Novel Chloroflexi genomes from the deepest ocean reveal metabolic strategies for the adaptation to deep-sea habitats
Abstract 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 sup...
| Main Authors: | , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
BMC
2022-05-01
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| Series: | Microbiome |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s40168-022-01263-6 |
| _version_ | 1828365169161404416 |
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| author | Rulong Liu Xing Wei Weizhi Song Li Wang Junwei Cao Jiaxin Wu Torsten Thomas Tao Jin Zixuan Wang Wenxia Wei Yuli Wei Haofeng Zhai Cheng Yao Ziyi Shen Jiangtao Du Jiasong Fang |
| author_facet | Rulong Liu Xing Wei Weizhi Song Li Wang Junwei Cao Jiaxin Wu Torsten Thomas Tao Jin Zixuan Wang Wenxia Wei Yuli Wei Haofeng Zhai Cheng Yao Ziyi Shen Jiangtao Du Jiasong Fang |
| author_sort | Rulong Liu |
| collection | DOAJ |
| description | Abstract 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. Video Abstract |
| first_indexed | 2024-04-14T05:27:05Z |
| format | Article |
| id | doaj.art-7d4ce4cada8147d88842514ac19b40bd |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-04-14T05:27:05Z |
| publishDate | 2022-05-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-7d4ce4cada8147d88842514ac19b40bd2022-12-22T02:09:56ZengBMCMicrobiome2049-26182022-05-0110111710.1186/s40168-022-01263-6Novel Chloroflexi genomes from the deepest ocean reveal metabolic strategies for the adaptation to deep-sea habitatsRulong Liu0Xing Wei1Weizhi Song2Li Wang3Junwei Cao4Jiaxin Wu5Torsten Thomas6Tao Jin7Zixuan Wang8Wenxia Wei9Yuli Wei10Haofeng Zhai11Cheng Yao12Ziyi Shen13Jiangtao Du14Jiasong Fang15Shanghai Engineering Research Center of Hadal Science and Technology, College of Marine Sciences, Shanghai Ocean UniversityShanghai Engineering Research Center of Hadal Science and Technology, College of Marine Sciences, Shanghai Ocean UniversityCentre for Marine Science & Innovation and School of Biological Earth and Environmental Science, University of New South WalesShanghai Engineering Research Center of Hadal Science and Technology, College of Marine Sciences, Shanghai Ocean UniversityShanghai Engineering Research Center of Hadal Science and Technology, College of Marine Sciences, Shanghai Ocean UniversityShanghai Engineering Research Center of Hadal Science and Technology, College of Marine Sciences, Shanghai Ocean UniversityCentre for Marine Science & Innovation and School of Biological Earth and Environmental Science, University of New South WalesBGI-ShenzhenTidal Flat Research Center of Jiangsu ProvinceShanghai Engineering Research Center of Hadal Science and Technology, College of Marine Sciences, Shanghai Ocean UniversityShanghai Engineering Research Center of Hadal Science and Technology, College of Marine Sciences, Shanghai Ocean UniversityShanghai Engineering Research Center of Hadal Science and Technology, College of Marine Sciences, Shanghai Ocean UniversityShanghai Engineering Research Center of Hadal Science and Technology, College of Marine Sciences, Shanghai Ocean UniversityShanghai Engineering Research Center of Hadal Science and Technology, College of Marine Sciences, Shanghai Ocean UniversityShanghai Engineering Research Center of Hadal Science and Technology, College of Marine Sciences, Shanghai Ocean UniversityShanghai Engineering Research Center of Hadal Science and Technology, College of Marine Sciences, Shanghai Ocean UniversityAbstract 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. Video Abstracthttps://doi.org/10.1186/s40168-022-01263-6ChloroflexiMetagenome-assembled-genomesMetabolic potentialPersistent organic pollutantPAHPCB |
| spellingShingle | Rulong Liu Xing Wei Weizhi Song Li Wang Junwei Cao Jiaxin Wu Torsten Thomas Tao Jin Zixuan Wang Wenxia Wei Yuli Wei Haofeng Zhai Cheng Yao Ziyi Shen Jiangtao Du Jiasong Fang Novel Chloroflexi genomes from the deepest ocean reveal metabolic strategies for the adaptation to deep-sea habitats Microbiome Chloroflexi Metagenome-assembled-genomes Metabolic potential Persistent organic pollutant PAH PCB |
| 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 | Chloroflexi Metagenome-assembled-genomes Metabolic potential Persistent organic pollutant PAH PCB |
| url | https://doi.org/10.1186/s40168-022-01263-6 |
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