Microbial transmission in the social microbiome and host health and disease

Amar Sarkar; Cameron J A McInroy; Siobhán Harty; Aura Raulo; Neil G O Ibata; Mireia Valles-Colomer; Katerina V-A Johnson; Ilana L Brito; Joseph Henrich; Elizabeth A Archie; Luis B Barreiro; Francesca S Gazzaniga; B Brett Finlay; Eugene V Koonin; Rachel N Carmody; Andrew H Moeller

doi:10.1016/j.cell.2023.12.014

Microbial transmission in the social microbiome and host health and disease

Cell. 2024 Jan 4;187(1):17-43. doi: 10.1016/j.cell.2023.12.014.

Authors

Amar Sarkar¹, Cameron J A McInroy², Siobhán Harty³, Aura Raulo⁴, Neil G O Ibata², Mireia Valles-Colomer⁵, Katerina V-A Johnson⁶, Ilana L Brito⁷, Joseph Henrich², Elizabeth A Archie⁸, Luis B Barreiro⁹, Francesca S Gazzaniga¹⁰, B Brett Finlay¹¹, Eugene V Koonin¹², Rachel N Carmody², Andrew H Moeller¹³

Affiliations

¹ Department of Human Evolutionary Biology, Harvard University, Cambridge, MA, USA. Electronic address: amarsarkar@g.harvard.edu.
² Department of Human Evolutionary Biology, Harvard University, Cambridge, MA, USA.
³ Independent, Tandy Court, Spitalfields, Dublin, Ireland.
⁴ Department of Biology, University of Oxford, Oxford, UK; Department of Computing, University of Turku, Turku, Finland.
⁵ Department of Medicine and Life Sciences, Pompeu Fabra University, Barcelona, Spain; Department of Cellular, Computational and Integrative Biology, University of Trento, Trento, Italy.
⁶ Institute of Psychology, Leiden University, Leiden, the Netherlands; Department of Psychiatry, University of Oxford, Oxford, UK.
⁷ Meinig School of Biomedical Engineering, Cornell University, Ithaca, NY, USA.
⁸ Department of Biological Sciences, University of Notre Dame, Notre Dame, IN, USA.
⁹ Committee on Immunology, University of Chicago, Chicago, IL, USA; Department of Medicine, University of Chicago, Chicago, IL, USA; Committee on Genetics, Genomics and Systems Biology, University of Chicago, Chicago, IL, USA.
¹⁰ Molecular Pathology Unit, Cancer Center, Massachusetts General Hospital Research Institute, Charlestown, MA, USA; Department of Pathology, Harvard Medical School, Boston, MA, USA.
¹¹ Department of Microbiology and Immunology, University of British Columbia, Vancouver, BC, Canada; Michael Smith Laboratories, University of British Columbia, Vancouver, BC, Canada; Department of Biochemistry, University of British Columbia, Vancouver, BC, Canada.
¹² National Center for Biotechnology Information, National Library of Medicine, Bethesda, MD, USA.
¹³ Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, USA.

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.

Keywords: antibiotic resistance; antibiotics; communicable diseases; immunity; microbial transmission; microbiota; non-communicable diseases; social determinants of health; social evolution; social networks; social transmission; social virome.

Publication types

Review
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Animals
Humans
Microbiota*
Noncommunicable Diseases
Social Factors*
Symbiosis*
Virulence

Abstract

Publication types

MeSH terms

Grants and funding