Influence of Bacillus thuringiensis and avermectins on gut physiology and microbiota in Colorado potato beetle: Impact of enterobacteria on susceptibility to insecticides.

Olga V Polenogova,Viktor V Glupov,Tatyana Alikina,Yury A Noskov,Tatyana N Klementeva,Jelizaveta Andrejeva,Marsel R Kabilov,Olga N Yaroslavtseva,Vadim Yu Kryukov,Viktor P Khodyrev,Natalya A Kryukova,Juan Luis Jurat-Fuentes

doi:10.1371/journal.pone.0248704

Abstract

Gut physiology and the bacterial community play crucial roles in insect susceptibility to infections and insecticides. Interactions among Colorado potato beetle Leptinotarsa decemlineata (Say), its bacterial associates, pathogens and xenobiotics have been insufficiently studied. In this paper, we present our study of the survival, midgut histopathology, activity of digestive enzymes and bacterial communities of L. decemlineata larvae under the influence of Bacillus thuringiensis var. tenebrionis (morrissoni) (Bt), a natural complex of avermectins and a combination of both agents. Moreover, we estimated the impact of culturable enterobacteria on the susceptibility of the larvae to Bt and avermectins. An additive effect between Bt and avermectins was established regarding the mortality of the larvae. Both agents led to the destruction of midgut tissues, a decrease in the activity of alpha-amylases and alkaline proteinases, a decrease in the Spiroplasma leptinotarsae relative abundance and a strong elevation of Enterobacteriaceae abundance in the midgut. Moreover, an elevation of the enterobacterial CFU count was observed under the influence of Bt and avermectins, and the greatest enhancement was observed after combined treatment. Insects pretreated with antibiotics were less susceptible to Bt and avermectins, but reintroduction of the predominant enterobacteria Enterobacter ludwigii, Citrobacter freundii and Serratia marcescens increased susceptibility to both agents. We suggest that enterobacteria play an important role in the acceleration of Bt infection and avermectin toxicoses in L. decemlineata and that the additive effect between Bt and avermectin may be mediated by alterations in the bacterial community.

Highlights

Colorado potato beetle Leptinotarsa decemlineata (Say) (Coleoptera: Crysomelidae) (CPB) is a cosmopolitan pest of Solanaceae with a high plasticity and high migratory ability [1]
We present our study of the survival, midgut histopathology, activity of digestive enzymes and bacterial communities of L. decemlineata larvae under the influence of Bacillus thuringiensis var. tenebrionis (Bt), a natural complex of avermectins and a combination of both agents
We showed that B. thuringiensis var. tenebrionis and avermectins interact additively in CPB larval mortality under laboratory conditions

Summary

Introduction

Colorado potato beetle Leptinotarsa decemlineata (Say) (Coleoptera: Crysomelidae) (CPB) is a cosmopolitan pest of Solanaceae with a high plasticity and high migratory ability [1]. In CPB cysteine and aspartic digestive proteases can participate in this process [11]. Their presence can act as a specificity factor and play a role in insect sensitivity to Bt. Bt-based insecticides have a low stability due to low resistance to various biotic and abiotic factors. Bt-based insecticides have a low stability due to low resistance to various biotic and abiotic factors This may lead to the need for repeated treatments or an increase in doses of bioinsecticides [12]. Several research groups have previously shown an additive effect between Bt and azadirachtin against different larval instars of Helicoverpa armigera (Lepidoptera) under laboratory conditions [13, 14]

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