Cryptic diversity of cellulose-degrading gut bacteria in industrialized humans

• 成果类型: Article
• 署名作者: Morais, Sarah; Winkler, Sarah; Zorea, Alvah; Levin, Liron; Nagies, Falk S. P.; Kapust, Nils; Lamed, Eva; Artan-Furman, Avital; Bolam, David N.; Yadav, Madhav P.; Bayer, Edward A.; Martin, William F.; Mizrahi, Itzhak
• 署名单位: Ben-Gurion University of the Negev; Ben-Gurion University of the Negev; Ben-Gurion University of the Negev; Ben-Gurion University of the Negev; Heinrich Heine University Dusseldorf; Weizmann Institute of Science; Newcastle University - UK; United States Department of Agriculture (USDA)
• 刊物名称: SCIENCE
• ISSN/ISSBN: 0036-12471
• DOI: 10.1126/science.adj9223
• 发表日期: 2024-03-15
• 关键词: dietary fiber; gene-cluster; metagenome; rumen; attachment; microbiota; genomes; enzymes; systems

摘要

INTRODUCTION Mammals, including humans, rely on their gut's microbial community to break down plant cell wall components, notably cellulose and associated polysaccharides. However, there is limited evidence for cellulose fermentation in the human gut despite the benefits of cellulose-containing dietary fiber for gut-microbiome health and overall human well-being. RATIONALE By investigating the presence of heretofore undescribed bacterial species within the human-gut microbiota that degrade complex cellulosic polysaccharides, we can reveal their potential sources and understand their intricate adaptations to diverse host lifestyles and diets. Insight into the prevalence and abundance of these bacteria across diverse mammalian species and a wide range of human populations will provide critical knowledge of their evolutionary origins, ancestral associations, and trajectories that enabled their incorporation into the human gut. RESULTS Previously unknown ruminococcal species were discovered in the human-gut microbiota and provisionally named Candidatus Ruminococcus primaciens, Ruminococcus hominiciens, and Ruminococcus ruminiciens, all of which assemble functional multienzymatic cellulosome systems that degrade crystalline cellulose. These species are prevalent among the great apes and other nonhuman primates, ancient human societies, hunter-gatherer communities, and rural populations. Although widespread geographically they are conspicuously rare within industrialized societies. Notably, they exhibit distinct host preferences wherein R. hominiciens is associated primarily with humans and great apes and R. primaciens predominantly inhabits the gut of nonhuman primates and ancient human populations. Moreover, these species display host-specific diversification, forming distinct clades within the phylogenetic tree and aligning with their respective hosts. Our evolutionary analysis strongly suggests that R. hominiciens likely originated in the ruminant gut and later transferred to humans, possibly during domestication. High gene expression levels were observed for these species, reflecting their considerable activity in their respective gut systems. Furthermore, their gene expression profile aligns with their hosts' dietary preferences, highlighting their adaptability. Our analyses show that these novel species adapt to their host ecosystems by acquiring genes from co-resident gut microbes. The human-associated strains possess functional adaptability highlighted by the acquisition of genes that can degrade specific plant fibers of monocots such as maize, rice, and wheat-major components of the human diet. Likewise, the nonhuman primate-associated strain exhibits the potential for degrading chitin, a polymer abundant in the insect exoskeleton, part of the diet of nonhuman primates. Our data provide insight into the ongoing colonization of these species within the human gut, particularly those originating from ruminants and nonhuman primates. Specific strains appear to represent intermediates between primate- and rumen-gut ecosystems, as evidenced by their gene content during establishment in the human intestine. CONCLUSION Our accumulated data indicate that ruminococcal lineages were more widespread in the past, evidenced by the high prevalence and abundance of these strains in ancient human populations and among hunter gatherer communities and rural societies, combined with their global distribution and low prevalence in industrialized societies. Differences in their prevalence among human populations may reflect dietary variation between industrialized and nonindustrialized societies. Dietary fiber intake appears to be a key factor as high-fiber diets are reported among Hadza hunter-gatherers whereas lower fiber intake is observed in rural populations and the least consumption of fiber occurs in industrialized societies. These findings collectively imply a decline of these species in the human gut, likely influenced by the shift toward westernized lifestyles, potentially impacting energy balance and other health-related aspects. The presence of transitional strains that recently colonized the human gut indicates that ruminants and nonhuman primates could be a source and reservoir for cellulosome-producing ruminococcal strains, which continue to colonize and adapt to the human gut. There may be potential for intentional reintroduction or enrichment of these species in the human gut through targeted dietary approaches and specialized probiotics. Cellulose degrading gut bacteria of hominids across evolutionary time. Previously unknown human gut cellulolytic ruminococcal species are highly prevalent in nonhuman primates, the great apes, ancient human populations, hunter-gatherer communities, and in rural populations but are rare in urbanized human populations.