Anaerobic Degradation of Non-Methane Alkanes by "Candidatus Methanoliparia" in Hydrocarbon Seeps of the Gulf of Mexico

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

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

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.

Original languageEnglish
JournalmBio
Volume10
Issue number4
DOIs
Publication statusPublished - 20 Aug 2019

Fingerprint

Gulf of Mexico
Alkanes
Hydrocarbons
Archaea
Oils
Ethane
Methane
Library Surveys
Metagenome
Bacteria
Oil and Gas Fields
Petroleum
Oceans and Seas
Sulfates
Ecosystem

Keywords

  • alkane degradation
  • archaea
  • methanogenesis
  • methyl-coenzyme M reductase
  • oil seeps

Cite this

Laso-Pérez, Rafael ; Hahn, Cedric ; van Vliet, Daan M. ; Tegetmeyer, Halina E. ; Schubotz, Florence ; Smit, Nadine T. ; Pape, Thomas ; Sahling, Heiko ; Bohrmann, Gerhard ; Boetius, Antje ; Knittel, Katrin ; Wegener, Gunter. / Anaerobic Degradation of Non-Methane Alkanes by "Candidatus Methanoliparia" in Hydrocarbon Seeps of the Gulf of Mexico. In: mBio. 2019 ; Vol. 10, No. 4.
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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.",
keywords = "alkane degradation, archaea, methanogenesis, methyl-coenzyme M reductase, oil seeps",
author = "Rafael Laso-P{\'e}rez and Cedric Hahn and {van Vliet}, {Daan M.} and Tegetmeyer, {Halina E.} and Florence Schubotz and Smit, {Nadine T.} and Thomas Pape and Heiko Sahling and Gerhard Bohrmann and Antje Boetius and Katrin Knittel and Gunter Wegener",
year = "2019",
month = "8",
day = "20",
doi = "10.1128/mBio.01814-19",
language = "English",
volume = "10",
journal = "mBio",
issn = "2150-7511",
publisher = "American Society for Microbiology",
number = "4",

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Laso-Pérez, R, Hahn, C, van Vliet, DM, Tegetmeyer, HE, Schubotz, F, Smit, NT, Pape, T, Sahling, H, Bohrmann, G, Boetius, A, Knittel, K & Wegener, G 2019, 'Anaerobic Degradation of Non-Methane Alkanes by "Candidatus Methanoliparia" in Hydrocarbon Seeps of the Gulf of Mexico', mBio, vol. 10, no. 4. https://doi.org/10.1128/mBio.01814-19

Anaerobic Degradation of Non-Methane Alkanes by "Candidatus Methanoliparia" in Hydrocarbon Seeps of the Gulf of Mexico. / Laso-Pérez, Rafael; Hahn, Cedric; van Vliet, Daan M.; Tegetmeyer, Halina E.; Schubotz, Florence; Smit, Nadine T.; Pape, Thomas; Sahling, Heiko; Bohrmann, Gerhard; Boetius, Antje; Knittel, Katrin; Wegener, Gunter.

In: mBio, Vol. 10, No. 4, 20.08.2019.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Anaerobic Degradation of Non-Methane Alkanes by "Candidatus Methanoliparia" in Hydrocarbon Seeps of the Gulf of Mexico

AU - Laso-Pérez, Rafael

AU - Hahn, Cedric

AU - van Vliet, Daan M.

AU - Tegetmeyer, Halina E.

AU - Schubotz, Florence

AU - Smit, Nadine T.

AU - Pape, Thomas

AU - Sahling, Heiko

AU - Bohrmann, Gerhard

AU - Boetius, Antje

AU - Knittel, Katrin

AU - Wegener, Gunter

PY - 2019/8/20

Y1 - 2019/8/20

N2 - 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.

AB - 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.

KW - alkane degradation

KW - archaea

KW - methanogenesis

KW - methyl-coenzyme M reductase

KW - oil seeps

U2 - 10.1128/mBio.01814-19

DO - 10.1128/mBio.01814-19

M3 - Article

VL - 10

JO - mBio

JF - mBio

SN - 2150-7511

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