Tetranychus urticae mites do not mount an induced immune response against bacteria.

Gonçalo Santos-Matos,Élio Sucena,Sara Magalhães,John Vontas,Nicky Wybouw,Maria Riga,Nelson E Martins,Thomas Van Leeuwen,Alexandre B Leitão,Miodrag Grbić,Flore Zélé

doi:10.1098/rspb.2017.0401

Abstract

The genome of the spider mite Tetranychus urticae, a herbivore, is missing important elements of the canonical Drosophila immune pathways necessary to fight bacterial infections. However, it is not known whether spider mites can mount an immune response and survive bacterial infection. In other chelicerates, bacterial infection elicits a response mediated by immune effectors leading to the survival of infected organisms. In T. urticae, infection by either Escherichia coli or Bacillus megaterium did not elicit a response as assessed through genome-wide transcriptomic analysis. In line with this, spider mites died within days even upon injection with low doses of bacteria that are non-pathogenic to Drosophila. Moreover, bacterial populations grew exponentially inside the infected spider mites. By contrast, Sancassania berlesei, a litter-dwelling mite, controlled bacterial proliferation and resisted infections with both Gram-negative and Gram-positive bacteria lethal to T. urticae. This differential mortality between mite species was absent when mites were infected with heat-killed bacteria. Also, we found that spider mites harbour in their gut 1000-fold less bacteria than S. berlesei. We show that T. urticae has lost the capacity to mount an induced immune response against bacteria, in contrast to other mites and chelicerates but similarly to the phloem feeding aphid Acyrthosiphon pisum. Hence, our results reinforce the putative evolutionary link between ecological conditions regarding exposure to bacteria and the architecture of the immune response.

Highlights

To deal with infection, arthropods rely on several defensive mechanisms that include behavioural avoidance, physical and chemical barriers, and the& 2017 The Authors
We show that T. urticae has lost the capacity to mount an induced immune response against bacteria, in contrast to other mites and chelicerates but to the phloem feeding aphid Acyrthosiphon pisum
This is not a general feature of hemipterans, because the Toll and Imd pathways along with several receptors and antimicrobial peptides (AMPs) were annotated in the genome of the brown planthopper, Nilaparvata lugens, and several Toll pathway genes were shown to be upregulated upon bacterial infection in this species [11]

Summary

Introduction

Arthropods rely on several defensive mechanisms that include behavioural avoidance, physical and chemical barriers, and the. In the pea aphid Acyrthosiphon pisum, a hemimetabolous insect, the Imd pathway is incomplete and several genes coding for receptors and common AMPs could not be identified This aphid species does not mount an immune response to bacterial infection [9,10]. Two general hypotheses may explain this observation: (i) the spider mite mounts an immune response based on a different genetic basis, as do other chelicerates or (ii) as in aphids, T. urticae does not possess an inducible anti-bacterial immune response To distinguish between these hypotheses, we present experimental data describing the response of mites to bacterial systemic infection, including host survival, bacterial proliferation in the host and transcriptional responses.

Results

Discussion