Drosophila immune priming against Pseudomonas aeruginosa is short-lasting and depends on cellular and humoral immunity

Abstract

Immune responses are traditionally divided into the innate and the adaptive arm, both of which are present in vertebrates, while only the innate arm is found in invertebrates. Immune priming experiments in Drosophila melanogaster and other invertebrates during the last decade have challenged this dogma, questioning the boundaries between innate and adaptive immunity. Studies on repeated inoculation of Drosophila with microbes reveal a long-lasting cellular immunity adaptation against particular microorganisms. Here we study the lasting effect of immune priming against infection with Pseudomonas aeruginosa, an opportunistic human pathogen that is lethal to the common fruit fly. Drosophila priming with heat-killed or low in virulence P. aeruginosa extends fly survival during a secondary lethal infection with a virulent strain of the same species. The protective immune response can last for more than 10 days after exposure to a persistent low-in-virulence live infection, but it is eliminated 7 days after the host is primed with heat-killed bacteria. Moreover, not only the cellular, but also the systemic NF-κB-mediated immune responses contribute to immune priming. Thus each microbe might elicit different mechanisms of immune priming that may or may not last for long.

Limited Specificity in the Injury and Infection Priming against Bacteria in Aedes aegypti Mosquitoes

“…Injury and infection priming is a memory-like response that is reportedly elicited in several (but not all) insect groups by bacteria, fungi, viruses, parasites and even inert molecules (LPS, heat-killed bacteria) ( Moret and Siva-Jothy, 2003 ; Sadd et al, 2005 ; Moret, 2006 ; Sadd and Schmid-Hempel, 2007 ; Roth et al, 2009 ; Hernández-Martínez et al, 2010 ; Tidbury et al, 2011 ; Tate and Rudolf, 2012 ; Christofi and Apidianakis, 2013 ). Despite the evidence of a widespread phenomenon, the mechanism(s) and molecule(s) associated with the induction of priming are as yet unclear (but see Contreras-Garduño et al, 2015 ; Ramirez et al, 2015 ).…”

“…There are studies showing that after previous exposure to a pathogen, there was specific protection against a subsequent lethal challenge. For instance, after previous contact of Drosophila melanogaster with different bacteria, individuals were able to increase its survival rate and specific phagocytic activity against the corresponding pathogen ( Pham et al, 2007 ; Christofi and Apidianakis, 2013 ). While different strains of Pseudomona aeruginosa elicit defense-specific genes ( Apidianakis et al, 2005 ).…”

Digenean-gastropod host associations inform on aspects of specific immunity in snails

“…The fruit fly Drosophila melanogaster employs various non-self recognition receptors that distinguish Gram (−) from Gram (+) bacteria or other pathogens, and activate different signaling pathways that generate transcriptional profiles to emphasize defense factors with greatest impact on the pathogens encountered (Ferrandon et al, 2007; Hoffmann and Reichart, 2002; Kraaijeveld et al, 2012). Moreover, previous encounters that result in immune elimination of pathogens lead to immune priming; fruit flies retain increased immune resistance to specific pathogens for about a week (Christofi and Apidianakis, 2013, Pham et al, 2007). Many of the authoritative papers in the field derived from studies of deuterostome invertebrates or of ecdysozoan protostomes, with studies of Lophotrochozoa, the other major branch of protostome invertebrates (Erwin et al, 2011), tending to lag behind.…”

Human pathogenic bacteria, fungi, and viruses inDrosophila

“…81 Nevertheless, this long-lasting effect is not universal and needs to be evaluated individually for each microbial species. 182 Furthermore, flies infected with S. pneumoniae lose circadian rhythms several days before dying. 82 Consistently, flies lacking the central clock proteins timeless or period have higher sensitivity to S. pneumoniae but also to L. monocytogenes infection.…”