Response to Bombyx mori nucleopolyhedrovirus infection in silkworm: Gut metabolites and microbiota

Shi, Xiujuan; Zhang, Yaxin; Zhu, Tianchen; Li, Nan; Sun, Sufei; Zhu, Min; Pan, Jun; Shen, Zeen; Hu, Xiaolong; Zhang, Xing; Gong, Chengliang

doi:10.1016/j.dci.2021.104227

Cited by 16 publications

(7 citation statements)

References 47 publications

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“…41 After HearNPV infection, bacterial community diversity decreased notably at both phylum and genus levels, as occurs in Bombyx mori. 42 Disruption of gut microbiota homeostasis by HearNPV likely reflects the proliferation of species involved in enhancing the host's immune response to infection. Specifically, the predominant Proteobacteria (Klebsiella and Sphingomonas) were replaced by Firmicutes (primarily Enterococcus).…”

Section: Discussionmentioning

confidence: 99%

“…Thus, baculovirus damage to the peritrophic matrix could enable some movement of microbiota from the gut lumen into midgut cells 41 . After HearNPV infection, bacterial community diversity decreased notably at both phylum and genus levels, as occurs in Bombyx mori 42 . Disruption of gut microbiota homeostasis by HearNPV likely reflects the proliferation of species involved in enhancing the host's immune response to infection.…”

Section: Discussionmentioning

confidence: 99%

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The gut microbiome of Helicoverpa armigera enhances immune response to baculovirus infection via suppression of Duox‐mediated reactive oxygen species

Tian

Guo

Michaud

et al. 2023

Pest Management Science

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BACKGROUNDBaculoviruses such as Helicoverpa armigera nucleopolyhedrovirus (HearNPV) infect their lepidopteran hosts via the larval midgut where they interact with host immune responses and gut microbiota. Here we demonstrate that gut microbiota proliferating in response to HearNPV infection promote larval immune responses which impede the infection process.RESULTSThe microbial load of the larval midgut increased following HearNPV infection, due primarily to increases in Enterococcus spp., whereas most other bacterial genera declined, with Firmicutes replacing Proteobacteria as the dominant phylum. Injection of abdominal prolegs of infected larvae with H2O2 promoted viral infection, diminished microbial abundance, and accelerated larval death, mimicking the effects of HearNPV infection, which up‐regulated dual oxidase (Duox) expression, increasing H2O2 levels in the midgut. Knockdown of Duox with RNAi reduced H2O2 production in the guts of infected larvae, increased bacterial loads, decreased viral replication, and improved larval survival. Germ‐free larvae were more susceptible to HearNPV than control larvae, exhibiting greater expression of Duox, higher levels of H2O2, and lower survival. Replenishment of gut bacteria in germ‐free larvae restored the base‐line immunity to HearNPV observed in normal larvae. Enterococcus spp., Levilactobacillus brevis, and Lactobacillus sp. bacteria were isolated and implicated in immunity restoration via replenishment in germ‐free larvae.CONCLUSIONThese findings illuminate how gut microbiota play important roles in larval defense against oral baculovirus infection, and suggest novel avenues of investigation to enhance the efficacy of baculoviruses and improve control of lepidopteran pests. © 2023 Society of Chemical Industry.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

The gut microbiome of Helicoverpa armigera enhances immune response to baculovirus infection via suppression of Duox‐mediated reactive oxygen species

Tian

Guo

Michaud

et al. 2023

Pest Management Science

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“…Comparing the midgut metabolites of infected and uninfected (Jingsong X Haoyue) silkworms, there were 13 differentially upregulated metabolites, including aspartic acid, asparagine, cysteine, isoleucine, lysine, methionine, phenylalanine, proline, threonine, tyrosine, valine, leucine, and serine ( Shi et al, 2021 ). The authors pointed out that, except for cysteine, isoleucine, proline, and serine, the other nine amino acids were essential for the growth and development of the silkworm ( Shi et al, 2021 ).…”

Section: Multi-omics Analysis Of Bmnpv-associated Genesmentioning

confidence: 99%

“…et al, 2020 ), suggested a complex mechanism for the role of proteins; moreover, the strong inhibitory effect of 5-pyridolactone on BmNPV ( Hua et al, 2021 ). Also, tryptophan and 9 other amino acids were all proved to be essential to the growth and development of the silkworm and were discovered through metabolomics ( Shi et al, 2021 ).…”

Section: Multi-omics Analysis Of Bmnpv-associated Genesmentioning

confidence: 99%

Multi-omics study and ncRNA regulation of anti-BmNPV in silkworms, Bombyx mori: an update

Fan,

Andoh,

Chen

2023

Front. Microbiol.

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Bombyx mori silkworm is an important economic insect which has a significant contribution to the improvement of the economy. Bombyx mori nucleopolyhedrovirus (BmNPV) is a vitally significant purulent virus that impedes the sustainable and stable development of the silkworm industry, resulting in substantial economic losses. In recent years, with the development of biotechnology, transcriptomics, proteomics, metabolomics, and the related techniques have been used to select BmNPV-resistant genes, proteins, and metabolites. The regulatory networks between viruses and hosts have been gradually clarified with the discovery of ncRNAs, such as miRNA, lncRNA, and circRNA in cells. Thus, this paper aims to highlight the results of current multi-omics and ncRNA studies on BmNPV resistance in the silkworm, providing some references for resistant strategies in the silkworm to BmNPV.

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“…These observations show that colonization of the gut by microbial communities generally confers resistance against pathogens. 43 Most research has focused on the global functions of microbial communities in insects, [45][46][47] while the contributions of specific microbial species to host defenses remain less understood. Consequently, in this study, the germfree larvae were re-colonized with a single gut symbiotic bacterium (the gut isolate Enterococcus strain, HcM7), followed by determination of their vitality after HycuNPV infection.…”

Section: Discussionmentioning

confidence: 99%

A gut‐isolated Enterococcus strain (HcM7) triggers the expression of antimicrobial peptides that aid resistance to nucleopolyhedrovirus infection of Hyphantria cunea larvae

Fan³

et al. 2023

Pest Management Science

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BackgroundCommensal microorganisms are widely distributed in insect gut tissues and play important roles in host nutrition, metabolism, reproductive regulation, and especially immune functioning and tolerance to pathogens. Consequently, gut microbiota represent a promising resource for the development of microbial‐based products for pest control and management. However, the interactions among host immunity, entomopathogen infections, and gut microbiota remain poorly understood for many arthropod pests.ResultsWe previously isolated an Enterococcus strain (HcM7) from Hyphantria cunea larvae guts that increased the survival rates of larvae challenged with nucleopolyhedrovirus (NPV). Here, we further investigated whether this Enterococcus strain stimulates a protective immune response against NPV proliferation. Infection bioassays demonstrated that re‐introduction of the HcM7 strain to germfree larvae preactivated the expression of several antimicrobial peptides (particularly H. cunea gloverin 1, HcGlv1), resulting in the significant repression of virus replication in host guts and hemolymph, and consequently improved host survivorship after NPV infection. Furthermore, silencing of the HcGlv1 gene by RNA interference markedly enhanced the deleterious effects of NPV infection, revealing a role of this gut symbiont‐induced gene in host defenses against pathogenic infections.ConclusionThese results show that some gut microorganisms can stimulate host immune systems, thereby contributing to resistance to entomopathogens. Furthermore, HcM7, as a functional symbiotic bacteria of H. cunea larvae, may be a potential target for increasing the effectiveness of biocontrol agents against this devastating pest. © 2023 Society of Chemical Industry.

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Response to Bombyx mori nucleopolyhedrovirus infection in silkworm: Gut metabolites and microbiota

Cited by 16 publications

References 47 publications

The gut microbiome of Helicoverpa armigera enhances immune response to baculovirus infection via suppression of Duox‐mediated reactive oxygen species

The gut microbiome of Helicoverpa armigera enhances immune response to baculovirus infection via suppression of Duox‐mediated reactive oxygen species

Multi-omics study and ncRNA regulation of anti-BmNPV in silkworms, Bombyx mori: an update

A gut‐isolated Enterococcus strain (HcM7) triggers the expression of antimicrobial peptides that aid resistance to nucleopolyhedrovirus infection of Hyphantria cunea larvae

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