Nematode infection and antinematode immunity in Drosophila

Ozakman, Yaprak; Eleftherianos, Ioannis

doi:10.1016/j.pt.2021.06.001

Cited by 11 publications

(18 citation statements)

References 97 publications

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“…Insect immunity is an obstacle for entomopathogens to kill their targets owing to the highly efficient cellular and humoral defense responses (Ozakman & Eleftherianos, 2021). Upon microbial pathogen infection, insects immediately recognize microbes with innate pattern recognition receptors (Stokes et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Immune responses of the Asian onion moth, Acrolepiopsis sapporensis, and their genetic factors from RNA‐Seq analysis

Hrithik

Kim

2023

Arch Insect Biochem Physiol

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A nonmodel insect, Acrolepiopsis sapporensis, has been analyzed in immune responses. The total hemocytes in the fifth instar larvae were 2.33 × 106 cells/mL. These hemocytes comprised at least five different types and different relative ratios: 47% granulocytes, 26% plasmatocytes, 11% oenocytoid, 8% prohemocytes, and 5% spherulocytes. Upon bacterial challenge, some of the hemocytes exhibited typical hemocyte‐spreading behaviors, such as focal adhesion, and filopodial and lamellipodial cytoplasmic extensions. The hemocyte behaviors induced cellular immune responses demonstrated by nodule formation. In addition, the plasma collected from the immune‐challenged larvae exhibited humoral immune responses by bacterial growth inhibition along with enhanced phenoloxidase enzyme activity. These cellular and humoral immune responses were further analyzed by determining the immune‐associated genes from a transcriptome generated by RNA‐Seq. A total of about 12 Gb sequences led to about 218,116 contigs, which were predicted to encode about 46,808 genes. Comparative expression analysis showed 8392 uniquely expressed genes in the immune‐challenged larvae. Differentially expressed gene (DEG) analysis among the commonly expressed genes indicated that 782 genes were upregulated and 548 genes were downregulated in the expressions after bacterial challenge. These immune‐associated genes included pattern recognition receptors, immune mediation/signaling genes, and various immune effectors. Specifically, the genetic components of the Toll, IMD, and JAK/STAT immune signaling pathways were included in the DEG database. These results demonstrate the immune responses of A. sapporensis larvae and suggest the genes associated with the immune responses in this nonmodel insect.

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Section: Introductionmentioning

confidence: 99%

Immune responses of the Asian onion moth, Acrolepiopsis sapporensis, and their genetic factors from RNA‐Seq analysis

Hrithik

Kim

2023

Arch Insect Biochem Physiol

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“…The success of S. carpocapsae life cycle depends on this structural change in order to gain the ability to feed, therefore it would be a significant hindrance from an evolutionarily standpoint to presume that the nematode predominately relies on the release of toxins and virulence factors from its mutualistic bacteria to fulfill its most basic biological need. Yet, the release of the mutualistic bacteria into the insect hemocoel occurs a few hours after the host barriers are breached by the nematodes, which indicates that the parasites must employ their own set of pathogenic strategies 37 , 38 . Furthermore, the initial containment of the bacteria within the nematode and the temporal delay in the secretion of the bacterial toxins weakens the original notion of the mutualistic bacterial partners being the primary tactical approach of the nematode-bacterial complex and instead it presumably forms a supportive strategy of the EPN’s arsenal.…”

Section: Discussionmentioning

confidence: 99%

Excreted secreted products from the parasitic nematode Steinernema carpocapsae manipulate the Drosophila melanogaster immune response

Jones

Tafesh-Edwards

Kenney

et al. 2022

Sci Rep

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Steinernema carpocapsae is an entomopathogenic nematode (EPN) that rapidly infects and kills a wide range of insect hosts and has been linked to host immunosuppression during the initial stages of infection. The lethal nature of S. carpocapsae infections has previously been credited to its symbiotic bacteria; however, it has become evident that the nematodes are able to effectively kill their hosts independently through their excretion/secretion products (ESPs). Here we examined how the adult Drosophila melanogaster immune system is modulated in response to S. carpocapsae ESPs in an attempt to ascertain individual pathogenic contributions of the isolated compound. We found that the S. carpocapsae ESPs decrease the survival of D. melanogaster adult flies, they induce the expression of certain antimicrobial peptide-encoding genes, and they cause significant reduction in phenoloxidase enzyme activity and delay in the melanization response in males flies. We also report that S. carpocapsae ESPs affect hemocyte numbers in both male and female individuals. Our results indicate the manipulative role of EPN ESPs and reveal sex-specific differences in the host response against nematode infection factors. These findings are beneficial as they promote our understanding of the molecular basis of nematode pathogenicity and the parasite components that influence nematode-host interactions.

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“…Due to serious environmental pollution caused by pesticide abuse in recent years, many scientists have sought efficient and environmentally friendly insecticides to reduce environmental pollution, such as evaluating microbial control agents applied to the soil-inhabiting stages of pests ( Ricci et al, 1996 ; Campos-Herrera et al, 2021 ; El Aimani et al, 2021 ). The entomopathogenic nematodes (EPNs) in the phylum Nematoda are obligate insect parasites, and the only free-living stage of the nematodes, the infective juvenile (IJ), carry symbiotic bacteria to infect many insects and can cause septicemia and death of host insects within 24–48 h ( Akhurst, 1980 ; Ozakman and Eleftherianos, 2021 ). EPNs belonging to the families Heterorhabditidae and Steinernematidae are safe to humans and the environment and do not involve resistance build-up by target pests ( Wakil et al, 2022 ).…”

Section: Introductionmentioning

confidence: 99%

Metabonomics reveals that entomopathogenic nematodes mediate tryptophan metabolites that kill host insects

Zhang

Wang²,

Zhao³

2022

Front. Microbiol.

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The entomopathogenic nematode (EPN) Steinernema feltiae, which carries the symbiotic bacterium Xenorhabdus bovienii in its gut, is an important biocontrol agent. This EPN could produce a suite of complex metabolites and toxin proteins and lead to the death of host insects within 24–48 h. However, few studies have been performed on the key biomarkers released by EPNs to kill host insects. The objective of this study was to examine what substances produced by EPNs cause the death of host insects. We found that all densities of nematode suspensions exhibited insecticidal activities after hemocoelic injection into Galleria mellonella larvae. EPN infection 9 h later led to immunosuppression by activating insect esterase activity, but eventually, the host insect darkened and died. Before insect immunity was activated, we applied a high-resolution mass spectrometry-based metabolomics approach to determine the hemolymph of the wax moth G. mellonella infected by EPNs. The results indicated that the tryptophan (Trp) pathway of G. mellonella was significantly activated, and the contents of kynurenine (Kyn) and 3-hydroxyanthranilic acid (3-HAA) were markedly increased. Additionally, 3-HAA was highly toxic to G. mellonella and resulted in corrected mortalities of 62.50%. Tryptophan metabolites produced by EPNs are a potential marker to kill insects, opening up a novel line of inquiry into exploring the infestation mechanism of EPNs.

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Nematode infection and antinematode immunity in Drosophila

Cited by 11 publications

References 97 publications

Immune responses of the Asian onion moth, Acrolepiopsis sapporensis, and their genetic factors from RNA‐Seq analysis

Immune responses of the Asian onion moth, Acrolepiopsis sapporensis, and their genetic factors from RNA‐Seq analysis

Excreted secreted products from the parasitic nematode Steinernema carpocapsae manipulate the Drosophila melanogaster immune response

Metabonomics reveals that entomopathogenic nematodes mediate tryptophan metabolites that kill host insects

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