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Evolution and Diversity of Insect Viruses

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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 (31 December 2020) | Viewed by 42617

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Dr. Eugene V. Ryabov

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Bee Research Laboratory, Beltsville Agricultural Research Center, Agricultural Research Service, USDA, Beltsville, MD, USA
Interests: RNA viruses of invertebrates and plants; virus discovery; virus evolution; virus-host interactions; bees
Special Issues, Collections and Topics in MDPI journals

Dr. Robert L. Harrison

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Guest Editor

USDA ARS Beltsville Agricultural Research Center, Beltsville, USA
Interests: insect-specific viruses; baculoviruses; iflaviruses; virus-host interactions
Special Issues, Collections and Topics in MDPI journals

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Dear Colleagues,

The development and deployment of high-throughput sequencing technologies and methods for analyzing data from large-scale sequencing projects have led to an explosion in the discovery of new viruses, both from familiar groups and from entirely novel families. Much of this new virus discovery has taken place in insect hosts. The amount of data from new virus genomes and virome projects has kept insect virologists busy with classification and characterization of new viruses and re-assessment of evolutionary relationships.

The reviews and original research papers in this Special Issue “Evolution and Diversity of Insect Viruses” are intended to summarize and exhibit contemporary research on the diversity and evolution of viruses that infect insects and related arthropods, as well as on the interactions of viruses and their insect hosts.

Dr. Eugene V. Ryabov
Dr. Robert L. Harrison
Guest Editors

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Keywords

viruses
insects
RNA viruses
DNA viruses
virus-host interactions
insect virus vector
antiviral RNAi response
virus evolution
virus diversity
next-generation sequencing
virome
virus taxonomy.

Published Papers (13 papers)

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Editorial

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2 pages, 161 KiB

Open AccessEditorial

Special Issue “Evolution and Diversity of Insect Viruses”

by Eugene V. Ryabov and Robert L. Harrison

Viruses 2022, 14(1), 2; https://0-doi-org.brum.beds.ac.uk/10.3390/v14010002 - 21 Dec 2021

Cited by 1 | Viewed by 1960

Abstract

Insects are crucial for ecosystem functions and services and directly influence human well-being and health [...] Full article

(This article belongs to the Special Issue Evolution and Diversity of Insect Viruses)

Research

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16 pages, 1962 KiB

Open AccessArticle

A New Strain of Virus Discovered in China Specific to the Parasitic Mite Varroa destructor Poses a Potential Threat to Honey Bees

by Gongwen Chen, Shuai Wang, Shuo Jia, Ye Feng, Fuliang Hu, Yanping Chen and Huoqing Zheng

Viruses 2021, 13(4), 679; https://0-doi-org.brum.beds.ac.uk/10.3390/v13040679 - 15 Apr 2021

Cited by 10 | Viewed by 2989

Abstract

The ectoparasitic mite, Varroa destructor, feeds directly on honey bees and serves as a vector for transmitting viruses among them. The Varroa mite causes relatively little damage to its natural host, the Eastern honey bee (Apis cerana) but it is the most devastating pest for the Western honey bee (Apis mellifera). Using Illumina HiSeq sequencing technology, we conducted a metatranscriptome analysis of the microbial community associated with Varroa mites. This study led to the identification of a new Chinese strain of Varroa destructor virus-2 (VDV-2), which is a member of the Iflaviridae family and was previously reported to be specific to Varroa mites. A subsequent epidemiological investigation of Chinese strain of VDV-2 (VDV-2-China) showed that the virus was highly prevalent among Varroa populations and was not identified in any of the adult workers from both A. mellifera and A.cerana colonies distributed in six provinces in China, clearly indicating that VDV-2-China is predominantly a Varroa-adapted virus. While A. mellifera worker pupae exposed to less than two Varroa mites tested negative for VDV-2-China, VDV-2-China was detected in 12.5% of the A. mellifera worker pupae that were parasitized by more than 10 Varroa mites, bringing into play the possibility of a new scenario where VDV-2 could be transmitted to the honey bees during heavy Varroa infestations. Bioassay for the VDV-2-China infectivity showed that A. cerana was not a permissive host for VDV-2-China, yet A. mellifera could be a biological host that supports VDV-2-China’s replication. The different replication dynamics of the virus between the two host species reflect their variation in terms of susceptibility to the virus infection, posing a potential threat to the health of the Western honey bee. The information gained from this study contributes to the knowledge concerning genetic variabilities and evolutionary dynamics of Varroa-borne viruses, thereby enhancing our understanding of underlying molecular mechanisms governing honey bee Varroosis. Full article

(This article belongs to the Special Issue Evolution and Diversity of Insect Viruses)

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14 pages, 1026 KiB

Open AccessArticle

Virus Prospecting in Crickets—Discovery and Strain Divergence of a Novel Iflavirus in Wild and Cultivated Acheta domesticus

by Joachim R. de Miranda, Fredrik Granberg, Piero Onorati, Anna Jansson and Åsa Berggren

Viruses 2021, 13(3), 364; https://0-doi-org.brum.beds.ac.uk/10.3390/v13030364 - 25 Feb 2021

Cited by 15 | Viewed by 3142

Abstract

Orthopteran insects have high reproductive rates leading to boom-bust population dynamics with high local densities that are ideal for short, episodic disease epidemics. Viruses are particularly well suited for such host population dynamics, due to their supreme ability to adapt to changing transmission criteria. However, very little is known about the viruses of Orthopteran insects. Since Orthopterans are increasingly reared commercially, for animal feed and human consumption, there is a risk that viruses naturally associated with these insects can adapt to commercial rearing conditions, and cause disease. We therefore explored the virome of the house cricket Acheta domesticus, which is both part of the natural Swedish landscape and reared commercially for the pet feed market. Only 1% of the faecal RNA and DNA from wild-caught A. domesticus consisted of viruses. These included both known and novel viruses associated with crickets/insects, their bacterial-fungal microbiome, or their plant food. Relatively abundant among these viral Operational Taxonomic Units (OTUs) was a novel Iflavirus, tentatively named Acheta domesticus Iflavirus (AdIV). Quantitative analyses showed that AdIV was also abundant in frass and insect samples from commercially reared crickets. Interestingly, the wild and commercial AdIV strains had short, extremely divergent variation hotspots throughout the genome, which may indicate specific adaptation to their hosts’ distinct rearing environments. Full article

(This article belongs to the Special Issue Evolution and Diversity of Insect Viruses)

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32 pages, 2279 KiB

Open AccessArticle

Metatranscriptome Analysis of Sympatric Bee Species Identifies Bee Virus Variants and a New Virus, Andrena-Associated Bee Virus-1

by Katie F. Daughenbaugh, Idan Kahnonitch, Charles C. Carey, Alexander J. McMenamin, Tanner Wiegand, Tal Erez, Naama Arkin, Brian Ross, Blake Wiedenheft, Asaf Sadeh, Nor Chejanovsky, Yael Mandelik and Michelle L. Flenniken

Viruses 2021, 13(2), 291; https://0-doi-org.brum.beds.ac.uk/10.3390/v13020291 - 12 Feb 2021

Cited by 14 | Viewed by 4628

Abstract

Bees are important plant pollinators in agricultural and natural ecosystems. High average annual losses of honey bee (Apis mellifera) colonies in some parts of the world, and regional population declines of some mining bee species (Andrena spp.), are attributed to multiple factors including habitat loss, lack of quality forage, insecticide exposure, and pathogens, including viruses. While research has primarily focused on viruses in honey bees, many of these viruses have a broad host range. It is therefore important to apply a community level approach in studying the epidemiology of bee viruses. We utilized high-throughput sequencing to evaluate viral diversity and viral sharing in sympatric, co-foraging bees in the context of habitat type. Variants of four common viruses (i.e., black queen cell virus, deformed wing virus, Lake Sinai virus 2, and Lake Sinai virus NE) were identified in honey bee and mining bee samples, and the high degree of nucleotide identity in the virus consensus sequences obtained from both taxa indicates virus sharing. We discovered a unique bipartite + ssRNA Tombo-like virus, Andrena-associated bee virus-1 (AnBV-1). AnBV-1 infects mining bees, honey bees, and primary honey bee pupal cells maintained in culture. AnBV-1 prevalence and abundance was greater in mining bees than in honey bees. Statistical modeling that examined the roles of ecological factors, including floral diversity and abundance, indicated that AnBV-1 infection prevalence in honey bees was greater in habitats with low floral diversity and abundance, and that interspecific virus transmission is strongly modulated by the floral community in the habitat. These results suggest that land management strategies that aim to enhance floral diversity and abundance may reduce AnBV-1 spread between co-foraging bees. Full article

(This article belongs to the Special Issue Evolution and Diversity of Insect Viruses)

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19 pages, 3347 KiB

Open AccessArticle

Nudivirus Sequences Identified from the Southern and Western Corn Rootworms (Coleoptera: Chrysomelidae)

by Sijun Liu, Thomas W. Sappington, Brad S. Coates and Bryony C. Bonning

Viruses 2021, 13(2), 269; https://0-doi-org.brum.beds.ac.uk/10.3390/v13020269 - 09 Feb 2021

Cited by 7 | Viewed by 2273

Abstract

Analysis of pooled genomic short read sequence data revealed the presence of nudivirus-derived sequences from U.S. populations of both southern corn rootworm (SCR, Diabrotica undecimpunctata howardi Barber) and western corn rootworm (WCR, Diabrotica virgifera virgifera LeConte). A near complete nudivirus genome sequence was assembled from sequence data for an SCR population with relatively high viral titers. A total of 147,179 bp was assembled from five contigs that collectively encode 109 putative open reading frames (ORFs) including 20 nudivirus core genes. In contrast, genome sequence recovery was incomplete for a second nudivirus from WCR, although sequences derived from this virus were present in three geographically dispersed populations. Only 48,989 bp were assembled with 48 putative ORFs including 13 core genes, representing about 20% of a typical nudivirus genome. Phylogenetic analysis indicated that both corn rootworm nudiviruses grouped with the third known nudivirus of beetles, Oryctes rhinoceros nudivirus in the genus Alphanudivirus. On the basis of phylogenetic and additional analyses, we propose further taxonomic separation of nudiviruses within Alphanudivirus and Betanudivirus into two subfamilies and five genera. Identification of nudivirus-derived sequences from two species of corn rootworm highlights the diversity of viruses associated with these agricultural insect pests. Full article

(This article belongs to the Special Issue Evolution and Diversity of Insect Viruses)

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31 pages, 14127 KiB

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Soybean Thrips (Thysanoptera: Thripidae) Harbor Highly Diverse Populations of Arthropod, Fungal and Plant Viruses

by Thanuja Thekke-Veetil, Doris Lagos-Kutz, Nancy K. McCoppin, Glen L. Hartman, Hye-Kyoung Ju, Hyoun-Sub Lim and Leslie. L. Domier

Viruses 2020, 12(12), 1376; https://0-doi-org.brum.beds.ac.uk/10.3390/v12121376 - 01 Dec 2020

Cited by 28 | Viewed by 3557

Abstract

Soybean thrips (Neohydatothrips variabilis) are one of the most efficient vectors of soybean vein necrosis virus, which can cause severe necrotic symptoms in sensitive soybean plants. To determine which other viruses are associated with soybean thrips, the metatranscriptome of soybean thrips, collected by the Midwest Suction Trap Network during 2018, was analyzed. Contigs assembled from the data revealed a remarkable diversity of virus-like sequences. Of the 181 virus-like sequences identified, 155 were novel and associated primarily with taxa of arthropod-infecting viruses, but sequences similar to plant and fungus-infecting viruses were also identified. The novel viruses were predicted to have positive-sense RNA, negative-stranded RNA, double-stranded RNA, and single-stranded DNA genomes. The assembled sequences included 100 contigs that represented at least 95% coverage of a virus genome or genome segment. Sequences represented 12 previously described arthropod viruses including eight viruses reported from Hubei Province in China, and 12 plant virus sequences of which six have been previously described. The presence of diverse populations of plant viruses within soybean thrips suggests they feed on and acquire viruses from multiple host plant species that could be transmitted to soybean. Assessment of the virome of soybean thrips provides, for the first time, information on the diversity of viruses present in thrips. Full article

(This article belongs to the Special Issue Evolution and Diversity of Insect Viruses)

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16 pages, 3683 KiB

Open AccessArticle

RNAseq of Deformed Wing Virus and Other Honey Bee-Associated Viruses in Eight Insect Taxa with or without Varroa Infestation

by Laura E. Brettell, Declan C. Schroeder and Stephen J. Martin

Viruses 2020, 12(11), 1229; https://0-doi-org.brum.beds.ac.uk/10.3390/v12111229 - 29 Oct 2020

Cited by 19 | Viewed by 3376

Abstract

The global spread of a parasitic mite (Varroa destructor) has resulted in Deformed wing virus (DWV), a previously rare pathogen, now dominating the viromes in honey bees and contributing to large-scale honey bee colony losses. DWV can be found in diverse insect taxa and has been implicated in spilling over from honey bees into associated (“apiary”) and other (“non-apiary”) insects. Here we generated next generation sequence data from 127 insect samples belonging to diverse taxa collected from Hawaiian islands with and without Varroa to identify whether the mite has indirectly affected the viral landscapes of key insect taxa across bees, wasps, flies and ants. Our data showed that, while Varroa was associated with a dramatic increase in abundance of (predominantly recombinant) DWV in honey bees (and no other honey bee-associated RNA virus), this change was not seen in any other taxa sampled. Honey bees share their environment with other insect populations and exist as a homogenous group, frequently sharing common viruses, albeit at low levels. Our data suggest that the threat of Varroa to increase viral load in an apiary does not automatically translate to an increase in virus load in other insects living in the wider community. Full article

(This article belongs to the Special Issue Evolution and Diversity of Insect Viruses)

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20 pages, 2457 KiB

Open AccessArticle

Metagenomic Approach with the NetoVIR Enrichment Protocol Reveals Virus Diversity within Ethiopian Honey Bees (Apis mellifera simensis)

by Haftom Gebremedhn, Ward Deboutte, Karel Schoonvaere, Peter Demaeght, Lina De Smet, Bezabeh Amssalu, Jelle Matthijnssens and Dirk C. de Graaf

Viruses 2020, 12(11), 1218; https://0-doi-org.brum.beds.ac.uk/10.3390/v12111218 - 27 Oct 2020

Cited by 15 | Viewed by 4056

Abstract

Metagenomics studies have accelerated the discovery of novel or divergent viruses of the honey bee. However, most of these studies predominantly focused on RNA viruses, and many suffer from the relatively low abundance of viral nucleic acids in the samples (i.e., compared to that of the host). Here, we explored the virome of the Ethiopian honey bee, Apis mellifera simensis, using an unbiased metagenomic approach in which the next-generation sequencing step was preceded by an enrichment protocol for viral particles. Our study revealed five well-known bee viruses and 25 atypical virus species, most of which have never been found in A. mellifera before. The viruses belong to Iflaviridae, Dicistroviridae, Secoviridae, Partitiviridae, Parvoviridae, Potyviridae, and taxonomically unclassified families. Fifteen of these atypical viruses were most likely plant-specific, and the remaining ten were presumed to be insect-specific. Apis mellifera filamentous virus (AmFV) was found in one sampling site out of 10. Two samples contained high read counts of a virus similar to Diatraea saccharales densovirus (DsDNV), which is a virus that causes high mortality in the sugarcane borer. AmFV and the DsDNV-like virus were the only DNA viruses found. Three viruses that primarily infect Drosophila spp. were also discovered: La Jolla virus (LJV), Kilifi virus (KiV), and Thika virus. Our study suggests that phoretic varroa mites are involved in the transmission of LJV and KiV and that both viruses replicate in mites and adult bees. We also found an overwhelming dominance of the deformed wing virus type B variant, which fits well with the apparently harmless infestation by Varroa destructor. It was suggested that Ethiopian bees have developed tolerance against virus infections as the result of natural selection. Full article

(This article belongs to the Special Issue Evolution and Diversity of Insect Viruses)

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21 pages, 9515 KiB

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Unmapped RNA Virus Diversity in Termites and Their Symbionts

by Callum Le Lay, Mang Shi, Aleš Buček, Thomas Bourguignon, Nathan Lo and Edward C. Holmes

Viruses 2020, 12(10), 1145; https://0-doi-org.brum.beds.ac.uk/10.3390/v12101145 - 09 Oct 2020

Cited by 22 | Viewed by 4041

Abstract

Despite their ecological importance, nothing is known about the diversity and abundance of RNA viruses in termites (Termitoidae). We used a metatranscriptomics approach to determine the RNA virome structure of 50 diverse species of termite that differ in both phylogenetic position and colony composition. From these samples, we identified 67 novel RNA viruses, characterized their genomes, quantified their abundance and inferred their evolutionary history. These viruses were found within or similar to those from the Togaviridae, Iflaviridae, Polycipiviridae, Flaviviridae, Leviviridae, Narnaviridae, Mitoviridae, Lispivirdae, Phasmaviridae, Picobirnaviridae and Partitiviridae. However, all viruses identified were novel and divergent, exhibiting only 20% to 45% amino acid identity to previously identified viruses. Our analysis suggested that 17 of the viruses identified were termite-infecting, with the remainder likely associated with the termite microbiome or diet. Unclassified sobemo-like and bunya-like viruses dominated termite viromes, while most of the phylogenetic diversity was provided by the picobirna- and mitovirus-like viruses. Of note was the identification of a novel flavi-like virus most closely related to those found in marine vertebrates and invertebrates. Notably, the sampling procedure had the strongest association with virome composition, with greater RNA virome diversity in libraries prepared from whole termite bodies than those that only sampled heads. Full article

(This article belongs to the Special Issue Evolution and Diversity of Insect Viruses)

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13 pages, 1847 KiB

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Genome Analysis of a Novel Clade b Betabaculovirus Isolated from the Legume Pest Matsumuraeses phaseoli (Lepidoptera: Tortricidae)

by Ruihao Shu, Qian Meng, Lin Miao, Hongbin Liang, Jun Chen, Yuan Xu, Luqiang Cheng, Wenyi Jin, Qilian Qin and Huan Zhang

Viruses 2020, 12(10), 1068; https://0-doi-org.brum.beds.ac.uk/10.3390/v12101068 - 23 Sep 2020

Cited by 4 | Viewed by 2074

Abstract

Matsumuraeses phaseoli is a Lepidopteran pest that primarily feeds on numerous species of cultivated legumes, such as Glycine and Phaseolus. It is widely distributed in northeast Asia. A novel granulovirus, designated as Matsumuraeses phaseoli granulovirus (MaphGV), was isolated from pathogenic M. phaseoli larvae that dwell in rolled leaves of Astragalus membranaceus, a Chinese medicinal herb. In this study, using next-generation sequencing, we report the complete genome of MaphGV. MaphGV genome comprises a double-stranded DNA of 116,875 bp, with 37.18% GC content. It has 128 hypothetical open reading frames (ORFs). Among them, 38 are baculovirus core genes, 18 are lepidopteran baculovirus conserved genes, and 5 are unique to Baculoviridae. MaphGV has one baculovirus repeat ORF (bro) and three inhibitors of apoptosis proteins (iap), including a newfound iap-6. We found two atypical baculoviral homologous regions (hrs) and four direct repeats (drs) in the MaphGV genome. Based on phylogenetic analysis, MaphGV belongs to Clade b of Betabaculovirus and is closely related to Cydia pomonellagranulovirus (CpGV) and Cryptophlebia leucotretagranulovirus (CrleGV). This novel baculovirus discovery and sequencing are invaluable in understanding the evolution of baculovirus and MaphGV may be a potential biocontrol agent against the bean ravaging pest. Full article

(This article belongs to the Special Issue Evolution and Diversity of Insect Viruses)

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11 pages, 2007 KiB

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Depicting the RNA Virome of Hematophagous Arthropods from Belgrade, Serbia

by Maja Stanojević, Kun Li, Gorana Stamenković, Bojan Ilić, Milan Paunović, Branislav Pešić, Ivana Đurić Maslovara, Marina Šiljić, Valentina Ćirković and Yongzhen Zhang

Viruses 2020, 12(9), 975; https://0-doi-org.brum.beds.ac.uk/10.3390/v12090975 - 02 Sep 2020

Cited by 17 | Viewed by 3540

Abstract

Hematophagous arthropods are important vectors for zoonotic pathogens. To date, a huge number of viruses have been identified in these arthropods, with a considerable proportion of them being human pathogens. However, the viromes of hematophagous arthropods are still largely unresearched. In this study, a number of arthropods were collected from Belgrade, Serbia including mosquitoes, ticks and bedbugs. The viromes of these arthropods were identified and characterized using Illumina MiSeq sequencing. In total, 21 viruses belonging to 11 families were characterized, with 11 of them representing novel species. These results may contribute to our knowledge of RNA viruses in arthropods and the discovery of novel human pathogens. Full article

(This article belongs to the Special Issue Evolution and Diversity of Insect Viruses)

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12 pages, 1487 KiB

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Aedes aegypti from Amazon Basin Harbor High Diversity of Novel Viral Species

by Geovani de Oliveira Ribeiro, Vanessa S. Morais, Fred Julio Costa Monteiro, Edcelha Soares D’Athaide Ribeiro, Marlisson Octavio da S Rego, Raimundo Nonato Picanço Souto, Fabiola Villanova, Roozbeh Tahmasebi, Philip Michael Hefford, Xutao Deng, Eric Delwart, Ester Cerdeira Sabino, Licia Natal Fernandes, Antonio Charlys da Costa and Élcio Leal

Viruses 2020, 12(8), 866; https://0-doi-org.brum.beds.ac.uk/10.3390/v12080866 - 08 Aug 2020

Cited by 10 | Viewed by 2989

Abstract

Viruses are the most diverse and abundant microorganisms on earth, highly adaptive to a wide range of hosts. Viral diversity within invertebrate hosts has gained notoriety in recent years in public health as several such viruses have been of medical importance. Aedes aegypti serves as a vector for several viruses that have caused epidemics within the last year throughout Brazil; including Dengue, Zika and Chikungunya. This study aimed to identify new viral agents within Aedes aegypti mosquito in a city of the Amazonian region, where it is highly endemic. Metagenomic investigation was performed on 60 mosquito pools and viral RNA sequences present in their microbiota were characterized using genomic and phylogenetic tools. In total, we identified five putative novel virus species related to the Sobemovirus genus, Iflavirus genus and Permutatetraviridae family. These findings indicate a diverse taxonomy of viruses present in the mosquito microbiota of the Amazon, the region with the greatest invertebrate diversity in the world. Full article

(This article belongs to the Special Issue Evolution and Diversity of Insect Viruses)

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16 pages, 1180 KiB

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Discovery of Two Novel Negeviruses in a Dungfly Collected from the Arctic

by Gang Lu, Zhuang-Xin Ye, Yu-Juan He, Yan Zhang, Xin Wang, Hai-Jian Huang, Ji-Chong Zhuo, Zong-Tao Sun, Fei Yan, Jian-Ping Chen, Chuan-Xi Zhang and Jun-Min Li

Viruses 2020, 12(7), 692; https://0-doi-org.brum.beds.ac.uk/10.3390/v12070692 - 27 Jun 2020

Cited by 16 | Viewed by 2888

Abstract

Negeviruses are a proposed group of insect-specific viruses that can be separated into two distinct phylogenetic clades, Nelorpivirus and Sandewavirus. Negeviruses are well-known for their wide geographic distribution and broad host range among hematophagous insects. In this study, the full genomes of two novel negeviruses from each of these clades were identified by RNA extraction and sequencing from a single dungfly (Scathophaga furcata) collected from the Arctic Yellow River Station, where these genomes are the first negeviruses from cold zone regions to be discovered. Nelorpivirus dungfly1 (NVD1) and Sandewavirus dungfly1 (SVD1) have the typical negevirus genome organization and there was a very high coverage of viral transcripts. Small interfering RNAs derived from both viruses were readily detected in S. furcata, clearly showing that negeviruses are targeted by the host antiviral RNA interference (RNAi) pathway. These results and subsequent in silico analysis (studies) of public database and published virome data showed that the hosts of nege-like viruses include insects belonging to many orders as well as various non-insects in addition to the hematophagous insects previously reported. Phylogenetic analysis reveals at least three further groups of negeviruses, as well as several poorly resolved solitary branches, filling in the gaps within the two sub-groups of negeviruses and plant-associated viruses in the Kitaviridae. The results of this study will contribute to a better understanding of the geographic distribution, host range, evolution and host antiviral immune responses of negeviruses. Full article

(This article belongs to the Special Issue Evolution and Diversity of Insect Viruses)

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