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Insects, Nematodes and Their Symbiotic Bacteria

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A special issue of Insects (ISSN 2075-4450).

Deadline for manuscript submissions: closed (31 March 2020) | Viewed by 34053

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Prof. Dr. Ulrich Theopold

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Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, SE 106 91 Stockholm, Sweden
Interests: innate immunity; insect immunity; entomopathogenic nematodes; Galleria mellonella; Drosophila melanogaster; Photorhabdus; Xenorhabdus; comparative immunology

Dr. Pavel Hyrsl

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Guest Editor

Institute of Experimental Biology, Department of Animal Physiology and Immunology, Faculty of Science, Masaryk University, UKB A36/123, Kamenice 753/5, Brno 62500, Czech Republic
Interests: innate immunity; insect immunity; entomopathogenic nematodes; Galleria mellonella; Drosophila melanogaster; Photorhabdus; Xenorhabdus; comparative immunology

Special Issue Information

Dear Colleagues,

Insect pathogenic nematodes (entomopathogenic nematodes—EPNs) are lethal parasites to their hosts, and are frequently used as biological agents in the control of insect pests. Lethality may be as a result of the virulence factors provided by the nematodes themselves, or often by mutualistically-associated bacteria. Insects are only infected by the free-living nematode stage (infective juveniles), which enter via the tracheal, digestive epithelia, or by penetrating the cuticle. Once inside their hosts, EPNs complete their development and may reproduce asexually or sexually. Their associated bacteria are released and multiply inside the hemocoel, which then provides the nematodes with a source of nutrients. Insect cadavers release the next generation of infective juveniles with the ingested symbiotic bacteria established in their guts. Recent large-scale studies have provided detailed insights into the nematode–bacteria association, their combined and individual infection success, and the effect of EPN infection on secreted factors from the insect hosts. Some of these secreted factors have been shown to have a protective role against the pathogenic complex. Thus, we invite submissions that address all aspects of the tripartite nematode/bacteria/insect interaction. Papers may cover the mutualistic interaction between nematodes and their bacteria; behaviours or pathogenesis of the nematodes and the bacteria, together or alone; and changes in insect physiology and immunology in response to EPN (with or without their bacteria).

Prof. Dr. Ulrich Theopold
Dr. Pavel Hyrsl
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Insects is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2600 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

Entomopathogenic nematodes
Heterorhabditis
Steinernema
Xenorhabdus
Photorhabdus
Insect immunity

Published Papers (10 papers)

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Editorial

Jump to: Research, Review

3 pages, 171 KiB

Open AccessEditorial

Special Issue: Insects, Nematodes, and Their Symbiotic Bacteria

by Ulrich Theopold, Alexis Dziedziech and Pavel Hyrsl

Insects 2020, 11(9), 577; https://doi.org/10.3390/insects11090577 - 28 Aug 2020

Cited by 2 | Viewed by 1999

Abstract

This special issue contains articles that add to the ever-expanding toolbox of insect pathogenic nematodes (entomopathogenic nematodes; EPNs) as well articles that provide new insights into the mutualistic interaction between EPNs and their hosts. The study of natural infection models such as EPNs allows detailed insight into micro- and macro-evolutionary dynamics of innate immune reactions, including known but also emerging branches of innate immunity. Additional new insights into the kinetics of EPN infections are gained by increased spatiotemporal resolution of advanced transcriptome studies and live imaging. Full article

(This article belongs to the Special Issue Insects, Nematodes and Their Symbiotic Bacteria)

Research

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19 pages, 1834 KiB

Open AccessArticle

Bioactive Excreted/Secreted Products of Entomopathogenic Nematode Heterorhabditis bacteriophora Inhibit the Phenoloxidase Activity during the Infection

by Sara Eliáš, Jana Hurychová, Duarte Toubarro, Jorge Frias, Martin Kunc, Pavel Dobeš, Nelson Simões and Pavel Hyršl

Insects 2020, 11(6), 353; https://doi.org/10.3390/insects11060353 - 05 Jun 2020

Cited by 12 | Viewed by 3259

Abstract

Entomopathogenic nematodes (EPNs) are efficient insect parasites, that are known for their mutualistic relationship with entomopathogenic bacteria and their use in biocontrol. EPNs produce bioactive molecules referred to as excreted/secreted products (ESPs), which have come to the forefront in recent years because of their role in the process of host invasion and the modulation of its immune response. In the present study, we confirmed the production of ESPs in the EPN Heterorhabditis bacteriophora, and investigated their role in the modulation of the phenoloxidase cascade, one of the key components of the insect immune system. ESPs were isolated from 14- and 21-day-old infective juveniles of H. bacteriophora, which were found to be more virulent than newly emerged nematodes, as was confirmed by mortality assays using Galleria mellonella larvae. The isolated ESPs were further purified and screened for the phenoloxidase-inhibiting activity. In these products, a 38 kDa fraction of peptides was identified as the main candidate source of phenoloxidase-inhibiting compounds. This fraction was further analyzed by mass spectrometry and the de novo sequencing approach. Six peptide sequences were identified in this active ESP fraction, including proteins involved in ubiquitination and the regulation of a Toll pathway, for which a role in the regulation of insect immune response has been proposed in previous studies. Full article

(This article belongs to the Special Issue Insects, Nematodes and Their Symbiotic Bacteria)

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15 pages, 1022 KiB

Open AccessArticle

Evaluation of the Field Efficacy of Heterorhabditis Bacteriophora Poinar (Rhabditida: Heterorhabditidae) and Synthetic Insecticides for the Control of Western Corn Rootworm Larvae

by Špela Modic, Primož Žigon, Aleš Kolmanič, Stanislav Trdan and Jaka Razinger

Insects 2020, 11(3), 202; https://doi.org/10.3390/insects11030202 - 24 Mar 2020

Cited by 11 | Viewed by 3045

Abstract

The western corn rootworm (WCR), Diabrotica virgifera virgifera LeConte (Coleoptera, Chrysomelidae), is an important insect pest of maize in North America and Central and Eastern Europe. In Central Europe, the larvae emerge in May and its three instars feed intensively on maize roots in June, causing plant lodging that leads to a loss of economic yield. A three-year field experiment (2016–2018) was conducted to compare the effectiveness i) of soil-applied granular insecticide based on the active ingredient tefluthrin, ii) of maize seeds dressed with thiacloprid, and iii) entomopathogenic nematodes Heterorhabditis bacteriophora Poinar (Rhabditida: Heterorhabditidae, product Dianem) against WCR larvae. An additional treatment with alcohol ethoxylate (i.e., soil conditioner) mixed with entomopathogenic nematodes was performed in 2017 and 2018 to check for any increase of entomopathogenic nematodes’ effectiveness. Field tests were carried out in two fields infested naturally with a WCR pest population, one in Bučečovci (Eastern Slovenia) and the other in Šmartno pri Cerkljah (northern Slovenia), exhibiting dissimilar pedo-climatic conditions and soil pest densities. The treatments were performed in five replicates per experiment in each year. The efficacy of the treatments was very similar at both locations, despite the approximately five-fold lower WCR soil pest densities in northern than in eastern Slovenia, as well as being constant over time. The largest number of WCR beetles was observed in the negative control, followed by that of beetles subjected to thiacloprid treatment (insignificant decrease taking into account the entire three-year dataset). Treatments with tefluthrin (44.1 ± 11.7%), H. bacteriophora (46.2 ± 7.4%), and H. bacteriophora + alcohol ethoxylate (49.2 ± 1.8%) significantly decreased the numbers of emerging beetles. Treatments of thiacloprid, H. bacteriophora, and H. bacteriophora + alcohol ethoxylate additionally led to significantly increased maize plant weights. Furthermore, entomopathogenic nematodes were able to persist in maize fields for almost five months at both experimental locations in silty and sandy loam soils. It was concluded that the control of WCR larvae in maize using the entomopathogenic nematode H. bacteriophora is as effective as a tefluthrin treatment, and could thus offer a sustainable Diabrotica v. virgifera biological control management option in Europe. Full article

(This article belongs to the Special Issue Insects, Nematodes and Their Symbiotic Bacteria)

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12 pages, 715 KiB

Open AccessArticle

First Record of the Entomopathogenic Nematode Steinernema litorale (Filipjev) (Rhabditida: Steinernematidae) and Its Symbiotic Bacterium from Turkey, and Its Efficacy Capability

by Esengül Özdemir, Şerife Bayram and İ. Alper Susurluk

Insects 2020, 11(3), 144; https://doi.org/10.3390/insects11030144 - 25 Feb 2020

Cited by 4 | Viewed by 2588

Abstract

The entomopathogenic nematode Steinernema litorale was isolated from Çamkoru Nature Park located in Ankara, Turkey, in September 2018. Steinernema litorale was recovered in 1 of 67 soil samples from a natural forest area; the soil was characterised as sandy loam. The isolated nematode S. litorale was identified based on morphological and molecular parameters. The symbiotic bacterium of S. litorale was determined as Xenorhabdus bovienii. Steinernema litorale was found for the first time in Turkey and the Middle East. The virulence of the isolate was tested on Galleria mellonella larvae. Different concentrations of the nematode (10, 25, 50, 75, and 100 infective juveniles (IJs/larvae) were used. While the LC₅₀ values at 48 h, 72 h, and 96 h were 153.419, 51.005, and 15.439 IJs, respectively, and the LT₅₀ values at 75 IJs and 100 IJs showed that this isolate is capable to control insect larvae within 50.083 and 36.266 h, respectively. Full article

(This article belongs to the Special Issue Insects, Nematodes and Their Symbiotic Bacteria)

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15 pages, 2931 KiB

Open AccessArticle

High-Resolution Infection Kinetics of Entomopathogenic Nematodes Entering Drosophila melanogaster

by Alexis Dziedziech, Sai Shivankar and Ulrich Theopold

Insects 2020, 11(1), 60; https://doi.org/10.3390/insects11010060 - 18 Jan 2020

Cited by 13 | Viewed by 3484

Abstract

Entomopathogenic nematodes (EPNs) have been a useful model for studying wound healing in insects due to their natural mechanism of entering an insect host either through the cuticle or an orifice. While many experiments have shed light on nematode and host behavior, as well as the host immune response, details regarding early nematode entry and proliferative events have been limited. Using high-resolution microscopy, we provide data on the early infection kinetics of Heterorhabditis bacteriophora and its symbiotic bacteria, Photorhabdus luminescens. EPNs appendage themselves to the host and enter through the host cuticle with a drill-like mechanism while leaving their outer sheath behind. EPNs immediately release their symbiotic bacteria in the host which leads to changes in host behavior and septicemia within 6 h while EPNs travel through the host in a predictable manner, congregating in the anterior end of the host. This paper sheds light on the entry and proliferative events of EPN infection, which will further aid in our understanding of wound healing and host immune activation at a high spatiotemporal resolution. Full article

(This article belongs to the Special Issue Insects, Nematodes and Their Symbiotic Bacteria)

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12 pages, 1075 KiB

Open AccessArticle

Effects of the Entomopathogenic Fungus Metarhizium anisopliae on the Mortality and Immune Response of Locusta migratoria

by Wuji Jiang, Yifan Peng, Jiayi Ye, Yiyi Wen, Gexin Liu and Jiaqin Xie

Insects 2020, 11(1), 36; https://doi.org/10.3390/insects11010036 - 31 Dec 2019

Cited by 33 | Viewed by 5107

Abstract

Entomopathogenic fungi are the key regulators of insect populations and some of them are important biological agents used in integrated pest management strategies. Compared with their ability to become resistant to insecticides, insect pests do not easily become resistant to the infection by entomopathogenic fungi. In this study, we evaluated the mortality and immune response of the serious crop pest Locusta migratoria manilensis after exposure to a new entomopathogenic fungus strain, Metarhizium anisopliae CQMa421. M. anisopliae CQMa421 could effectively infect and kill the L. migratoria adults and nymphs. The locust LT₅₀ under 1 × 10⁸ conidia/mL concentration of M. anisopliae was much lower than that under conidial concentration 1 × 10⁵ conidia/mL (i.e., 6.0 vs. 11.2 and 5.0 vs. 13.8 for adults and nymphs, respectively). The LC₅₀ (log₁₀) of M. anisopliae against locust adults and nymphs after 10 days was 5.2 and 5.6, respectively. Although the number of hemocytes in L. migratoria after exposure to M. anisopliae did not differ with that in the controls, the enzymatic activity of superoxide dismutase (SOD) and prophenoloxidase (ProPO) did differ between the two treatments. The activities of both SOD and ProPO under the M. anisopliae treatment were lower than that in the controls, except for the ProPO activity at 72 h and the SOD activity at 96 h. Further, the expression of the L. migratoria immune-related genes defensin, spaetzle, and attacin differed after exposure to M. anisopliae for 24 h to 96 h. Taken together, this study indicated that infection with M. anisopliae CQMa421 could cause the death of L. migratoria by interacting with the immune responses of the host, demonstrating that this fungal strain of M. anisopliae can be an efficient biocontrol agent against L. migratoria. Full article

(This article belongs to the Special Issue Insects, Nematodes and Their Symbiotic Bacteria)

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20 pages, 4562 KiB

Open AccessArticle

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

by Miltan Chandra Roy, Dongwoon Lee and Yonggyun Kim

Insects 2020, 11(1), 33; https://doi.org/10.3390/insects11010033 - 31 Dec 2019

Cited by 9 | Viewed by 3363

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. Full article

(This article belongs to the Special Issue Insects, Nematodes and Their Symbiotic Bacteria)

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14 pages, 1923 KiB

Open AccessArticle

Functional Characterization of Outer Membrane Proteins (OMPs) in Xenorhabdus nematophila and Photorhabdus luminescens through Insect Immune Defense Reactions

by Reyhaneh Darsouei, Javad Karimi and Gary B. Dunphy

Insects 2019, 10(10), 352; https://doi.org/10.3390/insects10100352 - 17 Oct 2019

Cited by 4 | Viewed by 2936

Abstract

Xenorhabdus nematophila and Photorhabdus luminescens are entomopathogenic bacterial symbionts that produce toxic proteins that can interfere with the immune system of insects. Herein, we show that outer membrane proteins (OMPs) could be involved as bacterial virulence factors. Purified totals OMPs of both bacterial species were injected into fifth instar larvae of Spodoptera exigua Hübner. Larvae were surveyed for cellular defenses fluctuations in total haemocyte counts (THC) and granulocyte percentage and for the humoral defenses protease, phospholipase A2 (PLA₂), and phenoloxidase (PO) activities at specific time intervals. Changes in the expression of the three inducible antimicrobial peptides (AMPs), cecropin, attacin, and spodoptericin, were also measured. Larvae treated with OMPs of both bacterial species had more haemocytes than did the negative controls. OMPs of X. nematophila caused more haemocyte destruction than did the OMPs of P. luminescens. The OMPs of both bacterial species initially activated insect defensive enzymes post-injection, the degree of activation varying with enzyme type. The AMPs, attacin, cecropin, and spodoptericin were up-regulated by OMP injections compared with the normal larvae. The expression of these three AMPs was maximal at four hours post injection (hpi) with P. luminescens OMPs treatment. Expression of the three AMPs in X. nematophila treated insects was irregular and lower than in the P. luminescens OMPs treatment. These findings provide insights into the role of OMPs of entomopathogenic nematode bacterial symbionts in countering the physiological defenses of insects. Full article

(This article belongs to the Special Issue Insects, Nematodes and Their Symbiotic Bacteria)

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Review

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8 pages, 736 KiB

Open AccessReview

Thioester-Containing Proteins in the Drosophila melanogaster Immune Response against the Pathogen Photorhabdus

by Ioannis Eleftherianos and Upasana Sachar

Insects 2020, 11(2), 85; https://doi.org/10.3390/insects11020085 - 28 Jan 2020

Cited by 5 | Viewed by 3139

Abstract

The fruit fly Drosophila melanogaster forms a magnificent model for interpreting conserved host innate immune signaling and functional processes in response to microbial assaults. In the broad research field of host-microbe interactions, model hosts are used in conjunction with a variety of pathogenic microorganisms to disentangle host immune system activities and microbial pathogenicity strategies. The pathogen Photorhabdus is considered an established model for analyzing bacterial virulence and symbiosis due to its unique life cycle that extends between two invertebrate hosts: an insect and a parasitic nematode. In recent years, particular focus has been given to the mechanistic participation of the D. melanogaster thioester-containing proteins (TEPs) in the overall immune capacity of the fly upon response against the pathogen Photorhabdus alone or in combination with its specific nematode vector Heterorhabditis bacteriophora. The original role of certain TEPs in the insect innate immune machinery was linked to the antibacterial and antiparasite reaction of the mosquito malaria vector Anopheles gambiae; however, revamped interest in the immune competence of these molecules has recently emerged from the D. melanogaster-Photorhabdus infection system. Here, we review the latest findings on this topic with the expectation that such information will refine our understanding of the evolutionary immune role of TEPs in host immune surveillance. Full article

(This article belongs to the Special Issue Insects, Nematodes and Their Symbiotic Bacteria)

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11 pages, 1341 KiB

Open AccessReview

Drosophila melanogaster Responses against Entomopathogenic Nematodes: Focus on Hemolymph Clots

by Alexis Dziedziech, Sai Shivankar and Ulrich Theopold

Insects 2020, 11(1), 62; https://doi.org/10.3390/insects11010062 - 19 Jan 2020

Cited by 14 | Viewed by 4125

Abstract

Several insect innate immune mechanisms are activated in response to infection by entomopathogenic nematodes (EPNs). In this review, we focus on the coagulation of hemolymph, which acts to stop bleeding after injury and prevent access of pathogens to the body cavity. After providing a general overview of invertebrate coagulation systems, we discuss recent findings in Drosophila melanogaster which demonstrate that clots protect against EPN infections. Detailed analysis at the cellular level provided insight into the kinetics of the secretion of Drosophila coagulation factors, including non-classical modes of secretion. Roughly, clot formation can be divided into a primary phase in which crosslinking of clot components depends on the activity of Drosophila transglutaminase and a secondary, phenoloxidase (PO)-dependent phase, characterized by further hardening and melanization of the clot matrix. These two phases appear to play distinct roles in two commonly used EPN infection models, namely Heterorhabditis bacteriophora and Steinernema carpocapsae. Finally, we discuss the implications of the coevolution between parasites such as EPNs and their hosts for the dynamics of coagulation factor evolution. Full article

(This article belongs to the Special Issue Insects, Nematodes and Their Symbiotic Bacteria)

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