Holistic Assessment of Rumen Microbiome Dynamics through Quantitative Metatranscriptomics Reveals Multifunctional Redundancy during Key Steps of Anaerobic Feed Degradation

ABSTRACT Ruminant livestock is a major source of the potent greenhouse gas methane. The complex rumen microbiome, consisting of bacteria, archaea, and microbial eukaryotes, facilitates anaerobic plant biomass degradation in the cow rumen, leading to methane emissions. Using an integrated approach co...

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Autores principales:	Andrea Söllinger, Alexander Tøsdal Tveit, Morten Poulsen, Samantha Joan Noel, Mia Bengtsson, Jörg Bernhardt, Anne Louise Frydendahl Hellwing, Peter Lund, Katharina Riedel, Christa Schleper, Ole Højberg, Tim Urich
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	archaea Methanomassiliicoccales carbohydrate active enzymes metatranscriptomics methane methanogenesis Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/b76f6bd41d57493f9dca7d198f4477f8
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spelling	oai:doaj.org-article:b76f6bd41d57493f9dca7d198f4477f82021-12-02T18:39:46ZHolistic Assessment of Rumen Microbiome Dynamics through Quantitative Metatranscriptomics Reveals Multifunctional Redundancy during Key Steps of Anaerobic Feed Degradation10.1128/mSystems.00038-182379-5077https://doaj.org/article/b76f6bd41d57493f9dca7d198f4477f82018-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00038-18https://doaj.org/toc/2379-5077ABSTRACT Ruminant livestock is a major source of the potent greenhouse gas methane. The complex rumen microbiome, consisting of bacteria, archaea, and microbial eukaryotes, facilitates anaerobic plant biomass degradation in the cow rumen, leading to methane emissions. Using an integrated approach combining multidomain quantitative metatranscriptomics with gas and volatile fatty acid (VFA) profiling, we aimed at obtaining the most comprehensive picture of the active rumen microbiome during feed degradation to date. Bacterial, archaeal, and eukaryotic biomass, but also methane emissions and VFA concentrations, increased drastically within an hour after feed intake. mRNA profiling revealed a dynamic response of carbohydrate-active enzyme transcripts, transcripts involved in VFA production and methanogenesis. While the relative abundances of functional transcripts did not mirror observed processes, such as methane emissions, transformation to mRNA abundance per gram of rumen fluid echoed ruminant processes. The microbiome composition was highly individual, with, e.g., ciliate, Neocallimastigaceae, Prevotellaceae, Succinivibrionaceae, and Fibrobacteraceae abundances differing between cows. Microbiome individuality was accompanied by inter- and intradomain multifunctional redundancy among microbiome members during feed degradation. This likely enabled the robust performance of the anaerobic degradation process in each rumen. Neocallimastigaceae and ciliates contributed an unexpectedly large share of transcripts for cellulose- and hemicellulose-degrading enzymes, respectively. Methyl-reducing but not CO2-reducing methanogens were positively correlated with methane emissions. While Methanomassiliicoccales switched from methanol to methylamines as electron acceptors, Methanosphaera became the dominating methanol-reducing methanogen. This study for the first time linked rumen meta-omics with processes and enabled holistic insights into the contribution of all microbiome members to feed degradation. IMPORTANCE Ruminant animals, such as cows, live in a tight symbiotic association with microorganisms, allowing them to feed on otherwise indigestible plant biomass as food sources. Methane is produced as an end product of the anaerobic feed degradation in ruminants and is emitted to the atmosphere, making ruminant animals among the major anthropogenic sources of the potent greenhouse gas methane. Using newly developed quantitative metatranscriptomics for holistic microbiome analysis, we here identified bacterial, archaeal, and eukaryotic key players and the short-term dynamics of the rumen microbiome during anaerobic plant biomass degradation and subsequent methane emissions. These novel insights might pave the way for novel ecologically and economically sustainable methane mitigation strategies, much needed in times of global climate change. Author Video: An author video summary of this article is available.Andrea SöllingerAlexander Tøsdal TveitMorten PoulsenSamantha Joan NoelMia BengtssonJörg BernhardtAnne Louise Frydendahl HellwingPeter LundKatharina RiedelChrista SchleperOle HøjbergTim UrichAmerican Society for MicrobiologyarticlearchaeaMethanomassiliicoccalescarbohydrate active enzymesmetatranscriptomicsmethanemethanogenesisMicrobiologyQR1-502ENmSystems, Vol 3, Iss 4 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	archaea Methanomassiliicoccales carbohydrate active enzymes metatranscriptomics methane methanogenesis Microbiology QR1-502
spellingShingle	archaea Methanomassiliicoccales carbohydrate active enzymes metatranscriptomics methane methanogenesis Microbiology QR1-502 Andrea Söllinger Alexander Tøsdal Tveit Morten Poulsen Samantha Joan Noel Mia Bengtsson Jörg Bernhardt Anne Louise Frydendahl Hellwing Peter Lund Katharina Riedel Christa Schleper Ole Højberg Tim Urich Holistic Assessment of Rumen Microbiome Dynamics through Quantitative Metatranscriptomics Reveals Multifunctional Redundancy during Key Steps of Anaerobic Feed Degradation
description	ABSTRACT Ruminant livestock is a major source of the potent greenhouse gas methane. The complex rumen microbiome, consisting of bacteria, archaea, and microbial eukaryotes, facilitates anaerobic plant biomass degradation in the cow rumen, leading to methane emissions. Using an integrated approach combining multidomain quantitative metatranscriptomics with gas and volatile fatty acid (VFA) profiling, we aimed at obtaining the most comprehensive picture of the active rumen microbiome during feed degradation to date. Bacterial, archaeal, and eukaryotic biomass, but also methane emissions and VFA concentrations, increased drastically within an hour after feed intake. mRNA profiling revealed a dynamic response of carbohydrate-active enzyme transcripts, transcripts involved in VFA production and methanogenesis. While the relative abundances of functional transcripts did not mirror observed processes, such as methane emissions, transformation to mRNA abundance per gram of rumen fluid echoed ruminant processes. The microbiome composition was highly individual, with, e.g., ciliate, Neocallimastigaceae, Prevotellaceae, Succinivibrionaceae, and Fibrobacteraceae abundances differing between cows. Microbiome individuality was accompanied by inter- and intradomain multifunctional redundancy among microbiome members during feed degradation. This likely enabled the robust performance of the anaerobic degradation process in each rumen. Neocallimastigaceae and ciliates contributed an unexpectedly large share of transcripts for cellulose- and hemicellulose-degrading enzymes, respectively. Methyl-reducing but not CO2-reducing methanogens were positively correlated with methane emissions. While Methanomassiliicoccales switched from methanol to methylamines as electron acceptors, Methanosphaera became the dominating methanol-reducing methanogen. This study for the first time linked rumen meta-omics with processes and enabled holistic insights into the contribution of all microbiome members to feed degradation. IMPORTANCE Ruminant animals, such as cows, live in a tight symbiotic association with microorganisms, allowing them to feed on otherwise indigestible plant biomass as food sources. Methane is produced as an end product of the anaerobic feed degradation in ruminants and is emitted to the atmosphere, making ruminant animals among the major anthropogenic sources of the potent greenhouse gas methane. Using newly developed quantitative metatranscriptomics for holistic microbiome analysis, we here identified bacterial, archaeal, and eukaryotic key players and the short-term dynamics of the rumen microbiome during anaerobic plant biomass degradation and subsequent methane emissions. These novel insights might pave the way for novel ecologically and economically sustainable methane mitigation strategies, much needed in times of global climate change. Author Video: An author video summary of this article is available.
format	article
author	Andrea Söllinger Alexander Tøsdal Tveit Morten Poulsen Samantha Joan Noel Mia Bengtsson Jörg Bernhardt Anne Louise Frydendahl Hellwing Peter Lund Katharina Riedel Christa Schleper Ole Højberg Tim Urich
author_facet	Andrea Söllinger Alexander Tøsdal Tveit Morten Poulsen Samantha Joan Noel Mia Bengtsson Jörg Bernhardt Anne Louise Frydendahl Hellwing Peter Lund Katharina Riedel Christa Schleper Ole Højberg Tim Urich
author_sort	Andrea Söllinger
title	Holistic Assessment of Rumen Microbiome Dynamics through Quantitative Metatranscriptomics Reveals Multifunctional Redundancy during Key Steps of Anaerobic Feed Degradation
title_short	Holistic Assessment of Rumen Microbiome Dynamics through Quantitative Metatranscriptomics Reveals Multifunctional Redundancy during Key Steps of Anaerobic Feed Degradation
title_full	Holistic Assessment of Rumen Microbiome Dynamics through Quantitative Metatranscriptomics Reveals Multifunctional Redundancy during Key Steps of Anaerobic Feed Degradation
title_fullStr	Holistic Assessment of Rumen Microbiome Dynamics through Quantitative Metatranscriptomics Reveals Multifunctional Redundancy during Key Steps of Anaerobic Feed Degradation
title_full_unstemmed	Holistic Assessment of Rumen Microbiome Dynamics through Quantitative Metatranscriptomics Reveals Multifunctional Redundancy during Key Steps of Anaerobic Feed Degradation
title_sort	holistic assessment of rumen microbiome dynamics through quantitative metatranscriptomics reveals multifunctional redundancy during key steps of anaerobic feed degradation
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/b76f6bd41d57493f9dca7d198f4477f8
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Holistic Assessment of Rumen Microbiome Dynamics through Quantitative Metatranscriptomics Reveals Multifunctional Redundancy during Key Steps of Anaerobic Feed Degradation

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