Anaerobic degradation of organic carbon supports uncultured microbial populations in estuarine sediments
Abstract Background A large proportion of prokaryotic microbes in marine sediments remains uncultured, hindering our understanding of their ecological functions and metabolic features. Recent environmental metagenomic studies suggested that many of these uncultured microbes contribute to the degrada...
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| Format: | Article |
| Language: | English |
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BMC
2023-04-01
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| Series: | Microbiome |
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| Online Access: | https://doi.org/10.1186/s40168-023-01531-z |
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| author | Tiantian Yu Weichao Wu Wenyue Liang Yinzhao Wang Jialin Hou Yunru Chen Marcus Elvert Kai-Uwe Hinrichs Fengping Wang |
| author_facet | Tiantian Yu Weichao Wu Wenyue Liang Yinzhao Wang Jialin Hou Yunru Chen Marcus Elvert Kai-Uwe Hinrichs Fengping Wang |
| author_sort | Tiantian Yu |
| collection | DOAJ |
| description | Abstract Background A large proportion of prokaryotic microbes in marine sediments remains uncultured, hindering our understanding of their ecological functions and metabolic features. Recent environmental metagenomic studies suggested that many of these uncultured microbes contribute to the degradation of organic matter, accompanied by acetogenesis, but the supporting experimental evidence is limited. Results Estuarine sediments were incubated with different types of organic matters under anaerobic conditions, and the increase of uncultured bacterial populations was monitored. We found that (1) lignin stimulated the increase of uncultured bacteria within the class Dehalococcoidia. Their ability to metabolize lignin was further supported by the presence of genes associated with a nearly complete degradation pathway of phenolic monomers in the Dehalococcoidia metagenome-assembled genomes (MAGs). (2) The addition of cellulose stimulated the increase of bacteria in the phylum Ca. Fermentibacterota and family Fibrobacterales, a high copy number of genes encoding extracellular endoglucanase or/and 1,4-beta-cellobiosidase for cellulose decomposition and multiple sugar transporters were present in their MAGs. (3) Uncultured lineages in the order Bacteroidales and the family Leptospiraceae were enriched by the addition of casein and oleic acid, respectively, a high copy number of genes encoding extracellular peptidases, and the complete β-oxidation pathway were found in those MAGs of Bacteroidales and Leptospiraceae, respectively. (4) The growth of unclassified bacteria of the order Clostridiales was found after the addition of both casein and cellulose. Their MAGs contained multiple copies of genes for extracellular peptidases and endoglucanase. Additionally, 13C-labeled acetate was produced in the incubations when 13C-labeled dissolved inorganic carbon was provided. Conclusions Our results provide new insights into the roles of microorganisms during organic carbon degradation in anaerobic estuarine sediments and suggest that these macro and single molecular organic carbons support the persistence and increase of uncultivated bacteria. Acetogenesis is an additional important microbial process alongside organic carbon degradation. Video Abstract |
| first_indexed | 2024-04-09T16:22:58Z |
| format | Article |
| id | doaj.art-8478074e3c6e49b3bcc9a0b3fb0c34aa |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-04-09T16:22:58Z |
| publishDate | 2023-04-01 |
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| series | Microbiome |
| spelling | doaj.art-8478074e3c6e49b3bcc9a0b3fb0c34aa2023-04-23T11:23:40ZengBMCMicrobiome2049-26182023-04-0111111410.1186/s40168-023-01531-zAnaerobic degradation of organic carbon supports uncultured microbial populations in estuarine sedimentsTiantian Yu0Weichao Wu1Wenyue Liang2Yinzhao Wang3Jialin Hou4Yunru Chen5Marcus Elvert6Kai-Uwe Hinrichs7Fengping Wang8School of Oceanography, Shanghai Jiao Tong UniversityOrganic Geochemistry Group, MARUM-Center for Marine Environmental Sciences, University of BremenState Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology, Shanghai Jiao Tong UniversityState Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology, Shanghai Jiao Tong UniversityState Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology, Shanghai Jiao Tong UniversityState Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology, Shanghai Jiao Tong UniversityOrganic Geochemistry Group, MARUM-Center for Marine Environmental Sciences, University of BremenOrganic Geochemistry Group, MARUM-Center for Marine Environmental Sciences, University of BremenSchool of Oceanography, Shanghai Jiao Tong UniversityAbstract Background A large proportion of prokaryotic microbes in marine sediments remains uncultured, hindering our understanding of their ecological functions and metabolic features. Recent environmental metagenomic studies suggested that many of these uncultured microbes contribute to the degradation of organic matter, accompanied by acetogenesis, but the supporting experimental evidence is limited. Results Estuarine sediments were incubated with different types of organic matters under anaerobic conditions, and the increase of uncultured bacterial populations was monitored. We found that (1) lignin stimulated the increase of uncultured bacteria within the class Dehalococcoidia. Their ability to metabolize lignin was further supported by the presence of genes associated with a nearly complete degradation pathway of phenolic monomers in the Dehalococcoidia metagenome-assembled genomes (MAGs). (2) The addition of cellulose stimulated the increase of bacteria in the phylum Ca. Fermentibacterota and family Fibrobacterales, a high copy number of genes encoding extracellular endoglucanase or/and 1,4-beta-cellobiosidase for cellulose decomposition and multiple sugar transporters were present in their MAGs. (3) Uncultured lineages in the order Bacteroidales and the family Leptospiraceae were enriched by the addition of casein and oleic acid, respectively, a high copy number of genes encoding extracellular peptidases, and the complete β-oxidation pathway were found in those MAGs of Bacteroidales and Leptospiraceae, respectively. (4) The growth of unclassified bacteria of the order Clostridiales was found after the addition of both casein and cellulose. Their MAGs contained multiple copies of genes for extracellular peptidases and endoglucanase. Additionally, 13C-labeled acetate was produced in the incubations when 13C-labeled dissolved inorganic carbon was provided. Conclusions Our results provide new insights into the roles of microorganisms during organic carbon degradation in anaerobic estuarine sediments and suggest that these macro and single molecular organic carbons support the persistence and increase of uncultivated bacteria. Acetogenesis is an additional important microbial process alongside organic carbon degradation. Video Abstracthttps://doi.org/10.1186/s40168-023-01531-zEstuarine sedimentOrganic carbonAnaerobic degradationUncultured bacteriaAcetogenesis |
| spellingShingle | Tiantian Yu Weichao Wu Wenyue Liang Yinzhao Wang Jialin Hou Yunru Chen Marcus Elvert Kai-Uwe Hinrichs Fengping Wang Anaerobic degradation of organic carbon supports uncultured microbial populations in estuarine sediments Microbiome Estuarine sediment Organic carbon Anaerobic degradation Uncultured bacteria Acetogenesis |
| title | Anaerobic degradation of organic carbon supports uncultured microbial populations in estuarine sediments |
| title_full | Anaerobic degradation of organic carbon supports uncultured microbial populations in estuarine sediments |
| title_fullStr | Anaerobic degradation of organic carbon supports uncultured microbial populations in estuarine sediments |
| title_full_unstemmed | Anaerobic degradation of organic carbon supports uncultured microbial populations in estuarine sediments |
| title_short | Anaerobic degradation of organic carbon supports uncultured microbial populations in estuarine sediments |
| title_sort | anaerobic degradation of organic carbon supports uncultured microbial populations in estuarine sediments |
| topic | Estuarine sediment Organic carbon Anaerobic degradation Uncultured bacteria Acetogenesis |
| url | https://doi.org/10.1186/s40168-023-01531-z |
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