Microbial transmission in the social microbiome and host health and disease

Abstract

Although social interactions are known to drive pathogen transmission, the contributions of socially transmissible host-associated mutualists and commensals to host health and disease remain poorly explored. We use the concept of the social microbiome-the microbial metacommunity of a social network of hosts-to analyze the implications of social microbial transmission for host health and disease. We investigate the contributions of socially transmissible microbes to both eco-evolutionary microbiome community processes (colonization resistance, the evolution of virulence, and reactions to ecological disturbance) and microbial transmission-based processes (transmission of microbes with metabolic and immune effects, inter-specific transmission, transmission of antibiotic-resistant microbes, and transmission of viruses). We consider the implications of social microbial transmission for communicable and non-communicable diseases and evaluate the importance of a socially transmissible component underlying canonically non-communicable diseases. The social transmission of mutualists and commensals may play a significant, under-appreciated role in the social determinants of health and may act as a hidden force in social evolution.

The authors thank Cary Allen-Blevins, Melanie Colvin, Arjun Dutta, Mira-Rose Kingsbury Lee, Timothy Kistner, Grace Rubin, Laura Schell, Emily Venable, and Nikolas Weyland for feedback on various aspects of the manuscript. A.S., C.J.A.M., S.H., N.G.O.I., K.V.-A.J., and J.H. declare no relevant funding. A.R. reports funding from the Kone Foundation (202007064). M.V.-C. reports funding from a Beatriz Galindo Junior Fellowship from the Spanish Ministry of Universities (BG22/00172) and a Knowledge Generation Project grant from the Spanish Ministry of Science and Innovation (PID2022-139328OA-I00). I.L.B. receives support from the NOMIS Foundation (GR108454-CON-80002144), the David and Lucile Packard Foundation, and from the Pew Charitable Trusts. E.A.A. reports funding from the National Science Foundation (DEB-1840223) and the National Institutes of Health (R01 AG071684). L.B.B. reports funding from the National Institutes of Health (R01 GM134376 and P30 DK042086). B.B.F. reports funding from the Canadian Institute for Advanced Research (FL-001238/Appt 2410; additional sponsor reference number: FS22-058/Appt 2410) and the Canadian Institutes of Health Research (FDN-159935). E.V.K. reports funding from the Intramural Research Program of the National Institutes of Health of the United States of America (National Library of Medicine). F.S.G. reports funding from the National Cancer Institute (1 K22 CA258960-01). R.N.C. reports funding from the National Science Foundation (BCS-1919892 and BCS-2142073), the William F. Milton Fund, and the Harvard University Dean’s Competitive Fund for Promising Scholarship. A.H.M. reports funding from the National Institute of General Medical Sciences (R35 GM138284). Figures 4 and 5 were originally prepared using BioRender.com