Ancient evolutionary origins of hepatitis E virus in rodents
Jo W.K. Cassiano M.H.A. de Oliveira-Filho E.F. Brünink S. Yansanjav A. Yihune M. Koshkina A.I. Lukashev A.N. Lavrenchenko L.A. Lebedev V.S. Olayemi A. Bangura U. Salas-Rojas M. Aguilar-Setién Á. Fichet-Calvet E. Drexler J.F.
17 December 2024National Academy of Sciences
Proceedings of the National Academy of Sciences of the United States of America
2024#121Issue 51
Hepatitis E virus (HEV; family Hepeviridae) infections cause >40,000 human deaths annually. Zoonotic infections predominantly originate from ungulates and occasionally from rats, highlighting the zoonotic potential of rodent-associated hepeviruses. We conducted host genomic data mining and uncovered two genetically divergent rodent-associated hepeviruses, and two bat-associated hepeviruses genetically related to known bat-associated strains. We thus analyzed 2,565 liver specimens from 108 rodent and shrew species sampled from globally understudied regions and hosts in Africa, Asia, and Latin America during 2011-2018 for hepeviruses by RT–PCR. We detected 63 positive field samples (2.5%, 95% CI 1.9-3.1) from 14 animal species, including two coinfections with genetically divergent strains and significant variation (X2, P < 0.001) in detection rates between study sites. Strain-specific qRT–PCR assays showed virus concentrations between 9.2 × 102 and 3.2 × 109 copies/g. We recovered 24 near-complete hepeviral genomes from rodents, shrews, and bats, all showing three partially overlapping open reading frames (ORFs), some including putative late domains that may be associated with quasi-envelopment. Rodent-derived hepeviruses grouped into five clades clustering in basal sister relationship to human- (31 to 84% distance in translated ORF1-3) and rat-associated HEV. Parsimony-based analyses and cophylogenetic reconciliations revealed that rodents were predominant sources of hepeviral cross-order host shifts. Bayesian ancestral state reconstructions substantiated a direct origin of human-associated HEV in ungulates such as swine and camelids (posterior probability 0.8), whereas the nonrecent evolutionary origins of human- and ungulate-associated HEV were projected to rodent hosts (posterior probability > 0.9). Our results elucidate the genealogy of human HEV and warrant increased surveillance and experimental risk assessments for rodent-associated hepeviruses. Copyright
evolution , hepatitis E virus , host , rodent , zoonosis
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Institute of Virology, Charité-Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Berlin, 10117, Germany
Mammalian Ecology Laboratory, Institute of Biology, Mongolian Academy of Sciences, Ulaanbaatar, 13330, Mongolia
Department of Zoological Sciences, Addis Ababa University, Addis Ababa, 1176, Ethiopia
Association for the Conservation of Biodiversity of Kazakhstan, Astana, 010000, Kazakhstan
Martsinovsky Institute of Medical Parasitology, Tropical and Vector Borne Diseases, Sechenov First Moscow State Medical University, Moscow, 119435, Russian Federation
Department of Mammalian Microevolution, Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, 119071, Russian Federation
Zoological Museum, Moscow State University, Moscow, 125009, Russian Federation
Natural History Museum, Obafemi Awolowo University, Osun State, Ile-Ife, 220005, Nigeria
Department of Public Health, College of Medical Sciences, Njala University, Bo, 232032, Sierra Leone
Implementation Research/Zoonoses Control, Bernhard Nocht Institute for Tropical Medicine, Hamburg, 20324, Germany
Unidad de Investigación Médica en Inmunología, Hospital de Pediatría, Centro Médico Nacional “Siglo XXI”, Instituto Mexicano del Seguro Social, Mexico City, 06720, Mexico
German Centre for Infection Research (DZIF), Charité-Universitätsmedizin Berlin, Berlin, 10117, Germany
Institute of Virology
Mammalian Ecology Laboratory
Department of Zoological Sciences
Association for the Conservation of Biodiversity of Kazakhstan
Martsinovsky Institute of Medical Parasitology
Department of Mammalian Microevolution
Zoological Museum
Natural History Museum
Department of Public Health
Implementation Research/Zoonoses Control
Unidad de Investigación Médica en Inmunología
German Centre for Infection Research (DZIF)
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