{"title":"Mutualism between degraders and nondegraders stabilizes the function of a natural biopolymer-degrading community","authors":"Liang Liu, Changfu Tian, Miaoxiao Wang, Ying Luo, Yaru Huang, Tingting Jiang, Hongwen Zhao, Qijun Yu, Entao Wang, Jinshui Yang, Hongli Yuan","doi":"10.1073/pnas.2500664122","DOIUrl":null,"url":null,"abstract":"Natural biopolymer-degrading microbial communities drive carbon biogeochemical cycling. Within these communities, polymer degraders facilitate the growth of nondegraders by breaking down polymers through extracellular enzymes. However, the contributions of nondegraders to community dynamics, as well as the mechanisms that limit their access to degradation products, remain poorly understood. Here, we investigate EMSD5, a lignocellulose-degrading microbial community that efficiently converts corncob into isopropanol. We demonstrate that nondegraders, such as <jats:italic toggle=\"yes\">Escherichia coli</jats:italic> , enable the growth of degraders (e.g., <jats:italic toggle=\"yes\">Lachnoclostridium</jats:italic> sp. and <jats:italic toggle=\"yes\">Clostridium beijerinckii</jats:italic> ) by creating anaerobic conditions and supplying biotin. Within such expanded niches, lignocellulose degradation proceeds sequentially, and the availability of breakdown products to <jats:italic toggle=\"yes\">E</jats:italic> . <jats:italic toggle=\"yes\">coli</jats:italic> is constrained by two interlinked processes. Specifically, <jats:italic toggle=\"yes\">Lachnoclostridium</jats:italic> sp. produces oligosaccharides that are largely inaccessible to <jats:italic toggle=\"yes\">E</jats:italic> . <jats:italic toggle=\"yes\">coli</jats:italic> . A subset of these oligosaccharides is utilized by <jats:italic toggle=\"yes\">C</jats:italic> . <jats:italic toggle=\"yes\">beijerinckii</jats:italic> to produce monosaccharides that support <jats:italic toggle=\"yes\">E</jats:italic> . <jats:italic toggle=\"yes\">coli</jats:italic> growth, while glycosidase secretion by <jats:italic toggle=\"yes\">C</jats:italic> . <jats:italic toggle=\"yes\">beijerinckii</jats:italic> is reduced under coculture conditions. Building on these findings, we designed a synthetic consortium by coculturing <jats:italic toggle=\"yes\">C. beijerinckii</jats:italic> with an engineered <jats:italic toggle=\"yes\">E</jats:italic> . <jats:italic toggle=\"yes\">coli</jats:italic> strain that expresses xylanase genes from an unculturable <jats:italic toggle=\"yes\">Lachnoclostridium</jats:italic> . This consortium achieved isopropanol production from hemicellulose without requiring anaerobic conditions. Our findings reveal the niche-expanding role of nondegraders and the processes that constrain their access to degradation products, offering insights into maintaining stable cooperation in biopolymer-degrading communities and designing efficient consortia for biopolymer conversion.","PeriodicalId":20548,"journal":{"name":"Proceedings of the National Academy of Sciences of the United States of America","volume":"12 1","pages":""},"PeriodicalIF":9.1000,"publicationDate":"2025-07-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Proceedings of the National Academy of Sciences of the United States of America","FirstCategoryId":"103","ListUrlMain":"https://doi.org/10.1073/pnas.2500664122","RegionNum":1,"RegionCategory":"综合性期刊","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"MULTIDISCIPLINARY SCIENCES","Score":null,"Total":0}
引用次数: 0
Abstract
Natural biopolymer-degrading microbial communities drive carbon biogeochemical cycling. Within these communities, polymer degraders facilitate the growth of nondegraders by breaking down polymers through extracellular enzymes. However, the contributions of nondegraders to community dynamics, as well as the mechanisms that limit their access to degradation products, remain poorly understood. Here, we investigate EMSD5, a lignocellulose-degrading microbial community that efficiently converts corncob into isopropanol. We demonstrate that nondegraders, such as Escherichia coli , enable the growth of degraders (e.g., Lachnoclostridium sp. and Clostridium beijerinckii ) by creating anaerobic conditions and supplying biotin. Within such expanded niches, lignocellulose degradation proceeds sequentially, and the availability of breakdown products to E . coli is constrained by two interlinked processes. Specifically, Lachnoclostridium sp. produces oligosaccharides that are largely inaccessible to E . coli . A subset of these oligosaccharides is utilized by C . beijerinckii to produce monosaccharides that support E . coli growth, while glycosidase secretion by C . beijerinckii is reduced under coculture conditions. Building on these findings, we designed a synthetic consortium by coculturing C. beijerinckii with an engineered E . coli strain that expresses xylanase genes from an unculturable Lachnoclostridium . This consortium achieved isopropanol production from hemicellulose without requiring anaerobic conditions. Our findings reveal the niche-expanding role of nondegraders and the processes that constrain their access to degradation products, offering insights into maintaining stable cooperation in biopolymer-degrading communities and designing efficient consortia for biopolymer conversion.
期刊介绍:
The Proceedings of the National Academy of Sciences (PNAS), a peer-reviewed journal of the National Academy of Sciences (NAS), serves as an authoritative source for high-impact, original research across the biological, physical, and social sciences. With a global scope, the journal welcomes submissions from researchers worldwide, making it an inclusive platform for advancing scientific knowledge.