When the microbiome shapes the host: immune evolution implications for infectious disease

This is a Preprint and has not been peer reviewed. This is version 3 of this Preprint.

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Comment #128 Mark Austin Hanson @ 2023-10-24 02:40

This manuscript was prepared and has been accepted for publication by Philosophical Transactions of the Royal Society B. This preprint is being posted with their permission to make the article available immediately, in advance of the issue which will be collected and processed in a few months time. -- Mark Austin Hanson

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Authors

Mark Austin Hanson 

Abstract

The microbiome includes both “mutualist” and “pathogen” microbes, regulated by the same innate immune architecture. A major question has therefore been: how do hosts prevent pathogenic infections while maintaining beneficial microbes? One idea suggests hosts can selectively activate innate immunity upon pathogenic infection, but not mutualist colonisation. Another idea posits that hosts can selectively attack pathogens, but not mutualists. Here I review evolutionary principles of microbe recognition and immune activation, and reflect on newly-observed immune effector-microbe specificity perhaps supporting the latter idea.
Recent work in Drosophila has found a surprising importance for single antimicrobial peptides in combatting specific ecologically-relevant microbes. The developing picture suggests these effectors have evolved for this purpose. Other defence responses like ROS bursts can also be uniquely effective against specific microbes. Signals in other model systems including nematodes, Hydra, oysters, and mammals, suggest that effector-microbe specificity may be a fundamental principle of host-pathogen interactions. I propose this effector-microbe specificity stems from weaknesses of the microbes themselves: if microbes have intrinsic weaknesses, hosts can evolve effectors that exploit those weaknesses. I define this host-microbe relationship as “the Achilles principle of immune evolution.” Incorporating this view helps interpret why some host-microbe interactions develop in a coevolutionary framework (e.g. Red Queen dynamics), or as a one-sided evolutionary response. This clarification should be valuable to better understand the principles behind host susceptibilities to infectious diseases.

DOI

https://doi.org/10.32942/X2M307

Subjects

Ecology and Evolutionary Biology, Environmental Microbiology and Microbial Ecology Life Sciences, Evolution, Immunity, Immunology and Infectious Disease, Immunology of Infectious Disease, Life Sciences, Molecular Genetics, Pathogenic Microbiology

Keywords

host-microbe interactions, host-pathogen, reactive oxygen species, AMPs, host defence peptide, microbiota, host-pathogen, reactive oxygen species, ROS, antimicrobial peptide, AMPs, host defence peptide, HDPs, microbiota, Microbiome

Dates

Published: 2023-10-23 16:43

Last Updated: 2023-10-30 14:28

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License

CC-BY Attribution-NonCommercial-ShareAlike 4.0 International

Additional Metadata

Language:
English

Conflict of interest statement:
None

Data and Code Availability Statement:
Not applicable