Abstract

In addition to its obligatory symbiont Buchnera aphidicola, the pea aphid Acyrthosiphon pisum can harbor several facultative bacterial symbionts which can be mutualistic in the context of various ecological interactions. Belonging to a genus where many members have been described as pathogen in invertebrates, Serratia symbiotica is one of the most common facultative partners found in aphids. The recent discovery of strains able to grow outside their host allowed us to simulate environmental acquisition of symbiotic bacteria by aphids. Here, we performed an experiment to characterize the A. pisum response to the ingestion of the free-living S. symbiotica CWBI-2.3T in comparison to the ingestion of the pathogenic Serratia marcescens Db11 at the early steps in the infection process. We found that, while S. marcescens Db11 killed the aphids within a few days, S. symbiotica CWBI-2.3T did not affect host survival and colonized the whole digestive tract within a few days. Gene expression analysis of immune genes suggests that S. symbiotica CWBI-2.3T did not trigger an immune reaction, while S. marcescens Db11 did, and supports the hypothesis of a fine-tuning of the host immune response set-up for fighting pathogens while maintaining mutualistic partners. Our results also suggest that the lysosomal system and the JNK pathway are possibly involved in the regulation of invasive bacteria in aphids and that the activation of the JNK pathway is IMD-independent in the pea aphid.

Highlights

  • As all living organisms, insects have to face a wide range of parasites and pathogens present in their environment

  • We chose to investigate the interaction between the pea aphid A. pisum and two closely related bacteria, S. symbiotica CWBI-2.3T and S. marcescens Db11, as models to understand how aphids handle mutualistic bacteria in comparison to invasive pathogens at the early steps of an infection operated via oral route

  • Our observations suggest that 1) the midgut provides an appropriate environment for S. symbiotica CWBI-2.3T to multiply and accumulate before migrating and disseminating into the whole gut, 2) the free-living S. symbiotica CWBI-2.3T strain is able to survive in the gut without apparent rejection from the host, 3) S. symbiotica CWBI-2.3T, which was originally hosted by A. fabae, it appears ubiquitous since it can found a refuge in the gut of an aphid species different from its original host

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Summary

Introduction

Insects have to face a wide range of parasites and pathogens present in their environment. Once pattern recognition receptors (PRRs) bind and recognize pathogen-associated molecular patterns (PAMPs), signaling pathways such as Toll, immune deficiency (IMD), Jun-N-terminal kinase (JNK) and Janus kinase/signal transducers and activators of transcription (JAK/STAT) pathways are activated, resulting in the expression of antimicrobial peptides (AMPs) [10]. In addition to these immune pathways, insects can count on other defense mechanisms such as heat shock proteins (HSPs) production [11,12], nitric oxides release [13], reactive oxygen species (ROS) production [14] and the lysosomal system activation [15]

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