A multi‐faceted approach testing the effects of previous bacterial exposure on resistance and tolerance

Abstract

Hosts can alter their strategy towards pathogens during their lifetime; that is, they can show phenotypic plasticity in immunity or life history. Immune priming is one such example, where a previous encounter with a pathogen confers enhanced protection upon secondary challenge, resulting in reduced pathogen load (i.e., resistance) and improved host survival. However, an initial encounter might also enhance tolerance, particularly to less virulent opportunistic pathogens that establish persistent infections. In this scenario, individuals are better able to reduce the negative fecundity consequences that result from a high pathogen burden. Finally, previous exposure may also lead to life‐history adjustments, such as terminal investment into reproduction. Using different Drosophila melanogaster host genotypes and two bacterial pathogens, Lactococcus lactis and Pseudomonas entomophila , we tested whether previous exposure results in resistance or tolerance and whether it modifies immune gene expression during an acute‐phase infection (one day post‐challenge). We then asked whether previous pathogen exposure affects chronic‐phase pathogen persistence and longer‐term survival (28 days post‐challenge). We predicted that previous exposure would increase host resistance to an early stage bacterial infection while it might come at a cost to host fecundity tolerance. We reasoned that resistance would be due in part to stronger immune gene expression after challenge. We expected that previous exposure would improve long‐term survival, that it would reduce infection persistence, and we expected to find genetic variation in these responses. We found that previous exposure to P. entomophila weakened host resistance to a second infection independent of genotype and had no effect on immune gene expression. Fecundity tolerance showed genotypic variation but was not influenced by previous exposure. However, L. lactis persisted as a chronic infection, whereas survivors cleared the more pathogenic P. entomophila infection. To our knowledge, this is the first study that addresses host tolerance to bacteria in relation to previous exposure, taking a multi‐faceted approach to address the topic. Our results suggest that previous exposure comes with transient costs to resistance during the early stage of infection in this host–pathogen system and that infection persistence may be bacterium‐specific.

Pathogen susceptibility and fitness costs explain variation in immune priming across natural populations of flour beetles

“…Thus, priming perhaps rescues post-infection by reducing the pathogen load. Prior studies also show that priming alters bacterial load, though the timing (Tate, Andolfatto, Demuth, & Graham, 2017) and direction of the impact varies (compare Pham, Dionne, -hiza, & Schneider, 2007;Kutzer, Kurtz, & Armitage, 2019).…”

“…Thus, priming perhaps rescues post‐infection by reducing the pathogen load. Prior studies also show that priming alters bacterial load, though the timing (Tate, Andolfatto, Demuth, & Graham, ) and direction of the impact varies (compare Pham, Dionne, Shirasu‐hiza, & Schneider, ; Kutzer, Kurtz, & Armitage, ). Together, these results indicate that pathogen‐mediated reduction in life span may impose strong selection for a priming response in natural populations, as predicted by theoretical models (Best et al, ) and observed in laboratory‐evolved populations (Khan et al, ).…”

Decomposing virulence to understand bacterial clearance in persistent infections

“…E. cloacae was isolated from a maize plant, but has been detected in the microbiota of D. melanogaster [44]. These bacterial species were chosen based on various studies, which together suggest that they may be expected to show a range of virulence [18,20,21,[45][46][47].…”

“…Disparate bacterial species have been shown to be able to chronically infect (here defined as a minimum of seven days) the host species used in this study, D. melanogaster [15,16,[18][19][20][21][22][23].…”

Genotypes and their interaction effects on reproduction and mating‐induced immune activation in Drosophila melanogaster

“…The question arises as to whether this translates into increased resistance against pathogens. Across four inbred D. melanogaster genotypes, AMP expression 24 hr after experimental bacterial infection varied according to genotype but expression did not correlate with the bacterial load (Kutzer, Kurtz, & Armitage, 2019). However, the expression in uninfected animals was not examined, so the above possibility remains to be tested.…”