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Bacillus thuringiensis Spores and Cry3A Toxins Act Synergistically to Expedite Colorado Potato Beetle Mortality

Ivan Dubovskiy, Ekaterina V. Grizanova, Daria Tereshchenko, Tatiana I. Krytsyna, Tatyana Alikina, Galina Kalmykova, Marsel Kabilov, Christopher Coates

Toxins, Volume: 13, Issue: 11, Start page: 746

Swansea University Authors: Ivan Dubovskiy, Christopher Coates

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DOI (Published version): 10.3390/toxins13110746

Abstract

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 Bacillus thuringiensis (Bt) enters the insect host via the mouth and must thwart...

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Published in: Toxins
ISSN: 2072-6651
Published: MDPI AG 2021
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URI: https://cronfa.swan.ac.uk/Record/cronfa58456
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The bacterial biopesticide Bacillus thuringiensis (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 Leptinotarsa decemlineata (CPB). Exposing the beetles to both Bt spores and their Cry3A toxins (crystalline &#x3B4;-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 &#x2013; key indicators of tissue damage. When Cry3A toxins are combined with spores, gross redox imbalance and &#x2018;oxidation stress&#x2019; 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 Pseudomonas abundance at 48 h post inoculation. 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spelling 2021-11-18T15:05:42.4568632 v2 58456 2021-10-25 Bacillus thuringiensis Spores and Cry3A Toxins Act Synergistically to Expedite Colorado Potato Beetle Mortality 411b6e5b2086d0ffc3e89b14127d2768 Ivan Dubovskiy Ivan Dubovskiy true false af160934b75bea5b8ba83d68b3d1a003 Christopher Coates Christopher Coates true false 2021-10-25 FGSEN 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 Bacillus thuringiensis (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 Leptinotarsa decemlineata (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 Pseudomonas 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. Journal Article Toxins 13 11 746 MDPI AG 2072-6651 immunotoxicology; ROS; oxidative stress; antioxidants; midgut microbiome; biocontrol; Leptinotarsa decemlineata; plant protection 21 10 2021 2021-10-21 10.3390/toxins13110746 COLLEGE NANME Science and Engineering - Faculty COLLEGE CODE FGSEN Swansea University Other Russian Science Foundation grant No. 19-16-00019; grant from the President RF № MK-318.2020.11 2021-11-18T15:05:42.4568632 2021-10-25T07:59:23.8647062 Faculty of Science and Engineering School of Biosciences, Geography and Physics - Biosciences Ivan Dubovskiy 1 Ekaterina V. Grizanova 2 Daria Tereshchenko 3 Tatiana I. Krytsyna 4 Tatyana Alikina 5 Galina Kalmykova 6 Marsel Kabilov 7 Christopher Coates 8 58456__21284__12eff497ef7a4880ab73fab3ac3ade95.pdf 45_Dubovskiy et al_TOXINS.pdf 2021-10-25T08:01:22.9523131 Output 2555509 application/pdf Version of Record true © 2021 by the authors. This is an open access article distributed under the terms of the Creative Commons Attribution (CC BY) license true eng https://creativecommons.org/licenses/by/4.0/
title Bacillus thuringiensis Spores and Cry3A Toxins Act Synergistically to Expedite Colorado Potato Beetle Mortality
spellingShingle Bacillus thuringiensis Spores and Cry3A Toxins Act Synergistically to Expedite Colorado Potato Beetle Mortality
Ivan Dubovskiy
Christopher Coates
title_short Bacillus thuringiensis Spores and Cry3A Toxins Act Synergistically to Expedite Colorado Potato Beetle Mortality
title_full Bacillus thuringiensis Spores and Cry3A Toxins Act Synergistically to Expedite Colorado Potato Beetle Mortality
title_fullStr Bacillus thuringiensis Spores and Cry3A Toxins Act Synergistically to Expedite Colorado Potato Beetle Mortality
title_full_unstemmed Bacillus thuringiensis Spores and Cry3A Toxins Act Synergistically to Expedite Colorado Potato Beetle Mortality
title_sort Bacillus thuringiensis Spores and Cry3A Toxins Act Synergistically to Expedite Colorado Potato Beetle Mortality
author_id_str_mv 411b6e5b2086d0ffc3e89b14127d2768
af160934b75bea5b8ba83d68b3d1a003
author_id_fullname_str_mv 411b6e5b2086d0ffc3e89b14127d2768_***_Ivan Dubovskiy
af160934b75bea5b8ba83d68b3d1a003_***_Christopher Coates
author Ivan Dubovskiy
Christopher Coates
author2 Ivan Dubovskiy
Ekaterina V. Grizanova
Daria Tereshchenko
Tatiana I. Krytsyna
Tatyana Alikina
Galina Kalmykova
Marsel Kabilov
Christopher Coates
format Journal article
container_title Toxins
container_volume 13
container_issue 11
container_start_page 746
publishDate 2021
institution Swansea University
issn 2072-6651
doi_str_mv 10.3390/toxins13110746
publisher MDPI AG
college_str Faculty of Science and Engineering
hierarchytype
hierarchy_top_id facultyofscienceandengineering
hierarchy_top_title Faculty of Science and Engineering
hierarchy_parent_id facultyofscienceandengineering
hierarchy_parent_title Faculty of Science and Engineering
department_str School of Biosciences, Geography and Physics - Biosciences{{{_:::_}}}Faculty of Science and Engineering{{{_:::_}}}School of Biosciences, Geography and Physics - Biosciences
document_store_str 1
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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 Bacillus thuringiensis (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 Leptinotarsa decemlineata (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 Pseudomonas 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.
published_date 2021-10-21T04:15:00Z
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