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The transcriptome response of the ruminal methanogen Methanobrevibacter ruminantium strain M1 to the inhibitor lauric acid.

ABSTRACT: Lauric acid (C12) is a medium-chain fatty acid that inhibits growth and production of the greenhouse gas methane by rumen methanogens such as Methanobrevibacter ruminantium. To understand the inhibitory mechanism of C12, a transcriptome analysis was performed in M. ruminantium strain M1 (DSM 1093) using RNA-Seq.Pure cell cultures in the exponential growth phase were treated with 0.4 mg/ml C12, dissolved in dimethyl sulfoxide (DMSO), for 1 h and transcriptomic changes were compared to DMSO-only treated cells (final DMSO concentration 0.2%). Exposure to C12 resulted in differential expression of 163 of the 2280 genes in the M1 genome (maximum log2-fold change 6.6). Remarkably, C12 hardly affected the expression of genes involved in methanogenesis. Instead, most affected genes encode cell-surface associated proteins (adhesion-like proteins, membrane-associated transporters and hydrogenases), and proteins involved in detoxification or DNA-repair processes. Enrichment analysis on the genes regulated in the C12-treated group showed a significant enrichment for categories 'cell surface' and 'mobile elements' (activated by C12), and for the categories 'regulation' and 'protein fate' (represssed). These results are useful to generate and test specific hypotheses on the mechanism how C12 affects rumen methanogens.

SUBMITTER: Zhou X

PROVIDER: S-EPMC5816558 | biostudies-literature | 2018 Feb

REPOSITORIES: biostudies-literature

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The transcriptome response of the ruminal methanogen Methanobrevibacter ruminantium strain M1 to the inhibitor lauric acid.

Zhou Xuan X Stevens Marc J A MJA Neuenschwander Stefan S Schwarm Angela A Kreuzer Michael M Bratus-Neuenschwander Anna A Zeitz Johanna O JO

BMC research notes 20180217 1

<h4>Objective</h4>Lauric acid (C<sub>12</sub>) is a medium-chain fatty acid that inhibits growth and production of the greenhouse gas methane by rumen methanogens such as Methanobrevibacter ruminantium. To understand the inhibitory mechanism of C<sub>12</sub>, a transcriptome analysis was performed in M. ruminantium strain M1 (DSM 1093) using RNA-Seq.<h4>Results</h4>Pure cell cultures in the exponential growth phase were treated with 0.4 mg/ml C<sub>12</sub>, dissolved in dimethyl sulfoxide (DMS ...[more]

PMID: 29454387

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Project description:Medium chain fatty acids (MCFA) have been shown to inhibit methanogenesis, disrupt the cell envelope, and decrease survival of Methanobrevibacter ruminantium M1 in a dose-, time-, and protonation level dependent way. However, the exact mechanisms behind these observations are still unknown. Although the biochemistry of the metabolic processes of M. ruminantium has been well studied and its genome sequence is now available, little is known about the overall transcriptome regulation of M. ruminantium in response to inhibitors like MCFA. In the present study, we used RNA Sequencing to evaluate the effects of lauric acid (C12) on M. ruminantium. Pure M. ruminantium cell cultures in the mid-exponential growth phase were exposed to C12 in concentrations of 0.4 mg/mL, dissolved in DMSO for 1 h, and the transcriptomic changes compared to DMSO-only treated control samples (final DMSO concentration 0.2 %), were investigated. Gene expression changes upon exposure to C12 were not dramatic in magnitude (log2 fold change mostly below +/- 3) and in gene number (214 genes). However, the observed expression changes affected mostly genes which encoded cell-surface associated proteins (adhesion-like proteins, membrane-associated transporters and hydrogenases), or proteins, which were involved in detoxification or DNA repair processes. The transcriptional response of M. ruminantium M1 to C12 did not specifically inhibit methanogenesis. Instead, the data indicated a non-specific antimicrobial action by lauric acid, which involves destruction of the cell membrane and interferences with cellular energetics in M. ruminantium. To date, there has been no systematic characterization of a ruminal methanogen transcriptome by deep sequencing. Our results give first hints on the molecular inhibitory mechanism of C12 on M. ruminantium. RNA profiles of M. ruminantium treated in vitro (lauric acid disolved in DMSO), non-treated=controls (DMSO supplementation) and non-treated=blanks (no supplementation) were generated by deep sequencing, in triplicates, by using Illumina HiSeq2500

Project description:BackgroundMethane (CH(4)) is a potent greenhouse gas (GHG), having a global warming potential 21 times that of carbon dioxide (CO(2)). Methane emissions from agriculture represent around 40% of the emissions produced by human-related activities, the single largest source being enteric fermentation, mainly in ruminant livestock. Technologies to reduce these emissions are lacking. Ruminant methane is formed by the action of methanogenic archaea typified by Methanobrevibacter ruminantium, which is present in ruminants fed a wide variety of diets worldwide. To gain more insight into the lifestyle of a rumen methanogen, and to identify genes and proteins that can be targeted to reduce methane production, we have sequenced the 2.93 Mb genome of M. ruminantium M1, the first rumen methanogen genome to be completed.Methodology/principal findingsThe M1 genome was sequenced, annotated and subjected to comparative genomic and metabolic pathway analyses. Conserved and methanogen-specific gene sets suitable as targets for vaccine development or chemogenomic-based inhibition of rumen methanogens were identified. The feasibility of using a synthetic peptide-directed vaccinology approach to target epitopes of methanogen surface proteins was demonstrated. A prophage genome was described and its lytic enzyme, endoisopeptidase PeiR, was shown to lyse M1 cells in pure culture. A predicted stimulation of M1 growth by alcohols was demonstrated and microarray analyses indicated up-regulation of methanogenesis genes during co-culture with a hydrogen (H(2)) producing rumen bacterium. We also report the discovery of non-ribosomal peptide synthetases in M. ruminantium M1, the first reported in archaeal species.Conclusions/significanceThe M1 genome sequence provides new insights into the lifestyle and cellular processes of this important rumen methanogen. It also defines vaccine and chemogenomic targets for broad inhibition of rumen methanogens and represents a significant contribution to worldwide efforts to mitigate ruminant methane emissions and reduce production of anthropogenic greenhouse gases.

Dataset Information

The transcriptome response of the ruminal methanogen Methanobrevibacter ruminantium strain M1 to the inhibitor lauric acid.

Publications

The transcriptome response of the ruminal methanogen Methanobrevibacter ruminantium strain M1 to the inhibitor lauric acid.

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