Lignin Unlocks Stealth Carbon Sinks in Cold Seeps via Microbial Enzymatic Gatekeeping
Cold seep ecosystems serve as critical hubs in marine carbon cycling through methane emissions and organic matter processing. While terrestrial lignin constitutes a major fraction of persistent organic carbon in cold seep sediments, its microbial transformation pathways in deep-sea cold seep environ...
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American Association for the Advancement of Science (AAAS)
2025-01-01
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| Series: | Research |
| Online Access: | https://spj.science.org/doi/10.34133/research.0848 |
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| author | Jialing Li Jingchun Feng Pandeng Wang Mengzhuo Zhu Yongji Huang Ying Wu Junning Fan Junlin Hu Xiyang Dong Yingli Zhou Xuanyu Tao Si Zhang |
| author_facet | Jialing Li Jingchun Feng Pandeng Wang Mengzhuo Zhu Yongji Huang Ying Wu Junning Fan Junlin Hu Xiyang Dong Yingli Zhou Xuanyu Tao Si Zhang |
| author_sort | Jialing Li |
| collection | DOAJ |
| description | Cold seep ecosystems serve as critical hubs in marine carbon cycling through methane emissions and organic matter processing. While terrestrial lignin constitutes a major fraction of persistent organic carbon in cold seep sediments, its microbial transformation pathways in deep-sea cold seep environments remain unexplored. Here, we present the first comprehensive analysis of lignin distribution across sediment horizons at the Haima cold seep, coupled with a multi-omics investigation of microbial lignin metabolism. Laboratory enrichment of sediment communities employing lignin as the exclusive carbon substrate revealed substantial microbial community restructuring dominated by Burkholderiales, Pseudomonadales, and Rhizobiales lineages. Integrated omics resolved 2-tiered metabolic cascades: (a) enzymatic depolymerization via dyP-type peroxidases and LigEFG-mediated β-aryl ether cleavage, targeting syringyl and diarylpropane subunits; (b) funneling of aromatic intermediates through 4,5-/3,4-PDOG (protocatechuate dioxygenase) pathways into central carbon metabolism. Although direct methanogenesis was undetected, methylotrophic potential was evidenced through methane cycle gene expression patterns by lignin decomposers. Phylogenetic surveys further demonstrated the global prevalence of lignin decomposers across 12 major cold seep systems. These decomposers showed marked divergence in enzymatic repertoires compared to degraders from other ecosystems. Our findings establish 3 paradigm shifts: (a) The turnover rates of terrestrial organic carbon are likely underestimated in deep-sea ecosystems; (b) microbial consortia employ combinatorial enzymatic strategies distinct from terrestrial decomposition regimes; (c) methyl shunting from lignin breakdown primes methanogenic precursors, revealing cryptic linkages between refractory carbon cycling and greenhouse gas reservoirs. |
| format | Article |
| id | doaj-art-df4b80dde8dd4080841f13da5c3f544e |
| institution | Kabale University |
| issn | 2639-5274 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | American Association for the Advancement of Science (AAAS) |
| record_format | Article |
| series | Research |
| spelling | doaj-art-df4b80dde8dd4080841f13da5c3f544e2025-08-25T19:58:39ZengAmerican Association for the Advancement of Science (AAAS)Research2639-52742025-01-01810.34133/research.0848Lignin Unlocks Stealth Carbon Sinks in Cold Seeps via Microbial Enzymatic GatekeepingJialing Li0Jingchun Feng1Pandeng Wang2Mengzhuo Zhu3Yongji Huang4Ying Wu5Junning Fan6Junlin Hu7Xiyang Dong8Yingli Zhou9Xuanyu Tao10Si Zhang11Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou 511458, China.Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou 511458, China.School of Pharmacy, Shenzhen University Medical School, Shenzhen University, Shenzhen 518055, China.School of Ecology, Environmental, and Resources, Guangdong University of Technology, Guangzhou 510006, China.South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China.State Key Laboratory of Estuarine and Coastal Research East China Normal University, Shanghai 200662, China.State Key Laboratory of Estuarine and Coastal Research East China Normal University, Shanghai 200662, China.Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou 511458, China.Key Laboratory of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources, Xiamen 361005, China.Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou 511458, China.Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou 511458, China.Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou 511458, China.Cold seep ecosystems serve as critical hubs in marine carbon cycling through methane emissions and organic matter processing. While terrestrial lignin constitutes a major fraction of persistent organic carbon in cold seep sediments, its microbial transformation pathways in deep-sea cold seep environments remain unexplored. Here, we present the first comprehensive analysis of lignin distribution across sediment horizons at the Haima cold seep, coupled with a multi-omics investigation of microbial lignin metabolism. Laboratory enrichment of sediment communities employing lignin as the exclusive carbon substrate revealed substantial microbial community restructuring dominated by Burkholderiales, Pseudomonadales, and Rhizobiales lineages. Integrated omics resolved 2-tiered metabolic cascades: (a) enzymatic depolymerization via dyP-type peroxidases and LigEFG-mediated β-aryl ether cleavage, targeting syringyl and diarylpropane subunits; (b) funneling of aromatic intermediates through 4,5-/3,4-PDOG (protocatechuate dioxygenase) pathways into central carbon metabolism. Although direct methanogenesis was undetected, methylotrophic potential was evidenced through methane cycle gene expression patterns by lignin decomposers. Phylogenetic surveys further demonstrated the global prevalence of lignin decomposers across 12 major cold seep systems. These decomposers showed marked divergence in enzymatic repertoires compared to degraders from other ecosystems. Our findings establish 3 paradigm shifts: (a) The turnover rates of terrestrial organic carbon are likely underestimated in deep-sea ecosystems; (b) microbial consortia employ combinatorial enzymatic strategies distinct from terrestrial decomposition regimes; (c) methyl shunting from lignin breakdown primes methanogenic precursors, revealing cryptic linkages between refractory carbon cycling and greenhouse gas reservoirs.https://spj.science.org/doi/10.34133/research.0848 |
| spellingShingle | Jialing Li Jingchun Feng Pandeng Wang Mengzhuo Zhu Yongji Huang Ying Wu Junning Fan Junlin Hu Xiyang Dong Yingli Zhou Xuanyu Tao Si Zhang Lignin Unlocks Stealth Carbon Sinks in Cold Seeps via Microbial Enzymatic Gatekeeping Research |
| title | Lignin Unlocks Stealth Carbon Sinks in Cold Seeps via Microbial Enzymatic Gatekeeping |
| title_full | Lignin Unlocks Stealth Carbon Sinks in Cold Seeps via Microbial Enzymatic Gatekeeping |
| title_fullStr | Lignin Unlocks Stealth Carbon Sinks in Cold Seeps via Microbial Enzymatic Gatekeeping |
| title_full_unstemmed | Lignin Unlocks Stealth Carbon Sinks in Cold Seeps via Microbial Enzymatic Gatekeeping |
| title_short | Lignin Unlocks Stealth Carbon Sinks in Cold Seeps via Microbial Enzymatic Gatekeeping |
| title_sort | lignin unlocks stealth carbon sinks in cold seeps via microbial enzymatic gatekeeping |
| url | https://spj.science.org/doi/10.34133/research.0848 |
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