<i>Bacillus thuringiensis</i> Spores and Cry3A Toxins Act Synergistically to Expedite Colorado Potato Beetle Mortality

The insect integument (exoskeleton) is an effective physiochemical barrier that limits disease-causing agents to a few portals of entry, including the gastrointestinal and reproductive tracts. The bacterial biopesticide <i>Bacillus thuringiensis</i> (Bt) enters the insect host via the mo...

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Autores principales: Ivan M. Dubovskiy, Ekaterina V. Grizanova, Daria Tereshchenko, Tatiana I. Krytsyna, Tatyana Alikina, Galina Kalmykova, Marsel Kabilov, Christopher J. Coates
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Publicado: MDPI AG 2021
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Acceso en línea:https://doaj.org/article/49ab8431585d41c18c2f09db4349808f
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spelling oai:doaj.org-article:49ab8431585d41c18c2f09db4349808f2021-11-25T19:08:31Z<i>Bacillus thuringiensis</i> Spores and Cry3A Toxins Act Synergistically to Expedite Colorado Potato Beetle Mortality10.3390/toxins131107462072-6651https://doaj.org/article/49ab8431585d41c18c2f09db4349808f2021-10-01T00:00:00Zhttps://www.mdpi.com/2072-6651/13/11/746https://doaj.org/toc/2072-6651The insect integument (exoskeleton) is an effective physiochemical barrier that limits disease-causing agents to a few portals of entry, including the gastrointestinal and reproductive tracts. The bacterial biopesticide <i>Bacillus thuringiensis</i> (Bt) enters the insect host via the mouth and must thwart gut-based defences to make its way into the body cavity (haemocoel) and establish infection. We sought to uncover the main antibacterial defences of the midgut and the pathophysiological features of Bt in a notable insect pest, the Colorado potato beetle <i>Leptinotarsa decemlineata</i> (CPB). Exposing the beetles to both Bt spores and their Cry3A toxins (crystalline δ-endotoxins) via oral inoculation led to higher mortality levels when compared to either spores or Cry3A toxins alone. Within 12 h post-exposure, Cry3A toxins caused a 1.5-fold increase in the levels of reactive oxygen species (ROS) and malondialdehyde (lipid peroxidation) within the midgut – key indicators of tissue damage. When Cry3A toxins are combined with spores, gross redox imbalance and ‘oxidation stress’ is apparent in beetle larvae. The insect detoxification system is activated when Bt spores and Cry3A toxins are administered alone or in combination to mitigate toxicosis, in addition to elevated mRNA levels of candidate defence genes (pattern-recognition receptor, stress-regulation, serine proteases, and prosaposin-like protein). The presence of bacterial spores and/or Cry3A toxins coincides with subtle changes in microbial community composition of the midgut, such as decreased <i>Pseudomonas</i> abundance at 48 h post inoculation. Both Bt spores and Cry3A toxins have negative impacts on larval health, and when combined, likely cause metabolic derangement, due to multiple tissue targets being compromised.Ivan M. DubovskiyEkaterina V. GrizanovaDaria TereshchenkoTatiana I. KrytsynaTatyana AlikinaGalina KalmykovaMarsel KabilovChristopher J. CoatesMDPI AGarticleimmunotoxicologyROSoxidative stressantioxidantsmidgut microbiomebiocontrolMedicineRENToxins, Vol 13, Iss 746, p 746 (2021)
institution DOAJ
collection DOAJ
language EN
topic immunotoxicology
ROS
oxidative stress
antioxidants
midgut microbiome
biocontrol
Medicine
R
spellingShingle immunotoxicology
ROS
oxidative stress
antioxidants
midgut microbiome
biocontrol
Medicine
R
Ivan M. Dubovskiy
Ekaterina V. Grizanova
Daria Tereshchenko
Tatiana I. Krytsyna
Tatyana Alikina
Galina Kalmykova
Marsel Kabilov
Christopher J. Coates
<i>Bacillus thuringiensis</i> Spores and Cry3A Toxins Act Synergistically to Expedite Colorado Potato Beetle Mortality
description The insect integument (exoskeleton) is an effective physiochemical barrier that limits disease-causing agents to a few portals of entry, including the gastrointestinal and reproductive tracts. The bacterial biopesticide <i>Bacillus thuringiensis</i> (Bt) enters the insect host via the mouth and must thwart gut-based defences to make its way into the body cavity (haemocoel) and establish infection. We sought to uncover the main antibacterial defences of the midgut and the pathophysiological features of Bt in a notable insect pest, the Colorado potato beetle <i>Leptinotarsa decemlineata</i> (CPB). Exposing the beetles to both Bt spores and their Cry3A toxins (crystalline δ-endotoxins) via oral inoculation led to higher mortality levels when compared to either spores or Cry3A toxins alone. Within 12 h post-exposure, Cry3A toxins caused a 1.5-fold increase in the levels of reactive oxygen species (ROS) and malondialdehyde (lipid peroxidation) within the midgut – key indicators of tissue damage. When Cry3A toxins are combined with spores, gross redox imbalance and ‘oxidation stress’ is apparent in beetle larvae. The insect detoxification system is activated when Bt spores and Cry3A toxins are administered alone or in combination to mitigate toxicosis, in addition to elevated mRNA levels of candidate defence genes (pattern-recognition receptor, stress-regulation, serine proteases, and prosaposin-like protein). The presence of bacterial spores and/or Cry3A toxins coincides with subtle changes in microbial community composition of the midgut, such as decreased <i>Pseudomonas</i> abundance at 48 h post inoculation. Both Bt spores and Cry3A toxins have negative impacts on larval health, and when combined, likely cause metabolic derangement, due to multiple tissue targets being compromised.
format article
author Ivan M. Dubovskiy
Ekaterina V. Grizanova
Daria Tereshchenko
Tatiana I. Krytsyna
Tatyana Alikina
Galina Kalmykova
Marsel Kabilov
Christopher J. Coates
author_facet Ivan M. Dubovskiy
Ekaterina V. Grizanova
Daria Tereshchenko
Tatiana I. Krytsyna
Tatyana Alikina
Galina Kalmykova
Marsel Kabilov
Christopher J. Coates
author_sort Ivan M. Dubovskiy
title <i>Bacillus thuringiensis</i> Spores and Cry3A Toxins Act Synergistically to Expedite Colorado Potato Beetle Mortality
title_short <i>Bacillus thuringiensis</i> Spores and Cry3A Toxins Act Synergistically to Expedite Colorado Potato Beetle Mortality
title_full <i>Bacillus thuringiensis</i> Spores and Cry3A Toxins Act Synergistically to Expedite Colorado Potato Beetle Mortality
title_fullStr <i>Bacillus thuringiensis</i> Spores and Cry3A Toxins Act Synergistically to Expedite Colorado Potato Beetle Mortality
title_full_unstemmed <i>Bacillus thuringiensis</i> Spores and Cry3A Toxins Act Synergistically to Expedite Colorado Potato Beetle Mortality
title_sort <i>bacillus thuringiensis</i> spores and cry3a toxins act synergistically to expedite colorado potato beetle mortality
publisher MDPI AG
publishDate 2021
url https://doaj.org/article/49ab8431585d41c18c2f09db4349808f
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