A model of proximate protection against pathogenic infection through shared immunity

Abstract

Drosophila melanogaster exhibits innate immune priming, a mechanism leading to protection upon repeated challenge with a given pathogen. However, whether immunological priming can be propagated from a challenged host to naive bystanders is unknown. Here, we show that priming half a vial of D. melanogaster adult flies with non-pathogenic Escherichia coli bacteria leads to protection of the whole vial from a lethal dose of the insect pathogen, Photorhabdus luminescens. The protective effect observed in these bystander flies was similar in magnitude to that of the E. coli primed hosts themselves but did not require transfer of E. coli to occur. This work broadens the scope of how immunological priming can occur and suggests that infected hosts can produce signals that influence immunity in their neighbors, leading to a shared immune collective.IMPORTANCEHere, we have introduced the new concept of shared immunity and priming by proximity. These findings are of particular significance because they indicate that the presence of compromised hosts can increase the response to the pathogenic challenge of healthy individuals that cohabitate within close distance. This shared immunity may involve proximate boosting of the host's immune defenses via the sensing of specific chemical, behavioral, or microbial signals. Determining the breadth, mechanistic basis, and translatability of these findings has the potential to transform biomedical research and public health.

Keywords: Drosophila; bacterial infection; immunity; shared immunity; shared protection.

Fig 1

Exposure of naive Drosophila melanogaster adult flies to flies infected with a non-pathogenic bacterium provides protection against subsequent infection with a potent bacterial pathogen. (A) Injection of D. melanogaster wild-type female adult flies with PBS and subsequent injection with PBS. (B) Injection of wild-type flies with 10,000 CFUs of the Escherichia coli non-pathogenic strain K-12, and 24 hours later injection with 500 CFUs of the insect pathogenic bacterium Photorhabdus luminescens strain TTO1. (C) Injection of wild-type flies with PBS or 10,000 CFUs of E. coli K-12, incubation of the two fly groups in the same vial for 24 hours, and subsequent injection of the PBS-injected group with 500 CFUs of P. luminescens TTO1. (D) Injection of D. melanogaster wild-type flies with PBS, and 24 hours later injection with 500 CFUs of P. luminescens TTO1. (E) Survival results for the four experimental treatments. The experiment was replicated five times, and in each experiment, 50 adult flies were used per experimental condition (Mantel-Cox, *P < 0.05; **P < 0.01).