Abstract

Insect vectors transmit viruses and bacteria that can cause severe diseases in plants and economic losses due to a decrease in crop production. Insect vectors, like all other organisms, are colonized by a community of various microorganisms, which can influence their physiology, ecology, evolution, and also their competence as vectors. The important ecological meaning of bacteriophages in various ecosystems and their role in microbial communities has emerged in the past decade. However, only a few phages have been described so far in insect microbiomes. The leafhopper Euscelidius variegatus is a laboratory vector of the phytoplasma causing Flavescence dorée, a severe grapevine disease that threatens viticulture in Europe. Here, the presence of a temperate bacteriophage in E. variegatus (named Euscelidius variegatus phage 1, EVP-1) was revealed through both insect transcriptome analyses and electron microscopic observations. The bacterial host was isolated in axenic culture and identified as the bacterial endosymbiont of E. variegatus (BEV), recently assigned to the genus Candidatus Symbiopectobacterium. BEV harbors multiple prophages that become active in culture, suggesting that different environments can trigger different mechanisms, finely regulating the interactions among phages. Understanding the complex relationships within insect vector microbiomes may help in revealing possible microbe influences on pathogen transmission, and it is a crucial step toward innovative sustainable strategies for disease management in agriculture.

Highlights

  • Like all other organisms, insects harbor a rich, dynamic, and interactive community of microorganisms, collectively known as the microbiome, which comprises living members, and elements considered as not living organisms and a whole spectrum of molecules produced by the microorganisms [1]

  • During the electron microscope observation of a partial viral purification obtained from a Euscelidius variegatus Torino (EvaTO) population [36], aimed at revealing insect virus particles, bacteriophage-like particles were serendipitously observed

  • We considered for the analysis only complete major capsid proteins from phages assigned to one of the nine Caudovirales families recognized by the International Committee on Taxonomy of Viruses (ICTV)

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Summary

Introduction

Insects harbor a rich, dynamic, and interactive community of microorganisms, collectively known as the microbiome, which comprises living members (microbiota), and elements considered as not living organisms (viruses, plasmids, prions, viroids, and free DNA) and a whole spectrum of molecules produced by the microorganisms [1]. Both microbiome composition and its modification influence insect ecology, physiology, evolution, and behavior through genetic and metabolic interactions. Fungi, protozoa, and viruses may be associated with their insect host permanently or transiently, the vast majority of these works have focused on bacterial communities [2,4]

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