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Viruses in Mass-Reared Invertebrates

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A special issue of Viruses (ISSN 1999-4915). This special issue belongs to the section "Insect Viruses".

Deadline for manuscript submissions: closed (30 June 2022) | Viewed by 34693

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Prof. Dr. Adly Abd-Alla

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Insect Pest Control Laboratory, Joint FAO/IAEA Division of Nuclear Techniques in Food & Agriculture, P.O. Box 100, Wagrammer Straße 5, A-1400 Vienna, Austria
Interests: virology; insect viruses; virus-host interaction; molecular virology; viral taxonomy; virus management; virus dynamics; virus detection
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Prof. Dr. Drion G. Boucias

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Entomology and Nematology Department, University of Florida, Gainesville, FL 32611, USA
Interests: insect pathology; insect disease interactions; microbial metabolites; epizootiology; microbial control; structure-function relationships; symbiont/pathogen interactions
Special Issues, Collections and Topics in MDPI journals

Dr. Vera I. D. Ros

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Laboratory of Virology, Wageningen University, Droevendaalsesteeg 1, 6708 PB, Wageningen, The Netherlands
Interests: virology; insect viruses; virus-host interactions; parasitic manipulation; behavioural manipulation; biological control; insect mass rearing; covert virus; virus latency

Special Issue Information

Dear colleagues,

Insects can be exposed to many viruses that can either infect insects (insect viruses or entomopathogenic viruses) or be transmitted to vertebrates (arboviruses) or plants (plant viruses). Entomopathogenic viruses can cause diseases in insects of natural populations as well as reared insects. So far, insect viruses have mainly been studied for their potential in biological control, i.e., for the control insect pest populations. However, recently, with the emerging interest in mass-rear insects – for human food or animal feed, waste management, biological control, pollination, or production of, e.g., silk and honey – there is an increasing need to detect, manage, and control entomopathogenic viruses in those mass-reared insects. In addition, viruses infect other invertebrates that are economically important for human food, i.e., shrimps and oysters or those that are important as fish baits or pet feed, i.e., earthworm, and have caused economic loses and therefore need be managed and controlled. To this end, studies on the development of early detection tools to identify virus infections in insect colonies as well as the development of sanitation methods (e.g., starting with virus-free insects) is urgently required. In addition, selection of virus-resistant insect strains with high tolerance to virus infection is recommended. Furthermore, analysis of the rearing procedure and selecting the best practice to avoid virus infections and maintain stress-free rearing conditions to rear healthy insects without compromising the insect’s immune system represents another promising strategy. Understanding the molecular dialogue between pathogenic viruses and their hosts and the associated microbiota that might affect the virus infection and host response is important for selecting the best conditions to maintain an equilibrium state toward avoiding disease outbreaks in reared insects.

Based on the above, we invite researchers to contribute original articles as well as reviews that will stimulate our continuing efforts to understand entomopathogenic virus infections in insect mass-rearing and to improve our knowledge of the molecular dialogues between viruses, their hosts, and the associated microbes; sensitive virus detection; and targeted treatments using a holistic approach in order to improve insect mass-rearing for various objectives.

Prof. Dr. Adly Abd-Alla
Prof. Dr. Drion G. Boucias
Dr. Vera I. D. Ros
Guest Editors

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Keywords

insect viruses
virus-host interactions
molecular virology
viral taxonomy
virus management
virus dynamics
virus detection
virus-host-symbiont interactions

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Viruses in Mass-Reared Invertebrates 2nd Edition in Viruses

Published Papers (11 papers)

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12 pages, 1721 KiB

Open AccessArticle

Identification of a Novel Solinvivirus with Nuclear Localization Associated with Mass Mortalities in Cultured Whiteleg Shrimp (Penaeus vannamei)

by Roberto Cruz-Flores, Thales P.D. Andrade, Hung N. Mai, Rod Russel R. Alenton and Arun K. Dhar

Viruses 2022, 14(10), 2220; https://doi.org/10.3390/v14102220 - 09 Oct 2022

Cited by 4 | Viewed by 1856

Abstract

The emergence and spread of disease-causing viruses in shrimp aquaculture is not uncommon. Since 2016, unusual mortalities have been affecting the Brazilian shrimp industry and we have associated these unusual mortalities with a novel variant of infectious myonecrosis virus (IMNV). The transcriptome analysis of these diseased shrimp showed an additional divergent viral sequence that we have assigned to the family Solinviviridae. The novel virus has been tentatively termed Penaeus vannamei solinvivirus (PvSV) (GenBank accession: OP265432). The full-length genome of the PvSV is 10.44 kb (excluding the poly A tail) and codes for a polyprotein of 3326 aa. Five conserved domains coding for a helicase, RdRp, calicivirus coat protein, G-patch and tegument protein were identified. The genome organization of the PvSV is similar to other (Nylan deria fulva virus 1) solinvivirus. A unique feature of this virus that differs from other members of the Solinviviridae is the presence of putative nuclear localization signals. The tissue tropism of this virus is wide, infecting cells of the hepatopancreas, gastrointestinal tract, lymphoid organ and muscle tissue. Another unique feature is that it is the only RNA virus of penaeid shrimp that shows a nuclear localization by in situ hybridization. The PvSV has a wide distribution in Brazil and has been found in the states of Maranhão State (Perizes de Baixo), Piaui State (Mexeriqueira), Ceará State (Camocim, Jaguaruana, Aracati and Alto Santo) and Pará State where it has been detected in coinfections with IMNV. The diagnostic methods developed here (real-time RT-PCR and in situ hybridization) are effective for the detection of the pathogen and should be employed to limit its spread. Furthermore, the identification of the PvSV shows the increasing host range of the relatively new family Solinviviridae. Full article

(This article belongs to the Special Issue Viruses in Mass-Reared Invertebrates)

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14 pages, 1630 KiB

Open AccessArticle

Applying Modified VP53A Recombinant Protein as an Anti-White Spot Syndrome Virus Biological Agent in Litopenaeus vannamei Farming

by Jeff Chia-Kai Hsu, Huai-Ting Huang, Han-Jia Lin, Hsin-Yiu Chou, Po-Yu Huang, Anuphap Prachumwat and Li-Li Chen

Viruses 2022, 14(7), 1353; https://doi.org/10.3390/v14071353 - 21 Jun 2022

Cited by 1 | Viewed by 1681

Abstract

Shrimp farming is an important economic activity. However, due to the spread of pathogens, shrimp aquaculture is becoming increasingly difficult. Many studies have confirmed that white spot syndrome virus (WSSV) recombinant proteins can inhibit viral infection. Among them, VP53 recombinant protein has been found to reduce mortality upon WSSV challenge. This study was conducted in Kaohsiung, Taiwan and reports the first field feeding trial to demonstrate that WSSV recombinant proteins can improve shrimp survival rates at a farming scale. Prior to the feeding trial, the shrimp were confirmed to be slightly infected with WSSV, Vibrio parahaemolyticus strains causing acute hepatopancreatic necrosis disease (AHPND), non-AHPND V. parahaemolyticus strains, and Enterocytozoon hepatopenaei (EHP), which are common pathogens that shrimp farmers often face. The shrimp were then divided into two groups: a control group (C group) fed with a commercial diet and a protein group (P group) fed with the same commercial feed with VP53 recombinant protein. Our findings indicated that the survival rate and expression of immune genes of the P group were higher than those of the C group. The intestinal microbiota of the two groups were also analysed. Collectively, our results confirmed that the recombinant WSSV envelope protein derivative can be used as an effective anti-virus biological agent in shrimp farms. Full article

(This article belongs to the Special Issue Viruses in Mass-Reared Invertebrates)

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14 pages, 1784 KiB

Open AccessArticle

First Evidence of Past and Present Interactions between Viruses and the Black Soldier Fly, Hermetia illucens

by Robert D. Pienaar, Clément Gilbert, Carole Belliardo, Salvador Herrero and Elisabeth A. Herniou

Viruses 2022, 14(6), 1274; https://doi.org/10.3390/v14061274 - 11 Jun 2022

Cited by 5 | Viewed by 2604

Abstract

Black soldier flies (BSFs, Hermetia illucens) are becoming a prominent research model encouraged by the insect as food and feed and waste bioconversion industries. Insect mass-rearing facilities are at risk from the spread of viruses, but so far, none have been described in BSFs. To fill this knowledge gap, a bioinformatic approach was undertaken to discover viruses specifically associated with BSFs. First, BSF genomes were screened for the presence of endogenous viral elements (EVEs). This led to the discovery and mapping of seven orthologous EVEs integrated into three BSF genomes originating from five viral families. Secondly, a virus discovery pipeline was used to screen BSF transcriptomes. This led to detecting a new exogenous totivirus that we named hermetia illucens totivirus 1 (HiTV1). Phylogenetic analyses showed this virus belongs to a clade of insect-specific totiviruses and is closely related to the largest EVE located on chromosome 1 of the BSF genome. Lastly, this EVE was found to express a small transcript in some BSFs infected by HiTV1. Altogether, this data mining study showed that far from being unscathed from viruses, BSFs bear traces of past interactions with several viral families and of present interactions with the exogenous HiTV1. Full article

(This article belongs to the Special Issue Viruses in Mass-Reared Invertebrates)

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11 pages, 2546 KiB

Open AccessArticle

CRISPR/Cas9-Mediated Disruption of the lef8 and lef9 to Inhibit Nucleopolyhedrovirus Replication in Silkworms

by Yujia Liu, Xiaoqian Zhang, Dongbin Chen, Dehong Yang, Chenxu Zhu, Linmeng Tang, Xu Yang, Yaohui Wang, Xingyu Luo, Manli Wang, Yongping Huang, Zhihong Hu and Zulian Liu

Viruses 2022, 14(6), 1119; https://doi.org/10.3390/v14061119 - 24 May 2022

Cited by 3 | Viewed by 1880

Abstract

Bombyx mori nucleopolyhedrovirus (BmNPV) is a pathogen that causes severe disease in silkworms. In a previous study, we demonstrated that by using the CRISPR/Cas9 system to disrupt the BmNPV ie-1 and me53 genes, transgenic silkworms showed resistance to BmNPV infection. Here, we used the same strategy to simultaneously target lef8 and lef9, which are essential for BmNPV replication. A PCR assay confirmed that double-stranded breaks were induced in viral DNA at targeted sequences in BmNPV-infected transgenic silkworms that expressed small guide RNAs (sgRNAs) and Cas9. Bioassays and qPCR showed that replication of BmNPV and mortality were significantly reduced in the transgenic silkworms in comparison with the control groups. Microscopy showed degradation of midgut cells in the BmNPV-infected wild type silkworms, but not in the transgenic silkworms. These results demonstrated that transgenic silkworms using the CRISPR/Cas9 system to disrupt BmNPV lef8 and lef9 genes could successfully prevent BmNPV infection. Our research not only provides more alternative targets for the CRISPR antiviral system, but also aims to provide new ideas for the application of virus infection research and the control of insect pests. Full article

(This article belongs to the Special Issue Viruses in Mass-Reared Invertebrates)

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14 pages, 1780 KiB

Open AccessArticle

Expanding the Medfly Virome: Viral Diversity, Prevalence, and sRNA Profiling in Mass-Reared and Field-Derived Medflies

by Luis Hernández-Pelegrín, Ángel Llopis-Giménez, Cristina Maria Crava, Félix Ortego, Pedro Hernández-Crespo, Vera I. D. Ros and Salvador Herrero

Viruses 2022, 14(3), 623; https://doi.org/10.3390/v14030623 - 17 Mar 2022

Cited by 7 | Viewed by 3879

Abstract

The Mediterranean fruit fly (medfly), Ceratitis capitata, is an agricultural pest of a wide range of fruits. The advent of high-throughput sequencing has boosted the discovery of RNA viruses infecting insects. In this article, we aim to characterize the RNA virome and viral sRNA profile of medfly. By means of transcriptome mining, we expanded the medfly RNA virome to 13 viruses, including two novel positive ssRNA viruses and the first two novel dsRNA viruses reported for medfly. Our analysis across multiple laboratory-reared and field-collected medfly samples showed the presence of a core RNA virome comprised of Ceratitis capitata iflavirus 2 and Ceratitis capitata negev-like virus 1. Furthermore, field-collected flies showed a higher viral diversity in comparison to the laboratory-reared flies. Based on the small RNA sequencing, we detected small interfering RNAs mapping to all the viruses present in each sample, except for Ceratitis capitata nora virus. Although the identified RNA viruses do not cause obvious symptoms in medflies, the outcome of their interaction may still influence the medfly’s fitness and ecology, becoming either a risk or an opportunity for mass-rearing and SIT applications. Full article

(This article belongs to the Special Issue Viruses in Mass-Reared Invertebrates)

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14 pages, 1927 KiB

Open AccessArticle

Construction of Baculovirus-Inducible CRISPR/Cas9 Antiviral System Targeting BmNPV in Bombyx mori

by Yujia Liu, Dongbin Chen, Xiaoqian Zhang, Shuqing Chen, Dehong Yang, Linmeng Tang, Xu Yang, Yaohui Wang, Xingyu Luo, Manli Wang, Zhihong Hu and Yongping Huang

Viruses 2022, 14(1), 59; https://doi.org/10.3390/v14010059 - 30 Dec 2021

Cited by 3 | Viewed by 2379

Abstract

The silkworm Bombyx mori is an economically important insect. The sericulture industry is seriously affected by pathogen infections. Of these pathogens, Bombyx mori nucleopolyhedrovirus (BmNPV) causes approximately 80% of the total economic losses due to pathogen infections. We previously constructed a BmNPV-specific CRISPR/Cas9 silkworm line with significantly enhanced resistance to BmNPV. In order to optimize the resistance properties and minimize its impact on economic traits, we constructed an inducible CRISPR/Cas9 system for use in transgenic silkworms. We used the 39k promoter, which is induced by viral infection, to express Cas9 and the U6 promoter to express four small guide RNA targeting the genes encoding BmNPV late expression factors 1 and 3 (lef-1 and lef-3, respectively), which are essential for viral DNA replication. The system was rapidly activated when the silkworm was infected and showed considerably higher resistance to BmNPV infection than the wild-type silkworm. The inducible system significantly reduced the development effects due to the constitutive expression of Cas9. No obvious differences in developmental processes or economically important characteristics were observed between the resulting transgenic silkworms and wild-type silkworms. Adoption of this accurate and highly efficient inducible CRISPR/Cas9 system targeting BmNPV DNA replication will result in enhanced antivirus measures during sericulture, and our work also provides insights into the broader application of the CRISPR/Cas9 system in the control of infectious diseases and insect pests. Full article

(This article belongs to the Special Issue Viruses in Mass-Reared Invertebrates)

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18 pages, 10125 KiB

Open AccessEditor’s ChoiceArticle

Characterization and Tissue Tropism of Newly Identified Iflavirus and Negeviruses in Glossina morsitans morsitans Tsetse Flies

by Irene K. Meki, Hannah-Isadora Huditz, Anton Strunov, René A. A. van der Vlugt, Henry M. Kariithi, Mohammadreza Rezapanah, Wolfgang J. Miller, Just M. Vlak, Monique M. van Oers and Adly M. M. Abd-Alla

Viruses 2021, 13(12), 2472; https://doi.org/10.3390/v13122472 - 10 Dec 2021

Cited by 5 | Viewed by 4432

Abstract

Tsetse flies cause major health and economic problems as they transmit trypanosomes causing sleeping sickness in humans (Human African Trypanosomosis, HAT) and nagana in animals (African Animal Trypanosomosis, AAT). A solution to control the spread of these flies and their associated diseases is the implementation of the Sterile Insect Technique (SIT). For successful application of SIT, it is important to establish and maintain healthy insect colonies and produce flies with competitive fitness. However, mass production of tsetse is threatened by covert virus infections, such as the Glossina pallidipes salivary gland hypertrophy virus (GpSGHV). This virus infection can switch from a covert asymptomatic to an overt symptomatic state and cause the collapse of an entire fly colony. Although the effects of GpSGHV infections can be mitigated, the presence of other covert viruses threaten tsetse mass production. Here we demonstrated the presence of two single-stranded RNA viruses isolated from Glossina morsitans morsitans originating from a colony at the Seibersdorf rearing facility. The genome organization and the phylogenetic analysis based on the RNA-dependent RNA polymerase (RdRp) revealed that the two viruses belong to the genera Iflavirus and Negevirus, respectively. The names proposed for the two viruses are Glossina morsitans morsitans iflavirus (GmmIV) and Glossina morsitans morsitans negevirus (GmmNegeV). The GmmIV genome is 9685 nucleotides long with a poly(A) tail and encodes a single polyprotein processed into structural and non-structural viral proteins. The GmmNegeV genome consists of 8140 nucleotides and contains two major overlapping open reading frames (ORF1 and ORF2). ORF1 encodes the largest protein which includes a methyltransferase domain, a ribosomal RNA methyltransferase domain, a helicase domain and a RdRp domain. In this study, a selective RT-qPCR assay to detect the presence of the negative RNA strand for both GmmIV and GmmNegeV viruses proved that both viruses replicate in G. m. morsitans. We analyzed the tissue tropism of these viruses in G. m. morsitans by RNA-FISH to decipher their mode of transmission. Our results demonstrate that both viruses can be found not only in the host’s brain and fat bodies but also in their reproductive organs, and in milk and salivary glands. These findings suggest a potential horizontal viral transmission during feeding and/or a vertically viral transmission from parent to offspring. Although the impact of GmmIV and GmmNegeV in tsetse rearing facilities is still unknown, none of the currently infected tsetse species show any signs of disease from these viruses. Full article

(This article belongs to the Special Issue Viruses in Mass-Reared Invertebrates)

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11 pages, 966 KiB

Open AccessArticle

Ten Years of Deformed Wing Virus (DWV) in Hawaiian Honey Bees (Apis mellifera), the Dominant DWV-A Variant Is Potentially Being Replaced by Variants with a DWV-B Coding Sequence

by Isobel Grindrod, Jessica L. Kevill, Ethel M. Villalobos, Declan C. Schroeder and Stephen John Martin

Viruses 2021, 13(6), 969; https://doi.org/10.3390/v13060969 - 24 May 2021

Cited by 13 | Viewed by 4253

Abstract

The combination of Deformed wing virus (DWV) and Varroa destructor is arguably one of the greatest threats currently facing western honey bees, Apis mellifera. Varroa’s association with DWV has decreased viral diversity and increased loads of DWV within honey bee populations. Nowhere has this been better studied than in Hawaii, where the arrival of Varroa progressively led to the dominance of the single master variant (DWV-A) on both mite-infested Hawaiian Islands of Oahu and Big Island. Now, exactly 10 years following the original study, we find that the DWV population has changed once again, with variants containing the RdRp coding sequence pertaining to the master variant B beginning to co-dominate alongside variants with the DWV-A RdRp sequence on the mite-infested islands of Oahu and Big Island. In speculation, based on other studies, it appears this could represent a stage in the journey towards the complete dominance of DWV-B, a variant that appears better adapted to be transmitted within honey bee colonies. Full article

(This article belongs to the Special Issue Viruses in Mass-Reared Invertebrates)

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13 pages, 1818 KiB

Open AccessArticle

Reduction in Virulence over Time in Ostreid herpesvirus 1 (OsHV-1) Microvariants between 2011 and 2015 in Australia

by Georgia Cain, Olivia Liu, Richard J. Whittington and Paul M. Hick

Viruses 2021, 13(5), 946; https://doi.org/10.3390/v13050946 - 20 May 2021

Cited by 1 | Viewed by 2440

Abstract

Microvariant genotypes of Ostreid herpesvirus 1 (OsHV-1) are associated with mass mortality events of Pacific oysters in many countries. The OsHV-1 microvariant (µVar) emerged in France 2008 and caused significant economic losses as it became endemic and displaced the previously dominant OsHV-1 reference genotype. Recently, considerable genotypic variation has been described for OsHV-1 microvariants, however, less is known about variation in viral phenotype. This study used an in vivo laboratory infection model to assess differences in total cumulative mortality, peak viral load, transmissibility, and dose-response for three OsHV-1 isolates obtained between 2011 and 2015 from endemic waterways in Australia. This followed field observations of apparent reductions in the severity of mass mortalities over this time. Significantly higher hazard of death and cumulative mortality were observed for an isolate obtained in 2011 compared to isolates from 2014–2015. In keeping with other studies, the hazard of death was higher in oysters challenged by injection compared to challenge by cohabitation and the mortality was higher when the initial dose was 1 × 10⁴ OsHV-1 DNA copies per oyster injection compared to 1 × 10² DNA copies. There was no difference in the quantity of OsHV-1 DNA at time of death that could be related to isolate or dose, suggesting similar pathogenetic processes in the individual oysters that succumbed to end-stage disease. While the isolates examined in this study were biased towards pathogenic types of OsHV-1, as they were collected during disease outbreaks, the variation in virulence that was observed, when combined with prior data on subclinical infections, suggests that surveillance for low virulence genotypes of OsHV-1 would be rewarding. This may lead to new approaches to disease management which utilize controlled exposure to attenuated strains of OsHV-1. Full article

(This article belongs to the Special Issue Viruses in Mass-Reared Invertebrates)

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17 pages, 3449 KiB

Open AccessArticle

Patterns in Genotype Composition of Indian Isolates of the Bombyx mori Nucleopolyhedrovirus and Bombyx mori Bidensovirus

by Mudasir Gani, Sergei Senger, Satish Lokanath, Pawan Saini, Kamlesh Bali, Rakesh Gupta, Vankadara Sivaprasad, Johannes A. Jehle and Jörg T. Wennmann

Viruses 2021, 13(5), 901; https://doi.org/10.3390/v13050901 - 13 May 2021

Cited by 6 | Viewed by 2435

Abstract

The mulberry silkworm, Bombyx mori (L.), is a model organism of lepidopteran insects with high economic importance. The viral diseases of the silkworm caused by Bombyx mori nucleopolyhedrovirus (BmNPV) and Bombyx mori bidensovirus (BmBDV) inflict huge economic losses and significantly impact the sericulture industry of India and other countries. To understand the distribution of Indian isolates of the BmNPV and to investigate their genetic composition, an in-depth population structure analysis was conducted using comprehensive and newly developed genomic analysis methods. The seven new Indian BmNPV isolates from Anantapur, Dehradun, Ghumarwin, Jammu, Kashmir, Mysore and Salem grouped in the BmNPV clade, and are most closely related to Autographa californica multiple nucleopolyhedrovirus and Rachiplusia ou multiple nucleopolyhedrovirus on the basis of gene sequencing and phylogenetic analyses of the partial polh, lef-8 and lef-9 gene fragments. The whole genome sequencing of three Indian BmNPV isolates from Mysore (-My), Jammu (-Ja) and Dehradun (-De) was conducted, and intra-isolate genetic variability was analyzed on the basis of variable SNP positions and the frequencies of alternative nucleotides. The results revealed that the BmNPV-De and BmNPV-Ja isolates are highly similar in their genotypic composition, whereas the population structure of BmNPV-My appeared rather pure and homogenous, with almost no or few genetic variations. The BmNPV-De and BmNPV-Ja samples further contained a significant amount of BmBDV belonging to the Bidnaviridae family. We elucidated the genotype composition within Indian BmNPV and BmBDV isolates, and the results presented have broad implications for our understanding of the genetic diversity and evolution of BmNPV and co-occurring BmBDV isolates. Full article

(This article belongs to the Special Issue Viruses in Mass-Reared Invertebrates)

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31 pages, 722 KiB

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A Systematic Review on Viruses in Mass-Reared Edible Insect Species

by Michela Bertola and Franco Mutinelli

Viruses 2021, 13(11), 2280; https://doi.org/10.3390/v13112280 - 15 Nov 2021

Cited by 24 | Viewed by 5285

Abstract

Edible insects are expected to become an important nutrient source for animals and humans in the Western world in the near future. Only a few studies on viruses in edible insects with potential for industrial rearing have been published and concern only some edible insect species. Viral pathogens that can infect insects could be non-pathogenic, or pathogenic to the insects themselves, or to humans and animals. The objective of this systematic review is to provide an overview of the viruses detected in edible insects currently considered for use in food and/or feed in the European Union or appropriate for mass rearing, and to collect information on clinical symptoms in insects and on the vector role of insects themselves. Many different virus species have been detected in edible insect species showing promise for mass production systems. These viruses could be a risk for mass insect rearing systems causing acute high mortality, a drastic decline in growth in juvenile stages and in the reproductive performance of adults. Furthermore, some viruses could pose a risk to human and animal health where insects are used for food and feed. Full article

(This article belongs to the Special Issue Viruses in Mass-Reared Invertebrates)

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