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Novel Chloroflexi genomes from the deepest ocean reveal metabolic strategies for the adaptation to deep-sea habitats

BACKGROUND: The deep sea harbors the majority of the microbial biomass in the ocean and is a key site for organic matter (OM) remineralization and storage in the biosphere. Microbial metabolism in the deep ocean is greatly controlled by the generally depleted but periodically fluctuating supply of O...

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Autores principales: Liu, Rulong, Wei, Xing, Song, Weizhi, Wang, Li, Cao, Junwei, Wu, Jiaxin, Thomas, Torsten, Jin, Tao, Wang, Zixuan, Wei, Wenxia, Wei, Yuli, Zhai, Haofeng, Yao, Cheng, Shen, Ziyi, Du, Jiangtao, Fang, Jiasong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9088039/
https://www.ncbi.nlm.nih.gov/pubmed/35538590
http://dx.doi.org/10.1186/s40168-022-01263-6
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author Liu, Rulong
Wei, Xing
Song, Weizhi
Wang, Li
Cao, Junwei
Wu, Jiaxin
Thomas, Torsten
Jin, Tao
Wang, Zixuan
Wei, Wenxia
Wei, Yuli
Zhai, Haofeng
Yao, Cheng
Shen, Ziyi
Du, Jiangtao
Fang, Jiasong
author_facet Liu, Rulong
Wei, Xing
Song, Weizhi
Wang, Li
Cao, Junwei
Wu, Jiaxin
Thomas, Torsten
Jin, Tao
Wang, Zixuan
Wei, Wenxia
Wei, Yuli
Zhai, Haofeng
Yao, Cheng
Shen, Ziyi
Du, Jiangtao
Fang, Jiasong
author_sort Liu, Rulong
collection PubMed
description BACKGROUND: The deep sea harbors the majority of the microbial biomass in the ocean and is a key site for organic matter (OM) remineralization and storage in the biosphere. Microbial metabolism in the deep ocean is greatly controlled by the generally depleted but periodically fluctuating supply of OM. Currently, little is known about metabolic potentials of dominant deep-sea microbes to cope with the variable OM inputs, especially for those living in the hadal trenches—the deepest part of the ocean. RESULTS: In this study, we report the first extensive examination of the metabolic potentials of hadal sediment Chloroflexi, a dominant phylum in hadal trenches and the global deep ocean. In total, 62 metagenome-assembled-genomes (MAGs) were reconstructed from nine metagenomic datasets derived from sediments of the Mariana Trench. These MAGs represent six novel species, four novel genera, one novel family, and one novel order within the classes Anaerolineae and Dehalococcoidia. Fragment recruitment showed that these MAGs are globally distributed in deep-sea waters and surface sediments, and transcriptomic analysis indicated their in situ activities. Metabolic reconstruction showed that hadal Chloroflexi mainly had a heterotrophic lifestyle, with the potential to degrade a wide range of organic carbon, sulfur, and halogenated compounds. Our results revealed for the first time that hadal Chloroflexi harbor pathways for the complete hydrolytic or oxidative degradation of various recalcitrant OM, including aromatic compounds (e.g., benzoate), polyaromatic hydrocarbons (e.g., fluorene), polychlorobiphenyl (e.g., 4-chlorobiphenyl), and organochlorine compounds (e.g., chloroalkanes, chlorocyclohexane). Moreover, these organisms showed the potential to synthesize energy storage compounds (e.g., trehalose) and had regulatory modules to respond to changes in nutrient conditions. These metabolic traits suggest that Chloroflexi may follow a “feast-or-famine” metabolic strategy, i.e., preferentially consume labile OM and store the energy intracellularly under OM-rich conditions, and utilize the stored energy or degrade recalcitrant OM for survival under OM-limited condition. CONCLUSION: This study expands the current knowledge on metabolic strategies in deep-ocean Chlorolfexi and highlights their significance in deep-sea carbon, sulfur, and halogen cycles. The metabolic plasticity likely provides Chloroflexi with advantages for survival under variable and heterogenic OM inputs in the deep ocean. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-022-01263-6.
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spelling pubmed-90880392022-05-11 Novel Chloroflexi genomes from the deepest ocean reveal metabolic strategies for the adaptation to deep-sea habitats Liu, Rulong Wei, Xing Song, Weizhi Wang, Li Cao, Junwei Wu, Jiaxin Thomas, Torsten Jin, Tao Wang, Zixuan Wei, Wenxia Wei, Yuli Zhai, Haofeng Yao, Cheng Shen, Ziyi Du, Jiangtao Fang, Jiasong Microbiome Research BACKGROUND: The deep sea harbors the majority of the microbial biomass in the ocean and is a key site for organic matter (OM) remineralization and storage in the biosphere. Microbial metabolism in the deep ocean is greatly controlled by the generally depleted but periodically fluctuating supply of OM. Currently, little is known about metabolic potentials of dominant deep-sea microbes to cope with the variable OM inputs, especially for those living in the hadal trenches—the deepest part of the ocean. RESULTS: In this study, we report the first extensive examination of the metabolic potentials of hadal sediment Chloroflexi, a dominant phylum in hadal trenches and the global deep ocean. In total, 62 metagenome-assembled-genomes (MAGs) were reconstructed from nine metagenomic datasets derived from sediments of the Mariana Trench. These MAGs represent six novel species, four novel genera, one novel family, and one novel order within the classes Anaerolineae and Dehalococcoidia. Fragment recruitment showed that these MAGs are globally distributed in deep-sea waters and surface sediments, and transcriptomic analysis indicated their in situ activities. Metabolic reconstruction showed that hadal Chloroflexi mainly had a heterotrophic lifestyle, with the potential to degrade a wide range of organic carbon, sulfur, and halogenated compounds. Our results revealed for the first time that hadal Chloroflexi harbor pathways for the complete hydrolytic or oxidative degradation of various recalcitrant OM, including aromatic compounds (e.g., benzoate), polyaromatic hydrocarbons (e.g., fluorene), polychlorobiphenyl (e.g., 4-chlorobiphenyl), and organochlorine compounds (e.g., chloroalkanes, chlorocyclohexane). Moreover, these organisms showed the potential to synthesize energy storage compounds (e.g., trehalose) and had regulatory modules to respond to changes in nutrient conditions. These metabolic traits suggest that Chloroflexi may follow a “feast-or-famine” metabolic strategy, i.e., preferentially consume labile OM and store the energy intracellularly under OM-rich conditions, and utilize the stored energy or degrade recalcitrant OM for survival under OM-limited condition. CONCLUSION: This study expands the current knowledge on metabolic strategies in deep-ocean Chlorolfexi and highlights their significance in deep-sea carbon, sulfur, and halogen cycles. The metabolic plasticity likely provides Chloroflexi with advantages for survival under variable and heterogenic OM inputs in the deep ocean. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-022-01263-6. BioMed Central 2022-05-10 /pmc/articles/PMC9088039/ /pubmed/35538590 http://dx.doi.org/10.1186/s40168-022-01263-6 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Liu, Rulong
Wei, Xing
Song, Weizhi
Wang, Li
Cao, Junwei
Wu, Jiaxin
Thomas, Torsten
Jin, Tao
Wang, Zixuan
Wei, Wenxia
Wei, Yuli
Zhai, Haofeng
Yao, Cheng
Shen, Ziyi
Du, Jiangtao
Fang, Jiasong
Novel Chloroflexi genomes from the deepest ocean reveal metabolic strategies for the adaptation to deep-sea habitats
title Novel Chloroflexi genomes from the deepest ocean reveal metabolic strategies for the adaptation to deep-sea habitats
title_full Novel Chloroflexi genomes from the deepest ocean reveal metabolic strategies for the adaptation to deep-sea habitats
title_fullStr Novel Chloroflexi genomes from the deepest ocean reveal metabolic strategies for the adaptation to deep-sea habitats
title_full_unstemmed Novel Chloroflexi genomes from the deepest ocean reveal metabolic strategies for the adaptation to deep-sea habitats
title_short Novel Chloroflexi genomes from the deepest ocean reveal metabolic strategies for the adaptation to deep-sea habitats
title_sort novel chloroflexi genomes from the deepest ocean reveal metabolic strategies for the adaptation to deep-sea habitats
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9088039/
https://www.ncbi.nlm.nih.gov/pubmed/35538590
http://dx.doi.org/10.1186/s40168-022-01263-6
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