Diverse hydrogen production and consumption pathways influence methane production in ruminants
Farmed ruminants are the largest source of anthropogenic methane emissions globally. The methanogenic archaea responsible for these emissions use molecular hydrogen (H 2 ), produced during bacterial and eukaryotic carbohydrate fermentation, as their primary energy source. In this work, we used compa...
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Published in | The ISME Journal Vol. 13; no. 10; pp. 2617 - 2632 |
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Main Authors | , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
London
Nature Publishing Group UK
01.10.2019
Nature Publishing Group |
Subjects | |
Online Access | Get full text |
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Summary: | Farmed ruminants are the largest source of anthropogenic methane emissions globally. The methanogenic archaea responsible for these emissions use molecular hydrogen (H
2
), produced during bacterial and eukaryotic carbohydrate fermentation, as their primary energy source. In this work, we used comparative genomic, metatranscriptomic and co-culture-based approaches to gain a system-wide understanding of the organisms and pathways responsible for ruminal H
2
metabolism. Two-thirds of sequenced rumen bacterial and archaeal genomes encode enzymes that catalyse H
2
production or consumption, including 26 distinct hydrogenase subgroups. Metatranscriptomic analysis confirmed that these hydrogenases are differentially expressed in sheep rumen. Electron-bifurcating [FeFe]-hydrogenases from carbohydrate-fermenting Clostridia (e.g.,
Ruminococcus
) accounted for half of all hydrogenase transcripts. Various H
2
uptake pathways were also expressed, including methanogenesis (
Methanobrevibacter
), fumarate and nitrite reduction (
Selenomonas
), and acetogenesis (
Blautia
). Whereas methanogenesis-related transcripts predominated in high methane yield sheep, alternative uptake pathways were significantly upregulated in low methane yield sheep. Complementing these findings, we observed significant differential expression and activity of the hydrogenases of the hydrogenogenic cellulose fermenter
Ruminococcus albus
and the hydrogenotrophic fumarate reducer
Wolinella succinogenes
in co-culture compared with pure culture. We conclude that H
2
metabolism is a more complex and widespread trait among rumen microorganisms than previously recognised. There is evidence that alternative hydrogenotrophs, including acetogenic and respiratory bacteria, can prosper in the rumen and effectively compete with methanogens for H
2
. These findings may help to inform ongoing strategies to mitigate methane emissions by increasing flux through alternative H
2
uptake pathways, including through animal selection, dietary supplementation and methanogenesis inhibitors. |
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Bibliography: | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 |
ISSN: | 1751-7362 1751-7370 |
DOI: | 10.1038/s41396-019-0464-2 |