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Virulent and necrotrophic strategies of Bacillus thuringiensis in susceptible and resistant insects, Galleria mellonella

Ekaterina V. Grizanova Orcid Logo, Tatiana I. Krytsyna Orcid Logo, Galina V. Kalmykova, Elina Sokolova Orcid Logo, Tatyana Alikina Orcid Logo, Marsel Kabilov, Christopher Coates, Ivan M. Dubovskiy

Microbial Pathogenesis, Volume: 175, Start page: 105958

Swansea University Author: Christopher Coates

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DOI (Published version): 10.1016/j.micpath.2022.105958

Abstract

Bacillus thuringiensis (Bt) is one of the most common entomopathogenic bacteria used as a biopesticide, and source of endotoxin genes for generating insect-resistant transgenic plants. The mechanisms underpinning an insect's susceptibility or resistance to B. thuringiensis are diverse. The bact...

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Published in: Microbial Pathogenesis
ISSN: 0882-4010
Published: Elsevier BV 2023
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URI: https://cronfa.swan.ac.uk/Record/cronfa62242
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Herein, we studied the progression of B. thuringiensis subsp. galleriae infection in two populations of wax moth larvae (Galleria mellonella) to gain further insight into the &#x201C;arms race&#x201D; between B. thuringiensis virulence and insect defences. Two doses of B. thuringiensis subsp. galleriae (spore and crystalline toxin mixtures) were administered orally to compare the responses of susceptible (S) and resistant to Bt (R) populations at &#x223C;30% mortality each. To investigate B. thuringiensis-insect antibiosis, we used a combination of in vivo infection trials, bacterial microbiome analysis, and RNAi targeting the antibacterial peptide gloverin. Within 48 hours post-inoculation, B. thuringiensis-resistant insects purged the midgut of bacteria, i.e., colony forming unit numbers fell below detectable levels. Second, B. thuringiensis rapidly modulated gene expression to initiate sporulation (linked to quorum sensing) when exposed to resistant insects in contrast to susceptible G. mellonella. We reinforce earlier findings that elevated levels of antimicrobial peptides, specifically gloverin, are found in the midgut of resistant insects, which is an evolutionary strategy to combat B. thuringiensis infection via its main portal of entry. 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spelling 2023-02-03T11:39:57.5132703 v2 62242 2023-01-03 Virulent and necrotrophic strategies of Bacillus thuringiensis in susceptible and resistant insects, Galleria mellonella af160934b75bea5b8ba83d68b3d1a003 Christopher Coates Christopher Coates true false 2023-01-03 Bacillus thuringiensis (Bt) is one of the most common entomopathogenic bacteria used as a biopesticide, and source of endotoxin genes for generating insect-resistant transgenic plants. The mechanisms underpinning an insect's susceptibility or resistance to B. thuringiensis are diverse. The bacterial lifecycle does not end with the death of a host, they continue to exploit the cadaver to reproduce and sporulate. Herein, we studied the progression of B. thuringiensis subsp. galleriae infection in two populations of wax moth larvae (Galleria mellonella) to gain further insight into the “arms race” between B. thuringiensis virulence and insect defences. Two doses of B. thuringiensis subsp. galleriae (spore and crystalline toxin mixtures) were administered orally to compare the responses of susceptible (S) and resistant to Bt (R) populations at ∼30% mortality each. To investigate B. thuringiensis-insect antibiosis, we used a combination of in vivo infection trials, bacterial microbiome analysis, and RNAi targeting the antibacterial peptide gloverin. Within 48 hours post-inoculation, B. thuringiensis-resistant insects purged the midgut of bacteria, i.e., colony forming unit numbers fell below detectable levels. Second, B. thuringiensis rapidly modulated gene expression to initiate sporulation (linked to quorum sensing) when exposed to resistant insects in contrast to susceptible G. mellonella. We reinforce earlier findings that elevated levels of antimicrobial peptides, specifically gloverin, are found in the midgut of resistant insects, which is an evolutionary strategy to combat B. thuringiensis infection via its main portal of entry. A sub-population of highly virulent B. thuringiensis can survive the enhanced immune defences of resistant G. mellonella by disrupting the midgut microbiome and switching rapidly to a necrotrophic strategy, prior to sporulation in the cadaver. Journal Article Microbial Pathogenesis 175 105958 Elsevier BV 0882-4010 Virulence factors; RNAi; Gloverin; Midgut microbiome; Cadavers; Innate immunity; Necrobiology 1 2 2023 2023-02-01 10.1016/j.micpath.2022.105958 COLLEGE NANME COLLEGE CODE Swansea University This research was supported in part by the Russian Science Foundation [Grant number 20-76-00025]. 2023-02-03T11:39:57.5132703 2023-01-03T11:45:54.4703129 Faculty of Science and Engineering School of Biosciences, Geography and Physics - Biosciences Ekaterina V. Grizanova 0000-0003-4103-1375 1 Tatiana I. Krytsyna 0000-0002-5197-3828 2 Galina V. Kalmykova 3 Elina Sokolova 0000-0002-0350-0903 4 Tatyana Alikina 0000-0003-2289-321x 5 Marsel Kabilov 6 Christopher Coates 7 Ivan M. Dubovskiy 8 Under embargo Under embargo 2023-01-03T11:47:50.1655136 Output 1408184 application/pdf Accepted Manuscript true 2023-12-24T00:00:00.0000000 ©2022 All rights reserved. All article content, except where otherwise noted, is licensed under a Creative Commons Attribution Non-Commercial No Derivatives License (CC-BY-NC-ND) true eng https://creativecommons.org/licenses/by-nc-nd/4.0/
title Virulent and necrotrophic strategies of Bacillus thuringiensis in susceptible and resistant insects, Galleria mellonella
spellingShingle Virulent and necrotrophic strategies of Bacillus thuringiensis in susceptible and resistant insects, Galleria mellonella
Christopher Coates
title_short Virulent and necrotrophic strategies of Bacillus thuringiensis in susceptible and resistant insects, Galleria mellonella
title_full Virulent and necrotrophic strategies of Bacillus thuringiensis in susceptible and resistant insects, Galleria mellonella
title_fullStr Virulent and necrotrophic strategies of Bacillus thuringiensis in susceptible and resistant insects, Galleria mellonella
title_full_unstemmed Virulent and necrotrophic strategies of Bacillus thuringiensis in susceptible and resistant insects, Galleria mellonella
title_sort Virulent and necrotrophic strategies of Bacillus thuringiensis in susceptible and resistant insects, Galleria mellonella
author_id_str_mv af160934b75bea5b8ba83d68b3d1a003
author_id_fullname_str_mv af160934b75bea5b8ba83d68b3d1a003_***_Christopher Coates
author Christopher Coates
author2 Ekaterina V. Grizanova
Tatiana I. Krytsyna
Galina V. Kalmykova
Elina Sokolova
Tatyana Alikina
Marsel Kabilov
Christopher Coates
Ivan M. Dubovskiy
format Journal article
container_title Microbial Pathogenesis
container_volume 175
container_start_page 105958
publishDate 2023
institution Swansea University
issn 0882-4010
doi_str_mv 10.1016/j.micpath.2022.105958
publisher Elsevier BV
college_str Faculty of Science and Engineering
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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
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description Bacillus thuringiensis (Bt) is one of the most common entomopathogenic bacteria used as a biopesticide, and source of endotoxin genes for generating insect-resistant transgenic plants. The mechanisms underpinning an insect's susceptibility or resistance to B. thuringiensis are diverse. The bacterial lifecycle does not end with the death of a host, they continue to exploit the cadaver to reproduce and sporulate. Herein, we studied the progression of B. thuringiensis subsp. galleriae infection in two populations of wax moth larvae (Galleria mellonella) to gain further insight into the “arms race” between B. thuringiensis virulence and insect defences. Two doses of B. thuringiensis subsp. galleriae (spore and crystalline toxin mixtures) were administered orally to compare the responses of susceptible (S) and resistant to Bt (R) populations at ∼30% mortality each. To investigate B. thuringiensis-insect antibiosis, we used a combination of in vivo infection trials, bacterial microbiome analysis, and RNAi targeting the antibacterial peptide gloverin. Within 48 hours post-inoculation, B. thuringiensis-resistant insects purged the midgut of bacteria, i.e., colony forming unit numbers fell below detectable levels. Second, B. thuringiensis rapidly modulated gene expression to initiate sporulation (linked to quorum sensing) when exposed to resistant insects in contrast to susceptible G. mellonella. We reinforce earlier findings that elevated levels of antimicrobial peptides, specifically gloverin, are found in the midgut of resistant insects, which is an evolutionary strategy to combat B. thuringiensis infection via its main portal of entry. A sub-population of highly virulent B. thuringiensis can survive the enhanced immune defences of resistant G. mellonella by disrupting the midgut microbiome and switching rapidly to a necrotrophic strategy, prior to sporulation in the cadaver.
published_date 2023-02-01T04:21:42Z
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