Occurrence of methane oxidizing bacteria and methanogenic archaea in Earth’s cave systems: a metagenomic analysis

Alexander Allenby; Mark Cunningham; Alexandra Hillebrand-Voiculescu; Jean-Christophe Comte; Rory Doherty; Deepak Kumaresan

doi:10.3389/fevo.2022.909865

Occurrence of methane oxidizing bacteria and methanogenic archaea in Earth’s cave systems: a metagenomic analysis

Alexander Allenby, Mark Cunningham, Alexandra Hillebrand-Voiculescu, Jean-Christophe Comte, Rory Doherty, Deepak Kumaresan

Geography & Environment

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Abstract

Karst ecosystems represent up to 25% of the land surface and recent studies highlight their potential role as a sink for atmospheric methane. Despite this, there is limited knowledge of the diversity and distribution of methane-oxidizing bacteria (MOB) or methanogens in karst caves and the sub-surface environment in general. Here, we performed a survey of 14 shotgun metagenomes from cave ecosystems covering a broad set of environmental conditions, to compare the relative abundance and phylogenetic diversity of MOB and methanogens, targeting biomarker genes for methane monooxygenase (pmoA and mmoX) and methyl-coenzyme M reductase (mcrA). Taxonomic analysis of metagenomes showed 0.02–1.28% of classified reads were related to known MOB, of which Gammaproteobacterial MOB were the most abundant making up on average 70% of the surveyed caves’ MOB community. Potential for biogenic methane production in caves was also observed, with 0.008–0.39% of reads classified to methanogens and was dominated by sequences related to Methanosarcina. We have also generated a cave ecosystems protein database (CEPD) based on protein level assembly of cave metagenomes that can be used to profile genes of interest.

Original language	English
Article number	909865
Number of pages	14
Journal	Frontiers in Ecology and Evolution
Early online date	15 Aug 2022
DOIs	https://doi.org/10.3389/fevo.2022.909865
Publication status	Published - 15 Aug 2022

Bibliographical note

Funding
This study received funding from NERC DTP studentship to AA (NE/S007377/1-2429402), Department for Economy NI studentship to MC and QUB for funding to DK. RD and DK were supported by DfE US-Ireland R&D partnership project 154. AH-V was supported by CNCS-UEFISCDI project PN-IIIP4-ID-PCCF-2016-0016, PCCF 16/2018 (DARKFOOD, PI Dr. O. T. Moldovan).
Acknowledgments
The authors thank the funders of this study for their support.

Keywords

methanotrophs
methanogens
methane
karst cave
biogeochemical cycles

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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© 2022 Allenby, Cunningham, Hillebrand-Voiculescu, Comte, Doherty and Kumaresan. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. https://creativecommons.org/licenses/by/4.0/
Final published version, 4.74 MBLicence: CC BY

Cite this

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abstract = "Karst ecosystems represent up to 25% of the land surface and recent studies highlight their potential role as a sink for atmospheric methane. Despite this, there is limited knowledge of the diversity and distribution of methane-oxidizing bacteria (MOB) or methanogens in karst caves and the sub-surface environment in general. Here, we performed a survey of 14 shotgun metagenomes from cave ecosystems covering a broad set of environmental conditions, to compare the relative abundance and phylogenetic diversity of MOB and methanogens, targeting biomarker genes for methane monooxygenase (pmoA and mmoX) and methyl-coenzyme M reductase (mcrA). Taxonomic analysis of metagenomes showed 0.02–1.28% of classified reads were related to known MOB, of which Gammaproteobacterial MOB were the most abundant making up on average 70% of the surveyed caves{\textquoteright} MOB community. Potential for biogenic methane production in caves was also observed, with 0.008–0.39% of reads classified to methanogens and was dominated by sequences related to Methanosarcina. We have also generated a cave ecosystems protein database (CEPD) based on protein level assembly of cave metagenomes that can be used to profile genes of interest.",

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author = "Alexander Allenby and Mark Cunningham and Alexandra Hillebrand-Voiculescu and Jean-Christophe Comte and Rory Doherty and Deepak Kumaresan",

note = "Funding This study received funding from NERC DTP studentship to AA (NE/S007377/1-2429402), Department for Economy NI studentship to MC and QUB for funding to DK. RD and DK were supported by DfE US-Ireland R&D partnership project 154. AH-V was supported by CNCS-UEFISCDI project PN-IIIP4-ID-PCCF-2016-0016, PCCF 16/2018 (DARKFOOD, PI Dr. O. T. Moldovan). Acknowledgments The authors thank the funders of this study for their support.",

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AU - Comte, Jean-Christophe

AU - Doherty, Rory

AU - Kumaresan, Deepak

N1 - Funding This study received funding from NERC DTP studentship to AA (NE/S007377/1-2429402), Department for Economy NI studentship to MC and QUB for funding to DK. RD and DK were supported by DfE US-Ireland R&D partnership project 154. AH-V was supported by CNCS-UEFISCDI project PN-IIIP4-ID-PCCF-2016-0016, PCCF 16/2018 (DARKFOOD, PI Dr. O. T. Moldovan). Acknowledgments The authors thank the funders of this study for their support.

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N2 - Karst ecosystems represent up to 25% of the land surface and recent studies highlight their potential role as a sink for atmospheric methane. Despite this, there is limited knowledge of the diversity and distribution of methane-oxidizing bacteria (MOB) or methanogens in karst caves and the sub-surface environment in general. Here, we performed a survey of 14 shotgun metagenomes from cave ecosystems covering a broad set of environmental conditions, to compare the relative abundance and phylogenetic diversity of MOB and methanogens, targeting biomarker genes for methane monooxygenase (pmoA and mmoX) and methyl-coenzyme M reductase (mcrA). Taxonomic analysis of metagenomes showed 0.02–1.28% of classified reads were related to known MOB, of which Gammaproteobacterial MOB were the most abundant making up on average 70% of the surveyed caves’ MOB community. Potential for biogenic methane production in caves was also observed, with 0.008–0.39% of reads classified to methanogens and was dominated by sequences related to Methanosarcina. We have also generated a cave ecosystems protein database (CEPD) based on protein level assembly of cave metagenomes that can be used to profile genes of interest.

AB - Karst ecosystems represent up to 25% of the land surface and recent studies highlight their potential role as a sink for atmospheric methane. Despite this, there is limited knowledge of the diversity and distribution of methane-oxidizing bacteria (MOB) or methanogens in karst caves and the sub-surface environment in general. Here, we performed a survey of 14 shotgun metagenomes from cave ecosystems covering a broad set of environmental conditions, to compare the relative abundance and phylogenetic diversity of MOB and methanogens, targeting biomarker genes for methane monooxygenase (pmoA and mmoX) and methyl-coenzyme M reductase (mcrA). Taxonomic analysis of metagenomes showed 0.02–1.28% of classified reads were related to known MOB, of which Gammaproteobacterial MOB were the most abundant making up on average 70% of the surveyed caves’ MOB community. Potential for biogenic methane production in caves was also observed, with 0.008–0.39% of reads classified to methanogens and was dominated by sequences related to Methanosarcina. We have also generated a cave ecosystems protein database (CEPD) based on protein level assembly of cave metagenomes that can be used to profile genes of interest.

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KW - methanogens

KW - methane

KW - karst cave

KW - biogeochemical cycles

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DO - 10.3389/fevo.2022.909865

M3 - Article

SN - 2296-701X

JO - Frontiers in Ecology and Evolution

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M1 - 909865

ER -

Occurrence of methane oxidizing bacteria and methanogenic archaea in Earth’s cave systems: a metagenomic analysis

Abstract

Bibliographical note

Keywords

UN SDGs

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