Methane inhibition alters the microbial community, hydrogen flow and fermentation response in the rumen of cattle

Management of metabolic hydrogen ([H]) in the rumen has been identified as an important consideration when reducing ruminant CH4 emissions. However, little is known about hydrogen flux and microbial rumen population responses to CH4 inhibition when animals are fed with slowly degradable diets. The e...

Full description

Bibliographic Details
Main Authors: Gonzalo Martinez-Fernandez, Stuart Edward Denman, Chunlei Yang, Jane Cheung, Makoto Mitsumori, Christopher Simon McSweeney
Format: Article
Language:English
Published: Frontiers Media S.A. 2016-07-01
Series:Frontiers in Microbiology
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fmicb.2016.01122/full
id doaj-f9c0d6e56531472f93507c07c645960e
record_format Article
spelling doaj-f9c0d6e56531472f93507c07c645960e2020-11-25T00:59:46ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2016-07-01710.3389/fmicb.2016.01122204456Methane inhibition alters the microbial community, hydrogen flow and fermentation response in the rumen of cattleGonzalo Martinez-Fernandez0Stuart Edward Denman1Chunlei Yang2Jane Cheung3Makoto Mitsumori4Christopher Simon McSweeney5CSIROCSIROZhejiang UniversityCSIRONational Institute of Livestock and Grassland ScienceCSIROManagement of metabolic hydrogen ([H]) in the rumen has been identified as an important consideration when reducing ruminant CH4 emissions. However, little is known about hydrogen flux and microbial rumen population responses to CH4 inhibition when animals are fed with slowly degradable diets. The effects of the anti-methanogenic compound, chloroform, on rumen fermentation, microbial ecology and H2 /CH4 production were investigated in vivo. Eight rumen fistulated Brahman steers were fed a roughage hay diet (Rhode grass hay) or roughage hay:concentrate diet (60:40) with increasing levels (low, mid and high) of chloroform in a cylcodextrin matrix. The increasing levels of chloroform resulted in an increase in H2 expelled as CH4 production decreased with no effect on dry matter intakes. The amount of expelled H2 per mole of decreased methane, was lower for the hay diet suggesting a more efficient redirection of hydrogen into other microbial products compared with hay:concentrate diet. A shift in rumen fermentation towards propionate and branched-chain fatty acids was observed for both diets. Animals fed with the hay:concentrate diet had both higher formate concentration and H2 expelled than those fed only roughage hay. Metabolomic analyses revealed an increase in the concentration of amino acids, organic and nucleic acids in the fluid phase for both diets when methanogenesis was inhibited. These changes in the rumen metabolism were accompanied by a shift in the microbiota with an increase in Bacteroidetes:Firmicutes ratio and a decrease in Archaea and Synergistetes for both diets. Within the Bacteroidetes family, some OTUs assigned to Prevotella were promoted under choloroform treatment. These bacteria may be partly responsible for the increase in amino acids and propionate in the rumen. No significant changes were observed for abundance of fibrolytic bacteria, protozoa and fungi, which suggests that fibre degradation was not impaired. The observed 30% decrease in methanogenesis did not adversely affect rumen metabolism and the rumen microbiota was able to adapt and redirect [H] into other microbial end-products for both diets. However, it is also required dietary supplements or microbial treatments to capture the additional H2 expelled by the animal to further improve rumen digestive efficiency.http://journal.frontiersin.org/Journal/10.3389/fmicb.2016.01122/fullHydrogenMethaneRumenMetabolitesmicrobial community16s sequencing
collection DOAJ
language English
format Article
sources DOAJ
author Gonzalo Martinez-Fernandez
Stuart Edward Denman
Chunlei Yang
Jane Cheung
Makoto Mitsumori
Christopher Simon McSweeney
spellingShingle Gonzalo Martinez-Fernandez
Stuart Edward Denman
Chunlei Yang
Jane Cheung
Makoto Mitsumori
Christopher Simon McSweeney
Methane inhibition alters the microbial community, hydrogen flow and fermentation response in the rumen of cattle
Frontiers in Microbiology
Hydrogen
Methane
Rumen
Metabolites
microbial community
16s sequencing
author_facet Gonzalo Martinez-Fernandez
Stuart Edward Denman
Chunlei Yang
Jane Cheung
Makoto Mitsumori
Christopher Simon McSweeney
author_sort Gonzalo Martinez-Fernandez
title Methane inhibition alters the microbial community, hydrogen flow and fermentation response in the rumen of cattle
title_short Methane inhibition alters the microbial community, hydrogen flow and fermentation response in the rumen of cattle
title_full Methane inhibition alters the microbial community, hydrogen flow and fermentation response in the rumen of cattle
title_fullStr Methane inhibition alters the microbial community, hydrogen flow and fermentation response in the rumen of cattle
title_full_unstemmed Methane inhibition alters the microbial community, hydrogen flow and fermentation response in the rumen of cattle
title_sort methane inhibition alters the microbial community, hydrogen flow and fermentation response in the rumen of cattle
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2016-07-01
description Management of metabolic hydrogen ([H]) in the rumen has been identified as an important consideration when reducing ruminant CH4 emissions. However, little is known about hydrogen flux and microbial rumen population responses to CH4 inhibition when animals are fed with slowly degradable diets. The effects of the anti-methanogenic compound, chloroform, on rumen fermentation, microbial ecology and H2 /CH4 production were investigated in vivo. Eight rumen fistulated Brahman steers were fed a roughage hay diet (Rhode grass hay) or roughage hay:concentrate diet (60:40) with increasing levels (low, mid and high) of chloroform in a cylcodextrin matrix. The increasing levels of chloroform resulted in an increase in H2 expelled as CH4 production decreased with no effect on dry matter intakes. The amount of expelled H2 per mole of decreased methane, was lower for the hay diet suggesting a more efficient redirection of hydrogen into other microbial products compared with hay:concentrate diet. A shift in rumen fermentation towards propionate and branched-chain fatty acids was observed for both diets. Animals fed with the hay:concentrate diet had both higher formate concentration and H2 expelled than those fed only roughage hay. Metabolomic analyses revealed an increase in the concentration of amino acids, organic and nucleic acids in the fluid phase for both diets when methanogenesis was inhibited. These changes in the rumen metabolism were accompanied by a shift in the microbiota with an increase in Bacteroidetes:Firmicutes ratio and a decrease in Archaea and Synergistetes for both diets. Within the Bacteroidetes family, some OTUs assigned to Prevotella were promoted under choloroform treatment. These bacteria may be partly responsible for the increase in amino acids and propionate in the rumen. No significant changes were observed for abundance of fibrolytic bacteria, protozoa and fungi, which suggests that fibre degradation was not impaired. The observed 30% decrease in methanogenesis did not adversely affect rumen metabolism and the rumen microbiota was able to adapt and redirect [H] into other microbial end-products for both diets. However, it is also required dietary supplements or microbial treatments to capture the additional H2 expelled by the animal to further improve rumen digestive efficiency.
topic Hydrogen
Methane
Rumen
Metabolites
microbial community
16s sequencing
url http://journal.frontiersin.org/Journal/10.3389/fmicb.2016.01122/full
work_keys_str_mv AT gonzalomartinezfernandez methaneinhibitionaltersthemicrobialcommunityhydrogenflowandfermentationresponseintherumenofcattle
AT stuartedwarddenman methaneinhibitionaltersthemicrobialcommunityhydrogenflowandfermentationresponseintherumenofcattle
AT chunleiyang methaneinhibitionaltersthemicrobialcommunityhydrogenflowandfermentationresponseintherumenofcattle
AT janecheung methaneinhibitionaltersthemicrobialcommunityhydrogenflowandfermentationresponseintherumenofcattle
AT makotomitsumori methaneinhibitionaltersthemicrobialcommunityhydrogenflowandfermentationresponseintherumenofcattle
AT christophersimonmcsweeney methaneinhibitionaltersthemicrobialcommunityhydrogenflowandfermentationresponseintherumenofcattle
_version_ 1725216302134460416