Guillaume Urtecho, Thomas Moody, Yiming Huang, Ravi U Sheth, Miles Richardson, Hélène C Descamps, Andrew Kaufman, Opeyemi Lekan, Zetian Zhang, Florencia Velez-Cortes, Yiming Qu, Lucas Cohen, Deirdre Ricaurte, Travis E Gibson, Georg K Gerber, Christoph A Thaiss, Harris H Wang
{"title":"哺乳动物肠道中超级定殖微生物群重塑生态位过程中的时空动态。","authors":"Guillaume Urtecho, Thomas Moody, Yiming Huang, Ravi U Sheth, Miles Richardson, Hélène C Descamps, Andrew Kaufman, Opeyemi Lekan, Zetian Zhang, Florencia Velez-Cortes, Yiming Qu, Lucas Cohen, Deirdre Ricaurte, Travis E Gibson, Georg K Gerber, Christoph A Thaiss, Harris H Wang","doi":"10.1016/j.cels.2024.10.007","DOIUrl":null,"url":null,"abstract":"<p><p>While fecal microbiota transplantation (FMT) has been shown to be effective in reversing gut dysbiosis, we lack an understanding of the fundamental processes underlying microbial engraftment in the mammalian gut. Here, we explored a murine gut colonization model leveraging natural inter-individual variations in gut microbiomes to elucidate the spatiotemporal dynamics of FMT. We identified a natural \"super-donor\" consortium that robustly engrafts into diverse recipients and resists reciprocal colonization. Temporal profiling of the gut microbiome showed an ordered succession of rapid engraftment by early colonizers within 72 h, followed by a slower emergence of late colonizers over 15-30 days. Moreover, engraftment was localized to distinct compartments of the gastrointestinal tract in a species-specific manner. Spatial metagenomic characterization suggested engraftment was mediated by simultaneous transfer of spatially co-localizing species from the super-donor consortia. These results offer a mechanism of super-donor colonization by which nutritional niches are expanded in a spatiotemporally dependent manner. A record of this paper's transparent peer review process is included in the supplemental information.</p>","PeriodicalId":93929,"journal":{"name":"Cell systems","volume":" ","pages":"1002-1017.e4"},"PeriodicalIF":0.0000,"publicationDate":"2024-11-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Spatiotemporal dynamics during niche remodeling by super-colonizing microbiota in the mammalian gut.\",\"authors\":\"Guillaume Urtecho, Thomas Moody, Yiming Huang, Ravi U Sheth, Miles Richardson, Hélène C Descamps, Andrew Kaufman, Opeyemi Lekan, Zetian Zhang, Florencia Velez-Cortes, Yiming Qu, Lucas Cohen, Deirdre Ricaurte, Travis E Gibson, Georg K Gerber, Christoph A Thaiss, Harris H Wang\",\"doi\":\"10.1016/j.cels.2024.10.007\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>While fecal microbiota transplantation (FMT) has been shown to be effective in reversing gut dysbiosis, we lack an understanding of the fundamental processes underlying microbial engraftment in the mammalian gut. Here, we explored a murine gut colonization model leveraging natural inter-individual variations in gut microbiomes to elucidate the spatiotemporal dynamics of FMT. We identified a natural \\\"super-donor\\\" consortium that robustly engrafts into diverse recipients and resists reciprocal colonization. Temporal profiling of the gut microbiome showed an ordered succession of rapid engraftment by early colonizers within 72 h, followed by a slower emergence of late colonizers over 15-30 days. Moreover, engraftment was localized to distinct compartments of the gastrointestinal tract in a species-specific manner. Spatial metagenomic characterization suggested engraftment was mediated by simultaneous transfer of spatially co-localizing species from the super-donor consortia. These results offer a mechanism of super-donor colonization by which nutritional niches are expanded in a spatiotemporally dependent manner. A record of this paper's transparent peer review process is included in the supplemental information.</p>\",\"PeriodicalId\":93929,\"journal\":{\"name\":\"Cell systems\",\"volume\":\" \",\"pages\":\"1002-1017.e4\"},\"PeriodicalIF\":0.0000,\"publicationDate\":\"2024-11-20\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Cell systems\",\"FirstCategoryId\":\"1085\",\"ListUrlMain\":\"https://doi.org/10.1016/j.cels.2024.10.007\",\"RegionNum\":0,\"RegionCategory\":null,\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"2024/11/13 0:00:00\",\"PubModel\":\"Epub\",\"JCR\":\"\",\"JCRName\":\"\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Cell systems","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1016/j.cels.2024.10.007","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/11/13 0:00:00","PubModel":"Epub","JCR":"","JCRName":"","Score":null,"Total":0}
Spatiotemporal dynamics during niche remodeling by super-colonizing microbiota in the mammalian gut.
While fecal microbiota transplantation (FMT) has been shown to be effective in reversing gut dysbiosis, we lack an understanding of the fundamental processes underlying microbial engraftment in the mammalian gut. Here, we explored a murine gut colonization model leveraging natural inter-individual variations in gut microbiomes to elucidate the spatiotemporal dynamics of FMT. We identified a natural "super-donor" consortium that robustly engrafts into diverse recipients and resists reciprocal colonization. Temporal profiling of the gut microbiome showed an ordered succession of rapid engraftment by early colonizers within 72 h, followed by a slower emergence of late colonizers over 15-30 days. Moreover, engraftment was localized to distinct compartments of the gastrointestinal tract in a species-specific manner. Spatial metagenomic characterization suggested engraftment was mediated by simultaneous transfer of spatially co-localizing species from the super-donor consortia. These results offer a mechanism of super-donor colonization by which nutritional niches are expanded in a spatiotemporally dependent manner. A record of this paper's transparent peer review process is included in the supplemental information.