Co-infecting Reptarenaviruses Can Be Vertically Transmitted in Boa Constrictor
Boid inclusion body disease (BIBD) is an often fatal disease affecting mainly constrictor snakes. BIBD has been associated with infection, and more recently with coinfection, by various reptarenavirus species (family Arenaviridae). Thus far BIBD has only been reported in captive snakes, and neither...
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| Published in | PLoS pathogens Vol. 13; no. 1; p. e1006179 |
|---|---|
| Main Authors | , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
01.01.2017
Public Library of Science (PLoS) |
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| Online Access | Get full text |
| ISSN | 1553-7374 1553-7366 1553-7374 |
| DOI | 10.1371/journal.ppat.1006179 |
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| Abstract | Boid inclusion body disease (BIBD) is an often fatal disease affecting mainly constrictor snakes. BIBD has been associated with infection, and more recently with coinfection, by various reptarenavirus species (family Arenaviridae). Thus far BIBD has only been reported in captive snakes, and neither the incubation period nor the route of transmission are known. Herein we provide strong evidence that co-infecting reptarenavirus species can be vertically transmitted in Boa constrictor. In total we examined five B. constrictor clutches with offspring ranging in age from embryos over perinatal abortions to juveniles. The mother and/or father of each clutch were initially diagnosed with BIBD and/or reptarenavirus infection by detection of the pathognomonic inclusion bodies (IB) and/or reptarenaviral RNA. By applying next-generation sequencing and de novo sequence assembly we determined the "reptarenavirome" of each clutch, yielding several nearly complete L and S segments of multiple reptarenaviruses. We further confirmed vertical transmission of the co-infecting reptarenaviruses by species-specific RT-PCR from samples of parental animals and offspring. Curiously, not all offspring obtained the full parental "reptarenavirome". We extended our findings by an in vitro approach; cell cultures derived from embryonal samples rapidly developed IB and promoted replication of some or all parental viruses. In the tissues of embryos and perinatal abortions, viral antigen was sometimes detected, but IB were consistently seen only in the juvenile snakes from the age of 2 mo onwards. In addition to demonstrating vertical transmission of multiple species, our results also indicate that reptarenavirus infection induces BIBD over time in the offspring. |
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| AbstractList | Boid inclusion body disease (BIBD) is an often fatal disease affecting mainly constrictor snakes. BIBD has been associated with infection, and more recently with coinfection, by various reptarenavirus species (family Arenaviridae). Thus far BIBD has only been reported in captive snakes, and neither the incubation period nor the route of transmission are known. Herein we provide strong evidence that co-infecting reptarenavirus species can be vertically transmitted in Boa constrictor. In total we examined five B. constrictor clutches with offspring ranging in age from embryos over perinatal abortions to juveniles. The mother and/or father of each clutch were initially diagnosed with BIBD and/or reptarenavirus infection by detection of the pathognomonic inclusion bodies (IB) and/or reptarenaviral RNA. By applying next-generation sequencing and de novo sequence assembly we determined the "reptarenavirome" of each clutch, yielding several nearly complete L and S segments of multiple reptarenaviruses. We further confirmed vertical transmission of the co-infecting reptarenaviruses by species-specific RT-PCR from samples of parental animals and offspring. Curiously, not all offspring obtained the full parental "reptarenavirome". We extended our findings by an in vitro approach; cell cultures derived from embryonal samples rapidly developed IB and promoted replication of some or all parental viruses. In the tissues of embryos and perinatal abortions, viral antigen was sometimes detected, but IB were consistently seen only in the juvenile snakes from the age of 2 mo onwards. In addition to demonstrating vertical transmission of multiple species, our results also indicate that reptarenavirus infection induces BIBD over time in the offspring.Boid inclusion body disease (BIBD) is an often fatal disease affecting mainly constrictor snakes. BIBD has been associated with infection, and more recently with coinfection, by various reptarenavirus species (family Arenaviridae). Thus far BIBD has only been reported in captive snakes, and neither the incubation period nor the route of transmission are known. Herein we provide strong evidence that co-infecting reptarenavirus species can be vertically transmitted in Boa constrictor. In total we examined five B. constrictor clutches with offspring ranging in age from embryos over perinatal abortions to juveniles. The mother and/or father of each clutch were initially diagnosed with BIBD and/or reptarenavirus infection by detection of the pathognomonic inclusion bodies (IB) and/or reptarenaviral RNA. By applying next-generation sequencing and de novo sequence assembly we determined the "reptarenavirome" of each clutch, yielding several nearly complete L and S segments of multiple reptarenaviruses. We further confirmed vertical transmission of the co-infecting reptarenaviruses by species-specific RT-PCR from samples of parental animals and offspring. Curiously, not all offspring obtained the full parental "reptarenavirome". We extended our findings by an in vitro approach; cell cultures derived from embryonal samples rapidly developed IB and promoted replication of some or all parental viruses. In the tissues of embryos and perinatal abortions, viral antigen was sometimes detected, but IB were consistently seen only in the juvenile snakes from the age of 2 mo onwards. In addition to demonstrating vertical transmission of multiple species, our results also indicate that reptarenavirus infection induces BIBD over time in the offspring. Boid inclusion body disease (BIBD) is an often fatal disease affecting mainly constrictor snakes. BIBD has been associated with infection, and more recently with coinfection, by various reptarenavirus species (family Arenaviridae). Thus far BIBD has only been reported in captive snakes, and neither the incubation period nor the route of transmission are known. Herein we provide strong evidence that co-infecting reptarenavirus species can be vertically transmitted in Boa constrictor. In total we examined five B. constrictor clutches with offspring ranging in age from embryos over perinatal abortions to juveniles. The mother and/or father of each clutch were initially diagnosed with BIBD and/or reptarenavirus infection by detection of the pathognomonic inclusion bodies (IB) and/or reptarenaviral RNA. By applying next-generation sequencing and de novo sequence assembly we determined the "reptarenavirome" of each clutch, yielding several nearly complete L and S segments of multiple reptarenaviruses. We further confirmed vertical transmission of the co-infecting reptarenaviruses by species-specific RT-PCR from samples of parental animals and offspring. Curiously, not all offspring obtained the full parental "reptarenavirome". We extended our findings by an in vitro approach; cell cultures derived from embryonal samples rapidly developed IB and promoted replication of some or all parental viruses. In the tissues of embryos and perinatal abortions, viral antigen was sometimes detected, but IB were consistently seen only in the juvenile snakes from the age of 2 mo onwards. In addition to demonstrating vertical transmission of multiple species, our results also indicate that reptarenavirus infection induces BIBD over time in the offspring. Boid inclusion body disease (BIBD) is an often fatal disease affecting mainly constrictor snakes. BIBD has been associated with infection, and more recently with coinfection, by various reptarenavirus species (family Arenaviridae ). Thus far BIBD has only been reported in captive snakes, and neither the incubation period nor the route of transmission are known. Herein we provide strong evidence that co-infecting reptarenavirus species can be vertically transmitted in Boa constrictor . In total we examined five B . constrictor clutches with offspring ranging in age from embryos over perinatal abortions to juveniles. The mother and/or father of each clutch were initially diagnosed with BIBD and/or reptarenavirus infection by detection of the pathognomonic inclusion bodies (IB) and/or reptarenaviral RNA. By applying next-generation sequencing and de novo sequence assembly we determined the “reptarenavirome” of each clutch, yielding several nearly complete L and S segments of multiple reptarenaviruses. We further confirmed vertical transmission of the co-infecting reptarenaviruses by species-specific RT-PCR from samples of parental animals and offspring. Curiously, not all offspring obtained the full parental “reptarenavirome”. We extended our findings by an in vitro approach; cell cultures derived from embryonal samples rapidly developed IB and promoted replication of some or all parental viruses. In the tissues of embryos and perinatal abortions, viral antigen was sometimes detected, but IB were consistently seen only in the juvenile snakes from the age of 2 mo onwards. In addition to demonstrating vertical transmission of multiple species, our results also indicate that reptarenavirus infection induces BIBD over time in the offspring. Members of the genus Reptarenavirus are “newcomers” of the family Arenaviridae and have been associated with boid inclusion body disease (BIBD), an economically important, fatal disease of captive boid snakes. Recently, we and others observed that snakes with BIBD commonly harbour several S and L segments (arenaviruses have a bisegmented genome), which we refer to as co-infection. The above renders reptarenaviruses rather unique and a model for studying viral co-infection. We herein report that reptarenaviruses, and remarkably a whole set of co-infecting reptarenavirus species (based on the nucleotide difference in the L segment), can be transmitted vertically i.e. from parents to offspring. While the parental animals had BIBD, we did not find evidence of the intracytoplasmic inclusions characteristic to BIBD in the infected embryos and perinatal abortions. However, we could confirm the development of BIBD in offspring from an age of 2 months. Our findings further suggest that vertical transmission can, and likely has, significantly influence(d) the evolution of reptarenaviruses, since co-infection will allow reassortment of the viral genomes. Boid inclusion body disease (BIBD) is an often fatal disease affecting mainly constrictor snakes. BIBD has been associated with infection, and more recently with coinfection, by various reptarenavirus species (family Arenaviridae). Thus far BIBD has only been reported in captive snakes, and neither the incubation period nor the route of transmission are known. Herein we provide strong evidence that co-infecting reptarenavirus species can be vertically transmitted in Boa constrictor. In total we examined five B. constrictor clutches with offspring ranging in age from embryos over perinatal abortions to juveniles. The mother and/or father of each clutch were initially diagnosed with BIBD and/or reptarenavirus infection by detection of the pathognomonic inclusion bodies (IB) and/or reptarenaviral RNA. By applying next-generation sequencing and de novo sequence assembly we determined the "reptarenavirome" of each clutch, yielding several nearly complete L and S segments of multiple reptarenaviruses. We further confirmed vertical transmission of the co-infecting reptarenaviruses by species-specific RT-PCR from samples of parental animals and offspring. Curiously, not all offspring obtained the full parental "reptarenavirome". We extended our findings by an in vitro approach; cell cultures derived from embryonal samples rapidly developed IB and promoted replication of some or all parental viruses. In the tissues of embryos and perinatal abortions, viral antigen was sometimes detected, but IB were consistently seen only in the juvenile snakes from the age of 2 mo onwards. In addition to demonstrating vertical transmission of multiple species, our results also indicate that reptarenavirus infection induces BIBD over time in the offspring. |
| Audience | Academic |
| Author | Sironen, Tarja Hetzel, Udo Vapalahti, Olli Kipar, Anja Korzyukov, Yegor Hepojoki, Jussi Keller, Saskia |
| AuthorAffiliation | Division of Clinical Research, UNITED STATES 1 Institute of Veterinary Pathology, Vetsuisse Faculty, University of Zürich, Zürich, Switzerland 3 University of Helsinki, Medicum, Department of Virology, Helsinki, Finland 2 University of Helsinki, Department of Veterinary Biosciences, Faculty of Veterinary Medicine, Helsinki, Finland 4 University of Helsinki and Helsinki University Hospital, Department of Virology, Helsinki, Finland |
| AuthorAffiliation_xml | – name: 4 University of Helsinki and Helsinki University Hospital, Department of Virology, Helsinki, Finland – name: 2 University of Helsinki, Department of Veterinary Biosciences, Faculty of Veterinary Medicine, Helsinki, Finland – name: 3 University of Helsinki, Medicum, Department of Virology, Helsinki, Finland – name: Division of Clinical Research, UNITED STATES – name: 1 Institute of Veterinary Pathology, Vetsuisse Faculty, University of Zürich, Zürich, Switzerland |
| Author_xml | – sequence: 1 givenname: Saskia orcidid: 0000-0002-9653-516X surname: Keller fullname: Keller, Saskia – sequence: 2 givenname: Udo surname: Hetzel fullname: Hetzel, Udo – sequence: 3 givenname: Tarja surname: Sironen fullname: Sironen, Tarja – sequence: 4 givenname: Yegor surname: Korzyukov fullname: Korzyukov, Yegor – sequence: 5 givenname: Olli orcidid: 0000-0003-2270-6824 surname: Vapalahti fullname: Vapalahti, Olli – sequence: 6 givenname: Anja surname: Kipar fullname: Kipar, Anja – sequence: 7 givenname: Jussi orcidid: 0000-0001-5699-214X surname: Hepojoki fullname: Hepojoki, Jussi |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/28114434$$D View this record in MEDLINE/PubMed |
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| Copyright | COPYRIGHT 2017 Public Library of Science 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: . PLoS Pathog 13(1): e1006179. doi:10.1371/journal.ppat.1006179 2017 Keller et al 2017 Keller et al 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: . PLoS Pathog 13(1): e1006179. doi:10.1371/journal.ppat.1006179 |
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| Notes | new_version ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Conceptualization: SK UH OV AK JH.Data curation: JH.Formal analysis: TS JH.Funding acquisition: UH AK OV.Investigation: SK UH TS YK JH.Methodology: SK UH TS OV AK JH.Project administration: UH AK JH.Resources: SK UH AK OV.Supervision: UH AK JH.Validation: SK UH YK JH.Visualization: SK UH TS OV AK JH.Writing – original draft: SK UH AK JH.Writing – review & editing: SK UH TS YK OV AK JH. The authors have declared that no competing interests exist. |
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| Snippet | Boid inclusion body disease (BIBD) is an often fatal disease affecting mainly constrictor snakes. BIBD has been associated with infection, and more recently... Boid inclusion body disease (BIBD) is an often fatal disease affecting mainly constrictor snakes. BIBD has been associated with infection, and more recently... |
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| SubjectTerms | Abortion Acids Animals Arenaviridae Infections - transmission Arenaviridae Infections - virology Arenavirus - genetics Arenaviruses Biology and Life Sciences Boidae - virology Coinfection Disease transmission Diseases Embryos Funding Genes Genomes High-Throughput Nucleotide Sequencing Immunohistochemistry Inclusion Bodies, Viral Infections Infectious Disease Transmission, Vertical Light Medicine and Health Sciences Offspring Pathology Phylogeny Pythons Research and Analysis Methods Reverse Transcriptase Polymerase Chain Reaction RNA polymerase RNA, Viral - analysis Snakes Veterinary medicine Virology Viruses |
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| Title | Co-infecting Reptarenaviruses Can Be Vertically Transmitted in Boa Constrictor |
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