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Relatives of rubella virus in diverse mammals

Nature volume 586, pages 424–428 (2020)Cite this article

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An Author Correction to this article was published on 17 November 2020

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Abstract

Since 1814, when rubella was first described, the origins of the disease and its causative agent, rubella virus (Matonaviridae: Rubivirus), have remained unclear1. Here we describe ruhugu virus and rustrela virus in Africa and Europe, respectively, which are, to our knowledge, the first known relatives of rubella virus. Ruhugu virus, which is the closest relative of rubella virus, was found in apparently healthy cyclops leaf-nosed bats (Hipposideros cyclops) in Uganda. Rustrela virus, which is an outgroup to the clade that comprises rubella and ruhugu viruses, was found in acutely encephalitic placental and marsupial animals at a zoo in Germany and in wild yellow-necked field mice (Apodemus flavicollis) at and near the zoo. Ruhugu and rustrela viruses share an identical genomic architecture with rubella virus2,3. The amino acid sequences of four putative B cell epitopes in the fusion (E1) protein of the rubella, ruhugu and rustrela viruses and two putative T cell epitopes in the capsid protein of the rubella and ruhugu viruses are moderately to highly conserved4,5,6. Modelling of E1 homotrimers in the post-fusion state predicts that ruhugu and rubella viruses have a similar capacity for fusion with the host-cell membrane5. Together, these findings show that some members of the family Matonaviridae can cross substantial barriers between host species and that rubella virus probably has a zoonotic origin. Our findings raise concerns about future zoonotic transmission of rubella-like viruses, but will facilitate comparative studies and animal models of rubella and congenital rubella syndrome.

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Fig. 1: Geographical locations of viruses and their hosts.
Fig. 2: Histopathology and immune reaction of RusV in the brain of a capybara, red-necked wallaby and donkey.
Fig. 3: Evolutionary relationships among viruses.
Fig. 4: Comparisons of the E1 envelope glycoproteins of RuV, RuhV and RusV.

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Data availability

Sequence data that support the findings of this study have been deposited in GenBank (accession numbers MN547623, MN552442 and MT274724–MT274737).

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Acknowledgements

We thank D. Hyeroba, K. Swaibu and J. Carag for assistance in the field; C. Langner and the zoo in Germany for assistance with sampling and for implementing timely response strategies; L. Bollinger, J. Wada and D. Rubbenstroth for their help improving the manuscript and figures; G. K. Rice for advice and assistance with bioinformatics scripts; P. Zitzow J. Lorke, S. Schuparis and G. Czerwinski for technical assistance; and C. Jelinek, D. Kaufmann, J. Pöhlig and C. Trapp for help with rodent trapping and dissection. This work was supported in part through US National Institute of Allergy and Infectious Diseases (NIAID) Virology Training Grants T32 AI078985 (to University of Wisconsin-Madison) and GEIS P0062_20_NM_06 (to K.A.B.-L.), and by the Federal Ministry of Education and Research within the research consortium ‘ZooBoCo’ (01KI1722A). This work was also partially supported through the prime contract of Laulima Government Solutions with NIAID under contract no. HHSN272201800013C and Battelle Memorial Institute’s former prime contract with NIAID under contract no. HHSN272200700016I. J.H.K. performed this work as a former employee of Battelle Memorial Institute and a current employee of Tunnell Government Services (TGS), a subcontractor of Laulima Government Solutions under contract no. HHSN272201800013C. Additional support was provided through the German Center for Infection Research (DZIF) TTU ‘Emerging Infections’ (to R.G.U.), and by the University of Wisconsin-Madison Global Health Institute, Institute for Regional and International Studies, and John D. MacArthur Professorship Chair (to T.L.G.). The views and conclusions contained in this document are those of the authors and should not be interpreted as necessarily representing the official policies or positions, either expressed or implied, of the US Department of Health and Human Services, Department of the Navy, Department of Defense, US Government, or any of the institutions and companies affiliated with the authors. In no event shall any of these entities have any responsibility or liability for any use, misuse, inability to use, or reliance upon the information contained herein. The US departments do not endorse any products or commercial services mentioned in this publication. K.A.B.-L. is an employee of the US Government. This work was prepared as part of her official duties. Title 17 U.S.C. § 105 provides that ‘Copyright protection under this title is not available for any work of the United States Government.’ Title 17 U.S.C. § 101 defines a U.S. Government work as a work prepared by a military service member or employee of the U.S. Government as part of that person’s official duties. The study protocol was reviewed and approved by the University of Wisconsin-Madison Institutional Animal Care and Use Committee in compliance with all applicable federal regulations governing the protection of animals and research.

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Author notes

  1. These authors contributed equally: Andrew J. Bennett, Adrian C. Paskey, Arnt Ebinger

Authors and Affiliations

  1. Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, WI, USA

    Andrew J. Bennett & Tony L. Goldberg

  2. Department of Microbiology and Immunology, Uniformed Services University of the Health Sciences, Bethesda, MD, USA

    Adrian C. Paskey & Kimberly A. Bishop-Lilly

  3. Leidos, Reston, VA, USA

    Adrian C. Paskey

  4. Genomics and Bioinformatics Department, Biological Defense Research Directorate, Naval Medical Research Center–Frederick, Fort Detrick, Frederick, MD, USA

    Adrian C. Paskey & Kimberly A. Bishop-Lilly

  5. Institute of Diagnostic Virology, Friedrich-Loeffler-Institut, Greifswald-Insel Riems, Germany

    Arnt Ebinger, Florian Pfaff, Dirk Höper & Martin Beer

  6. State Office for Agriculture, Food Safety and Fisheries, Rostock, Germany

    Grit Priemer

  7. Department of Experimental Animal Facilities and Biorisk Management, Friedrich-Loeffler-Institut, Greifswald-Insel Riems, Germany

    Angele Breithaupt

  8. Institute of Novel and Emerging Infectious Diseases, Friedrich-Loeffler-Institut, Greifswald-Insel Riems, Germany

    Elisa Heuser & Rainer G. Ulrich

  9. German Center for Infection Research (DZIF), Hamburg-Lübeck-Borstel-Insel Riems, Greifswald-Insel Riems, Germany

    Elisa Heuser & Rainer G. Ulrich

  10. Integrated Research Facility at Fort Detrick, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Fort Detrick, Frederick, MD, USA

    Jens H. Kuhn

  11. Global Health Institute, University of Wisconsin-Madison, Madison, WI, USA

    Tony L. Goldberg

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Contributions

A.J.B., A.C.P., A.E., J.H.K., K.A.B.-L., M.B. and T.L.G. contributed to the study conception and design. A.B., A.J.B., A.C.P., A.E., E.H., G.P., K.A.B.-L., M.B., R.G.U. and T.L.G. contributed to sample and data collection. A.B., A.J.B., A.C.P., A.E., F.P., D.H., E.H., J.H.K., K.A.B.-L., M.B., R.G.U. and T.L.G. contributed to data analyses, interpretation and writing. All authors read and approved the final manuscript.

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Correspondence to Martin Beer or Tony L. Goldberg.

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Extended data figures and tables

Extended Data Fig. 1 RNA in situ hybridization of RusV.

a–e, Detection of RusV RNA using in the brain tissues of a donkey (a), red-necked wallaby (b), capybara (c) and yellow-necked field mice (d, e). Chromogenic labelling (fast red) with probes against the NSP-coding region of RusV are visible in neuronal cell bodies (arrow) but not in adjacent glial cells (arrowhead). Scale bars, 50 μm. f, Negative control probe against the bacterial gene dapB, which encodes dihydrodipicolinate reductase. Lack of chromogenic labelling (fast red). Scale bar, 100 µm. All sections were counterstained with Mayer’s haematoxylin. RNAscope results were evaluated on at least three slides per animal, yielding comparable results in all cases. In situ hybridization was performed according to the manufacturer’s instructions, including a positive control probe against peptidylprolyl isomerase B (cyclophilin B) and a negative control probe against dihydrodipicolinate reductase (DapB). Evaluation and interpretation were performed by a board-certified pathologist (DiplECVP) with more than 13 years of experience.

Extended Data Fig. 2 Average substitution rates at non-synonymous and synonymous sites, and the ratio of dN/dS for aligned, concatenated amino acid sequences.

a–c, The average substitution rates at non-synonymous (dN; dashed lines) and synonymous (dS; grey lines) sites, and the ratio of dN/dS (solid lines) for aligned, concatenated amino acid sequences were compared for RuV and RuhV (a), RuV and RusV (b), and RuhV and RusV (c) using sliding windows (100-residue window length, 10 residue steps). Protein domains are labelled on the x axes. MT, methyltransferase; Y, Q and X, domains of unknown function; Pro, protease; Hel, helicase; RdRp, RNA-directed RNA polymerase; NT1, neutralizing epitope 1.

Extended Data Fig. 3 Phylogenetic analyses of the coding sequences of envelope glycoprotein E1, and the helicase and RNA-directed RNA polymerase p90.

a, b, Phylogenetic analyses of the coding sequences (CDS) of the envelope glycoprotein E1 (a) and the helicase and RNA-directed RNA polymerase p90 (b) of RuV, RuhV and RusV, including all sequences obtained in this study (GenBank accession numbers are listed in parentheses). Numbers above branches represent bootstrap values; scale bars indicate amino acid substitutions per site.

Extended Data Table 1 RusV in small mammals from northeastern Germany
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Extended Data Table 2 RusV distribution in tissues from zoo animals
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Extended Data Table 3 RusV distribution in tissues of A. flavicollis
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Extended Data Table 4 Genomic features of RuhV and RusV
Full size table
Extended Data Table 5 Conservation of B and T cell epitopes in E1 fusion proteins
Full size table
Extended Data Table 6 Immunohistochemical markers and applications
Full size table

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Bennett, A.J., Paskey, A.C., Ebinger, A. et al. Relatives of rubella virus in diverse mammals. Nature 586, 424–428 (2020). https://doi.org/10.1038/s41586-020-2812-9

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