4.6 Article

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

Journal

PLOS ONE
Volume 16, Issue 3, Pages -

Publisher

PUBLIC LIBRARY SCIENCE
DOI: 10.1371/journal.pone.0248704

Keywords

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Funding

  1. Russian Science Foundation [19-76-00032]
  2. Russian Foundation for Basic Research [18-34-20060]
  3. Russian Science Foundation [19-76-00032] Funding Source: Russian Science Foundation

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The study showed an additive effect of Bt and avermectins on the mortality of Colorado potato beetle larvae, resulting in destruction of midgut tissues and decreased activity of digestive enzymes. The abundance of Enterobacteriaceae increased significantly in the midgut, and reintroduction of predominant enterobacteria enhanced susceptibility to both agents in insects pretreated with antibiotics. This suggests that enterobacteria play a significant role in accelerating Bt infection and avermectin toxicoses in L. decemlineata, and the additive effect between Bt and avermectins may be mediated by alterations in the bacterial community.
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.

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