The venom composition and parthenogenesis mechanism of the parasitoid wasp Microctonus hyperodae, a declining biocontrol agent

Inwood, Sarah N; Harrop, Thomas W. R.; Dearden, Peter K.

doi:10.1016/j.ibmb.2022.103897

Cited by 6 publications

(25 citation statements)

References 117 publications

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“…Candidate VLP virulence proteins were selected according to their peptide abundance (PSM for Peptide-Spectrum Matches) value and only proteins with a PSM value higher than 50 were retained (Table S10). Some proteins that have been described in parasitoid wasp venoms (Inwood et al, 2023; S. Moreau & Asgari, 2015; Poirié et al, 2014), such as a serpin, a peroxiredoxin, a calreticulin and an aminopeptidase, have been found in CcapiVLPs. Further investigation on the serpin showed that the gene encoding this protein is a member of a multigenic family, which comprises 15 members in Campoplex spp .…”

Section: Resultsmentioning

confidence: 99%

“…Several studies have suggested calreticulin works as an antagonist, competing for binding sites with host calreticulins, thus inhibiting hemocyte encapsulation (Cha et al, 2015; L. Wang et al, 2013; G. Zhang et al, 2006). Aminopeptidase activity or proteins have been detected in the venoms of several parasitoid wasps (Becchimanzi et al, 2020; Dani et al, 2005; Inwood et al, 2023; Mathé-Hubert et al, 2016; Teng et al, 2017), although the functions of these enzymes in the interaction are not clear they could be involved in general degradation of host tissues.…”

Section: Discussionmentioning

confidence: 99%

“…We therefore searched for virulence protein candidates which have similar functions to virulence proteins from other domesticated viruses or venom proteins. Of these virulence protein candidates, we found a serine protease inhibitor (serpin), which is a protein that has also been detected in venom of several parasitoid wasps and in MdBV (Microplitis demolitor Bracovirus) (Beck & Strand, 2007;Inwood et al, 2023;Moreau & Asgari, 2015;Poirié et al, 2014;Quicke & Butcher, 2021). These proteins have been shown to inhibit the proteolytic cascade leading to the production of phenoloxidase (PO), involved in the melanisation reaction (Beck & Strand, 2007;Colinet et al, 2009).…”

Section: Ccapivlps and Vcvlp Do Not Share The Same Vlp Contentmentioning

confidence: 90%

“…Zhang et al, 2006). Aminopeptidase activity or proteins have been detected in the venoms of several parasitoid wasps (Becchimanzi et al, 2020;Dani et al, 2005;Inwood et al, 2023;Mathé-Hubert et al, 2016;Teng et al, 2017), although the functions of these enzymes in the interaction are not clear they could be involved in general degradation of host tissues. It has often been described that genes encoding virulence proteins are part of multigenic families expanded in species harbouring them.…”

Section: Ccapivlps and Vcvlp Do Not Share The Same Vlp Contentmentioning

confidence: 99%

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Discovery of new endogenous viral elements in campoplegine wasps (Ichneumonidae, Campopleginae, Campoplex) suggests a widespread nudivirus domestication event

de Araujo,

Leobold,

Cariou

et al. 2023

Preprint

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Viral endogenization is a widespread phenomenon that generally results in non-functional viral elements. In parasitoid wasps, nudiviruses have been involved in three independent domestication events and play a key role in parasitism success. In Campopleginae (Ichneumonidae), endogenized ichnovirus presence is widespread, with the exception ofVenturia canescens(Ichneumonidae Campopleginae), which is known to harbour an endogenous nudivirus that enables the wasp to produce Virus-Like-Particles (VLPs). So far, in Campopleginae, the nudivirus endogenization event was an isolated case restricted toV. canescens.Using third generation sequencing technologies, microscopy and mass spectrometry, we described new cases of domesticated nudiviruses in campoplegine wasps of the genusCampoplex. We found endogenized viruses inCampoplexgenomes which belong to the Alphanudivrius genus and derive from the same endogenization event as the virus found inV. canescens,suggesting that this integration event could be much more widespread in Campopleginae than previously thought. These nudiviruses are organised in highly conserved clusters, but this organisation appears to have changed relatively to free viruses during the domestication process. We showed thatCampoplex capitatorproduces in its ovaries VLPs that are similar morphologically toV. canescensVLPs, with almost the same protein content, except for a strikingly different virulence proteins, a sign of different evolutionary paths taken to respond to distinct evolutive pressure. While ichnovirus remnants have been previously found inV. canescens, no trace of ichnovirus could be detected inCampoplexgenomes, meaning that the evolutionary history of viral integrations in Campopleginae is more complex than previously imagined.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Ccapivlps and Vcvlp Do Not Share The Same Vlp Contentmentioning

confidence: 90%

Section: Ccapivlps and Vcvlp Do Not Share The Same Vlp Contentmentioning

confidence: 99%

See 2 more Smart Citations

Discovery of new endogenous viral elements in campoplegine wasps (Ichneumonidae, Campopleginae, Campoplex) suggests a widespread nudivirus domestication event

de Araujo,

Leobold,

Cariou

et al. 2023

Preprint

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“…Soon after parasitism, ASW are reproductively sterilised by M. hyperodae , with some internal organs consumed by the developing larvae (leaving the digestive system and some thoracic tissue intact), and there is a marked reduction in flight capacity [ 6 , 11 – 13 ]. Previous research has identified venom components in M. hyperodae , with hypothesised links between some of these components and the changes observed in parasitised ASW [ 14 , 15 ]. Recent work has also demonstrated that M. hyperodae carries a novel exogenous dsDNA virus, Microctonus hyperodae filamentous virus (MhFV), which is related to another parasitoid-infecting virus that lowers the rate of egg encapsulation during parasitism [ 16 ].…”

Section: Introductionmentioning

confidence: 99%

Immune system modulation & virus transmission during parasitism identified by multi-species transcriptomics of a declining insect biocontrol system

Inwood,

Harrop,

Shields

et al. 2024

BMC Genomics

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Background The Argentine stem weevil (ASW, Listronotus bonariensis) is a significant pasture pest in Aotearoa New Zealand, primarily controlled by the parasitoid biocontrol agent Microctonus hyperodae. Despite providing effective control of ASW soon after release, M. hyperodae parasitism rates have since declined significantly, with ASW hypothesised to have evolved resistance to its biocontrol agent. While the parasitism arsenal of M. hyperodae has previously been investigated, revealing many venom components and an exogenous novel DNA virus Microctonus hyperodae filamentous virus (MhFV), the effects of said arsenal on gene expression in ASW during parasitism have not been examined. In this study, we performed a multi-species transcriptomic analysis to investigate the biology of ASW parasitism by M. hyperodae, as well as the decline in efficacy of this biocontrol system. Results The transcriptomic response of ASW to parasitism by M. hyperodae involves modulation of the weevil’s innate immune system, flight muscle components, and lipid and glucose metabolism. The multispecies approach also revealed continued expression of venom components in parasitised ASW, as well as the transmission of MhFV to weevils during parasitism and some interrupted parasitism attempts. Transcriptomics did not detect a clear indication of parasitoid avoidance or other mechanisms to explain biocontrol decline. Conclusions This study has expanded our understanding of interactions between M. hyperodae and ASW in a biocontrol system of critical importance to Aotearoa-New Zealand’s agricultural economy. Transmission of MhFV to ASW during successful and interrupted parasitism attempts may link to a premature mortality phenomenon in ASW, hypothesised to be a result of a toxin-antitoxin system. Further research into MhFV and its potential role in ASW premature mortality is required to explore whether manipulation of this viral infection has the potential to increase biocontrol efficacy in future.

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Scaffold-level genome assemblies of two parasitoid biocontrol wasps reveal the parthenogenesis mechanism and an associated novel virus

Inwood

Skelly²,

Harrop

et al. 2023

Preprint

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Background: Biocontrol is a key technology for the control of pest species. Microctonus parasitoid wasps (Hymenoptera: Braconidae) have been released in Aotearoa New Zealand as biocontrol agents, targeting three different pest weevil species. Despite their value as biocontrol agents, no genome assemblies are currently available for these Microctonus wasps, limiting investigations into key biological differences between the different species and strains. Methods and findings: Here we present high-quality genomes for Microctonus hyperodae and Microctonus aethiopoides, assembled with short read sequencing and Hi-C scaffolding. These assemblies have total lengths of 106.7 Mb for M. hyperodae and 129.2 Mb for M. aethiopoides, with scaffold N50 values of 9 Mb and 23 Mb respectively. With these assemblies we investigated differences in reproductive mechanisms, and association with viruses between Microctonus wasps. Meiosis-specific genes are conserved in asexual Microctonus, with in-situ hybridisation validating expression of one of these genes in the ovaries of asexual Microctonus aethiopoides. This implies asexual reproduction in these Microctonus wasps involves meiosis, with the potential for sexual reproduction maintained. Investigation of viral gene content revealed candidate genes that may be involved in virus-like particle production in M. aethiopoides, as well as a novel virus infecting M. hyperodae, for which a complete genome was assembled. Conclusion and significance: These are the first published genomes for Microctonus wasps used for biocontrol in Aotearoa New Zealand, which will be valuable resources for continued investigation and monitoring of these biocontrol systems. Understanding the biology underpinning Microctonus biocontrol is crucial if we are to maintain its efficacy, or in the case of M. hyperodae to understand what may have influenced the significant decline of biocontrol efficacy. The potential for sexual reproduction in asexual Microctonus is significant given that empirical modelling suggests this asexual reproduction is likely to have contributed to biocontrol decline. Furthermore the identification of a novel virus in M. hyperodae highlights a previously unknown aspect of this biocontrol system, which may contribute to premature mortality of the host pest . These findings have potential to be exploited in future in attempt to increase the effectiveness of M. hyperodae biocontrol.

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The venom composition and parthenogenesis mechanism of the parasitoid wasp Microctonus hyperodae, a declining biocontrol agent

Cited by 6 publications

References 117 publications

Discovery of new endogenous viral elements in campoplegine wasps (Ichneumonidae, Campopleginae, Campoplex) suggests a widespread nudivirus domestication event

Discovery of new endogenous viral elements in campoplegine wasps (Ichneumonidae, Campopleginae, Campoplex) suggests a widespread nudivirus domestication event

Immune system modulation & virus transmission during parasitism identified by multi-species transcriptomics of a declining insect biocontrol system

Scaffold-level genome assemblies of two parasitoid biocontrol wasps reveal the parthenogenesis mechanism and an associated novel virus

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