Fernanda Mandelli, Marcele Pandeló Martins, Mariana Chinaglia, Evandro Antonio de Lima, Mariana Abrahão Bueno Morais, Tatiani Brenelli Lima, Lucélia Cabral, Renan Augusto Siqueira Pirolla, Felipe Jun Fuzita, Douglas Antônio Alvaredo Paixão, Maxuel de Oliveira Andrade, Lucia Daniela Wolf, Plinio Salmazo Vieira, Gabriela Felix Persinoti, Mario Tyago Murakami
{"title":"来自食草动物肠道微生物群的功能增强型碳水化合物利用位点,由食物中的β-葡聚糖提供燃料。","authors":"Fernanda Mandelli, Marcele Pandeló Martins, Mariana Chinaglia, Evandro Antonio de Lima, Mariana Abrahão Bueno Morais, Tatiani Brenelli Lima, Lucélia Cabral, Renan Augusto Siqueira Pirolla, Felipe Jun Fuzita, Douglas Antônio Alvaredo Paixão, Maxuel de Oliveira Andrade, Lucia Daniela Wolf, Plinio Salmazo Vieira, Gabriela Felix Persinoti, Mario Tyago Murakami","doi":"10.1038/s41522-024-00578-6","DOIUrl":null,"url":null,"abstract":"<p><p>Gut microbiota members from the Bacteroidota phylum play a pivotal role in mammalian health and metabolism. They thrive in this diverse ecosystem due to their notable ability to cope with distinct recalcitrant dietary glycans via polysaccharide utilization loci (PULs). Our study reveals that a PUL from an herbivore gut bacterium belonging to the Bacteroidota phylum, with a gene composition similar to that in the human gut, exhibits extended functionality. While the human gut PUL targets mixed-linkage β-glucans specifically, the herbivore gut PUL also efficiently processes linear and substituted β-1,3-glucans. This gain of function emerges from molecular adaptations in recognition proteins and carbohydrate-active enzymes, including a β-glucosidase specialized for β(1,6)-glucosyl linkages, a typical substitution in β(1,3)-glucans. These findings broaden the existing model for non-cellulosic β-glucans utilization by gut bacteria, revealing an additional layer of functional and evolutionary complexity within the gut microbiota, beyond conventional gene insertions/deletions to intricate biochemical interactions.</p>","PeriodicalId":19370,"journal":{"name":"npj Biofilms and Microbiomes","volume":"10 1","pages":"105"},"PeriodicalIF":7.8000,"publicationDate":"2024-10-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11471779/pdf/","citationCount":"0","resultStr":"{\"title\":\"A functionally augmented carbohydrate utilization locus from herbivore gut microbiota fueled by dietary β-glucans.\",\"authors\":\"Fernanda Mandelli, Marcele Pandeló Martins, Mariana Chinaglia, Evandro Antonio de Lima, Mariana Abrahão Bueno Morais, Tatiani Brenelli Lima, Lucélia Cabral, Renan Augusto Siqueira Pirolla, Felipe Jun Fuzita, Douglas Antônio Alvaredo Paixão, Maxuel de Oliveira Andrade, Lucia Daniela Wolf, Plinio Salmazo Vieira, Gabriela Felix Persinoti, Mario Tyago Murakami\",\"doi\":\"10.1038/s41522-024-00578-6\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Gut microbiota members from the Bacteroidota phylum play a pivotal role in mammalian health and metabolism. They thrive in this diverse ecosystem due to their notable ability to cope with distinct recalcitrant dietary glycans via polysaccharide utilization loci (PULs). Our study reveals that a PUL from an herbivore gut bacterium belonging to the Bacteroidota phylum, with a gene composition similar to that in the human gut, exhibits extended functionality. While the human gut PUL targets mixed-linkage β-glucans specifically, the herbivore gut PUL also efficiently processes linear and substituted β-1,3-glucans. This gain of function emerges from molecular adaptations in recognition proteins and carbohydrate-active enzymes, including a β-glucosidase specialized for β(1,6)-glucosyl linkages, a typical substitution in β(1,3)-glucans. These findings broaden the existing model for non-cellulosic β-glucans utilization by gut bacteria, revealing an additional layer of functional and evolutionary complexity within the gut microbiota, beyond conventional gene insertions/deletions to intricate biochemical interactions.</p>\",\"PeriodicalId\":19370,\"journal\":{\"name\":\"npj Biofilms and Microbiomes\",\"volume\":\"10 1\",\"pages\":\"105\"},\"PeriodicalIF\":7.8000,\"publicationDate\":\"2024-10-14\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11471779/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"npj Biofilms and Microbiomes\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://doi.org/10.1038/s41522-024-00578-6\",\"RegionNum\":1,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"BIOTECHNOLOGY & APPLIED MICROBIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"npj Biofilms and Microbiomes","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1038/s41522-024-00578-6","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"BIOTECHNOLOGY & APPLIED MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0
摘要
类杆菌门的肠道微生物群成员在哺乳动物的健康和新陈代谢中发挥着举足轻重的作用。它们通过多糖利用位点(PULs)处理独特的难处理膳食糖的显著能力使它们在这个多样化的生态系统中茁壮成长。我们的研究发现,属于类杆菌门的一种食草动物肠道细菌的多糖利用位点(PUL)具有与人类肠道细菌相似的基因组成,并具有扩展功能。人类肠道 PUL 专攻混合连接的 β-葡聚糖,而食草动物肠道 PUL 也能有效处理线性和取代的 β-1,3-葡聚糖。这种功能的增加源于识别蛋白和碳水化合物活性酶的分子适应性,其中包括专门处理β(1,6)-葡萄糖基连接的β-葡萄糖苷酶,这是β(1,3)-葡聚糖中的典型替代物。这些发现拓宽了肠道细菌利用非纤维素 β-葡聚糖的现有模式,揭示了肠道微生物群内功能和进化的另一层复杂性,超越了传统的基因插入/缺失,而是错综复杂的生化相互作用。
A functionally augmented carbohydrate utilization locus from herbivore gut microbiota fueled by dietary β-glucans.
Gut microbiota members from the Bacteroidota phylum play a pivotal role in mammalian health and metabolism. They thrive in this diverse ecosystem due to their notable ability to cope with distinct recalcitrant dietary glycans via polysaccharide utilization loci (PULs). Our study reveals that a PUL from an herbivore gut bacterium belonging to the Bacteroidota phylum, with a gene composition similar to that in the human gut, exhibits extended functionality. While the human gut PUL targets mixed-linkage β-glucans specifically, the herbivore gut PUL also efficiently processes linear and substituted β-1,3-glucans. This gain of function emerges from molecular adaptations in recognition proteins and carbohydrate-active enzymes, including a β-glucosidase specialized for β(1,6)-glucosyl linkages, a typical substitution in β(1,3)-glucans. These findings broaden the existing model for non-cellulosic β-glucans utilization by gut bacteria, revealing an additional layer of functional and evolutionary complexity within the gut microbiota, beyond conventional gene insertions/deletions to intricate biochemical interactions.
期刊介绍:
npj Biofilms and Microbiomes is a comprehensive platform that promotes research on biofilms and microbiomes across various scientific disciplines. The journal facilitates cross-disciplinary discussions to enhance our understanding of the biology, ecology, and communal functions of biofilms, populations, and communities. It also focuses on applications in the medical, environmental, and engineering domains. The scope of the journal encompasses all aspects of the field, ranging from cell-cell communication and single cell interactions to the microbiomes of humans, animals, plants, and natural and built environments. The journal also welcomes research on the virome, phageome, mycome, and fungome. It publishes both applied science and theoretical work. As an open access and interdisciplinary journal, its primary goal is to publish significant scientific advancements in microbial biofilms and microbiomes. The journal enables discussions that span multiple disciplines and contributes to our understanding of the social behavior of microbial biofilm populations and communities, and their impact on life, human health, and the environment.