Gut microbiota mediate Plutella xylostella susceptibility to Bt Cry1Ac protoxin is associated with host immune response

Li, Shuzhong; Xu, Xi; Mandal, Surajit De; Shakeel, Muhammad; Hua, Yi-Jun; Shoukat, Rana Fartab; Fu, Dongran; Jin, Fengliang

doi:10.1016/j.envpol.2020.116271

Cited by 40 publications

(32 citation statements)

References 55 publications

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“…Acinetobacter has a very high abundance in the nymph stage, but extremely low abundance in the adult stage. The vast majority of Acinetobacter bacteria have strong drug resistance ( Li et al, 2021 ). In China, due to the large-scale planting of Bt crops, A. suturalis has risen from secondary pests in cotton fields to primary pests.…”

Section: Discussionmentioning

confidence: 99%

“…Once ingested by the susceptible insect larvae, these cry proteins (present in the form of protoxin) are proteolytically processed by midgut proteases to the active toxin that subsequently binds to specific protein receptors of the midgut epithelium leading to cell disruption and eventual death of the insect larvae ( Pardo-López et al, 2013 ). The introduction of the intestinal isolate Acinetobacter guillouiae into Plutella xylostella significantly enhances its sensitivity to Bt Cry1Ac protoxin, and Acinetobacter plays an important role in the immune response of insects ( Li et al, 2021 ). During the nymph period, its ability to resist the stimulation of external agents is relatively weak.…”

Section: Discussionmentioning

confidence: 99%

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Gut Bacterial Diversity in Different Life Cycle Stages of Adelphocoris suturalis (Hemiptera: Miridae)

et al. 2021

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Bacteria and insects have a mutually beneficial symbiotic relationship. Bacteria participate in several physiological processes such as reproduction, metabolism, and detoxification of the host. Adelphocoris suturalis is considered a pest by the agricultural industry and is now a major pest in cotton, posing a serious threat to agricultural production. As with many insects, various microbes live inside A. suturalis. However, the microbial composition and diversity of its life cycle have not been well-studied. To identify the species and community structure of symbiotic bacteria in A. suturalis, we used the HiSeq platform to perform high-throughput sequencing of the V3–V4 region in the 16S rRNA of symbiotic bacteria found in A. suturalis throughout its life stages. Our results demonstrated that younger nymphs (1st and 2nd instar nymphs) have higher species richness. Proteobacteria (87.06%) and Firmicutes (9.43%) were the dominant phyla of A. suturalis. At the genus level, Erwinia (28.98%), Staphylococcus (5.69%), and Acinetobacter (4.54%) were the dominant bacteria. We found that the relative abundance of Erwinia was very stable during the whole developmental stage. On the contrary, the relative abundance of Staphylococcus, Acinetobacter, Pseudomonas, and Corynebacterium showed significant dynamic changes at different developmental stages. Functional prediction of symbiotic bacteria mainly focuses on metabolic pathways. Our findings document symbiotic bacteria across the life cycle of A. suturalis, as well as differences in both the composition and richness in nymph and adult symbiotic bacteria. Our analysis of the bacteria in A. suturalis provides important information for the development of novel biological control strategies.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Gut Bacterial Diversity in Different Life Cycle Stages of Adelphocoris suturalis (Hemiptera: Miridae)

et al. 2021

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“…On the one hand, Cry toxins induce damage of certain insect cells, such as mid-intestinal epithelial cells, which cause the interruption of insect feeding and affect the final survival of insects; on the other hand, during the epithelial cell damage, the Cry toxins lead to imbalance of the intestinal microbiota homeostasis. Then, the dysregulated intestinal microbiota and Cry toxin join to stimulate the excessive intestinal immune response ( Mason et al, 2011 ) and aggravate the damage to host tissues such as the peritrophic matrix, which causes some intestinal opportunistic pathogens or pathogens to enter into the hemocoel, leading to their rapid proliferation which significantly increases the total bacterial load in the hemolymph, causing host sepsis and accelerating the insect death ( Caccia et al, 2016 ; Li et al, 2021 ). In addition, others claim that after cell damage, water molecules can enter the cell more easily through aquaporin to combat the ion imbalance caused by the Cry toxins; yet, excessive water entry will induce the cells to swell, leading to their death ( Endo et al, 2017 ).…”

Section: The Insecticidal Mechanisms Of Cry Toxinsmentioning

confidence: 99%

“…It is worth noting that the same intestinal bacteria may play contrary roles in different insects. For example, after the reintroduction of E. mundtii into P. xylostella without intestinal microbiota, the host regained its sensitivity to Cry1Ac protoxin ( Li et al, 2021 ).…”

Section: The Resistance Mechanisms Of Insects Against Cry Toxinsmentioning

confidence: 99%

Which Is Stronger? A Continuing Battle Between Cry Toxins and Insects

Luo

et al. 2021

Front. Microbiol.

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In this article, we review the latest works on the insecticidal mechanisms of Bacillus thuringiensis Cry toxins and the resistance mechanisms of insects against Cry toxins. Currently, there are two models of insecticidal mechanisms for Cry toxins, namely, the sequential binding model and the signaling pathway model. In the sequential binding model, Cry toxins are activated to bind to their cognate receptors in the mid-intestinal epithelial cell membrane, such as the glycophosphatidylinositol (GPI)-anchored aminopeptidases-N (APNs), alkaline phosphatases (ALPs), cadherins, and ABC transporters, to form pores that elicit cell lysis, while in the signaling pathway model, the activated Cry toxins first bind to the cadherin receptor, triggering an extensive cell signaling cascade to induce cell apoptosis. However, these two models cannot seem to fully describe the complexity of the insecticidal process of Cry toxins, and new models are required. Regarding the resistance mechanism against Cry toxins, the main method insects employed is to reduce the effective binding of Cry toxins to their cognate cell membrane receptors by gene mutations, or to reduce the expression levels of the corresponding receptors by trans-regulation. Moreover, the epigenetic mechanisms, host intestinal microbiota, and detoxification enzymes also play significant roles in the insects’ resistance against Cry toxins. Today, high-throughput sequencing technologies like transcriptomics, proteomics, and metagenomics are powerful weapons for studying the insecticidal mechanisms of Cry toxins and the resistance mechanisms of insects. We believe that this review shall shed some light on the interactions between Cry toxins and insects, which can further facilitate the development and utilization of Cry toxins.

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“… Hilbeck et al (2018) found that gut bacteria can enhance the insecticidal activity of the Cry toxin protein by causing bacterial septicemia in P. xylostella . Li et al (2021) found that Bt Cry1Ac toxin interacts with the gut bacteria of P. xylostella to accelerate larval death. Moreover, a pathogenic insect fungus called Beauveria bassiana has been shown to interact with the gut microbiota of mosquitoes, thereby accelerating mosquito mortality ( Wei et al, 2017 ).…”

Section: Introductionmentioning

confidence: 99%

Bt GS57 Interaction With Gut Microbiota Accelerates Spodoptera exigua Mortality

Zhao

et al. 2022

Front. Microbiol.

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The Beet armyworm Spodoptera exigua (Lepidoptera: Noctuidae, Spodoptera) is an important global polyphagous pest. Pathogen infection could destroy the intestinal microbial homeostasis of insects, leading to the death of the host. However, the effect of the host intestinal microbial community on the insecticidal effect of Bacillus thuringiensis is rarely studied. In this study, the genome characteristics of Bt GS57 and the diversity and functions of the gut bacteria in S. exigua are investigated using crystal morphology, biological activity, and Illumina HiSeq high-throughput sequencing. The total size of the Bt GS57 genome is 6.17 Mbp with an average G + C content of 35.66%. Furthermore, the Bt GS57 genome contains six cry genes: cry1Ca, cry1Da, cry2Ab, cry9Ea, cry1Ia, and cry1Aa, and a vegetative insecticidal protein gene vip3Aa. The Bt GS57 strain can produce biconical crystals, mainly expressing 70 kDa and 130 kDa crystal proteins. The LC50 value of the Bt GS57 strain against the S. exigua larvae was 0.339 mg mL–1. Physiological and biochemical reactions showed that Bt GS57 belongs to B.t. var. thuringiensis. In addition, we found that B. thuringiensis can cause a dynamic change in the gut microbiota of S. exigua, with a significant reduction in bacterial diversity and a substantial increase in bacterial load. In turn, loss of gut microbiota significantly decreased the B. thuringiensis susceptibility of S. exigua larvae. Our findings reveal the vital contribution of the gut microbiota in B. thuringiensis-killing activity, providing new insights into the mechanisms of B. thuringiensis pathogenesis in insects.

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Gut microbiota mediate Plutella xylostella susceptibility to Bt Cry1Ac protoxin is associated with host immune response

Cited by 40 publications

References 55 publications

Gut Bacterial Diversity in Different Life Cycle Stages of Adelphocoris suturalis (Hemiptera: Miridae)

Gut Bacterial Diversity in Different Life Cycle Stages of Adelphocoris suturalis (Hemiptera: Miridae)

Which Is Stronger? A Continuing Battle Between Cry Toxins and Insects

Bt GS57 Interaction With Gut Microbiota Accelerates Spodoptera exigua Mortality

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