Hess, Matthias
Effect of the macroalgae Asparagopsis taxiformis on methane production and rumen microbiome assemblage
title Effect of the macroalgae Asparagopsis taxiformis on methane production and rumen microbiome assemblage
title_full Effect of the macroalgae Asparagopsis taxiformis on methane production and rumen microbiome assemblage
title_fullStr Effect of the macroalgae Asparagopsis taxiformis on methane production and rumen microbiome assemblage
title_full_unstemmed Effect of the macroalgae Asparagopsis taxiformis on methane production and rumen microbiome assemblage
title_short Effect of the macroalgae Asparagopsis taxiformis on methane production and rumen microbiome assemblage
title_sort effect of the macroalgae asparagopsis taxiformis on methane production and rumen microbiome assemblage
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7803124/
https://www.ncbi.nlm.nih.gov/pubmed/33499933
http://dx.doi.org/10.1186/s42523-019-0004-4
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