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

Grizanova, Ekaterina V.; Крыцына, Т. И.; Kalmykova, G. V.; Sokolova, Elina; Alikina, Tatyana; Kabilov, Мarsel R.; Coates, Christopher J.; Dubovskiy, Ivan M.

doi:10.1016/j.micpath.2022.105958

Cited by 6 publications

(3 citation statements)

References 49 publications

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“…Any observed effects on the immune response were as a result of the presence of this genus of bacteria. A previous study also found only Enterococcus species in the G. mellonella gut ( 52 ); however, more recently published studies have also identified, along with Enterococcus but in lower abundances, Enterobacter, Bacillus, Halomonas, Shewanella, Pseudomonas, Variovorax, Staphylococcus, Serratia , and Escherichia–Shigella present in the late-larval instar of G. mellonella ( 28 , 41 , 53 – 56 ). With a more diverse microbiota, shifts in the dominance between bacterial groups post-pathogen infection have been observed.…”

Section: Discussionmentioning

confidence: 88%

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The immunostimulatory role of an Enterococcus-dominated gut microbiota in host protection against bacterial and fungal pathogens in Galleria mellonella larvae

Upfold,

Rejasse,

Nielsen-Leroux

et al. 2023

Front. Insect Sci.

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Understanding the intricate interplay between the gut microbiota and the immune response in insects is crucial, given its diverse impact on the pathogenesis of various microbial species. The microbiota’s modulation of the host immune system is one such mechanism, although its complete impact on immune responses remains elusive. This study investigated the tripartite interaction between the gut microbiota, pathogens, and the host’s response in Galleria mellonella larvae reared under axenic (sterile) and conventional (non-sterile) conditions. The influence of the microbiota on host fitness during infections was evaluated via two different routes: oral infection induced by Bacillus thuringiensis subsp. galleriae (Btg), and topical infection induced by Metarhizium robertsii (Mr). We observed that larvae without a microbiota can successfully fulfill their life cycle, albeit with more variation in their developmental time. We subsequently performed survival assays on final-instar larvae, using the median lethal dose (LD50) of Btg and Mr. Our findings indicated that axenic larvae were more vulnerable to an oral infection of Btg; specifically, a dose that was calculated to be half-lethal for the conventional group resulted in a 90%–100% mortality rate in the axenic group. Through a dual-analysis experimental design, we could identify the status of the gut microbiota using 16S rRNA sequencing and assess the level of immune-related gene expression in the same group of larvae at basal conditions and during infection. This analysis revealed that the microbiota of our conventionally reared population was dominated entirely by four Enterococcus species, and these species potentially stimulated the immune response in the gut, due to the increased basal expression of two antimicrobial peptides (AMPs)—gallerimycin and gloverin—in the conventional larvae compared with the axenic larvae. Furthermore, Enterococcus mundtii, isolated from the gut of conventional larvae, showed inhibition activity against Btg in vitro. Lastly, other immune effectors, namely, phenoloxidase activity in the hemolymph and total reactive oxygen/nitrogen species (ROS/RNS) in the gut, were tested to further investigate the extent of the stimulation of the microbiota on the immune response. These findings highlight the immune-modulatory role of the Enterococcus-dominated gut microbiota, an increasingly reported microbiota assemblage of laboratory populations of Lepidoptera, and its influence on the host’s response to oral and topical infections.

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Section: Discussionmentioning

confidence: 88%

“…To test the immune response via oral infection, we used Bacillus thuringiensis subsp. galleriae 69-6 (Btg), a pathogenic strain known to infect G. mellonella ( 27 , 28 ). B. thuringiensis is a Gram-positive, spore-forming bacteria found in soil environments, which produces cry and cyt δ-endotoxins with entomopathogenic properties.…”

Section: Introductionmentioning

confidence: 99%

The immunostimulatory role of an Enterococcus-dominated gut microbiota in host protection against bacterial and fungal pathogens in Galleria mellonella larvae

Upfold,

Rejasse,

Nielsen-Leroux

et al. 2023

Front. Insect Sci.

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show abstract

“…thuringiensis subsp. galleriae treatment, the gram-negative Enterobacteraceae was prevalent in the midgut of Bt-resistant Galleria mellonella, while the gram-positive Enterococcus and Bt were enriched in the susceptible strain, which indicated that clearing the midgut from gram-positive bacteria may contribute to the resistance in G. mellonella [48]. Furthermore, the larval mortalities of both ACB-BtS and ACB-AbR treated by Cry1Ab protein were reduced significantly after eliminating the gut bacteria.…”

Section: Discussionmentioning

confidence: 94%

Comparison of Gut Microbial Community between Bt-Resistant and Susceptible Strains of Ostrinia furnacalis

Wang

et al. 2023

Agronomy

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Bacillus thuringiensis is an effective entomopathogen, and its crystal toxin expressed in transgenic crops has been widely used for pest control. However, insect resistance risk is the main threat to the continued successful utility of Bt crops. Several studies reported the role of midgut microbiota in Bt resistance, but the mechanism remains controversial. In the present study, using high-throughput sequencing of the bacterial 16S ribosomal RNA gene, we surveyed the midgut bacterial flora of Ostrinia furnacalis from one Bt-susceptible (ACB-BtS) and two Bt-resistant (ACB-AbR and ACB-FR) strains and explored the mortality of O. furnacalis after eliminating the gut bacteria. Gut bacterial diversity in Bt-resistant strains was significantly lower in Bt-resistant than in Bt-susceptible strains. Ordination analyses and statistical tests showed that the bacterial community of ACB-AbR was distinguishable from ACB-BtS. The genus Halomonas was dominated in ACB-BtS, but the unclassified_Enterobacteriaceae was the most enriched genus in ACB-AbR and ACB-FR. Furthermore, interactions of the bacterial community are more complex in Bt-resistant strains than in Bt-susceptible strains. Moreover, the mortalities of ACB-AbR and ACB-BtS strains treated by the Cry1Ab toxin were significantly reduced after eliminating the gut bacteria. Our findings suggest that Bt stressors structured in the midgut bacterial community and the microbiota have the potential to regulate the Bt-induced killing mechanism.

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Plant Recombinant Gene Technology for Pest Control in the Twenty-First Century: From Simple Transgenesis to CRISPR/Cas

Dubovskiy,

Grizanova,

Gerasimova

2024

Gene Editing in Plants

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

Cited by 6 publications

References 49 publications

The immunostimulatory role of an Enterococcus-dominated gut microbiota in host protection against bacterial and fungal pathogens in Galleria mellonella larvae

The immunostimulatory role of an Enterococcus-dominated gut microbiota in host protection against bacterial and fungal pathogens in Galleria mellonella larvae

Comparison of Gut Microbial Community between Bt-Resistant and Susceptible Strains of Ostrinia furnacalis

Plant Recombinant Gene Technology for Pest Control in the Twenty-First Century: From Simple Transgenesis to CRISPR/Cas

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