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Evolutionary Origins of Enteric Hepatitis Viruses Downloaded from http://perspectivesinmedicine.cshlp.org/ on September 26, 2021 - Published by Cold Spring Harbor Laboratory Press Evolutionary Origins of Enteric Hepatitis Viruses Anna-Lena Sander,1,2 Victor Max Corman,1,2 Alexander N. Lukashev,3,4 and Jan Felix Drexler1,2 1Charité-Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Institute of Virology, Berlin 10117, Germany 2German Center for Infection Research (DZIF), Germany 3Martsinovsky Institute of Medical Parasitology, Tropical and Vector Borne Diseases, Sechenov University, 119991 Moscow, Russia 4Chumakov Federal Scientific Center for Research and Development of Immune-and-Biological Preparations, 142782 Moscow, Russia Correspondence: [email protected] The enterically transmitted hepatitis A (HAV) and hepatitis E viruses (HEV) are the leading causes of acute viral hepatitis in humans. Despite the discovery of HAVand HEV 40–50 years ago, their evolutionary origins remain unclear. Recent discoveries of numerous nonprimate hepatoviruses and hepeviruses allow revisiting the evolutionary history of these viruses. In this review, we provide detailed phylogenomic analyses of primate and nonprimate hepato- viruses and hepeviruses. We identify conserved and divergent genomic properties and cor- roborate historical interspecies transmissions by phylogenetic comparisons and recombina- tion analyses. We discuss the likely non-recent origins of human HAV and HEV precursors carried by mammals other than primates, and detail current zoonotic HEV infections. The novel nonprimate hepatoviruses and hepeviruses offer exciting new possibilities for future research focusing on host range and the unique biological properties of HAV and HEV. epatitis Avirus (HAV) and hepatitis E virus tions in the world are acquired through contam- H(HEV) are the most common causes of inated water and food (Sattar et al. 2000; Guth- acute viral hepatitis in humans, infecting mil- mann et al. 2006; Renou et al. 2014). lions and causing about 11,000 and 44,000 HAV is classified within the genus Hepato- deaths worldwide, respectively (WHO 2017). virus of the family Picornaviridae (Cristina and www.perspectivesinmedicine.org HAV and HEV were identified in the early Costa-Mattioli 2007), whereas HEV is within days of hepatitis virus discovery about 40–50 the genus Orthohepevirus of the family Hepevir- years ago (Feinstone et al. 1973; Balayan et al. idae (Smith et al. 2014). Although these viruses 1983). During the route to discovery of HAV, an are classified within different virus families, they epidemiological link to animals was suspected share unique biological properties. Recent stud- (Robertson 2001). However, zoonotic transmis- ies reveal that HAV and HEV occur as typical sion is not known for HAV. In contrast, infec- nonenveloped viruses in feces. In contrast, in tions with certain HEV genotypes can be zoo- blood they can exist as lipid-layered particles, notic in temperate climates (Dalton et al. 2008). challenging the concept that viruses are either However, the majority of HAV and HEV infec- enveloped or nonenveloped, and implying spe- Editors: Stanley M. Lemon and Christopher Walker Additional Perspectives on Enteric Hepatitis Viruses available at www.perspectivesinmedicine.org Copyright © 2018 Cold Spring Harbor Laboratory Press; all rights reserved Advanced Online Article. Cite this article as Cold Spring Harb Perspect Med doi: 10.1101/cshperspect.a031690 1 Downloaded from http://perspectivesinmedicine.cshlp.org/ on September 26, 2021 - Published by Cold Spring Harbor Laboratory Press A.-L. Sander et al. cial cellular entry mechanisms (Takahashi et al. (Carnivora). Despite the hugely increased diver- 2010; Feng et al. 2013). sity of the genus, classification of all novel he- Nonprimate HEV-related viruses have been patoviruses within a single genus is warranted identified in even-toed ungulates, rodents, bats, by considerably larger sequence distances to and fish over recent decades (Meng 2010; Drex- the next closely related Picornaviridae genus ler et al. 2012b; Smith et al. 2014). In contrast, Tremovirus (Drexler et al. 2015) and criteria for the existence of nonprimate hepatoviruses was picornavirus classification from the ICTV (Zell only discovered recently (Drexler et al. 2015). et al. 2017). The recent expansion of the spectrum of non- As shown in Figure 1B, the genetic diversity primate hepatoviruses and hepeviruses enables of hepeviruses exceeds the known diversity of new insights into the evolutionary history of hepatoviruses. This is consistent with their clas- HAV and HEV. sification as a family (note that the scale of the hepevirus phylogeny is about twice that of the hepatovirus phylogeny). As for HAV, hepevi- EXPANSION OF THE KNOWN GENETIC ruses infecting humans represent only a small DIVERSITY OF HEPATOVIRUSES AND proportion of the known virus diversity. They HEPEVIRUSES are classified within a single species termed Or- Until recently, the genus Hepatovirus contained thohepevirus A, which currently comprises eight only the species HAV comprising six genotypes. HEV genotypes. HEV gt1 and gt2 are found in Genotypes (gt)I–III infect humans, and gtIV– humans only, whereas HEV gt3 and gt4 infect gtVI were found sporadically in different species humans, even-toed ungulates (mainly pigs), rab- of Old World monkeys (Cristina and Costa-Mat- bits, and small carnivores. HEV gt5 and gt6 are tioli 2007). As shown in Figure 1A, primate associated with pigs and wild boars (Smith et al. HAVs now represent only a small fraction of 2016), and HEV gt7 and gt8 are associated with the hepatovirus genetic diversity. In 2015, 13 camelids (Woo et al. 2014, 2016; Rasche et al. new putative Hepatovirus species were reported 2016a). As for HAV, a huge diversity of nonpri- from various small mammals, representing >20 mate viruses defines the genetic space of the different mammalian species and three orders family Hepeviridae, including at least three ad- (Drexler et al. 2015). Another two novel hepato- ditional Orthohepevirus species and as-yet-un- viruses were described from seals in the United classified hepeviruses from a moose, falcon, and States (Anthony et al. 2015) and from Chinese tree shrew (National Library of Medicine (US) woodchucks (Yu et al. 2016). Finally, another NCBI, 1988a, Accession No. KR_905549.1; Lin new hepatovirus was identified in a tree shrew et al. 2014; Reuter et al. 2016). In sum, unique www.perspectivesinmedicine.org during transcriptome sequencing (National Li- orthohepeviruses have been found in eight dis- brary of Medicine (US) NCBI, 1988b, Accession tinct mammalian host orders, including several No. KT_877158.1). The expanded genus Hepa- orders in which hepatoviruses have also been tovirus now comprises nine species named found (Primates, Scandentia, Rodentia, Carniv- Hepatovirus A (HAV) through Hepatovirus I ora, Chiroptera), as well as even-toed ungulates according to the International Committee on including pigs, camels, deer, cattle, swine, moose the Taxonomy of Viruses (ICTV) (Zell et al. (Artiodactyla), rabbits (Lagomorpha), and birds 2017). Another seven putative Hepatovirus spe- (Aves). A sister genus termed Piscihepevirus is cies can be predicted using partial genomic data defined by a trout hepevirus (Batts et al. 2011; as a surrogate criterion for species delineation Smith et al. 2014). (Drexler et al. 2015). These 16 putative virus species were recovered from six different orders THE DIFFERENT RELEVANCE OF ANIMAL of mammalian hosts, including humans and RESERVOIRS FOR HUMAN INFECTIONS monkeys (order Primates), rodents (Rodentia), a tree shrew (Scandentia), bats (Chiroptera), Despite the diversity of animal hepatoviruses, hedgehogs and shrews (Eulipotyphla), and seals so far no zoonotic transmission of HAV has 2 Advanced Online Article. Cite this article as Cold Spring Harb Perspect Med doi: 10.1101/cshperspect.a031690 Downloaded from http://perspectivesinmedicine.cshlp.org/ on September 26, 2021 - Published by Cold Spring Harbor Laboratory Press A gtIII gtII gtV gtI HAV 1.0 Tremovirus B gt1 gt4 gt6 gt5 gt2 gt7 gt8 Orthohepe C gt3 Orthohepe B HEV 1.0 Piscihepevirus Orthohepe A Orthohepe D M73218 H. sap. gt1a C M73218 H. sap. gt1a M74506 H. sap. gt2a M74506 H. sap. gt2a AB290312 S. scr. gt3 KC618403 H. sap. JQ953664 S. scr. gt3 FJ705359 S. scr. gt3c HEV HEV JQ013794 H. sap. gt3h KJ701409 H. sap. KC618403 H. sap. ORF 1 FJ998008 S. scr. gt3i ORF 2 FJ705359 S. scr. gt3c 0.5 JQ013794 H. sap. gt3h 0.5 KJ701409 H. sap. AB290312 S. scr. gt3 FJ998008 S. scr. gt3i JQ953664 S. scr. gt3 AB189072 H. sap. AB189072 H. sap. AB189071 C. nip. AB189070 S. scr. AB189070 S. scr. AB189071 C. nip. AB248520 H. sap. AB248520 H. sap. AB780453 S. scr. AB780453 S. scr. JQ953665 S. scr. JQ953665 S. scr. JQ013793 H. sap. JQ013793 H. sap. FJ906895 O. cun. gt3ra FJ906895 O. cun. gt3ra JQ013792 O. cun. JQ013792 O. cun. KJ496144 C. dro. gt7 HQ634346 H. sap. KT818608 H. sap. EU366959 S. scr. KJ496143 C. dro. gt7a GU119960 S. scr. GU119960 S. scr. AB197673 H. sap. gt4a AB197673 H. sap. gt4a DQ450072 S. scr. gt4i HQ634346 H. sap. AY594199 S. scr. EU366959 S. scr. AJ272108 H. sap. gt4d FJ610232 S. scr. FJ610232 S. scr. AY594199 S. scr. KT818608 H. sap. AJ272108 H. sap. gt4d KJ496144 C. dro. gt7 DQ450072 S. scr. gt4i KJ496143 C. dro. gt7a Figure 1. Genetic diversity of hepatoviruses and hepeviruses and evidence for zoonotic transmission of hepevi- ruses to humans. (A) Bayesian phylogeny of the full genome of hepatoviruses.
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