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Host Immunosuppression Induced by Steinernema feltiae, an Entomopathogenic Nematode, through Inhibition of Eicosanoid Biosynthesis.

ABSTRACT: Steinernema feltiae K1 (Filipjev) (Nematode: Steinernematidae), an entomopathogenic nematode, was isolated and identified based on its morphological and molecular diagnostic characteristics. Its infective juveniles (IJs) were highly pathogenic to three lepidopteran (LC50 = 23.7-25.0 IJs/larva) and one coleopteran (LC50 = 39.3 IJs/larva) insect species. Infected larvae of the diamondback moth, Plutella xylostella (L.) (Insecta: Lepidoptera), exhibited significant reduction in phospholipase A2 (PLA2) activity in their plasma. The decrease of PLA2 activity was followed by significant septicemia of the larvae infected with S. feltiae. Insecticidal activity induced by S. feltiae was explained by significant immunosuppression in cellular immune responses measured by hemocyte nodule formation and total hemocyte count (THC). Although S. feltiae infection suppressed nodule formation and THC in the larvae, an addition of arachidonic acid (AA, a catalytic product of PLA2) rescued these larvae from fatal immunosuppression. In contrast, an addition of dexamethasone (a specific PLA2 inhibitor) enhanced the nematode's pathogenicity in a dose-dependent manner. To discriminate the immunosuppressive activity of a symbiotic bacterium (Xenorhabdus bovienii (Proteobacteria: Enterobacterales)) from the nematode, kanamycin was applied to after nematode infection. It significantly inhibited the bacterial growth in the hemolymph. Compared to nematode treatment alone, the addition of antibiotics to nematode infection partially rescued the immunosuppression measured by phenol oxidase activity. Consequently, treatment with antibiotics significantly rescued the larvae from the insecticidal activity of S. feltiae. These results suggest that immunosuppression induced by infection of S. feltiae depends on its symbiotic bacteria by inhibiting eicosanoid biosynthesis, resulting in significant insect mortality. However, the addition of antibiotics or AA could not completely rescue the virulence of the nematode, suggesting that the nematode itself also plays a role in its insecticidal activity.

SUBMITTER: Chandra Roy M

PROVIDER: S-EPMC7023448 | biostudies-literature | 2019 Dec

REPOSITORIES: biostudies-literature

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Host Immunosuppression Induced by Steinernema feltiae, an Entomopathogenic Nematode, through Inhibition of Eicosanoid Biosynthesis.

Chandra Roy Miltan M Lee Dongwoon D Kim Yonggyun Y

Insects 20191231 1

Steinernema feltiae K1 (Filipjev) (Nematode: Steinernematidae), an entomopathogenic nematode, was isolated and identified based on its morphological and molecular diagnostic characteristics. Its infective juveniles (IJs) were highly pathogenic to three lepidopteran (LC50 = 23.7-25.0 IJs/larva) and one coleopteran (LC50 = 39.3 IJs/larva) insect species. Infected larvae of the diamondback moth, Plutella xylostella (L.) (Insecta: Lepidoptera), exhibited significa ...[more]

PMID: 31906089

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Project description:BackgroundThe entomopathogenic nematode Steinernema carpocapsae has been used worldwide as a biocontrol agent for insect pests, making it an interesting model for understanding parasite-host interactions. Two models propose that these interactions are co-evolutionary processes in such a way that equilibrium is never reached. In one model, known as "arms race", new alleles in relevant genes are fixed in both host and pathogens by directional positive selection, producing recurrent and alternating selective sweeps. In the other model, known as"trench warfare", persistent dynamic fluctuations in allele frequencies are sustained by balancing selection. There are some examples of genes evolving according to both models, however, it is not clear to what extent these interactions might alter genome-level evolutionary patterns and intraspecific diversity. Here we investigate some of these aspects by studying genomic variation in S. carpocapsae and other pathogenic and free-living nematodes from phylogenetic clades IV and V.ResultsTo look for signatures of an arms-race dynamic, we conducted massive scans to detect directional positive selection in interspecific data. In free-living nematodes, we detected a significantly higher proportion of genes with sites under positive selection than in parasitic nematodes. However, in these genes, we found more enriched Gene Ontology terms in parasites. To detect possible effects of dynamic polymorphisms interactions we looked for signatures of balancing selection in intraspecific genomic data. The observed distribution of Tajima's D values in S. carpocapsae was more skewed to positive values and significantly different from the observed distribution in the free-living Caenorhabditis briggsae. Also, the proportion of significant positive values of Tajima's D was elevated in genes that were differentially expressed after induction with insect tissues as compared to both non-differentially expressed genes and the global scan.ConclusionsOur study provides a first portrait of the effects that lifestyle might have in shaping the patterns of selection at the genomic level. An arms-race between hosts and pathogens seems to be affecting specific genetic functions but not necessarily increasing the number of positively selected genes. Trench warfare dynamics seem to be acting more generally in the genome, likely focusing on genes responding to the interaction, rather than targeting specific genetic functions.

Project description:Entomopathogenic nematodes (EPNs) employ a sophisticated chemosensory apparatus to detect potential hosts. Understanding the molecular basis of relevant host-finding behaviours could facilitate improved EPN biocontrol approaches, and could lend insight to similar behaviours in economically important mammalian parasites. FMRFamide-like peptides are enriched and conserved across the Phylum Nematoda, and have been linked with motor and sensory function, including dispersal and aggregating behaviours in the free living nematode Caenorhabditis elegans. The RNA interference (RNAi) pathway of Steinernema carpocapsae was characterised in silico, and employed to knockdown the expression of the FMRFamide-like peptide 21 (GLGPRPLRFamide) gene (flp-21) in S. carpocapsae infective juveniles; a first instance of RNAi in this genus, and a first in an infective juvenile of any EPN species. Our data show that 5 mg/ml dsRNA and 50 mM serotonin triggers statistically significant flp-21 knockdown (-84%***) over a 48 h timecourse, which inhibits host-finding (chemosensory), dispersal, hyperactive nictation and jumping behaviours. However, whilst 1 mg/ml dsRNA and 50 mM serotonin also triggers statistically significant flp-21 knockdown (-51%**) over a 48 h timecourse, it does not trigger the null sensory phenotypes; statistically significant target knockdown can still lead to false negative results, necessitating appropriate experimental design. SPME GC-MS volatile profiles of two EPN hosts, Galleria mellonella and Tenebrio molitor reveal an array of shared and unique compounds; these differences had no impact on null flp-21 RNAi phenotypes for the behaviours assayed. Localisation of flp-21 / FLP-21 to paired anterior neurons by whole mount in situ hybridisation and immunocytochemistry corroborates the RNAi data, further suggesting a role in sensory modulation. These data can underpin efforts to study these behaviours in other economically important parasites, and could facilitate molecular approaches to EPN strain improvement for biocontrol.

Dataset Information

Host Immunosuppression Induced by Steinernema feltiae, an Entomopathogenic Nematode, through Inhibition of Eicosanoid Biosynthesis.

Publications

Host Immunosuppression Induced by <i>Steinernema feltiae</i>, an Entomopathogenic Nematode, through Inhibition of Eicosanoid Biosynthesis.

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