Genomic Insights into Adaptations of Trimethylamine-Utilizing Methanogens to Diverse Habitats, Including the Human Gut

ABSTRACT Archaea of the order Methanomassiliicoccales use methylated amines such as trimethylamine as the substrates for methanogenesis. They form two large phylogenetic clades and reside in diverse environments, from soil to the human gut. Two genera, one from each clade, inhabit the human gut: Met...

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Autores principales: Jacobo de la Cuesta-Zuluaga, Tim D. Spector, Nicholas D. Youngblut, Ruth E. Ley
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Publicado: American Society for Microbiology 2021
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spelling oai:doaj.org-article:77ff21b8bd1e43ea8eb98708cec18cda2021-12-02T19:36:37ZGenomic Insights into Adaptations of Trimethylamine-Utilizing Methanogens to Diverse Habitats, Including the Human Gut10.1128/mSystems.00939-202379-5077https://doaj.org/article/77ff21b8bd1e43ea8eb98708cec18cda2021-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00939-20https://doaj.org/toc/2379-5077ABSTRACT Archaea of the order Methanomassiliicoccales use methylated amines such as trimethylamine as the substrates for methanogenesis. They form two large phylogenetic clades and reside in diverse environments, from soil to the human gut. Two genera, one from each clade, inhabit the human gut: Methanomassiliicoccus, which has one cultured representative, and “Candidatus Methanomethylophilus,” which has none. Questions remain regarding their distribution across biomes and human populations, their association with other taxa in the gut, and whether host genetics correlate with their abundance. To gain insight into the Methanomassiliicoccales clade, particularly its human-associated members, we performed a genomic comparison of 72 Methanomassiliicoccales genomes and assessed their presence in metagenomes derived from the human gut (n = 4,472, representing 22 populations), nonhuman animal gut (n = 145), and nonhost environments (n = 160). Our analyses showed that all taxa are generalists; they were detected in animal gut and environmental samples. We confirmed two large clades, one enriched in the gut and the other enriched in the environment, with notable exceptions. Genomic adaptations to the gut include genome reduction and genes involved in the shikimate pathway and bile resistance. Genomic adaptations differed by clade, not habitat preference, indicating convergent evolution between the clades. In the human gut, the relative abundance of Methanomassiliicoccales spp. correlated with trimethylamine-producing bacteria and was unrelated to host genotype. Our results shed light on the microbial ecology of this group and may help guide Methanomassiliicoccales-based strategies for trimethylamine mitigation in cardiovascular disease. IMPORTANCE Methanomassiliicoccales are less-known members of the human gut archaeome. Members of this order use methylated amines, including trimethylamine, in methane production. This group has only one cultured representative; how its members adapted to inhabit the mammalian gut and how they interact with other microbes is largely unknown. Using bioinformatics methods applied to DNA from a wide range of samples, we profiled the abundances of these Archaea spp. in environmental and host-associated microbial communities. We observed two groups of Methanomassiliicoccales, one largely host associated and one largely found in environmental samples, with some exceptions. When host associated, these Archaea have smaller genomes and possess genes related to bile resistance and aromatic amino acid precursors. We did not detect Methanomassiliicoccales in all human populations tested, but when present, they were correlated with bacteria known to produce trimethylamine. Due to their metabolism of trimethylamine, these intriguing Archaea may form the basis of novel therapies for cardiovascular disease.Jacobo de la Cuesta-ZuluagaTim D. SpectorNicholas D. YoungblutRuth E. LeyAmerican Society for MicrobiologyarticleMethanomassiliicoccalesarchaeacomparative genomicshuman gutmetagenomesmicrobiomeMicrobiologyQR1-502ENmSystems, Vol 6, Iss 1 (2021)
institution DOAJ
collection DOAJ
language EN
topic Methanomassiliicoccales
archaea
comparative genomics
human gut
metagenomes
microbiome
Microbiology
QR1-502
spellingShingle Methanomassiliicoccales
archaea
comparative genomics
human gut
metagenomes
microbiome
Microbiology
QR1-502
Jacobo de la Cuesta-Zuluaga
Tim D. Spector
Nicholas D. Youngblut
Ruth E. Ley
Genomic Insights into Adaptations of Trimethylamine-Utilizing Methanogens to Diverse Habitats, Including the Human Gut
description ABSTRACT Archaea of the order Methanomassiliicoccales use methylated amines such as trimethylamine as the substrates for methanogenesis. They form two large phylogenetic clades and reside in diverse environments, from soil to the human gut. Two genera, one from each clade, inhabit the human gut: Methanomassiliicoccus, which has one cultured representative, and “Candidatus Methanomethylophilus,” which has none. Questions remain regarding their distribution across biomes and human populations, their association with other taxa in the gut, and whether host genetics correlate with their abundance. To gain insight into the Methanomassiliicoccales clade, particularly its human-associated members, we performed a genomic comparison of 72 Methanomassiliicoccales genomes and assessed their presence in metagenomes derived from the human gut (n = 4,472, representing 22 populations), nonhuman animal gut (n = 145), and nonhost environments (n = 160). Our analyses showed that all taxa are generalists; they were detected in animal gut and environmental samples. We confirmed two large clades, one enriched in the gut and the other enriched in the environment, with notable exceptions. Genomic adaptations to the gut include genome reduction and genes involved in the shikimate pathway and bile resistance. Genomic adaptations differed by clade, not habitat preference, indicating convergent evolution between the clades. In the human gut, the relative abundance of Methanomassiliicoccales spp. correlated with trimethylamine-producing bacteria and was unrelated to host genotype. Our results shed light on the microbial ecology of this group and may help guide Methanomassiliicoccales-based strategies for trimethylamine mitigation in cardiovascular disease. IMPORTANCE Methanomassiliicoccales are less-known members of the human gut archaeome. Members of this order use methylated amines, including trimethylamine, in methane production. This group has only one cultured representative; how its members adapted to inhabit the mammalian gut and how they interact with other microbes is largely unknown. Using bioinformatics methods applied to DNA from a wide range of samples, we profiled the abundances of these Archaea spp. in environmental and host-associated microbial communities. We observed two groups of Methanomassiliicoccales, one largely host associated and one largely found in environmental samples, with some exceptions. When host associated, these Archaea have smaller genomes and possess genes related to bile resistance and aromatic amino acid precursors. We did not detect Methanomassiliicoccales in all human populations tested, but when present, they were correlated with bacteria known to produce trimethylamine. Due to their metabolism of trimethylamine, these intriguing Archaea may form the basis of novel therapies for cardiovascular disease.
format article
author Jacobo de la Cuesta-Zuluaga
Tim D. Spector
Nicholas D. Youngblut
Ruth E. Ley
author_facet Jacobo de la Cuesta-Zuluaga
Tim D. Spector
Nicholas D. Youngblut
Ruth E. Ley
author_sort Jacobo de la Cuesta-Zuluaga
title Genomic Insights into Adaptations of Trimethylamine-Utilizing Methanogens to Diverse Habitats, Including the Human Gut
title_short Genomic Insights into Adaptations of Trimethylamine-Utilizing Methanogens to Diverse Habitats, Including the Human Gut
title_full Genomic Insights into Adaptations of Trimethylamine-Utilizing Methanogens to Diverse Habitats, Including the Human Gut
title_fullStr Genomic Insights into Adaptations of Trimethylamine-Utilizing Methanogens to Diverse Habitats, Including the Human Gut
title_full_unstemmed Genomic Insights into Adaptations of Trimethylamine-Utilizing Methanogens to Diverse Habitats, Including the Human Gut
title_sort genomic insights into adaptations of trimethylamine-utilizing methanogens to diverse habitats, including the human gut
publisher American Society for Microbiology
publishDate 2021
url https://doaj.org/article/77ff21b8bd1e43ea8eb98708cec18cda
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