Single innate immune effectors control ecological microbiome bacteria across evolutionary timescales

Abstract

AbstractAntimicrobial peptides are host-encoded antibiotics that combat invading microbes and help shape the microbiome in plants and animals. However, little is known about how the host antimicrobial peptide repertoire is evolutionarily adapted to its microbiome. Here we characterize the function and evolution of theDiptericinantimicrobial peptide family of Diptera. Using mutations affecting the twoDiptericins(Dpt) ofD. melanogaster, we reveal the specific role ofDptAagainst the pathogenProvidencia rettgeriandDptBagainst the gut mutualistAcetobacter. Strikingly, presence ofDptA-orDptB-like genes across Diptera correlates with the presence ofProvidenciaandAcetobacterin their environment. Moreover, presence ofDptA-andDpB-like genes is sufficient to predict host resistance against infection by these bacteria across a broad range of fly species. Our study explains the evolutionary logic behind the bursts of rapid evolution of an antimicrobial peptide family, and reveals how the host immune repertoire adapts itself to changing microbial environments.