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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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2019-08-01
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| Series: | mBio |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.01814-19 |
| _version_ | 1818404610400845824 |
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| 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 |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-14T08:42:53Z |
| format | Article |
| id | doaj.art-8b0d773c6df54246a368a49c0a4ca8a2 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-14T08:42:53Z |
| publishDate | 2019-08-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-8b0d773c6df54246a368a49c0a4ca8a22022-12-21T23:09:16ZengAmerican Society for MicrobiologymBio2150-75112019-08-0110410.1128/mBio.01814-19Anaerobic Degradation of Non-Methane Alkanes by “<italic toggle="yes">Candidatus</italic> Methanoliparia” in Hydrocarbon Seeps of the Gulf of MexicoRafael Laso-Pérez0Cedric Hahn1Daan M. van Vliet2Halina E. Tegetmeyer3Florence Schubotz4Nadine T. Smit5Thomas Pape6Heiko Sahling7Gerhard Bohrmann8Antje Boetius9Katrin Knittel10Gunter Wegener11Max-Planck Institute for Marine Microbiology, Bremen, GermanyMax-Planck Institute for Marine Microbiology, Bremen, GermanyLaboratory of Microbiology, Wageningen University and Research, Wageningen, The NetherlandsAlfred Wegener Institute Helmholtz Center for Polar and Marine Research, Bremerhaven, GermanyMARUM, Center for Marine Environmental Sciences and Department of Geosciences, University of Bremen, Bremen, GermanyMARUM, Center for Marine Environmental Sciences and Department of Geosciences, University of Bremen, Bremen, GermanyMARUM, Center for Marine Environmental Sciences and Department of Geosciences, University of Bremen, Bremen, GermanyMARUM, Center for Marine Environmental Sciences and Department of Geosciences, University of Bremen, Bremen, GermanyMARUM, Center for Marine Environmental Sciences and Department of Geosciences, University of Bremen, Bremen, GermanyMax-Planck Institute for Marine Microbiology, Bremen, GermanyMax-Planck Institute for Marine Microbiology, Bremen, GermanyMax-Planck Institute for Marine Microbiology, Bremen, GermanyABSTRACT 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.https://journals.asm.org/doi/10.1128/mBio.01814-19alkane degradationarchaeamethanogenesismethyl-coenzyme M reductaseoil seeps |
| spellingShingle | 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 mBio alkane degradation archaea methanogenesis methyl-coenzyme M reductase oil seeps |
| title | 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_short | 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 |
| topic | alkane degradation archaea methanogenesis methyl-coenzyme M reductase oil seeps |
| url | https://journals.asm.org/doi/10.1128/mBio.01814-19 |
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