Abstract
Evolution of antimicrobial peptides (AMPs) has been shown to be driven by recurrent duplications and balancing/positive selection in response to new or altered bacterial pathogens. We use Alvinella pompejana, the most eurythermal animal known on Earth, to decipher the selection patterns acting on AMP in an ecological rather than controlled infection approach. The preproalvinellacin multigenic family presents the uniqueness to encode a molecular chaperone (BRICHOS) together with an AMP (alvinellacin) that controls the vital ectosymbiosis of Alvinella. In stark contrast to what is observed in the context of the Red queen paradigm, we demonstrate that exhibiting a vital and highly conserved ecto-symbiosis in the face of thermal fluctuations has led to a peculiar selective trend promoting the adaptive diversification of the molecular chaperone of the AMP, but not of the AMP itself. Because BRICHOS stabilizes beta-stranded peptides, this polymorphism likely represents an eurythermal adaptation to stabilize the structure of alvinellacin, thus hinting at its efficiency to select and control the epibiosis across the range of temperatures experienced by the worm; Our results fill some knowledge gaps concerning the function of BRICHOS in invertebrates and offer perspectives for studying immune genes in an evolutionary ecological framework.
Highlights
Antimicrobial peptides (AMPs) constitute key components of the innate immune system that rapidly eradicate or incapacitate pathogenic agents such as viruses, bacteria or fungi attempting to invade and proliferate multicellular eukaryotes[1,2,3]
We took advantage of the peculiar microbial and physico-chemical ecology of the extremophile annelid Alvinella pompejana, the most eurythermal and amongst the most thermo-tolerant animals known on Earth, to decipher the selection patterns acting on an antimicrobial peptides (AMPs), namely alvinellacin, in an evolutionary ecological framework
The originality of the present study lies in the search for the signature of adaptive evolution in an AMP not in the context of pathogenicity, but rather in the context of the evolutionary constraints imposed by the obligatory maintenance of a specific, complex and vital ectosymbiosis in the face of eurythermality
Summary
Antimicrobial peptides (AMPs) constitute key components of the innate immune system that rapidly eradicate or incapacitate pathogenic agents such as viruses, bacteria or fungi attempting to invade and proliferate multicellular eukaryotes[1,2,3]. Annelids are suited to study the adaptation of external immunity to changing and harsh environmental conditions because (i) they are amongst the rare metazoans able to thrive in extreme and highly fluctuating habitats (e.g. hydrothermal vents, highly polluted anoxic sediments, polar environments), and (ii) they do not have barriers (i.e. exoskeleton or shell) to physically protect their skin from direct biotic/abiotic interactions. One intriguing point is how natural selection has operated on the worm’s external immunity to maintain this intimate and highly specific partnership present in all worms collected throughout its known geographic range (6,000 km)[28] In this context, the main goal of this study was to determine how external immune effectors, such as the preproalvinellacin gene, have been selected to maintain their efficiency at selecting and controlling the eurythermal epibiotic community in an extreme and fluctuating habitat. The originality of the present study lies in the search for the signature of adaptive evolution in an AMP (here alvinellacin) not in the context of pathogenicity, but rather in the context of the evolutionary constraints imposed by the obligatory maintenance of a specific, complex and vital ectosymbiosis in the face of eurythermality
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