Characterization of Two Marine Lignin-Degrading Consortia and the Potential Microbial Lignin Degradation Network in Nearshore Regions
ABSTRACT Terrestrial organic carbon such as lignin is an important component of the global marine carbon. However, the structural complexity and recalcitrant nature of lignin are deemed challenging for biodegradation. It has been speculated that bacteria play important roles in lignin degradation in...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-06-01
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| Series: | Microbiology Spectrum |
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| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.04424-22 |
| _version_ | 1827925094566985728 |
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| author | Yvette Ley Xiao-Yu Cheng Zhi-Yue Ying Ning-Yi Zhou Ying Xu |
| author_facet | Yvette Ley Xiao-Yu Cheng Zhi-Yue Ying Ning-Yi Zhou Ying Xu |
| author_sort | Yvette Ley |
| collection | DOAJ |
| description | ABSTRACT Terrestrial organic carbon such as lignin is an important component of the global marine carbon. However, the structural complexity and recalcitrant nature of lignin are deemed challenging for biodegradation. It has been speculated that bacteria play important roles in lignin degradation in the marine system. However, the extent of the involvement of marine microorganisms in lignin degradation and their contribution to the oceanic carbon cycle remains elusive. In this study, two bacterial consortia capable of degrading alkali lignin (a model compound of lignin), designated LIG-B and LIG-S, were enriched from the nearshore sediments of the East and South China Seas. Consortia LIG-B and LIG-S mainly comprised of the Proteobacteria phylum with Nitratireductor sp. (71.6%) and Halomonas sp. (91.6%), respectively. Lignin degradation was found more favorable in consortium LIG-B (max 57%) than in LIG-S (max 18%). Ligninolytic enzymes laccase (Lac), manganese peroxidase (MnP), and lignin peroxidase (LiP) capable of decomposing lignin into smaller fragments were all active in both consortia. The newly emerged low-molecular-weight aromatics, organic acids, and other lignin-derived compounds in biotreated alkali lignin also evidently showed the depolymerization of lignin by both consortia. The lignin degradation pathways reconstructed from consortium LIG-S were found to be more comprehensive compared to consortium LIG-B. It was further revealed that catabolic genes, involved in the degradation of lignin and its derivatives through multiple pathways via protocatechuate and catechol, are present not only in lignin-degrading consortia LIG-B and LIG-S but also in 783 publicly available metagenomic-assembled genomes from nine nearshore regions. IMPORTANCE Numerous terrigenous lignin-containing plant materials are constantly discharged from rivers and estuaries into the marine system. However, only low levels of terrigenous organic carbon, especially lignin, are detected in the global marine system due to the abundance of active heterotrophic microorganisms driving the carbon cycle. Simultaneously, the lack of knowledge on lignin biodegradation has hindered our understanding of the oceanic carbon cycle. Moreover, bacteria have been speculated to play important roles in the marine lignin biodegradation. Here, we enriched two bacterial consortia from nearshore sediments capable of utilizing alkali lignin for cell growth while degrading it into smaller molecules and reconstructed the lignin degradation network. In particular, this study highlights that marine microorganisms in nearshore regions mostly undergo similar pathways using protocatechuate and catechol as ring-cleavage substrates to drive lignin degradation as part of the oceanic carbon cycle, regardless of whether they are in sediments or water column. |
| first_indexed | 2024-03-13T05:20:14Z |
| format | Article |
| id | doaj.art-8976a12d87ca4eb2a775aa5d4458b000 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-13T05:20:14Z |
| publishDate | 2023-06-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-8976a12d87ca4eb2a775aa5d4458b0002023-06-15T13:18:33ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-06-0111310.1128/spectrum.04424-22Characterization of Two Marine Lignin-Degrading Consortia and the Potential Microbial Lignin Degradation Network in Nearshore RegionsYvette Ley0Xiao-Yu Cheng1Zhi-Yue Ying2Ning-Yi Zhou3Ying Xu4State Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic and Developmental Sciences, and School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, ChinaState Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic and Developmental Sciences, and School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, ChinaState Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic and Developmental Sciences, and School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, ChinaState Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic and Developmental Sciences, and School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, ChinaState Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic and Developmental Sciences, and School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, ChinaABSTRACT Terrestrial organic carbon such as lignin is an important component of the global marine carbon. However, the structural complexity and recalcitrant nature of lignin are deemed challenging for biodegradation. It has been speculated that bacteria play important roles in lignin degradation in the marine system. However, the extent of the involvement of marine microorganisms in lignin degradation and their contribution to the oceanic carbon cycle remains elusive. In this study, two bacterial consortia capable of degrading alkali lignin (a model compound of lignin), designated LIG-B and LIG-S, were enriched from the nearshore sediments of the East and South China Seas. Consortia LIG-B and LIG-S mainly comprised of the Proteobacteria phylum with Nitratireductor sp. (71.6%) and Halomonas sp. (91.6%), respectively. Lignin degradation was found more favorable in consortium LIG-B (max 57%) than in LIG-S (max 18%). Ligninolytic enzymes laccase (Lac), manganese peroxidase (MnP), and lignin peroxidase (LiP) capable of decomposing lignin into smaller fragments were all active in both consortia. The newly emerged low-molecular-weight aromatics, organic acids, and other lignin-derived compounds in biotreated alkali lignin also evidently showed the depolymerization of lignin by both consortia. The lignin degradation pathways reconstructed from consortium LIG-S were found to be more comprehensive compared to consortium LIG-B. It was further revealed that catabolic genes, involved in the degradation of lignin and its derivatives through multiple pathways via protocatechuate and catechol, are present not only in lignin-degrading consortia LIG-B and LIG-S but also in 783 publicly available metagenomic-assembled genomes from nine nearshore regions. IMPORTANCE Numerous terrigenous lignin-containing plant materials are constantly discharged from rivers and estuaries into the marine system. However, only low levels of terrigenous organic carbon, especially lignin, are detected in the global marine system due to the abundance of active heterotrophic microorganisms driving the carbon cycle. Simultaneously, the lack of knowledge on lignin biodegradation has hindered our understanding of the oceanic carbon cycle. Moreover, bacteria have been speculated to play important roles in the marine lignin biodegradation. Here, we enriched two bacterial consortia from nearshore sediments capable of utilizing alkali lignin for cell growth while degrading it into smaller molecules and reconstructed the lignin degradation network. In particular, this study highlights that marine microorganisms in nearshore regions mostly undergo similar pathways using protocatechuate and catechol as ring-cleavage substrates to drive lignin degradation as part of the oceanic carbon cycle, regardless of whether they are in sediments or water column.https://journals.asm.org/doi/10.1128/spectrum.04424-22lignin biodegradationlignin-derived aromaticsligninolytic enzymesmarine consortianearshore regions |
| spellingShingle | Yvette Ley Xiao-Yu Cheng Zhi-Yue Ying Ning-Yi Zhou Ying Xu Characterization of Two Marine Lignin-Degrading Consortia and the Potential Microbial Lignin Degradation Network in Nearshore Regions Microbiology Spectrum lignin biodegradation lignin-derived aromatics ligninolytic enzymes marine consortia nearshore regions |
| title | Characterization of Two Marine Lignin-Degrading Consortia and the Potential Microbial Lignin Degradation Network in Nearshore Regions |
| title_full | Characterization of Two Marine Lignin-Degrading Consortia and the Potential Microbial Lignin Degradation Network in Nearshore Regions |
| title_fullStr | Characterization of Two Marine Lignin-Degrading Consortia and the Potential Microbial Lignin Degradation Network in Nearshore Regions |
| title_full_unstemmed | Characterization of Two Marine Lignin-Degrading Consortia and the Potential Microbial Lignin Degradation Network in Nearshore Regions |
| title_short | Characterization of Two Marine Lignin-Degrading Consortia and the Potential Microbial Lignin Degradation Network in Nearshore Regions |
| title_sort | characterization of two marine lignin degrading consortia and the potential microbial lignin degradation network in nearshore regions |
| topic | lignin biodegradation lignin-derived aromatics ligninolytic enzymes marine consortia nearshore regions |
| url | https://journals.asm.org/doi/10.1128/spectrum.04424-22 |
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