Effects of an entomopathogen nematode on the immune response of the insect pest red palm weevil: Focus on the host antimicrobial response

Binda-Rossetti, Simona; Mastore, Maristella; Protasoni, Marina; Brivio, Maurizio Francesco

doi:10.1016/j.jip.2015.11.001

Cited by 36 publications

(33 citation statements)

References 55 publications

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“…The latter finding is based on the facts that heat-killed X. nematophila is recognized by immune surveillance systems and induces AMP expression (4,12,13) and that when wild-type X. nematophila is coinjected with an immunogenic bacterial strain it prevents induction of AMP expression (4). X. nematophila can inhibit phagocytosis and nodulation by secreting phospholipase A 2 (PLA 2 ) inhibitors (5,6,8,9,(14)(15)(16).…”

mentioning

confidence: 99%

The Global Transcription Factor Lrp Is both Essential for and Inhibitory to Xenorhabdus nematophila Insecticidal Activity

Casanova-Torres

Shokal

Morag

et al. 2017

Appl Environ Microbiol

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In the entomopathogenic bacterium Xenorhabdus nematophila, cell-tocell variation in the abundance of the Lrp transcription factor leads to virulence modulation; low Lrp levels are associated with a virulent phenotype and suppression of antimicrobial peptides (AMPs) in Manduca sexta insects, while cells that lack lrp or express high Lrp levels are virulence attenuated and elicit AMP expression. To better understand the basis of these phenotypes, we examined X. nematophila strains expressing fixed Lrp levels. Unlike the lrp-null mutant, the high-lrp strain is fully virulent in Drosophila melanogaster, suggesting that these two strains have distinct underlying causes of virulence attenuation in M. sexta. Indeed, the lrp-null mutant was defective in cytotoxicity against M. sexta hemocytes relative to that in the high-lrp and low-lrp strains. Further, supernatant derived from the lrp-null mutant but not from the high-lrp strain was defective in inhibiting weight gain when fed to 1st instar M. sexta. These data suggest that contributors to the lrp-null mutant virulence attenuation phenotype are the lack of Lrp-dependent cytotoxic and extracellular oral growth inhibitory activities, which may be particularly important for virulence in D. melanogaster. In contrast, the high-Lrp strain was sensitive to the antimicrobial peptide cecropin, had a transient survival defect in M. sexta, and had reduced extracellular levels of insecticidal activity, measured by injection of supernatant into 4th instar M. sexta. Thus, high-lrp strain virulence attenuation may be explained by its hypersensitivity to M. sexta host immunity and its inability to secrete one or more insecticidal factors.IMPORTANCE Adaptation of a bacterial pathogen to host environments can be achieved through the coordinated regulation of virulence factors that can optimize success under prevailing conditions. In the insect pathogen Xenorhabdus nematophila, the global transcription factor Lrp is necessary for virulence when injected into Manduca sexta or Drosophila melanogaster insect hosts. However, high levels of Lrp, either naturally occurring or artificially induced, cause attenuation of X. nematophila virulence in M. sexta but not D. melanogaster. Here, we present evidence suggesting that the underlying cause of high-Lrp-dependent virulence attenuation in M. sexta is hypersensitivity to host immune responses and decreased insecticidal activity and that high-Lrp virulence phenotypes are insect host specific. This knowledge suggests that X. nematophila faces varied challenges depending on the type of insect host it infects and that its success in these environments depends on Lrp-dependent control of a multifactorial virulence repertoire.

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confidence: 99%

The Global Transcription Factor Lrp Is both Essential for and Inhibitory to Xenorhabdus nematophila Insecticidal Activity

Casanova-Torres

Shokal

Morag

et al. 2017

Appl Environ Microbiol

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“…Since it was thought that the bacteria were the main contributor to insect death, most research has focused on the pathogenic effect of the bacteria rather than the nematode678. Nevertheless, growing evidence suggests a more active role of the nematode in the pathogenic process910. In fact, a set of expanded gene families that are likely involved in parasitism were predicted in a recent genome analysis of Steinernema species11.…”

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confidence: 99%

The genome, transcriptome, and proteome of the nematode Steinernema carpocapsae: evolutionary signatures of a pathogenic lifestyle

Rougon‐Cardoso

Flores-Ponce

Ramos-Aboites

et al. 2016

Sci Rep

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The entomopathogenic nematode Steinernema carpocapsae has been widely used for the biological control of insect pests. It shares a symbiotic relationship with the bacterium Xenorhabdus nematophila, and is emerging as a genetic model to study symbiosis and pathogenesis. We obtained a high-quality draft of the nematode’s genome comprising 84,613,633 bp in 347 scaffolds, with an N50 of 1.24 Mb. To improve annotation, we sequenced both short and long RNA and conducted shotgun proteomic analyses. S. carpocapsae shares orthologous genes with other parasitic nematodes that are absent in the free-living nematode C. elegans, it has ncRNA families that are enriched in parasites, and expresses proteins putatively associated with parasitism and pathogenesis, suggesting an active role for the nematode during the pathogenic process. Host and parasites might engage in a co-evolutionary arms-race dynamic with genes participating in their interaction showing signatures of positive selection. Our analyses indicate that the consequence of this arms race is better characterized by positive selection altering specific functions instead of just increasing the number of positively selected genes, adding a new perspective to these co-evolutionary theories. We identified a protein, ATAD-3, that suggests a relevant role for mitochondrial function in the evolution and mechanisms of nematode parasitism.

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“…Varied activity spectra have also been found for several insects’ lysozymes and LLPs (53–57). Interestingly, all of the categories and subcategories cited above were represented in the two tissues, indicating that their antimicrobial responses are diversified and that the factors responsible for their disappearance in the hemolymph (24, 41) probably act at a post-transcriptional level. About a half of the genes presented similar and significant induction profiles in the hemocytes and in the fat body.…”

Section: Resultsmentioning

confidence: 99%

“…These interactions have firstly been studied from the NBC point of view, which allowed the identification of a multitude of immunoevasive and immunosuppressive strategies. For instance, studies in Rhynchophorus ferrugineus and Galleria mellonella have respectively shown that the cuticle of S. carpocapsae is not recognized by the host’s immune system (24, 25) and that the nematode secretes protease inhibitors impairing the coagulation responses (26, 27). Studies in diverse insect models have also shown that both partners produce factors impairing melanization (28–31), hemocyte’s viability (32–36) and the production of cellular immune responses by several ways (27–29, 31, 37, 38).…”

Section: Introductionmentioning

confidence: 99%

“…Studies in diverse insect models have also shown that both partners produce factors impairing melanization (28–31), hemocyte’s viability (32–36) and the production of cellular immune responses by several ways (27–29, 31, 37, 38). Finally, both X. nematophila and S. carpocapsae secrete proteolytic factors degrading cecropin AMPs (39, 40) and the bacterium has also been shown to reduce more globally the hemolymph antimicrobial activity, as well as AMP transcription in lepidopteran models (24, 39, 41, 42).…”

Section: Introductionmentioning

confidence: 99%

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Partner-specific induction ofSpodoptera frugiperdaimmune genes in response to the entomopathogenic nematobacterial complexSteinernema carpocapsae-Xenorhabdus nematophila

Huot

Bigourdan

Pagès

et al. 2019

Preprint

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13The Steinernema carpocapsae-Xenorhabdus nematophila association is a nematobacterial complex (NBC) 14 used in biological control of insect crop pests. The ability of this dual pathogen to infest and kill an insect 15 strongly depends on the dialogue between the host's immune system and each partner of the complex. Even 16 though this dialogue has been extensively studied from the two partners' points of view in several insect 17 models, still little is known about the structure and the molecular aspects of the insects' immune response 18 to the dual infection. Here, we used the lepidopteran pest Spodoptera frugiperda as a model to analyze the 19 respective impact of each NBC partner in the spatiotemporal immune responses that are induced after 20 infestation. To this aim, we first analyzed the expression variations of the insect's immune genes in the fat 21 bodies and hemocytes of infested larvae by using previously obtained RNAseq data. We then selected 22 representative immune genes for RT-qPCR investigations of the temporal variations of their expressions 23 after infestation and of their induction levels after independent injections of each partner. We found that 24 the fat body and the hemocytes both produce potent and stable immune responses to the infestation by the 25 NBC, which correspond to combinations of bacterium-and nematode-induced ones. Consistent with the 26 nature of each pathogen, we showed that X. nematophila mainly induces genes classically involved in 27 antibacterial responses, whereas S. carpocapsae is responsible for the induction of lectins and of genes 28 expected to be involved in melanization and cellular encapsulation. In addition, we found that two clusters 29 of unknown genes dramatically induced by the NBC also present partner-specific induction profiles, which 30 paves the way for their functional characterization. Finally, we discuss putative relationships between the 31 variations of the expression of some immune genes and the NBC's immunosuppressive strategies. 32 3 33Author summary 34 Entomopathogenic nematodes (EPNs) are living in the soil and prey upon insect larvae. They enter the 35 insect by the natural orifices, and reach the hemocoel through the intestinal epithelium. There, they release 36 their symbiotic bacteria that will develop within the insect and eventually kill it. Nematodes can then feed 37 and reproduce on the insect cadaver. By using transcriptomic approaches, we previously showed that 38 Lepidoptera larvae (caterpillars of the fall armyworm Spodoptera frugiperda) produce a strong immune 39 response in reaction to infestation by EPNs. However, we do not know if this immune reaction is triggered 40 by the nematode itself -Steinernema carpacapsae -or its symbiotic bacteria -Xenorhabdus nematophila. 41 To answer this question, we present in this work a careful annotation of immunity genes in S. frugiperda 42 and surveyed their activation by quantitative PCR in reaction to an injection of the bacteria alone, the axenic 43 nematode or the ...

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Effects of an entomopathogen nematode on the immune response of the insect pest red palm weevil: Focus on the host antimicrobial response

Cited by 36 publications

References 55 publications

The Global Transcription Factor Lrp Is both Essential for and Inhibitory to Xenorhabdus nematophila Insecticidal Activity

The Global Transcription Factor Lrp Is both Essential for and Inhibitory to Xenorhabdus nematophila Insecticidal Activity

The genome, transcriptome, and proteome of the nematode Steinernema carpocapsae: evolutionary signatures of a pathogenic lifestyle

Partner-specific induction ofSpodoptera frugiperdaimmune genes in response to the entomopathogenic nematobacterial complexSteinernema carpocapsae-Xenorhabdus nematophila

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