Multiple Mammarenaviruses Circulating in Angolan Rodents
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
34070551
PubMed Central
PMC8227972
DOI
10.3390/v13060982
PII: v13060982
Knihovny.cz E-zdroje
- Klíčová slova
- Angola, Mastomys natalensis, Micaelamys namaquensis, Mus triton, hantaviruses, mammarenaviruses, phylogeny,
- MeSH
- Arenaviridae klasifikace genetika MeSH
- fylogeneze MeSH
- genom virový MeSH
- infekce viry z čeledi Arenaviridae veterinární MeSH
- lékařská geografie MeSH
- prevalence MeSH
- RNA virová MeSH
- sekvenování celého genomu MeSH
- zdroje nemoci virologie MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- RNA virová MeSH
Rodents are a speciose group of mammals with strong zoonotic potential. Some parts of Africa are still underexplored for the occurrence of rodent-borne pathogens, despite this high potential. Angola is at the convergence of three major biogeographical regions of sub-Saharan Africa, each harbouring a specific rodent community. This rodent-rich area is, therefore, strategic for studying the diversity and evolution of rodent-borne viruses. In this study we examined 290 small mammals, almost all rodents, for the presence of mammarenavirus and hantavirus RNA. While no hantavirus was detected, we found three rodent species positive for distinct mammarenaviruses with a particularly high prevalence in Namaqua rock rats (Micaelamys namaquensis). We characterised four complete virus genomes, which showed typical mammarenavirus organisation. Phylogenetic and genetic distance analyses revealed: (i) the presence of a significantly divergent strain of Luna virus in Angolan representatives of the ubiquitous Natal multimammate mouse (Mastomys natalensis), (ii) a novel Okahandja-related virus associated with the Angolan lineage of Micaelamys namaquensis for which we propose the name Bitu virus (BITV) and (iii) the occurrence of a novel Mobala-like mammarenavirus in the grey-bellied pygmy mouse (Mus triton) for which we propose the name Kwanza virus (KWAV). This high virus diversity in a limited host sample size and in a relatively small geographical area supports the idea that Angola is a hotspot for mammarenavirus diversity.
Department of Botany and Zoology Faculty of Science Masaryk University 611 37 Brno Czech Republic
Institute of Vertebrate Biology of the Czech Academy of Sciences 603 65 Brno Czech Republic
Zobrazit více v PubMed
Shi M., Lin X.D., Chen X., Tian J.H., Chen L.J., Li K., Wang W., Eden J.S., Shen J.J., Liu L., et al. Author Correction: The evolutionary history of vertebrate RNA viruses. Nat. Cell Biol. 2018;561:E6. doi: 10.1038/s41586-018-0310-0. PubMed DOI
Mordecai G.J., Miller K.M., Di Cicco E., Schulze A.D., Kaukinen K.H., Ming T.J., Li S., Tabata A., Teffer A., A Patterson D., et al. Endangered wild salmon infected by newly discovered viruses. eLife. 2019;8:47615. doi: 10.7554/eLife.47615. PubMed DOI PMC
Dietz J., Kolesnik E., Heckers K.O., Klingberg M.N., Marschang R.E. Detection of an arenavirus in a group of captive wagler’s pit vipers (tropidolaemus wagleri) J. Zoo Wildl. Med. 2020;51:236–240. doi: 10.1638/2018-0179. PubMed DOI
Downs W.G., Anderson C.R., Spence L., Aitken T.H.G., Greenhall A.H. Tacaribe Virus, a New Agent Isolated from Artibeus Bats and Mosquitoes in Trinidad, West Indies. Am. J. Trop. Med. Hyg. 1963;12:640–646. doi: 10.4269/ajtmh.1963.12.640. PubMed DOI
Wu Z., Du J., Lu L., Yang L., Dong J., Sun L., Zhu Y., Liu Q., Jin Q. Detection of Hantaviruses and Arenaviruzses in three-toed jerboas from the Inner Mongolia Autonomous Region, China. Emerg. Microbes Infect. 2018;7:1–3. doi: 10.1038/s41426-018-0036-y. PubMed DOI PMC
Radoshitzky S.R., Buchmeier M.J., Charrel R.N., Clegg J.C.S., Gonzalez J.-P.J., Günther S., Hepojoki J., Kuhn J.H., Lukashevich I.S., Romanowski V., et al. ICTV Virus Taxonomy Profile: Arenaviridae. J. Gen. Virol. 2019;100:1200–1201. doi: 10.1099/jgv.0.001280. PubMed DOI
Frame J.D., Baldwin J.M., Gocke D.J., Troup J.M. Lassa Fever, a New Virus Disease of Man from West Africa. I. Clinical description and pathological findings. Am. J. Trop. Med. Hyg. 1970;19:670–676. doi: 10.4269/ajtmh.1970.19.670. PubMed DOI
Briese T., Paweska J.T., McMullan L., Hutchison S.K., Street C., Palacios G., Khristova M.L., Weyer J., Swanepoel R., Egholm M., et al. Genetic Detection and Characterization of Lujo Virus, a New Hemorrhagic Fever–Associated Arenavirus from Southern Africa. PLoS Pathog. 2009;5:e1000455. doi: 10.1371/journal.ppat.1000455. PubMed DOI PMC
Kronmann K.C., Nimo-Paintsil S., Guirguis F., Kronmann L.C., Bonney K., Obiri-Danso K., Ampofo W., Fichet-Calvet E. Two Novel Arenaviruses Detected in Pygmy Mice, Ghana. Emerg. Infect. Dis. 2013;19:1832–1835. doi: 10.3201/eid1911.121491. PubMed DOI PMC
Olayemi A., Cadar D., Magassouba N., Obadare A., Kourouma F., Oyeyiola A., Fasogbon S., Igbokwe J., Rieger T., Bockholt S., et al. New Hosts of The Lassa Virus. Sci. Rep. 2016;6:25280. doi: 10.1038/srep25280. PubMed DOI PMC
Meheretu Y., Čížková D., Těšíková J., Welegerima K., Tomas Z., Kidane D., Girmay K., Schmidt-Chanasit J., Bryja J., Günther S., et al. High Diversity of RNA Viruses in Rodents, Ethiopia. Emerg. Infect. Dis. 2012;18:2047–2050. doi: 10.3201/eid1812.120596. PubMed DOI PMC
Goüy de Bellocq J., Borremans B., Katakweba A., Makundi R., Baird S.J., Becker-Ziaja B., Günther S., Leirs H. Sympatric Occurrence of 3 Arenaviruses, Tanzania. Emerg. Infect. Dis. 2010;16:692–695. doi: 10.3201/eid1604.091721. PubMed DOI PMC
Palacios G., Savji N., Hui J., Da Rosa A.T., Popov V., Briese T., Tesh R., Lipkin W.I. Genomic and phylogenetic characterization of Merino Walk virus, a novel arenavirus isolated in South Africa. J. Gen. Virol. 2010;91:1315–1324. doi: 10.1099/vir.0.017798-0. PubMed DOI PMC
Witkowski P.T., Kallies R., Hoveka J., Auste B., Ithete N.L., Šoltys K., Szemes T., Drosten C., Preiser W., Klempa B., et al. Novel Arenavirus Isolates from Namaqua Rock Mice, Namibia, Southern Africa. Emerg. Infect. Dis. 2015;21:1213–1216. doi: 10.3201/eid2107.141341. PubMed DOI PMC
Gonzalez J.P., McCormick J.B., Saluzzo J.F., Herve J.P., Georges A.J., Johnson K.M. An Arenavirus Isolated from Wild-Caught Rodents (Praomys Species) in the Central African Republic. Intervirology. 1983;19:105–112. doi: 10.1159/000149344. PubMed DOI
N′Dilimabaka N., Berthet N., Rougeron V., Mangombi J.B., Durand P., Maganga G.D., Bouchier C., Schneider B.S., Fair J., Renaud F., et al. Evidence of Lymphocytic Choriomeningitis Virus (LCMV) in Domestic Mice in Gabon: Risk of Emergence of LCMV Encephalitis in Central Africa. J. Virol. 2014;89:1456–1460. doi: 10.1128/JVI.01009-14. PubMed DOI PMC
Krásová J., Mikula O., Bryja J., Baptista N.L., António T., Aghová T., Šumbera R. Biogeography of Angolan rodents: The first glimpse based on phylogenetic evidence. Divers Distrib. 2021 under review.
Linder H.P., de Klerk H.M., Born J., Burgess N.D., Fjeldså J., Rahbek C. The partitioning of Africa: Statistically defined bio-geographical regions in sub-Saharan Africa. J. Biogeogr. 2012;39:1189–1205. doi: 10.1111/j.1365-2699.2012.02728.x. DOI
Colangelo P., Verheyen E., Leirs H., Tatard C., Denys C., Dobigny G., Duplantier J.-M., Brouat C., Granjon L., Lecompte E. A mitochondrial phylogeographic scenario for the most widespread African rodent, Mastomys natalensis. Biol. J. Linn. Soc. 2013;108:901–916. doi: 10.1111/bij.12013. DOI
Ishii A., Thomas Y., Moonga L., Nakamura I., Ohnuma A., Hang’Ombe B.M., Takada A.S., Mweene A., Sawa H. Novel Arenavirus, Zambia. Emerg. Infect. Dis. 2011;17:1921–1924. doi: 10.3201/eid1710.10452. PubMed DOI PMC
Cuypers L.N., Baird S.J.E., Hánová A., Locus T., Katakweba A.S., Gryseels S., Bryja J., Leirs H., Goüy de Bellocq J. Three arenaviruses in three subspecific natal multimammate mouse taxa in Tanzania: Same host specificity, but different spatial genetic structure? Virus Evol. 2020;6 doi: 10.1093/ve/veaa039. PubMed DOI PMC
Wulff H., McIntosh B.M., Hamner D.B., Johnson K.M. Isolation of an arenavirus closely related to Lassa virus from Masto-mys natalensis in south-east Africa. Bull. World Health Organ. 1977;55:441–444. PubMed PMC
Johnson K.M., Taylor P., Elliott L.H., Tomori O. Recovery of a Lassa-Related Arenavirus in Zimbabwe. Am. J. Trop. Med. Hyg. 1981;30:1291–1293. doi: 10.4269/ajtmh.1981.30.1291. PubMed DOI
Ishii A., Orba Y., Sasaki M., Kobayashi S., Moonga L., Hang’ombe B.M., Mweene A.S., Omori R., Ito K., Hall W.W., et al. ICTV Taxonomic Proposal 2016.019aM.A.v2.Mammarenavirus_sp. Create Species Solwezi Mamma-Renavirus in the Genus Mammarenavirus, Family Arenaviridae. [(accessed on 18 July 2016)];2016 Available online: http://www.ictv.global/proposals-16/2016.019aM.A.v2.Mammarenavirus_sp.pdf.
Bryja J., Šumbera R., Peterhans J.C.K., Aghová T., Bryjová A., Mikula O., Nicolas V., Denys C., Verheyen E. Evolutionary history of the thicket rats (genus Grammomys ) mirrors the evolution of African forests since late Miocene. J. Biogeogr. 2017;44:182–194. doi: 10.1111/jbi.12890. DOI
Klempa B., Fichet-Calvet E., Lecompte E., Auste B., Aniskin V., Meisel H., Denys C., Koivogui L., Ter Meulen J., Krüger D.H. Hantavirus in African Wood Mouse, Guinea. Emerg. Infect. Dis. 2006;12:838–840. doi: 10.3201/eid1205.051487. PubMed DOI PMC
Gonzalez J.P., McCormick J.B., Baudon D., Gautun J.P., Meunier D.Y., Dournon E., Georges A.J. Serological Evidence for Hantaan-related virus in Africa. Lancet. 1984;2:1036–1037. doi: 10.1016/S0140-6736(84)91130-9. PubMed DOI
Sumibcay L., Kadjo B., Gu S.H., Kang H.J., Lim B.K., Cook J.A., Song J.W., Yanagihara R. Divergent lineage of a novel hantavirus in the banana pipistrelle (Neoromicia nanus) in Côte d’Ivoire. Virol. J. 2012;9:34. doi: 10.1186/1743-422X-9-34. PubMed DOI PMC
Weiss S., Witkowski P.T., Auste B., Nowak K., Weber N., Fahr J., Mombouli J.-V., Wolfe N.D., Drexler J.F., Drosten C., et al. Hantavirus in Bat, Sierra Leone. Emerg. Infect. Dis. 2012;18:159–161. doi: 10.3201/eid1801.111026. PubMed DOI PMC
Witkowski P.T., Drexler J.F., Kallies R., Ličková M., Bokorová S., Mananga G.D., Szemes T., Leroy E.M., Krüger D.H., Drosten C., et al. Phylogenetic analysis of a newfound bat-borne hantavirus supports a laurasiatherian host association for ancestral mammalian hantaviruses. Infect. Genet. Evol. 2016;41:113–119. doi: 10.1016/j.meegid.2016.03.036. PubMed DOI
Těšíková J., Bryjová A., Bryja J., Lavrenchenko L.A., Goüy de Bellocq J. Hantavirus Strains in East Africa Related to Western African Hantaviruses. Vector-Borne Zoonotic Dis. 2017;17:278–280. doi: 10.1089/vbz.2016.2022. PubMed DOI
Klempa B., Fichet-Calvet E., Lecompte E., Auste B., Aniskin V., Meisel H., Barrière P., Koivogui L., Ter Meulen J., Krüger D.H. Novel Hantavirus Sequences in Shrew, Guinea. Emerg. Infect. Dis. 2007;13:520–522. doi: 10.3201/eid1303.061198. PubMed DOI PMC
Kang H.J., Kadjo B., Dubey S., Jacquet F., Yanagihara R. Molecular evolution of Azagny virus, a newfound hantavirus harbored by the West African pygmy shrew (Crocidura obscurior) in Côte d’Ivoire. Virol. J. 2011;8:373. doi: 10.1186/1743-422X-8-373. PubMed DOI PMC
Gu S.H., Nicolas V., Lalis A., Sathirapongsasuti N., Yanagihara R. Complete genome sequence and molecular phylogeny of a newfound hantavirus harbored by the Doucet’s musk shrew (Crocidura douceti) in Guinea. Infect. Genet. Evol. 2013;20:118–123. doi: 10.1016/j.meegid.2013.08.016. PubMed DOI PMC
Kang H.J., Stanley W.T., Esselstyn J.A., Gu S.H., Yanagihara R. Expanded Host Diversity and Geographic Distribution of Hantaviruses in Sub-Saharan Africa. J. Virol. 2014;88:7663–7667. doi: 10.1128/JVI.00285-14. PubMed DOI PMC
Meheretu Y., Stanley W.T., Craig E.W., Goüy de Bellocq J., Bryja J., Leirs H., Pahlmann M., Günther S. Tigray Orthohantavirus Infects Two Related Rodent Species Adapted to Different Elevations in Ethiopia. Vector-Borne Zoonotic Dis. 2019;19:950–953. doi: 10.1089/vbz.2019.2452. PubMed DOI PMC
Diagne M.M., Dieng I., Granjon L., Lucaccioni H., Sow A., Ndiaye O., Faye M., Bâ K., Bâ Y., Diallo M., et al. Seoul Orthohantavirus in Wild Black Rats, Senegal, 2012–2013. Emerg. Infect. Dis. 2020;26:2460–2464. doi: 10.3201/eid2610.201306. PubMed DOI PMC
Irwin D.M., Kocher T.D., Wilson A.C. Evolution of the cytochromeb gene of mammals. J. Mol. Evol. 1991;32:128–144. doi: 10.1007/BF02515385. PubMed DOI
Krásová J., Mikula O., Mazoch V., Bryja J., Říčan O., Šumbera R. Evolution of the Grey-bellied pygmy mouse group: Highly structured molecular diversity with predictable geographic ranges but morphological crypsis. Mol. Phylogenetics Evol. 2019;130:143–155. doi: 10.1016/j.ympev.2018.10.016. PubMed DOI
Vieth S., Drosten C., Lenz O., Vincent M., Omilabu S., Hass M., Becker-Ziaja B., Ter Meulen J., Nichol S.T., Schmitz H., et al. RT-PCR assay for detection of Lassa virus and related Old World arenaviruses targeting the L gene. Trans. R. Soc. Trop. Med. Hyg. 2007;101:1253–1264. doi: 10.1016/j.trstmh.2005.03.018. PubMed DOI
Ehichioya D.U., Hass M., Becker-Ziaja B., Ehimuan J., Asogun D.A., Fichet-Calvet E., Kleinsteuber K., Lelke M., Ter Meulen J., Akpede G.O., et al. Current Molecular Epidemiology of Lassa Virus in Nigeria. J. Clin. Microbiol. 2010;49:1157–1161. doi: 10.1128/JCM.01891-10. PubMed DOI PMC
Rózsa L., Reiczigel J., Majoros G. Quantifying parasites in samples of hosts. J. Parasitol. 2000;86:228–232. doi: 10.1645/0022-3395(2000)086[0228:QPISOH]2.0.CO;2. PubMed DOI
Reiczigel J. Confidence intervals for the binomial parameter: Some new considerations. Stat. Med. 2003;22:611–621. doi: 10.1002/sim.1320. PubMed DOI
Goüy de Bellocq J., Bryjová A., Martynov A.A., Lavrenchenko L.A. Dhati Welel virus, the missing mammarenavirus of the widespread Mastomys natalensis. J. Vertebr. Biol. 2020;69:1–11. doi: 10.25225/jvb.20018. DOI
Andrews S. Babraham Bioinformatics. Babraham Institute; Cambridge, UK: 2010. FastQC: A quality control tool for high throughput sequence data.
Jiang H., Lei R., Ding S.-W., Zhu S. Skewer: A fast and accurate adapter trimmer for next-generation sequencing paired-end reads. BMC Bioinform. 2014;15:182. doi: 10.1186/1471-2105-15-182. PubMed DOI PMC
Bankevich A., Nurk S., Antipov D., Gurevich A.A., Dvorkin M., Kulikov A.S., Lesin V.M., Nikolenko S.I., Pham S., Prjibelski A.D., et al. SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing. J. Comput. Biol. 2012;19:455–477. doi: 10.1089/cmb.2012.0021. PubMed DOI PMC
Laetsch D.R., Blaxter M.L. BlobTools: Interrogation of genome assemblies [version 1; peer review: 2 approved with reservations] F1000Research. 2017;6:1287. doi: 10.12688/f1000research.12232.1. DOI
Edgar R.C. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–1797. doi: 10.1093/nar/gkh340. PubMed DOI PMC
Miller M.A., Pfeiffer W., Schwartz T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees; Proceedings of the Gateway Computing Environments Workshop (GCE); New Orleans, LA, USA. 14 November 2010; Nov 14, pp. 1–8.
Darriba D., Taboada G.L., Doallo R., Posada D. jModelTest 2: More models, new heuristics and high-performance computing. Nat. Methods. 2012;9:772. doi: 10.1038/nmeth.2109. PubMed DOI PMC
Bao Y., Chetvernin V., Tatusova T. Improvements to pairwise sequence comparison (PASC): A genome-based web tool for virus classification. Arch. Virol. 2014;159:3293–3304. doi: 10.1007/s00705-014-2197-x. PubMed DOI PMC
Kumar S., Stecher G., Li M., Knyaz C., Tamura K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 2018;35:1547–1549. doi: 10.1093/molbev/msy096. PubMed DOI PMC
Morin B., Coutard B., Lelke M., Ferron F., Kerber R., Jamal S., Frangeul A., Baronti C., Charrel R., De Lamballerie X., et al. The N-Terminal Domain of the Arenavirus L Protein Is an RNA Endonuclease Essential in mRNA Transcription. PLoS Pathog. 2010;6:e1001038. doi: 10.1371/journal.ppat.1001038. PubMed DOI PMC
Whitton J.L., Tishon A., Lewicki H., Gebhard J., Cook T., Salvato M., Joly E., Oldstone M.B. Molecular analyses of a five-amino-acid cytotoxic T-lymphocyte (CTL) epitope: An immunodominant region which induces nonreciprocal CTL cross-reactivity. J. Virol. 1989;63:4303–4310. doi: 10.1128/JVI.63.10.4303-4310.1989. PubMed DOI PMC
Gonzalez J.P., Sanchez A., Rico-Hesse R. Molecular phylogeny of Guanarito virus, an emerging arenavirus affecting hu-mans. Am. J. Trop. Med. Hyg. 1995;53:1–6. doi: 10.4269/ajtmh.1995.53.1. PubMed DOI
Bonhomme C.J., Capul A.A., Lauron E.J., Bederka L.H., Knopp K.A., Buchmeier M.J. Glycosylation modulates arenavirus glycoprotein expression and function. Virology. 2011;409:223–233. doi: 10.1016/j.virol.2010.10.011. PubMed DOI PMC
Gryseels S., Rieger T., Oestereich L., Cuypers B., Borremans B., Makundi R., Leirs H., Günther S., Goüy de Bellocq J. Gairo virus, a novel arenavirus of the widespread Mastomys natalensis: Genetically divergent, but ecologically similar to Lassa and Morogoro viruses. Virology. 2015;476:249–256. doi: 10.1016/j.virol.2014.12.011. PubMed DOI
Nicolas V., Fabre P.-H., Bryja J., Denys C., Verheyen E., Missoup A.D., Olayemi A., Katuala P., Dudu A., Colyn M., et al. The phylogeny of the African wood mice (Muridae, Hylomyscus) based on complete mitochondrial genomes and five nuclear genes reveals their evolutionary history and undescribed diversity. Mol. Phylogenetics Evol. 2020;144:106703. doi: 10.1016/j.ympev.2019.106703. PubMed DOI
Russo I.-R.M., Chimimba C.T., Bloomer P. Bioregion heterogeneity correlates with extensive mitochondrial DNA diversity in the Namaqua rock mouse, Micaelamys namaquensis (Rodentia: Muridae) from southern Africa—Evidence for a species complex. BMC Evol. Biol. 2010;10:307. doi: 10.1186/1471-2148-10-307. PubMed DOI PMC
Ishii A., Thomas Y., Moonga L., Nakamura I., Ohnuma A., Hang’Ombe B.M., Takada A., Mweene A.S., Sawa H. Molecular surveillance and phylogenetic analysis of Old World arenaviruses in Zambia. J. Gen. Virol. 2012;93:2247–2251. doi: 10.1099/vir.0.044099-0. PubMed DOI
Lecompte E., Ter Meulen J., Emonet S., Daffis S., Charrel R.N. Genetic identification of Kodoko virus, a novel arenavirus of the African pigmy mouse (Mus Nannomys minutoides) in West Africa. Virology. 2007;364:178–183. doi: 10.1016/j.virol.2007.02.008. PubMed DOI
Coulibaly-N’Golo D., Allali B., Kouassi S.K., Fichet-Calvet E., Becker-Ziaja B., Rieger T., Ölschläger S., Dosso H., Denys C., Ter Meulen J., et al. Novel Arenavirus Sequences in Hylomyscus sp. and Mus (Nannomys) setulosus from Côte d’Ivoire: Implications for Evolution of Arenaviruses in Africa. PLoS ONE. 2011;6:e20893. doi: 10.1371/journal.pone.0020893. PubMed DOI PMC
Moreno H., Rastrojo A., Pryce R., Fedeli C., Zimmer G., Bowden T.A., Gerold G., Kunz S. A novel circulating tamiami mammarenavirus shows potential for zoonotic spillover. PLoS Negl. Trop. Dis. 2020;14:e0009004. doi: 10.1371/journal.pntd.0009004. PubMed DOI PMC