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Ranavirus research: 10 years of global collaboration


While the discovery of ranaviruses goes back to the 1960s, it’s not until 2010 that a group of researchers decided to organize the first symposium spanning all the facets associated with a wildlife pathogen. This first meeting was held in 2011 and gave birth to the Global Ranavirus Consortium. Ten years later, this collection of papers aims at exposing the advances made by researchers from around the world in disciplines like taxonomy and molecular biology, physiology and immunology, epidemiology and ecology, including the more recent forays into biosecurity. Following the 5th instalment of the symposium, this collection would demonstrate how a global collaboration has been the perfect platform to explore a group of viruses affecting both invertebrates and cold-blooded vertebrates across all the continents. 

  • OPEN ACCESS
    Global patterns of ranavirus detections
    FACETS • Vol. 6 • pp. 912 - 924
    Ranaviruses are emerging pathogens of poikilothermic vertebrates. In 2015 the Global Ranavirus Reporting System (GRRS) was established as a centralized, open access, online database for reports of the presence (and absence) of ranavirus around the globe. The GRRS has multiple data layers (e.g., location, date, host(s) species, and methods of detection) of use to those studying the epidemiology, ecology, and evolution of this group of viruses. Here we summarize the temporal, spatial, diagnostic, and host-taxonomic patterns of ranavirus reports in the GRRS. The number, distribution, and host diversity of ranavirus reports have increased dramatically since the mid 1990s, presumably in response to increased interest in ranaviruses and the conservation of their hosts, and also the availability of molecular diagnostics. Yet there are clear geographic and taxonomic biases among the reports. We encourage ranavirus researchers to add their studies to the portal because such collation can provide collaborative opportunities and unique insights to our developing knowledge of this pathogen and the emerging infectious disease that it causes.
  • OPEN ACCESS
    Ten years of ranavirus research (2010–2019): an analysis of global research trends
    FACETS • Vol. 6 • pp. 44 - 57
    Ranaviruses are large nucleocytoplasmic DNA viruses that infect ectothermic vertebrates. Here we report the results of a scientometric analysis of the field of ranavirology for the last 10 years. Using bibliometric tools we analyse trends, identify top publications and journals, and visualise the ranavirus collaboration landscape. The Web of Science core collection contains 545 ranavirus-related publications from 2010 to 2019, with more publications produced every year and a total of 6830 citations. Research output is primarily driven by the United States and People’s Republic of China, who together account for more than 60% of ranavirus publications. We also observed a positive correlation between the average number of co-authors on ranavirus publications and the year of publication, indicating that overall collaboration is increasing. A keyword analysis of ranavirus publications from 2010 to 2019 reveals several areas of research interest including; ecology, immunology, virology/molecular biology, genetics, ichthyology, and herpetology. While ranavirus research is conducted globally, relatively few publications have co-authors from both European and Asian countries, possibly because closer countries (geographical distance) are more likely to share co-authors. To this end, efforts should be made to foster collaborations across geopolitical and cultural boundaries, especially between countries with shared research interests as ultimately, understanding global pathogens, like ranaviruses, will require global collaboration.
  • OPEN ACCESS
    Phylogenomic characterization of ranaviruses isolated from cultured fish and amphibians in Thailand
    FACETS • Vol. 5 • No. 1 • pp. 963 - 979
    Ranaviruses are emerging pathogens associated with worldwide epizootics in farmed and wild ectothermic vertebrates. In this study, we determined the full genomes of eight ranaviruses isolated from marbled sleeper goby (Oxyeleotris marmorata), goldfish (Carassius auratus), guppy (Poecilia reticulata), tiger frog (Hoplobatrachus tigerinus), Asian grass frog (Fejervarya limnocharis), and East Asian bullfrog (H. rugulosus) cultured or imported into Thailand. These ranaviral isolates induced the same cytopathic effects (i.e., progression of coalescing round plaques) in epithelioma papulosum cyprini (EPC) cell cultures. Transmission electron microscopy of infected EPC cells revealed cytoplasmic viral particles with ultrastructural features typical for ranaviruses. Pairwise genetic comparisons of the complete major capsid protein coding sequences from the Thai ranaviruses displayed the highest identity (99.8%–100%) to a ranavirus (tiger frog virus; TFV) isolated from diseased tiger frogs cultured in China, a slightly lower identity (99.3%–99.4%) to a ranavirus (Wamena virus; WV) isolated from diseased green tree pythons (Morelia viridis) illegally exported from Papua New Guinea, and a lower identity to 35 other ranaviruses (93.7%–98.6%). Phylogenomic analyses supported the eight Thai ranaviruses, Chinese TFV, and WV as a subclade within a larger frog virus 3 clade. Our findings confirm the spread of TFV among cultured fish and amphibians in Asia and likely in reptiles in Oceania. Biosecurity measures are needed to ensure TFV does not continue to spread throughout Southeast Asia and to other parts of the world via international trade.
  • OPEN ACCESS
    Temperature-dependent infection of freshwater turtle hatchlings, Emydura macquarii krefftii, inoculated with a ranavirus isolate (Bohle iridovirus, Iridoviridae)
    FACETS • Vol. 5 • No. 1 • pp. 821 - 830
    Fish, amphibians, and reptiles exhibit temperature-dependent ranaviral disease. We performed an experimental infection at four different environmental temperatures (16, 22, 28, and 34 °C) to investigate the effect of temperature on ranaviral infection in Krefft’s turtle (Emydura macquarii krefftii). Infection rates and viral loads were determined by quantitative polymerase chain reaction to detect ranaviral DNA in liver samples at 21 d postexposure. The rate of infection differed across the temperature treatment groups. Infection rates were 44%, 90%, 60%, and 10% for the 16, 22, 28, and 34 °C temperature groups, respectively. Highest viral load was observed in the 28 °C temperature group, and there was a statistically significant difference in viral load between the 16 and 28 °C temperature groups (p = 0.027). Based on the results of this study, the temperature of maximal infection rate for ranaviral infection in Krefft’s river turtles is estimated to be 23.2 °C (SD = 4.5). The findings of this study can inform management decisions in terms of disease control and treatment and form a platform for modelling disease outbreaks.
  • OPEN ACCESS
    Lack of molecular detection of frog virus 3-like ranavirus (FV3) in mosquitoes during natural outbreak and nonoutbreak conditions
    FACETS • Vol. 5 • No. 1 • pp. 812 - 820
    Ranaviruses are worldwide pathogens of ectothermic vertebrates that can threaten herptile conservation efforts. Identifying transmission routes is critical for understanding disease ecology and promoting species conservation. Frog virus 3 (FV3) DNA was detected in mosquitoes during a ranavirus outbreak in semicaptive box turtles, but the role that insect vectors play under natural conditions is unknown. To address this knowledge gap, we collected mosquito species known to take blood meals from reptiles and amphibians (Aedes canadensis, Culex erraticus, Culex territans, and Uranotaenia sapphirina) from mid-May to early August, 2014, at four study sites in Vermilion County, Illinois, two of which had historic or ongoing FV3 outbreaks in box turtles and amphibians. Mosquitoes were batched by date and species, DNA was extracted, and quantitative polymerase chain reaction was performed for detection of FV3. FV3 was not detected despite one of the sites having an active FV3 outbreak during the study period. Our findings indicate that FV3 detection is uncommon in mosquitoes during outbreak and nonoutbreak conditions at these sites in Illinois. Thus, we cannot establish that mosquitoes contribute to transmission during natural mortality events without performing further studies.
  • OPEN ACCESS
    Ranaviruses in captive and wild Australian lizards
    FACETS • Vol. 5 • No. 1 • pp. 758 - 768
    Ranaviral infections have been associated with mass mortality events in captive and wild amphibian, fish, and reptile populations globally. In Australia, two distinct types of ranaviruses have been isolated: epizootic haematopoietic necrosis virus in fish and a Frog virus 3-like ranavirus in amphibians. Experimental studies and serum surveys have demonstrated that several Australian native fish, amphibian, and reptile species are susceptible to infection and supported the theory that ranavirus is naturally circulating in Australian herpetofauna. However, ranaviral infections have not been detected in captive or wild lizards in Australia. Oral-cloacal swabs were collected from 42 wild lizards from northern Queensland and 83 captive lizards from private collections held across three states/territories. Samples were tested for ranaviral DNA using a quantitative PCR assay. This assay detected ranaviral DNA in 30/83 (36.1%) captive and 33/42 (78.6%) wild lizard samples. This is the first time molecular evidence of ranavirus has been reported in Australian lizards.
  • OPEN ACCESS
    Sublethal effects of wild-type and a vIF-2α-knockout Frog virus 3 on postmetamorphic wood frogs (Rana sylvatica): potential for a stage-specific reservoir
    FACETS • Vol. 5 • No. 1 • pp. 738 - 757
    Ranaviruses have been associated with rising numbers of mass die-offs in amphibian populations around the globe. However, most studies on ranaviruses to date focused on larval amphibians. To assess the role of postmetamorphic amphibians in the epidemiology of ranaviruses and to determine the role of viral immune-suppression genes, we performed a bath-exposure study on post-metamorphic wood frogs (Rana sylvatica) using environmentally relevant concentrations of wild-type Frog virus 3 (WT FV3), and a gene-knockout mutant (KO FV3), deficient for the putative immune-suppression gene vIF-2α. We observed a 42% infection rate and 5% mortality across the virus challenges, with infection rates and viral loads following a dose-dependent pattern. Individuals exposed to the knockout variant exhibited significantly decreased growth and increased lethargy compared with wild-type treatments. Although 85% of exposed individuals exhibited common signs of ranavirosis throughout the experiment, most of these individuals did not exhibit signs of infection by 40 d post-exposure. Overall, we showed that even a single short time exposure to environmentally relevant concentrations of ranavirus may cause sublethal infections in postmetamorphic amphibians, highlighting the importance of this life stage in the epidemiology of ranaviruses. Our study also supports the importance of the vIF-2α gene in immune-suppression in infected individuals.
  • OPEN ACCESS
    Amphibian ranaviruses in Europe: important directions for future research
    FACETS • Vol. 5 • No. 1 • pp. 598 - 614
    Ranaviruses are an emerging group of pathogens capable of infecting all cold-blooded vertebrates. In Europe, ranaviruses pose a particularly potent threat to wild amphibian populations. Since the 1980s research on amphibian-infecting ranaviruses in Europe has been growing. The wide distribution of amphibian populations in Europe, the ease with which many are monitored, and the tractable nature of counterpart ex situ experimental systems have provided researchers with a unique opportunity to study many aspects of host–ranavirus interactions in the wild. These characteristics of European amphibian populations will also enable researchers to lead the way as the field of host–ranavirus interactions progresses. In this review, we provide a summary of the current key knowledge regarding amphibian infecting ranaviruses throughout Europe. We then outline important areas of further research and suggest practical ways each could be pursued. We address the study of potential interactions between the amphibian microbiome and ranaviruses, how pollution may exacerbate ranaviral disease either as direct stressors of amphibians or indirect modification of the amphibian microbiome. Finally, we discuss the need for continued surveillance of ranaviral emergence in the face of climate change.
  • OPEN ACCESS
    Discovery of granulocyte-lineage cells in the skin of the amphibian Xenopus laevis
    FACETS • Vol. 5 • No. 1 • pp. 571 - 597
    The ranavirus Frog Virus 3 (FV3) and the chytrid fungus Batrachochytrium dendrobatidis (Bd) are significant contributors to the global amphibian declines and both pathogens target the amphibian skin. We previously showed that tadpoles and adults of the anuran amphibian Xenopus laevis express notable levels of granulocyte chemokine genes (cxcl8a and cxcl8b) within their skin and likely possess skin-resident granulocytes. Presently, we show that tadpole and adult X. laevis indeed possess granulocyte-lineage cells within their epidermises that are distinct from their skin mast cells, which are found predominantly in lower dermal layers. These esterase-positive cells responded to (r)CXCL8a and rCXCL8b in a concentration- and CXCR1/CXCR2-dependent manner, possessed polymorphonuclear granulocyte morphology, granulocyte marker surface staining, and exhibited distinct immune gene expression from conventional granulocytes. Our past work indicates that CXCL8b recruits immunosuppressive granulocytes, and here we demonstrated that enriching esterase-positive skin granulocytes with rCXCL8b (but not rCXCL8a) may increase tadpole susceptibility to FV3 and adult frog susceptibility to Bd. Furthermore, pharmacological depletion of skin-resident granulocytes increased tadpole susceptibility to FV3. This manuscript provides new insights into the composition and roles of immune cells within the amphibian skin, which is a critical barrier against pathogenic contributors to the amphibian declines.
  • OPEN ACCESS
    An examination of the Iridovirus core genes for reconstructing Ranavirus phylogenies
    FACETS • Vol. 5 • No. 1 • pp. 523 - 533
    Ranaviruses are globally emerging infections of poikilothermic vertebrates and belong to the viral family Iridoviridae. The six species of ranaviruses are responsible for unknown numbers of infections and disease and mortality events around the world in amphibians, fish, and reptiles. Genomic investigations have shown that there are 24 core genes shared by all iridoviruses. In this study, we examine the utility of each of these genes in reconstructing phylogenetic relationships across six species of Ranavirus. We also performed dot-plot analysis for the 17 isolates in the study. For large-scale differentiation, using the major capsid protein gene creates a tree similar to the whole genome tree. Other comparable genes include open reading frame (ORF) 19R (a serine–theonine protein kinase) and ORF 88R (Erv I/Alr Family protein). The poorest candidate for phylogenetic reconstruction, due to high homology, was ORF 1R (a putative replication factor and (or) DNA binding-packing protein). There are a plethora of genes that may be useful to examine phylogenies at smaller scales (e.g., to examine local adaptation); however, they do not necessarily belong to the set of highly conserved core genes.

Curators

Dr. David Lesbarrères
Guest Editor
Laurentian University
Dr. Ellen Ariel
Guest Editor
James Cook University
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