Hydrogen cross-feeding among rumen biohydrogenation, propionogenesis and methanogenesis drives the milk fatty acid profile in dairy goats

Rumen microbial biohydrogenation (RBH) is the major factor responsible for the bovine milk rich in saturated fatty acids (FAs). Here, we evaluated the effects of nutritional manipulation of ruminal propionogenesis and methanogenesis, two primary hydrogen sinks, on the RBH and milk FA profiles in viv...

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Main Authors: Jinlei Tan, Yuqi Wu, Huixin Dong, Shuaishuai Li, Huai Jiang, Qingyan Yin, Junhu Yao, Zongjun Li
Format: Article
Language:English
Published: Cambridge University Press 2024-01-01
Series:Animal Nutriomics
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Online Access:https://www.cambridge.org/core/product/identifier/S297737762400022X/type/journal_article
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author Jinlei Tan
Yuqi Wu
Huixin Dong
Shuaishuai Li
Huai Jiang
Qingyan Yin
Junhu Yao
Zongjun Li
author_facet Jinlei Tan
Yuqi Wu
Huixin Dong
Shuaishuai Li
Huai Jiang
Qingyan Yin
Junhu Yao
Zongjun Li
author_sort Jinlei Tan
collection DOAJ
description Rumen microbial biohydrogenation (RBH) is the major factor responsible for the bovine milk rich in saturated fatty acids (FAs). Here, we evaluated the effects of nutritional manipulation of ruminal propionogenesis and methanogenesis, two primary hydrogen sinks, on the RBH and milk FA profiles in vivo and in vitro using three propionogenesis enhancers (fumarate [FUM], biotin and monensin) and one methanogenesis inhibitor (N-[2-(nitrooxy)ethyl]-3-pyridinecarboxamide [NPD]). The in vivo results showed that inclusion of FUM in lactating dairy goat diet could protect dietary unsaturated FAs against RBH with increased proportions of C18:2n − 6 (by 33.5%), C18:3n − 3 (by 38.1%) and RBH intermediates (e.g. trans-10 C18:1 and trans-11 C18:1) in rumen contents. Additionally, FUM supplementation increased the milk Δ9 desaturase index (by 15.5%) with higher cis-9 monounsaturated FAs in the milk. As a result, FUM increased the proportions of polyunsaturated and monounsaturated FAs in the milk with lower atherogenicity index (by −15.3%) and thrombogenicity index (by −19.5%). Conversely, supplementing NPD increased RBH completeness (by 7.4%) with higher milk atherogenicity index (by 10.5%) and thrombogenicity index (by 8.7%). The adverse effects of NPD on the milk FA profiles can be eliminated when supplemented in combination with FUM. The metagenomic analyses showed that neither FUM nor NPD affect the rumen microbial α- or β-diversity at the strain or gene level. The in vitro study showed that the conversion rate of FUM to propionate was increased from 54.7% to 80.6% when FUM supplemented in combination with biotin and monensin, resulting a higher anti-RBH potential. Accordingly, manipulation of ruminal methanogenesis and propionogenesis can redirect hydrogen toward or away from RBH and thereby influence the milk FA profiles. FUM is a promising feed additive in ruminant not only to reduce the methane emissions as previously proved but also to improve the nutritional desirability of the milk FA profiles for human health.
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publishDate 2024-01-01
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record_format Article
series Animal Nutriomics
spelling doaj-art-b83916e4ed9a4e1ab0eff84dd2ec088e2025-08-20T03:40:28ZengCambridge University PressAnimal Nutriomics2977-37762977-37842024-01-01110.1017/anr.2024.22Hydrogen cross-feeding among rumen biohydrogenation, propionogenesis and methanogenesis drives the milk fatty acid profile in dairy goatsJinlei Tan0Yuqi Wu1Huixin Dong2Shuaishuai Li3Huai Jiang4Qingyan Yin5Junhu Yao6Zongjun Li7https://orcid.org/0000-0002-8986-3472College of Animal Science and Technology, Northwest A&F University, Yangling, ChinaCollege of Animal Science and Technology, Northwest A&F University, Yangling, ChinaCollege of Animal Science and Technology, Northwest A&F University, Yangling, ChinaCollege of Animal Science and Technology, Northwest A&F University, Yangling, ChinaCollege of Animal Science and Technology, Northwest A&F University, Yangling, ChinaCollege of Animal Science and Technology, Northwest A&F University, Yangling, ChinaCollege of Animal Science and Technology, Northwest A&F University, Yangling, ChinaCollege of Animal Science and Technology, Northwest A&F University, Yangling, ChinaRumen microbial biohydrogenation (RBH) is the major factor responsible for the bovine milk rich in saturated fatty acids (FAs). Here, we evaluated the effects of nutritional manipulation of ruminal propionogenesis and methanogenesis, two primary hydrogen sinks, on the RBH and milk FA profiles in vivo and in vitro using three propionogenesis enhancers (fumarate [FUM], biotin and monensin) and one methanogenesis inhibitor (N-[2-(nitrooxy)ethyl]-3-pyridinecarboxamide [NPD]). The in vivo results showed that inclusion of FUM in lactating dairy goat diet could protect dietary unsaturated FAs against RBH with increased proportions of C18:2n − 6 (by 33.5%), C18:3n − 3 (by 38.1%) and RBH intermediates (e.g. trans-10 C18:1 and trans-11 C18:1) in rumen contents. Additionally, FUM supplementation increased the milk Δ9 desaturase index (by 15.5%) with higher cis-9 monounsaturated FAs in the milk. As a result, FUM increased the proportions of polyunsaturated and monounsaturated FAs in the milk with lower atherogenicity index (by −15.3%) and thrombogenicity index (by −19.5%). Conversely, supplementing NPD increased RBH completeness (by 7.4%) with higher milk atherogenicity index (by 10.5%) and thrombogenicity index (by 8.7%). The adverse effects of NPD on the milk FA profiles can be eliminated when supplemented in combination with FUM. The metagenomic analyses showed that neither FUM nor NPD affect the rumen microbial α- or β-diversity at the strain or gene level. The in vitro study showed that the conversion rate of FUM to propionate was increased from 54.7% to 80.6% when FUM supplemented in combination with biotin and monensin, resulting a higher anti-RBH potential. Accordingly, manipulation of ruminal methanogenesis and propionogenesis can redirect hydrogen toward or away from RBH and thereby influence the milk FA profiles. FUM is a promising feed additive in ruminant not only to reduce the methane emissions as previously proved but also to improve the nutritional desirability of the milk FA profiles for human health.https://www.cambridge.org/core/product/identifier/S297737762400022X/type/journal_articledairy goatfumaratemethanogenesis inhibitormilk fatty acid profilerumen biohydrogenation
spellingShingle Jinlei Tan
Yuqi Wu
Huixin Dong
Shuaishuai Li
Huai Jiang
Qingyan Yin
Junhu Yao
Zongjun Li
Hydrogen cross-feeding among rumen biohydrogenation, propionogenesis and methanogenesis drives the milk fatty acid profile in dairy goats
Animal Nutriomics
dairy goat
fumarate
methanogenesis inhibitor
milk fatty acid profile
rumen biohydrogenation
title Hydrogen cross-feeding among rumen biohydrogenation, propionogenesis and methanogenesis drives the milk fatty acid profile in dairy goats
title_full Hydrogen cross-feeding among rumen biohydrogenation, propionogenesis and methanogenesis drives the milk fatty acid profile in dairy goats
title_fullStr Hydrogen cross-feeding among rumen biohydrogenation, propionogenesis and methanogenesis drives the milk fatty acid profile in dairy goats
title_full_unstemmed Hydrogen cross-feeding among rumen biohydrogenation, propionogenesis and methanogenesis drives the milk fatty acid profile in dairy goats
title_short Hydrogen cross-feeding among rumen biohydrogenation, propionogenesis and methanogenesis drives the milk fatty acid profile in dairy goats
title_sort hydrogen cross feeding among rumen biohydrogenation propionogenesis and methanogenesis drives the milk fatty acid profile in dairy goats
topic dairy goat
fumarate
methanogenesis inhibitor
milk fatty acid profile
rumen biohydrogenation
url https://www.cambridge.org/core/product/identifier/S297737762400022X/type/journal_article
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AT shuaishuaili hydrogencrossfeedingamongrumenbiohydrogenationpropionogenesisandmethanogenesisdrivesthemilkfattyacidprofileindairygoats
AT huaijiang hydrogencrossfeedingamongrumenbiohydrogenationpropionogenesisandmethanogenesisdrivesthemilkfattyacidprofileindairygoats
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AT junhuyao hydrogencrossfeedingamongrumenbiohydrogenationpropionogenesisandmethanogenesisdrivesthemilkfattyacidprofileindairygoats
AT zongjunli hydrogencrossfeedingamongrumenbiohydrogenationpropionogenesisandmethanogenesisdrivesthemilkfattyacidprofileindairygoats