A core microbiome signature as an indicator of health

Guojun Wu; Ting Xu; Naisi Zhao; Yan Y Lam; Xiaoying Ding; Dongqin Wei; Jian Fan; Yajuan Shi; Xiaofeng Li; Mi Li; Shenjie Ji; Xuejiao Wang; Huaqing Fu; Feng Zhang; Yu Shi; Chenhong Zhang; Yongde Peng; Liping Zhao

doi:10.1016/j.cell.2024.09.019

A core microbiome signature as an indicator of health

Cell. 2024 Oct 7:S0092-8674(24)01038-9. doi: 10.1016/j.cell.2024.09.019. Online ahead of print.

Authors

Guojun Wu¹, Ting Xu², Naisi Zhao³, Yan Y Lam⁴, Xiaoying Ding⁵, Dongqin Wei⁶, Jian Fan⁶, Yajuan Shi⁶, Xiaofeng Li⁶, Mi Li⁶, Shenjie Ji⁶, Xuejiao Wang⁵, Huaqing Fu², Feng Zhang⁷, Yu Shi⁸, Chenhong Zhang⁹, Yongde Peng¹⁰, Liping Zhao¹¹

Affiliations

¹ Department of Biochemistry and Microbiology, School of Environmental and Biological Sciences and Center for Microbiome, Nutrition, and Health, New Jersey Institute for Food, Nutrition, and Health, Rutgers, The State University of New Jersey, New Brunswick, NJ 08901, USA; Rutgers-Jiaotong Joint Laboratory for Microbiome and Human Health, New Brunswick, NJ, USA.
² State Key Laboratory of Microbial Metabolism and Ministry of Education Key Laboratory of Systems Biomedicine, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China.
³ Department of Public Health and Community Medicine, School of Medicine, Tufts University, Boston, MA 02111, USA.
⁴ Department of Medicine, School of Clinical Medicine, LKS Faculty of Medicine, The University of Hong Kong, Hong Kong SAR, China.
⁵ Department of Endocrinology and Metabolism, Shanghai General Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200080, China.
⁶ Department of Endocrinology and Metabolism, Qidong People's Hospital, Qidong, Jiangsu 226200, China.
⁷ Nutrition Department (Clinical Study Center of Functional Food), The Affiliated Hospital of Jiangnan University Wuxi, Wuxi, Jiangsu 214122, China.
⁸ Department of Endocrinology and Metabolism, Qidong People's Hospital, Qidong, Jiangsu 226200, China. Electronic address: 2383994147@qq.com.
⁹ State Key Laboratory of Microbial Metabolism and Ministry of Education Key Laboratory of Systems Biomedicine, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China. Electronic address: zhangchenhong@sjtu.edu.cn.
¹⁰ Department of Endocrinology and Metabolism, Shanghai General Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200080, China. Electronic address: pengyongde0908@126.com.
¹¹ State Key Laboratory of Microbial Metabolism and Ministry of Education Key Laboratory of Systems Biomedicine, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China; Department of Biochemistry and Microbiology, School of Environmental and Biological Sciences and Center for Microbiome, Nutrition, and Health, New Jersey Institute for Food, Nutrition, and Health, Rutgers, The State University of New Jersey, New Brunswick, NJ 08901, USA; Rutgers-Jiaotong Joint Laboratory for Microbiome and Human Health, New Brunswick, NJ, USA. Electronic address: liping.zhao@rutgers.edu.

PMID: 39378879
DOI: 10.1016/j.cell.2024.09.019

Abstract

The gut microbiota is crucial for human health, functioning as a complex adaptive system akin to a vital organ. To identify core health-relevant gut microbes, we followed the systems biology tenet that stable relationships signify core components. By analyzing metagenomic datasets from a high-fiber dietary intervention in type 2 diabetes and 26 case-control studies across 15 diseases, we identified a set of stably correlated genome pairs within co-abundance networks perturbed by dietary interventions and diseases. These genomes formed a "two competing guilds" (TCGs) model, with one guild specialized in fiber fermentation and butyrate production and the other characterized by virulence and antibiotic resistance. Our random forest models successfully distinguished cases from controls across multiple diseases and predicted immunotherapy outcomes through the use of these genomes. Our guild-based approach, which is genome specific, database independent, and interaction focused, identifies a core microbiome signature that serves as a holistic health indicator and a potential common target for health enhancement.

Keywords: core microbiome; guilds; gut health; stable relationships.