Anaerobic Degradation of Non-Methane Alkanes by “<italic toggle="yes">Candidatus</italic> Methanoliparia” in Hydrocarbon Seeps of the Gulf of Mexico

ABSTRACT Crude oil and gases in the seabed provide an important energy source for subsurface microorganisms. We investigated the role of archaea in the anaerobic degradation of non-methane alkanes in deep-sea oil seeps from the Gulf of Mexico. We identified microscopically the ethane and short-chain...

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Autores principales: Rafael Laso-Pérez, Cedric Hahn, Daan M. van Vliet, Halina E. Tegetmeyer, Florence Schubotz, Nadine T. Smit, Thomas Pape, Heiko Sahling, Gerhard Bohrmann, Antje Boetius, Katrin Knittel, Gunter Wegener
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Publicado: American Society for Microbiology 2019
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spelling oai:doaj.org-article:8b0d773c6df54246a368a49c0a4ca8a22021-11-15T16:22:09ZAnaerobic Degradation of Non-Methane Alkanes by “<italic toggle="yes">Candidatus</italic> Methanoliparia” in Hydrocarbon Seeps of the Gulf of Mexico10.1128/mBio.01814-192150-7511https://doaj.org/article/8b0d773c6df54246a368a49c0a4ca8a22019-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01814-19https://doaj.org/toc/2150-7511ABSTRACT Crude oil and gases in the seabed provide an important energy source for subsurface microorganisms. We investigated the role of archaea in the anaerobic degradation of non-methane alkanes in deep-sea oil seeps from the Gulf of Mexico. We identified microscopically the ethane and short-chain alkane oxidizers “Candidatus Argoarchaeum” and “Candidatus Syntrophoarchaeum” forming consortia with bacteria. Moreover, we found that the sediments contain large numbers of cells from the archaeal clade “Candidatus Methanoliparia,” which was previously proposed to perform methanogenic alkane degradation. “Ca. Methanoliparia” occurred abundantly as single cells attached to oil droplets in sediments without apparent bacterial or archaeal partners. Metagenome-assembled genomes of “Ca. Methanoliparia” encode a complete methanogenesis pathway including a canonical methyl-coenzyme M reductase (MCR) but also a highly divergent MCR related to those of alkane-degrading archaea and pathways for the oxidation of long-chain alkyl units. Its metabolic genomic potential and its global detection in hydrocarbon reservoirs suggest that “Ca. Methanoliparia” is an important methanogenic alkane degrader in subsurface environments, producing methane by alkane disproportionation as a single organism. IMPORTANCE Oil-rich sediments from the Gulf of Mexico were found to contain diverse alkane-degrading groups of archaea. The symbiotic, consortium-forming “Candidatus Argoarchaeum” and “Candidatus Syntrophoarchaeum” are likely responsible for the degradation of ethane and short-chain alkanes, with the help of sulfate-reducing bacteria. “Ca. Methanoliparia” occurs as single cells associated with oil droplets. These archaea encode two phylogenetically different methyl-coenzyme M reductases that may allow this organism to thrive as a methanogen on a substrate of long-chain alkanes. Based on a library survey, we show that “Ca. Methanoliparia” is frequently detected in oil reservoirs and may be a key agent in the transformation of long-chain alkanes to methane. Our findings provide evidence for the important and diverse roles of archaea in alkane-rich marine habitats and support the notion of a significant functional versatility of the methyl coenzyme M reductase.Rafael Laso-PérezCedric HahnDaan M. van VlietHalina E. TegetmeyerFlorence SchubotzNadine T. SmitThomas PapeHeiko SahlingGerhard BohrmannAntje BoetiusKatrin KnittelGunter WegenerAmerican Society for Microbiologyarticlealkane degradationarchaeamethanogenesismethyl-coenzyme M reductaseoil seepsMicrobiologyQR1-502ENmBio, Vol 10, Iss 4 (2019)
institution DOAJ
collection DOAJ
language EN
topic alkane degradation
archaea
methanogenesis
methyl-coenzyme M reductase
oil seeps
Microbiology
QR1-502
spellingShingle alkane degradation
archaea
methanogenesis
methyl-coenzyme M reductase
oil seeps
Microbiology
QR1-502
Rafael Laso-Pérez
Cedric Hahn
Daan M. van Vliet
Halina E. Tegetmeyer
Florence Schubotz
Nadine T. Smit
Thomas Pape
Heiko Sahling
Gerhard Bohrmann
Antje Boetius
Katrin Knittel
Gunter Wegener
Anaerobic Degradation of Non-Methane Alkanes by “<italic toggle="yes">Candidatus</italic> Methanoliparia” in Hydrocarbon Seeps of the Gulf of Mexico
description ABSTRACT Crude oil and gases in the seabed provide an important energy source for subsurface microorganisms. We investigated the role of archaea in the anaerobic degradation of non-methane alkanes in deep-sea oil seeps from the Gulf of Mexico. We identified microscopically the ethane and short-chain alkane oxidizers “Candidatus Argoarchaeum” and “Candidatus Syntrophoarchaeum” forming consortia with bacteria. Moreover, we found that the sediments contain large numbers of cells from the archaeal clade “Candidatus Methanoliparia,” which was previously proposed to perform methanogenic alkane degradation. “Ca. Methanoliparia” occurred abundantly as single cells attached to oil droplets in sediments without apparent bacterial or archaeal partners. Metagenome-assembled genomes of “Ca. Methanoliparia” encode a complete methanogenesis pathway including a canonical methyl-coenzyme M reductase (MCR) but also a highly divergent MCR related to those of alkane-degrading archaea and pathways for the oxidation of long-chain alkyl units. Its metabolic genomic potential and its global detection in hydrocarbon reservoirs suggest that “Ca. Methanoliparia” is an important methanogenic alkane degrader in subsurface environments, producing methane by alkane disproportionation as a single organism. IMPORTANCE Oil-rich sediments from the Gulf of Mexico were found to contain diverse alkane-degrading groups of archaea. The symbiotic, consortium-forming “Candidatus Argoarchaeum” and “Candidatus Syntrophoarchaeum” are likely responsible for the degradation of ethane and short-chain alkanes, with the help of sulfate-reducing bacteria. “Ca. Methanoliparia” occurs as single cells associated with oil droplets. These archaea encode two phylogenetically different methyl-coenzyme M reductases that may allow this organism to thrive as a methanogen on a substrate of long-chain alkanes. Based on a library survey, we show that “Ca. Methanoliparia” is frequently detected in oil reservoirs and may be a key agent in the transformation of long-chain alkanes to methane. Our findings provide evidence for the important and diverse roles of archaea in alkane-rich marine habitats and support the notion of a significant functional versatility of the methyl coenzyme M reductase.
format article
author Rafael Laso-Pérez
Cedric Hahn
Daan M. van Vliet
Halina E. Tegetmeyer
Florence Schubotz
Nadine T. Smit
Thomas Pape
Heiko Sahling
Gerhard Bohrmann
Antje Boetius
Katrin Knittel
Gunter Wegener
author_facet Rafael Laso-Pérez
Cedric Hahn
Daan M. van Vliet
Halina E. Tegetmeyer
Florence Schubotz
Nadine T. Smit
Thomas Pape
Heiko Sahling
Gerhard Bohrmann
Antje Boetius
Katrin Knittel
Gunter Wegener
author_sort Rafael Laso-Pérez
title Anaerobic Degradation of Non-Methane Alkanes by “<italic toggle="yes">Candidatus</italic> Methanoliparia” in Hydrocarbon Seeps of the Gulf of Mexico
title_short Anaerobic Degradation of Non-Methane Alkanes by “<italic toggle="yes">Candidatus</italic> Methanoliparia” in Hydrocarbon Seeps of the Gulf of Mexico
title_full Anaerobic Degradation of Non-Methane Alkanes by “<italic toggle="yes">Candidatus</italic> Methanoliparia” in Hydrocarbon Seeps of the Gulf of Mexico
title_fullStr Anaerobic Degradation of Non-Methane Alkanes by “<italic toggle="yes">Candidatus</italic> Methanoliparia” in Hydrocarbon Seeps of the Gulf of Mexico
title_full_unstemmed Anaerobic Degradation of Non-Methane Alkanes by “<italic toggle="yes">Candidatus</italic> Methanoliparia” in Hydrocarbon Seeps of the Gulf of Mexico
title_sort anaerobic degradation of non-methane alkanes by “<italic toggle="yes">candidatus</italic> methanoliparia” in hydrocarbon seeps of the gulf of mexico
publisher American Society for Microbiology
publishDate 2019
url https://doaj.org/article/8b0d773c6df54246a368a49c0a4ca8a2
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