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At Least Seven Distinct Rotavirus Genotype Constellations in Bats with Evidence Of bioRxiv preprint doi: https://doi.org/10.1101/2020.08.13.250464; this version posted October 26, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 At least seven distinct rotavirus genotype constellations in bats with evidence of 2 reassortment and zoonotic transmissions 3 4 Ceren Simseka; Victor Max Cormanb,o; Hermann Ulrich Everlingc; Alexander N. 5 Lukashevd; Andrea Rascheb,o; Gael Darren Magangae,f; Tabea Bingeri; Daan Jansena; 6 Leen Bellera; Ward Debouttea; Florian Gloza-Rauschg; Antje Seebens-Hoyerg; Stoian 7 Yordanovh; Augustina Sylverkeni,j; Samuel Oppongj; Yaw Adu Sarkodiej; Peter Vallok; 8 Eric M. Leroyl; Mathieu Bourgarelm,n,; Kwe Claude Yindaa*; Marc Van Ransta; Christian 9 Drostenb,o; Jan Felix Drexlerb,o; Jelle Matthijnssensa 10 11 a KU Leuven - University of Leuven, Department of Microbiology, Immunology and 12 Transplantation, Rega Institute for Medical Research, Leuven, Belgium 13 b Charité-Universitätsmedizin Berlin, corporate member 14 of Freie Universität Berlin, Humbolt-Universität zu Berlin and Berlin Institute of Health, 15 Institute of Virology, 10117 Berlin, Germany 16 c Institute of Virology, University of Bonn Medical Centre, Bonn, Germany 17 d Sechenov University, Moscow, Russia 18 e Centre International de Recherches Médicales de Franceville, Franceville, Gabon 19 f Université des Sciences et Technique de Masuku, Institut National d’Agronomie et de 20 Biotechnologies, Franceville, Gabon 21 g Noctalis, Centre for Bat Protection and Information, Bad Segeberg, Germany 22 h Forestry Board Directorate of Strandja Natural Park, Malko Tarnovo, Bulgaria 23 i Kumasi Centre for Collaborative Research in Tropical Medicine (KCCR), Kumasi, 24 Ghana 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.08.13.250464; this version posted October 26, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 25 j Kwame Nkrumah University of Science and Technology, Kumasi, Ghana 26 k Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, v.v.i., 27 Brno 28 l Institut de Recherche pour le Développement, UMR 224 (MIVEGEC), 29 IRD/CNRS/Montpellier University, Montpellier, France 30 m CIRAD, UMR ASTRE, Harare, Zimbabwe 31 n ASTRE, Montpellier University, CIRAD, INRA, Montpellier, France 32 o German Centre for Infection Research (DZIF), associated partner Charité 33 Universitätsmedizin Berlin, 10117 Berlin, Germany 34 35 Running title: Genetic diversity of bat rotaviruses 36 37 #Address correspondence to Jelle Matthijnssens, [email protected]; Jan 38 Felix Drexler: [email protected] 39 40 Ceren Simsek, Victor Max Corman and Hermann Ulrich Everling contributed equally to 41 this work. Author order was determined on mutual agreement. 42 43 *Present address: Laboratory of Virology, Rocky Mountain Laboratories, Division of 44 Intramural Research, National Institute of Allergy and Infectious Diseases, National 45 Institutes of Health, Hamilton, Montana, USA 46 47 Abstract: 236 words 48 Text: 4037 words 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.08.13.250464; this version posted October 26, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 49 ABSTRACT 50 Bats host many viruses pathogenic to humans, and increasing evidence suggests that 51 Rotavirus A (RVA) also belongs to this list. Rotaviruses cause diarrheal disease in many 52 mammals and birds, and their segmented genomes allow them to reassort and increase 53 their genetic diversity. Eighteen out of 2,142 bat fecal samples (0.8%) collected from 54 Europe, Central America and Africa were PCR-positive for RVA and 11 of those were 55 fully characterized using viral metagenomics. Upon contrasting their genomes with 56 publicly available data, at least 7 distinct bat RVA genotype constellations (GCs) were 57 identified, including evidence of reassortments and 6 novel genotypes. Some of these 58 constellations are spread across the world, whereas others appear to be geographically 59 restricted. Our analyses also suggest that several unusual human and equine RVA 60 strains might be of bat RVA origin, based on their phylogenetic clustering, despite 61 varying levels of nucleotide sequence identities between them. Although SA11 is one of 62 the most widely used reference strains for RVA research and forms the backbone of a 63 reverse genetics system, its origin remained enigmatic. Remarkably, the majority of the 64 genotypes of SA11-like strains were shared with Gabonese bat RVAs, suggesting a 65 potential common origin. Overall, our findings suggest an underexplored genetic 66 diversity of RVAs in bats, which is likely only the tip of the iceberg. Increasing contact 67 between humans and bat wildlife will further increase the zoonosis risk, which warrants 68 closer attention to these viruses. 69 70 Importance 71 The increased research on bat coronaviruses after SARS-CoV and MERS-CoVallowed 72 the very rapid identification of SARS-CoV-2. This is an excellent example of the 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.08.13.250464; this version posted October 26, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 73 importance of knowing viruses harbored by wildlife in general and bats in particular, for 74 global preparedness against emerging viral pathogens. The current effort to characterize 75 bat rotavirus strains from 3 continents shed light on the vast genetic diversity of 76 rotaviruses and also hinted at a bat origin for several atypical rotaviruses in humans and 77 animals, implying that zoonoses of bat rotaviruses might occur more frequently than 78 currently realized. 79 80 81 Keywords: Viral metagenomics, bat rotavirus, rotavirus genetic diversity, SA11, 82 zoonosis 83 84 85 Author Contributions 86 C.D, J.F.D, J.M and M.V.R designed the research; V.M.C., H.U.E., A.N.L., A.R., G.D.M., 87 T.B., F.G.R., A.SH., S.Y., A.S, S.O., Y.A.S., P.V., M.B. and E.M.L. were involved in 88 sample collection; V.M.C., H.U.E., A.N.L. and C.S. performed the research; C.S., D.J., 89 L.B., W.D., H.U.E., V.M.C. and K.C.Y. contributed in data analysis; J.F.D., C.D., C.S. 90 and J.M. drafted the paper; final version was approved by all co-authors. 91 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.08.13.250464; this version posted October 26, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 92 INTRODUCTION 93 Rotaviruses are the leading cause of diarrheal disease in the young of mammals and 94 birds. In humans, rotaviruses are responsible for 122,000-216,000 deaths in under 5- 95 year old infants on a yearly basis, mainly in developing countries (1). The Rotavirus 96 genus belongs to the family Reoviridae and contains 9 species designated as A-I (RVA- 97 RVI). The rotavirus genome consists of 11 dsRNA segments encoding 6 structural viral 98 proteins (VP1-6) and 6 non-structural proteins (NSP1-6) (2). 99 The RVA outer capsid antigens, VP4 and VP7 are used for a dual classification system 100 defining P-genotype (VP4 is Protease sensitive) and G-genotype (VP7 is Glycosylated), 101 respectively (2). However, as gene reassortment is a common phenomenon for viruses 102 with a segmented genome after co-infection, a more comprehensive classification 103 approach became necessary to better account for the genome evolution and genetic 104 diversity of RVAs. In 2008, a nucleotide sequence-based, complete genome 105 classification system was developed for RVA, define genotypes for each of the 11 gene 106 segment. These genotypes allowed extending the dual classification to full ‘genotype 107 constellations’ classification (3, 4). The gene assignments are reported as Gx-P[x]-Ix-Rx- 108 Cx-Mx-Ax-Nx-Tx-Ex-Hx, where ‘x’ denotes the particular genotype. The Rotavirus 109 Classification Working Group (RCWG) was formed in order to assign new genotypes to 110 rotavirus genes which could not be assigned to an established genotype (5). 111 Accumulating whole genome sequencing data demonstrate that there are typical GCs 112 present in most animal species. Two of them, Wa-like and DS-1-like, are responsible for 113 most of the human disease and designated as I1-R1-C1-M1-A1-N1-T1-E1-H1 and I2- 114 R2-C2-M2-A2-N2-T2-E2-H2, respectively, for the non-G/P genotypes (3). Furthermore, 115 various animal species are known to have specific GCs such as I2-R2-C2-M2- 5 bioRxiv preprint doi: https://doi.org/10.1101/2020.08.13.250464; this version posted October 26, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license.
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