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Genomic Insights into Niche Partitioning across Sediment Depth among Anaerobic Methane-Oxidizing Archaea in Global Methane Seeps
Marine sediments are important methane reservoirs. Methane efflux from the seabed is significantly restricted by anaerobic methanotrophic (ANME) archaea through a process known as anaerobic oxidation of methane (AOM). Different clades of ANME archaea occupy distinct niches in methane seeps, but thei...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
American Society for Microbiology
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10134854/ https://www.ncbi.nlm.nih.gov/pubmed/36927099 http://dx.doi.org/10.1128/msystems.01179-22 |
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author | Chen, Jiawei Li, Yingdong Zhong, Cheng Xu, Zhimeng Lu, Guangyuan Jing, Hongmei Liu, Hongbin |
author_facet | Chen, Jiawei Li, Yingdong Zhong, Cheng Xu, Zhimeng Lu, Guangyuan Jing, Hongmei Liu, Hongbin |
author_sort | Chen, Jiawei |
collection | PubMed |
description | Marine sediments are important methane reservoirs. Methane efflux from the seabed is significantly restricted by anaerobic methanotrophic (ANME) archaea through a process known as anaerobic oxidation of methane (AOM). Different clades of ANME archaea occupy distinct niches in methane seeps, but their underlying molecular mechanisms still need to be fully understood. To provide genetic explanations for the niche partitioning of ANME archaea, we applied comparative genomic analysis to ANME archaeal genomes retrieved from global methane seeps. Our results showed that ANME-2 archaea are more prevalent than ANME-1 archaea in shallow sediments because they carry genes that encode a significantly higher number of outer membrane multiheme c-type cytochromes and flagellar proteins. These features make ANME-2 archaea perform direct interspecies electron transfer better and benefit more from electron acceptors in AOM. Besides, ANME-2 archaea carry genes that encode extra peroxidase compared to ANME-1 archaea, which may lead to ANME-2 archaea better tolerating oxygen toxicity. In contrast, ANME-1 archaea are more competitive in deep layers than ANME-2 archaea because they carry extra genes (mtb and mtt) for methylotrophic methanogenesis and a significantly higher number of frh and mvh genes for hydrogenotrophic methanogenesis. Additionally, ANME-1 archaea carry exclusive genes (sqr, TST, and mddA) involved in sulfide detoxification compared to ANME-2 archaea, leading to stronger sulfide tolerance. Overall, this study reveals the genomic mechanisms shaping the niche partitioning among ANME archaea in global methane seeps. IMPORTANCE Anaerobic methanotrophic (ANME) archaea are important methanotrophs in marine sediment, controlling the flux of biologically generated methane, which plays an essential role in the marine carbon cycle and climate change. So far, no strain of this lineage has been isolated in pure culture, which makes metagenomics one of the fundamental approaches to reveal their metabolic potential. Although the niche partitioning of ANME archaea was frequently reported in different studies, whether this pattern was consistent in global methane seeps had yet to be verified, and little was known about the genetic mechanisms underlying it. Here, we reviewed and analyzed the community structure of ANME archaea in global methane seeps and indicated that the niche partitioning of ANME archaea was statistically supported. Our comparative genomic analysis indicated that the capabilities of interspecies electron transfer, methanogenesis, and the resistance of oxygen and hydrogen sulfide could be critical in defining the distribution of ANME archaea in methane seep sediment. |
format | Online Article Text |
id | pubmed-10134854 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | American Society for Microbiology |
record_format | MEDLINE/PubMed |
spelling | pubmed-101348542023-04-28 Genomic Insights into Niche Partitioning across Sediment Depth among Anaerobic Methane-Oxidizing Archaea in Global Methane Seeps Chen, Jiawei Li, Yingdong Zhong, Cheng Xu, Zhimeng Lu, Guangyuan Jing, Hongmei Liu, Hongbin mSystems Research Article Marine sediments are important methane reservoirs. Methane efflux from the seabed is significantly restricted by anaerobic methanotrophic (ANME) archaea through a process known as anaerobic oxidation of methane (AOM). Different clades of ANME archaea occupy distinct niches in methane seeps, but their underlying molecular mechanisms still need to be fully understood. To provide genetic explanations for the niche partitioning of ANME archaea, we applied comparative genomic analysis to ANME archaeal genomes retrieved from global methane seeps. Our results showed that ANME-2 archaea are more prevalent than ANME-1 archaea in shallow sediments because they carry genes that encode a significantly higher number of outer membrane multiheme c-type cytochromes and flagellar proteins. These features make ANME-2 archaea perform direct interspecies electron transfer better and benefit more from electron acceptors in AOM. Besides, ANME-2 archaea carry genes that encode extra peroxidase compared to ANME-1 archaea, which may lead to ANME-2 archaea better tolerating oxygen toxicity. In contrast, ANME-1 archaea are more competitive in deep layers than ANME-2 archaea because they carry extra genes (mtb and mtt) for methylotrophic methanogenesis and a significantly higher number of frh and mvh genes for hydrogenotrophic methanogenesis. Additionally, ANME-1 archaea carry exclusive genes (sqr, TST, and mddA) involved in sulfide detoxification compared to ANME-2 archaea, leading to stronger sulfide tolerance. Overall, this study reveals the genomic mechanisms shaping the niche partitioning among ANME archaea in global methane seeps. IMPORTANCE Anaerobic methanotrophic (ANME) archaea are important methanotrophs in marine sediment, controlling the flux of biologically generated methane, which plays an essential role in the marine carbon cycle and climate change. So far, no strain of this lineage has been isolated in pure culture, which makes metagenomics one of the fundamental approaches to reveal their metabolic potential. Although the niche partitioning of ANME archaea was frequently reported in different studies, whether this pattern was consistent in global methane seeps had yet to be verified, and little was known about the genetic mechanisms underlying it. Here, we reviewed and analyzed the community structure of ANME archaea in global methane seeps and indicated that the niche partitioning of ANME archaea was statistically supported. Our comparative genomic analysis indicated that the capabilities of interspecies electron transfer, methanogenesis, and the resistance of oxygen and hydrogen sulfide could be critical in defining the distribution of ANME archaea in methane seep sediment. American Society for Microbiology 2023-03-16 /pmc/articles/PMC10134854/ /pubmed/36927099 http://dx.doi.org/10.1128/msystems.01179-22 Text en Copyright © 2023 Chen et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Research Article Chen, Jiawei Li, Yingdong Zhong, Cheng Xu, Zhimeng Lu, Guangyuan Jing, Hongmei Liu, Hongbin Genomic Insights into Niche Partitioning across Sediment Depth among Anaerobic Methane-Oxidizing Archaea in Global Methane Seeps |
title | Genomic Insights into Niche Partitioning across Sediment Depth among Anaerobic Methane-Oxidizing Archaea in Global Methane Seeps |
title_full | Genomic Insights into Niche Partitioning across Sediment Depth among Anaerobic Methane-Oxidizing Archaea in Global Methane Seeps |
title_fullStr | Genomic Insights into Niche Partitioning across Sediment Depth among Anaerobic Methane-Oxidizing Archaea in Global Methane Seeps |
title_full_unstemmed | Genomic Insights into Niche Partitioning across Sediment Depth among Anaerobic Methane-Oxidizing Archaea in Global Methane Seeps |
title_short | Genomic Insights into Niche Partitioning across Sediment Depth among Anaerobic Methane-Oxidizing Archaea in Global Methane Seeps |
title_sort | genomic insights into niche partitioning across sediment depth among anaerobic methane-oxidizing archaea in global methane seeps |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10134854/ https://www.ncbi.nlm.nih.gov/pubmed/36927099 http://dx.doi.org/10.1128/msystems.01179-22 |
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