The World of Rhabdoviruses

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

Deadline for manuscript submissions: 20 February 2025 | Viewed by 10736

Special Issue Editors


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Guest Editor
Institut Pasteur, National Reference Centre for Rabies, WHO Collaborating Center for Reference and Research on Rabies, Lyssavirus Epidemiology and Neuropathology Unit, 75724 Paris, France
Interests: rabies; lyssavirus; rhabdovirus; animal reservoir; bat; epidemiology; virus diffusion; host-virus interaction; surveillance; public health; one health; control programs; zoonosis
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Guest Editor
ANSES (French Agency for Food, Environmental and Occupational Health and Safety), Maisons-Alfort, France
Interests: fish virus genetic diversity

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Guest Editor
Embrapa Cassava and Fruits and Biological Institute, Av. Conselheiro Rodrigues Alves, 1252, CEP 04014-002, São Paulo, SP, Brazil
Interests: Brevipalpus-transmitted viruses; dichorhavirus; rhabdovirus; cilevirus; kitavirus, mites; host–virus-vector interactions

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Guest Editor
London School of Hygiene & Tropical Medicine, London, UK
Interests: virus genetic diversity; virus reservoir; reverse genetics; virus detection; virus replication

Special Issue Information

Dear Colleagues,

The world of rhabdoviruses remains one the most large and diverse within the virosphere, with 45 genera and 275 species identified thus far. However, this viral universe is still in expansion, with many new rhabdoviruses awaiting official classification. Despite few exceptions, viruses belonging to the family Rhabdoviridae share some common characteristics, such as: a negative-sense, single-stranded RNA genome with at least five canonical genes (nucleoprotein or N, phosphoprotein or P, matrix or M, glycoprotein or G and RNA-dependent RNA polymerase or L); a bullet-shaped or bacilliform morphology; and a lipid envelope derived from the cytoplasmic membrane of the host cell.

Apart from these common features, rhabdovirus members occupy many ecological environments, and they are associated with a broad geographic distribution. Indeed, at least 10% of these viruses are isolated from plants, and over half of them are able to infect diverse vertebrates, including reptiles, fish, birds, and various mammals. Additionally, a significant number of rhabdoviruses have been identified in arthropods, playing an important role in terms of virus dynamics and transmission.

Within each of these ecological niches, there are some important members of the virus whose infections can induce major impacts on these ecosystems. As an example, more than 20 rhabdoviruses can infect humans, some causing severe diseases such as the well-known rabies, which is due to lyssavirus infection and is responsible for nearly 59,000 deaths worldwide each year. Other rhabdoviruses can also have important consequences for cattle and breeding, such as different members of the genera Vesiculovirus and Ephemerovirus, which can lead to high costs in terms of production losses. Fish and other aquatic animals can also be affected by rhabdovirus infection by at least three virus genera (Novirhabdovirus, Perhabdovirus and Siniperhavirus), leading to significant economic losses for fishing industries. Plants and crops can also be heavily impacted by specific and well-adapted rhabdoviruses. On top of these situations, numerous rhabdoviruses are considered as arboviruses, with insects and other arthropods playing active roles in virus dynamics and their dissemination to other animals or plants, or in arthropods themselves, leading to potential virus emergence.

Apart from these taxonomic, ecological or epidemiological considerations, rhabdoviruses also represent relevant models to study various aspects of the field of viral ‘molecular life’, from a structural analysis of the viral proteins to understanding the mechanisms of replication or cell/host interplay. In addition, rhabdoviruses have been widely used as biological tools in research and even in medicine (vesiculovirus-based pseudotypes, neural tracking using rabies virus systems or proteins, etc.).

Thus, the world of rhabdoviruses represents an amazing and expanding field of research and investigation, with multiple effects on the fields of virology, biology, plants, animal or human health, therapeutic/medicine and zoonotic emergence.

In this context, the aim of this Special Issue is to provide a comprehensive overview of the biology, ecology and evolution of rhabdoviruses, as well as to contribute to filling the gaps of knowledge in this field. The Special Issue would like to include articles from leading experts in the field that cover various aspects of rhabdovirus research, including virus–host interactions, viral pathogenesis, the development of novel therapeutics and vaccines, as well as the importance of rhabdoviruses in emerging infectious diseases and strategies for virus control. Overall, "The World of Rhabdoviruses" provides a valuable resource for researchers and clinicians interested in this important group of viruses and highlights the need for interdisciplinary approaches to studying this highly diverse group of infectious agents.

This Special Issue encourages the submission of articles covering the following research areas, but topics are not limited to these:

  • Rhabdovirus detection and characterization;
  • Rhabdovirus diversity and evolution;
  • Interactions between rhabdovirus and host cell;
  • Determination of rhabdovirus epidemiology, ecology and mechanisms of dissemination in natural reservoirs or secondary hosts;
  • Development and evaluation of antiviral drugs and vaccines dedicated to rhabdoviruses;
  • Rhabdoviruses as biological tools;
  • Rhabdovirus infections’ impact in a changing world (in the context of One Health and Planetary Health concepts);
  • Surveillance and control programs of rhabdoviruses.

Dr. Laurent Dacheux
Dr. Laurent Bigarré
Dr. Juliana Freitas-Astua
Dr. Dongsheng Luo
Guest Editors

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Keywords

  • rhabdovirus
  • animal
  • plant
  • insect
  • fish
  • vertebrate
  • arbovirus
  • reservoir
  • emergence
  • epidemiology
  • evolution
  • diversity
  • transmission
  • animal model
  • cellular model
  • structure
  • molecular interaction
  • diagnostic
  • antiviral drugs
  • vaccine
  • surveillance
  • control program
  • one health
  • economy

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Published Papers (7 papers)

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15 pages, 4715 KiB  
Article
Structural Heterogeneity of the Rabies Virus Virion
by Xiaoying Cai, Kang Zhou, Ana Lucia Alvarez-Cabrera, Zhu Si, Hui Wang, Yao He, Cally Li and Z. Hong Zhou
Viruses 2024, 16(9), 1447; https://doi.org/10.3390/v16091447 - 11 Sep 2024
Viewed by 1039
Abstract
Rabies virus (RABV) is among the first recognized viruses of public health concern and has historically contributed to the development of viral vaccines. Despite these significances, the three-dimensional structure of the RABV virion remains unknown due to the challenges in isolating structurally homogenous [...] Read more.
Rabies virus (RABV) is among the first recognized viruses of public health concern and has historically contributed to the development of viral vaccines. Despite these significances, the three-dimensional structure of the RABV virion remains unknown due to the challenges in isolating structurally homogenous virion samples in sufficient quantities needed for structural investigation. Here, by combining the capabilities of cryogenic electron tomography (cryoET) and microscopy (cryoEM), we determined the three-dimensional structure of the wild-type RABV virion. Tomograms of RABV virions reveal a high level of structural heterogeneity among the bullet-shaped virion particles encompassing the glycoprotein (G) trimer-decorated envelope and the nucleocapsid composed of RNA, nucleoprotein (N), and matrix protein (M). The structure of the trunk region of the virion was determined by cryoEM helical reconstruction, revealing a one-start N-RNA helix bound by a single layer of M proteins at an N:M ratio of 1. The N-M interaction differs from that in fellow rhabdovirus vesicular stomatitis virus (VSV), which features two layers of M stabilizing the N-RNA helix at an M:N ratio of 2. These differences in both M-N stoichiometry and binding allow RABV to flex its N-RNA helix more freely and point to different mechanisms of viral assembly between these two bullet-shaped rhabdoviruses. Full article
(This article belongs to the Special Issue The World of Rhabdoviruses)
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33 pages, 4331 KiB  
Article
Host Jump of an Exotic Fish Rhabdovirus into a New Class of Animals Poses a Disease Threat to Amphibians
by Eveline J. Emmenegger, Emma K. Bueren, Carla M. Conway, George E. Sanders, A. Noble Hendrix, Tamara Schroeder, Emiliano Di Cicco, Phuc H. Pham, John S. Lumsden and Sharon C. Clouthier
Viruses 2024, 16(8), 1193; https://doi.org/10.3390/v16081193 - 25 Jul 2024
Viewed by 1282
Abstract
Spring viremia of carp virus (SVCV) is a rhabdovirus that primarily infects cyprinid finfishes and causes a disease notifiable to the World Organization for Animal Health. Amphibians, which are sympatric with cyprinids in freshwater ecosystems, are considered non-permissive hosts of rhabdoviruses. The potential [...] Read more.
Spring viremia of carp virus (SVCV) is a rhabdovirus that primarily infects cyprinid finfishes and causes a disease notifiable to the World Organization for Animal Health. Amphibians, which are sympatric with cyprinids in freshwater ecosystems, are considered non-permissive hosts of rhabdoviruses. The potential host range expansion of SVCV in an atypical host species was evaluated by testing the susceptibility of amphibians native to the Pacific Northwest. Larval long-toed salamanders Ambystoma macrodactylum and Pacific tree frog Pseudacris regilla tadpoles were exposed to SVCV strains from genotypes Ia, Ib, Ic, or Id by either intraperitoneal injection, immersion, or cohabitation with virus-infected koi Cyprinus rubrofuscus. Cumulative mortality was 100% for salamanders injected with SVCV, 98–100% for tadpoles exposed to virus via immersion, and 0–100% for tadpoles cohabited with SVCV-infected koi. Many of the animals that died exhibited clinical signs of disease and SVCV RNA was found by in situ hybridization in tissue sections of immersion-exposed tadpoles, particularly in the cells of the gastrointestinal tract and liver. SVCV was also detected by plaque assay and RT-qPCR testing in both amphibian species regardless of the virus exposure method, and viable virus was detected up to 28 days after initial exposure. Recovery of infectious virus from naïve tadpoles cohabited with SVCV-infected koi further demonstrated that SVCV transmission can occur between classes of ectothermic vertebrates. Collectively, these results indicated that SVCV, a fish rhabdovirus, can be transmitted to and cause lethal disease in two amphibian species. Therefore, members of all five of the major vertebrate groups (mammals, birds, reptiles, fish, and amphibians) appear to be vulnerable to rhabdovirus infections. Future research studying potential spillover and spillback infections of aquatic rhabdoviruses between foreign and domestic amphibian and fish species will provide insights into the stressors driving novel interclass virus transmission events. Full article
(This article belongs to the Special Issue The World of Rhabdoviruses)
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10 pages, 1065 KiB  
Communication
Single Amino Acid Substitution in the Matrix Protein of Rabies Virus Is Associated with Neurovirulence in Mice
by Michiko Harada, Aya Matsuu, Yoshihiro Kaku, Akiko Okutani, Yusuke Inoue, Guillermo Posadas-Herrera, Satoshi Inoue and Ken Maeda
Viruses 2024, 16(5), 699; https://doi.org/10.3390/v16050699 - 28 Apr 2024
Cited by 1 | Viewed by 1496
Abstract
Rabies is a fatal encephalitic infectious disease caused by the rabies virus (RABV). RABV is highly neurotropic and replicates in neuronal cell lines in vitro. The RABV fixed strain, HEP-Flury, was produced via passaging in primary chicken embryonic fibroblast cells. HEP-Flury showed [...] Read more.
Rabies is a fatal encephalitic infectious disease caused by the rabies virus (RABV). RABV is highly neurotropic and replicates in neuronal cell lines in vitro. The RABV fixed strain, HEP-Flury, was produced via passaging in primary chicken embryonic fibroblast cells. HEP-Flury showed rapid adaptation when propagated in mouse neuroblastoma (MNA) cells. In this study, we compared the growth of our previously constructed recombinant HEP (rHEP) strain—based on the sequence of the HEP (HEP-Flury) strain—with that of the original HEP strain. The original HEP strain exhibited higher titer than rHEP and a single substitution at position 80 in the matrix (M) protein M(D80N) after incubation in MNA cells, which was absent in rHEP. In vivo, intracerebral inoculation of the rHEP-M(D80N) strain with this substitution resulted in enhanced viral growth in the mouse brain and a significant loss of body weight in the adult mice. The number of viral antigen-positive cells in the brains of adult mice inoculated with the rHEP-M(D80N) strain was significantly higher than that with the rHEP strain at 5 days post-inoculation. Our findings demonstrate that a single amino acid substitution in the M protein M(D80N) is associated with neurovirulence in mice owing to adaptation to mouse neuronal cells. Full article
(This article belongs to the Special Issue The World of Rhabdoviruses)
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16 pages, 3486 KiB  
Article
Heterologous Exchanges of Glycoprotein and Non-Virion Protein in Novirhabdoviruses: Assessment of Virulence in Yellow Perch (Perca flavescens) and Rainbow Trout (Oncorhynchus mykiss)
by Vikram N. Vakharia, Arun Ammayappan, Shamila Yusuff, Tarin M. Tesfaye and Gael Kurath
Viruses 2024, 16(4), 652; https://doi.org/10.3390/v16040652 - 22 Apr 2024
Cited by 1 | Viewed by 1189
Abstract
Infectious hematopoietic necrosis virus (IHNV) and viral hemorrhagic septicemia virus (VHSV) are rhabdoviruses in two different species belonging to the Novirhabdovirus genus. IHNV has a narrow host range restricted to trout and salmon species, and viruses in the M genogroup of IHNV have [...] Read more.
Infectious hematopoietic necrosis virus (IHNV) and viral hemorrhagic septicemia virus (VHSV) are rhabdoviruses in two different species belonging to the Novirhabdovirus genus. IHNV has a narrow host range restricted to trout and salmon species, and viruses in the M genogroup of IHNV have high virulence in rainbow trout (Oncorhynchus mykiss). In contrast, the VHSV genotype IVb that invaded the Great Lakes in the United States has a broad host range, with high virulence in yellow perch (Perca flavescens), but not in rainbow trout. By using reverse-genetic systems of IHNV-M and VHSV-IVb strains, we generated six IHNV:VHSV chimeric viruses in which the glycoprotein (G), non-virion-protein (NV), or both G and NV genes of IHNV-M were replaced with the analogous genes from VHSV-IVb, and vice versa. These chimeric viruses were used to challenge groups of rainbow trout and yellow perch. The parental recombinants rIHNV-M and rVHSV-IVb were highly virulent in rainbow trout and yellow perch, respectively. Parental rIHNV-M was avirulent in yellow perch, and chimeric rIHNV carrying G, NV, or G and NV genes from VHSV-IVb remained low in virulence in yellow perch. Similarly, the parental rVHSV-IVb exhibited low virulence in rainbow trout, and chimeric rVHSV with substituted G, NV, or G and NV genes from IHNV-M remained avirulent in rainbow trout. Thus, the G and NV genes of either virus were not sufficient to confer high host-specific virulence when exchanged into a heterologous species genome. Some exchanges of G and/or NV genes caused a loss of host-specific virulence, providing insights into possible roles in viral virulence or fitness, and interactions between viral proteins. Full article
(This article belongs to the Special Issue The World of Rhabdoviruses)
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17 pages, 4523 KiB  
Article
Two Novel Betarhabdovirins Infecting Ornamental Plants and the Peculiar Intracellular Behavior of the Cytorhabdovirus in the Liana Aristolochia gibertii
by Pedro Luis Ramos-González, Maria Amelia Vaz Alexandre, Matheus Potsclam-Barro, Lígia Maria Lembo Duarte, Gianluca L. Michea Gonzalez, Camila Chabi-Jesus, Alyne F. Ramos, Ricardo Harakava, Harri Lorenzi, Juliana Freitas-Astúa and Elliot Watanabe Kitajima
Viruses 2024, 16(3), 322; https://doi.org/10.3390/v16030322 - 21 Feb 2024
Viewed by 1378
Abstract
Two novel members of the subfamily Betarhabdovirinae, family Rhabdoviridae, were identified in Brazil. Overall, their genomes have the typical organization 3′-N-P-P3-M-G-L-5′ observed in mono-segmented plant-infecting rhabdoviruses. In aristolochia-associated cytorhabdovirus (AaCV), found in the liana aristolochia (Aristolochia gibertii Hook), an [...] Read more.
Two novel members of the subfamily Betarhabdovirinae, family Rhabdoviridae, were identified in Brazil. Overall, their genomes have the typical organization 3′-N-P-P3-M-G-L-5′ observed in mono-segmented plant-infecting rhabdoviruses. In aristolochia-associated cytorhabdovirus (AaCV), found in the liana aristolochia (Aristolochia gibertii Hook), an additional short orphan ORF encoding a transmembrane helix was detected between P3 and M. The AaCV genome and inferred encoded proteins share the highest identity values, consistently < 60%, with their counterparts of the yerba mate chlorosis-associated virus (Cytorhabdovirus flaviyerbamate). The second virus, false jalap virus (FaJV), was detected in the herbaceous plant false jalap (Mirabilis jalapa L.) and represents together with tomato betanucleorhabdovirus 2, originally found in tomato plants in Slovenia, a tentative new species of the genus Betanucleorhabdovirus. FaJV particles accumulate in the perinuclear space, and electron-lucent viroplasms were observed in the nuclei of the infected cells. Notably, distinct from typical rhabdoviruses, most virions of AaCV were observed to be non-enclosed within membrane-bounded cavities. Instead, they were frequently seen in close association with surfaces of mitochondria or peroxisomes. Unlike FaJV, AaCV was successfully graft-transmitted to healthy plants of three species of the genus Aristolochia, while mechanical and seed transmission proved unsuccessful for both viruses. Data suggest that these viruses belong to two new tentative species within the subfamily Betarhabdovirinae. Full article
(This article belongs to the Special Issue The World of Rhabdoviruses)
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54 pages, 6211 KiB  
Article
Novel Tri-Segmented Rhabdoviruses: A Data Mining Expedition Unveils the Cryptic Diversity of Cytorhabdoviruses
by Nicolas Bejerman, Ralf Dietzgen and Humberto Debat
Viruses 2023, 15(12), 2402; https://doi.org/10.3390/v15122402 - 10 Dec 2023
Cited by 5 | Viewed by 1550
Abstract
Cytorhabdoviruses (genus Cytorhabdovirus, family Rhabdoviridae) are plant-infecting viruses with enveloped, bacilliform virions. Established members of the genus Cytorhabdovirus have unsegmented single-stranded negative-sense RNA genomes (ca. 10–16 kb) which encode four to ten proteins. Here, by exploring large publicly available metatranscriptomics datasets, [...] Read more.
Cytorhabdoviruses (genus Cytorhabdovirus, family Rhabdoviridae) are plant-infecting viruses with enveloped, bacilliform virions. Established members of the genus Cytorhabdovirus have unsegmented single-stranded negative-sense RNA genomes (ca. 10–16 kb) which encode four to ten proteins. Here, by exploring large publicly available metatranscriptomics datasets, we report the identification and genomic characterization of 93 novel viruses with genetic and evolutionary cues of cytorhabdoviruses. Strikingly, five unprecedented viruses with tri-segmented genomes were also identified. This finding represents the first tri-segmented viruses in the family Rhabdoviridae, and they should be classified in a novel genus within this family for which we suggest the name “Trirhavirus”. Interestingly, the nucleocapsid and polymerase were the only typical rhabdoviral proteins encoded by those tri-segmented viruses, whereas in three of them, a protein similar to the emaravirus (family Fimoviridae) silencing suppressor was found, while the other predicted proteins had no matches in any sequence databases. Genetic distance and evolutionary insights suggest that all these novel viruses may represent members of novel species. Phylogenetic analyses, of both novel and previously classified plant rhabdoviruses, provide compelling support for the division of the genus Cytorhabdovirus into three distinct genera. This proposed reclassification not only enhances our understanding of the evolutionary dynamics within this group of plant rhabdoviruses but also illuminates the remarkable genomic diversity they encompass. This study not only represents a significant expansion of the genomics of cytorhabdoviruses that will enable future research on the evolutionary peculiarity of this genus but also shows the plasticity in the rhabdovirus genome organization with the discovery of tri-segmented members with a unique evolutionary trajectory. Full article
(This article belongs to the Special Issue The World of Rhabdoviruses)
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8 pages, 1428 KiB  
Brief Report
Sequences Related to Chimay Rhabdovirus Are Widely Distributed in Ixodes ricinus Ticks across England and Wales
by Mirjam Schilling, Megan Golding, Ben P. Jones, Karen L. Mansfield, Sara Gandy, Jolyon Medlock and Nicholas Johnson
Viruses 2024, 16(4), 504; https://doi.org/10.3390/v16040504 - 26 Mar 2024
Viewed by 1513
Abstract
Ticks are the main arthropod vector of pathogens to humans and livestock in the British Isles. Despite their role as a vector of disease, many aspects of tick biology, ecology, and microbial association are poorly understood. To address this, we investigated the composition [...] Read more.
Ticks are the main arthropod vector of pathogens to humans and livestock in the British Isles. Despite their role as a vector of disease, many aspects of tick biology, ecology, and microbial association are poorly understood. To address this, we investigated the composition of the microbiome of adult and nymphal Ixodes ricinus ticks. The ticks were collected on a dairy farm in Southwest England and RNA extracted for whole genome sequencing. Sequences were detected from a range of microorganisms, particularly tick-associated viruses, bacteria, and nematodes. A majority of the viruses were attributed to phlebo-like and nairo-like virus groups, demonstrating a high degree of homology with the sequences present in I. ricinus from mainland Europe. A virus sharing a high sequence identity with Chimay rhabdovirus, previously identified in ticks from Belgium, was detected. Further investigations of I. ricinus ticks collected from additional sites in England and Wales also identified Chimay rhabdovirus viral RNA with varying prevalence in all tick populations. This suggests that Chimay rhabdovirus has a wide distribution and highlights the need for an extended exploration of the tick microbiome in the United Kingdom (UK). Full article
(This article belongs to the Special Issue The World of Rhabdoviruses)
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