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Maximizing efficiency of rumen microbial protein production

Rumen microbes produce cellular protein inefficiently partly because they do not direct all ATP toward growth. They direct some ATP toward maintenance functions, as long-recognized, but they also direct ATP toward reserve carbohydrate synthesis and energy spilling (futile cycles that dissipate heat)...

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Autores principales: Hackmann, Timothy J., Firkins, Jeffrey L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4432691/
https://www.ncbi.nlm.nih.gov/pubmed/26029197
http://dx.doi.org/10.3389/fmicb.2015.00465
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author Hackmann, Timothy J.
Firkins, Jeffrey L.
author_facet Hackmann, Timothy J.
Firkins, Jeffrey L.
author_sort Hackmann, Timothy J.
collection PubMed
description Rumen microbes produce cellular protein inefficiently partly because they do not direct all ATP toward growth. They direct some ATP toward maintenance functions, as long-recognized, but they also direct ATP toward reserve carbohydrate synthesis and energy spilling (futile cycles that dissipate heat). Rumen microbes expend ATP by vacillating between (1) accumulation of reserve carbohydrate after feeding (during carbohydrate excess) and (2) mobilization of that carbohydrate thereafter (during carbohydrate limitation). Protozoa account for most accumulation of reserve carbohydrate, and in competition experiments, protozoa accumulated nearly 35-fold more reserve carbohydrate than bacteria. Some pure cultures of bacteria spill energy, but only recently have mixed rumen communities been recognized as capable of the same. When these communities were dosed glucose in vitro, energy spilling could account for nearly 40% of heat production. We suspect that cycling of glycogen (a major reserve carbohydrate) is a major mechanism of spilling; such cycling has already been observed in single-species cultures of protozoa and bacteria. Interconversions of short-chain fatty acids (SCFA) may also expend ATP and depress efficiency of microbial protein production. These interconversions may involve extensive cycling of intermediates, such as cycling of acetate during butyrate production in certain butyrivibrios. We speculate this cycling may expend ATP directly or indirectly. By further quantifying the impact of reserve carbohydrate accumulation, energy spilling, and SCFA interconversions on growth efficiency, we can improve prediction of microbial protein production and guide efforts to improve efficiency of microbial protein production in the rumen.
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spelling pubmed-44326912015-05-29 Maximizing efficiency of rumen microbial protein production Hackmann, Timothy J. Firkins, Jeffrey L. Front Microbiol Microbiology Rumen microbes produce cellular protein inefficiently partly because they do not direct all ATP toward growth. They direct some ATP toward maintenance functions, as long-recognized, but they also direct ATP toward reserve carbohydrate synthesis and energy spilling (futile cycles that dissipate heat). Rumen microbes expend ATP by vacillating between (1) accumulation of reserve carbohydrate after feeding (during carbohydrate excess) and (2) mobilization of that carbohydrate thereafter (during carbohydrate limitation). Protozoa account for most accumulation of reserve carbohydrate, and in competition experiments, protozoa accumulated nearly 35-fold more reserve carbohydrate than bacteria. Some pure cultures of bacteria spill energy, but only recently have mixed rumen communities been recognized as capable of the same. When these communities were dosed glucose in vitro, energy spilling could account for nearly 40% of heat production. We suspect that cycling of glycogen (a major reserve carbohydrate) is a major mechanism of spilling; such cycling has already been observed in single-species cultures of protozoa and bacteria. Interconversions of short-chain fatty acids (SCFA) may also expend ATP and depress efficiency of microbial protein production. These interconversions may involve extensive cycling of intermediates, such as cycling of acetate during butyrate production in certain butyrivibrios. We speculate this cycling may expend ATP directly or indirectly. By further quantifying the impact of reserve carbohydrate accumulation, energy spilling, and SCFA interconversions on growth efficiency, we can improve prediction of microbial protein production and guide efforts to improve efficiency of microbial protein production in the rumen. Frontiers Media S.A. 2015-05-15 /pmc/articles/PMC4432691/ /pubmed/26029197 http://dx.doi.org/10.3389/fmicb.2015.00465 Text en Copyright © 2015 Hackmann and Firkins. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Hackmann, Timothy J.
Firkins, Jeffrey L.
Maximizing efficiency of rumen microbial protein production
title Maximizing efficiency of rumen microbial protein production
title_full Maximizing efficiency of rumen microbial protein production
title_fullStr Maximizing efficiency of rumen microbial protein production
title_full_unstemmed Maximizing efficiency of rumen microbial protein production
title_short Maximizing efficiency of rumen microbial protein production
title_sort maximizing efficiency of rumen microbial protein production
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4432691/
https://www.ncbi.nlm.nih.gov/pubmed/26029197
http://dx.doi.org/10.3389/fmicb.2015.00465
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