Short-sighted evolution of virulence for invasive gut microbes: from hypothesis to tests

• Type of Material: Article
• Authors: Pauline Deirdre Scanlan, University College Cork; Fernando Baquero, Instituto Ramón y Cajal de Investigación Sanitaria; Bruce Levin, Emory University
• Language: English
• Date: 2024-07-25
• Publisher: SORTEE
• Publication Version: Preprint (Prior to Peer Review)
• Copyright Statement: 2024 Authors
• License: Creative Commons Attribution 4.0 International
• Final Published Version (URL): https://doi.org/10.32942/X2W915
• Title of Journal or Parent Work: EcoEvoRxiv
• Grant/Funding Information: PDS would like to acknowledge the financial support of a Royal Society-Science Foundation 390 Ireland University Research Fellowship (URF\R\201031) and thank Hugh Harris, Brandon Berryhill, Teresa Gil-Gil, and Andrew Smith for reading an early version of the manuscript. FB thanks the Carlos III Institute for Health Research of Spain (ISCIII) and Centro de Investigación Biomédica en Red (CIBERESP, CB06/02/0053). BRL thanks the U.S. National Institute of General Medical Sciences for their funding support via R35GM136407, the U.S. National Institute of Allergy and Infectious Diseases for their funding support via U19AI158080-02.
• Keywords: short-sighted evolution; Escherichia coli; gut microbiota; virulence
• Research Categories: Health Sciences, Public Health; Biology, Virology

Abstract

Why microbes harm their hosts is a fundamental question in evolutionary biology with broad relevance to our understanding of infectious diseases. Several hypotheses have been proposed to explain this "evolution of virulence." In this perspective, we re-examine one of these hypotheses in the specific context of the human gut microbiome, namely short-sighted evolution. According to the short-sighted evolution hypothesis, virulence is a product of niche expansion within a colonized host, whereby variants of commensal microbes establish populations in tissues and sites where the infection causes morbidity or mortality. This evolution is short-sighted in that the evolved variants that infect those tissues and sites are not transmitted to other hosts. The specific hypothesis that we propose is that some bacteria responsible for invasive infections and disease are the products of the short-sighted evolution of commensal bacteria residing in the gut microbiota. We present observations in support of this hypothesis and discuss the challenges inherent in assessing its general application to infections and diseases associated with specific members of the gut microbiota. We then describe how this hypothesis can be tested using genomic data and animal model experiments and outline how such studies will serve to provide fundamental information about both the evolution and genetic basis of virulence, and the bacteria of the intensively studied yet poorly understood habitats including the gut microbiomes of humans and other mammals.