[en] Viruses belonging to the Family Dicistroviridae have attracted a great deal of attention from scientists owing to their negative impact on agricultural economics as well as their recent identification as potential aetiological agents of febrile illness in human patients. On the other hand, some Dicistrovirus are also studied for their potential biopesticide properties. To date, Dicistrovirus characterized in Africa mainland remain scarce. By using HTS technology on insectivorous bat faeces (Hipposideros Caffer) sampled in a cave used by humans to collect bat guano (bat manure) as fertilizer in Zimbabwe, we characterized the full-length sequences of three Dicistrovirus belonging to the Cripavirus and Aparavirus genus: Big Sioux River Virus-Like (BSRV-Like), Acute Bee Paralysis Virus (ABPV) and Aphid Lethal Paralysis Virus (ALPV). Phylogenetic analyses of ORF-1 and ORF-2 genes showed a complex evolutionary history between BSRV and close viruses as well as for the Aparavirus genus. We provide herewith the first evidence of the presence of Dicistrovirus in Zimbabwe and highlight the need to further document the impact of such viruses on crops as well as in beekeeping activities in Zimbabwe which represent a crucial source of income for Zimbabwean people.
Disciplines :
Zoology
Author, co-author :
Bourgarel, Mathieu
Noel, Valerie
Pfukenyi, Davies
Becquart, Pierre
Cerqueira, Frédérique
Barrachina, Célia
Boue, Vanina
Talignani, Loic
Matope, Gift
Misse, Dorothee
Morand, Serge
Liegeois, Florian
Michaux, Johan ; Université de Liège - ULiège > Département des sciences de la vie > Laboratoire de génétique de la conservation
Pan, X.; Cao, Z.; Yuan, J.; Shi, Z.; Yuan, X.; Lin, L.; Xu, Y.; Yao, J.; Hao, G.; Shen, J. Isolation and characterization of a novel dicistrovirus associated with moralities of the great freshwater prawn, Macrobrachium rosenbergii. Int. J. Mol. Sci. 2016, 17, 204. [CrossRef]
Tantillo, G.; Bottaro, M.; Di Pinto, A.; Martella, V.; Di Pinto, P.; Terio, V. Virus infections of honeybees Apis Mellifera. Ital. J. Food Saf. 2015, 4, 5364. [CrossRef]
Victoria, J.G.; Kapoor, A.; Li, L.; Blinkova, O.; Slikas, B.; Wang, C.; Naeem, A.; Zaidi, S.; Delwart, E. Metagenomic analyses of viruses in stool samples from children with acute flaccid paralysis. J. Virol. 2009, 83, 4642-4651. [CrossRef]
Gomariz-Zilber, E.; Thomas-Orillard, M. Drosophila C virus and Drosophila hosts: A good association in various environments. J. Evol. Biol. 1993, 6, 677-689. [CrossRef]
Wamonje, F.O.; Michuki, G.N.; Braidwood, L.A.; Njuguna, J.N.; Musembi Mutuku, J.; Djikeng, A.; Harvey, J.J.W.; Carr, J.P. Viral metagenomics of aphids present in bean and maize plots on mixed-use farms in Kenya reveals the presence of three dicistroviruses including a novel Big Sioux River virus-like dicistrovirus. Virol. J. 2017, 14, 188. [CrossRef] [PubMed]
D'Arcy, C.J.; Burnett, P.A.; Hewings, A.D. Detection, biological effects, and transmission of a virus of the aphid Rhopalosiphum padi. Virology 1981, 114, 268-272. [CrossRef]
Hatfill, S.J.; Williamson, C.; Kirby, R.; von Wechmar, M.B. Identification and localization of aphid lethal paralysis virus particles in thin tissue sections of the Rhopalosiphum padi aphid by in situ nucleic acid hybridization. J. Invertebr. Pathol. 1990, 55, 265-271. [CrossRef]
Reinganum, C.; O'Loughlin, G.T.; Hogan, T.W. A nonoccluded virus of the field crickets Teleogryllus oceanicus and T. commodus (Orthoptera: Gryllidae). J. Invertebr. Pathol. 1970, 16, 214-220. [CrossRef]
Remnant, E.J.; Mather, N.; Gillard, T.L.; Yagound, B.; Beekman, M. Direct transmission by injection affects competition among RNA viruses in honeybees. Proc. R. Soc. B Biol. Sci. 2019, 286. [CrossRef]
Carissimo, G.; Eiglmeier, K.; Reveillaud, J.; Holm, I.; Diallo, M.; Diallo, D.; Vantaux, A.; Kim, S.; Ménard, D.; Siv, S.; et al. Identification and characterization of two novel RNA viruses from Anopheles gambiae species complex mosquitoes. PLoS ONE 2016, 11, e0153881. [CrossRef]
Feng, Y.; Krueger, E.N.; Liu, S.; Dorman, K.; Bonning, B.C.; Miller, W.A. Discovery of known and novel viral genomes in soybean aphid by deep sequencing. Phytobiomes J. 2017, 1, 36-45. [CrossRef]
Nakasu, E.Y.T.; Hedil, M.; Nagata, T.; Michereff-Filho, M.; Lucena, V.S.; Inoue-Nagata, A.K. Complete genome sequence and phylogenetic analysis of a novel dicistrovirus associated with the whitefly Bemisia tabaci. Virus Res. 2019, 260, 49-52. [CrossRef]
Roberts, J.M.K.; Anderson, D.L.; Durr, P.A. Metagenomic analysis of Varroa-free Australian honey bees (Apis mellifera) shows a diverse Picornavirales virome. J. Gen. Virol. 2018, 99, 818-826. [CrossRef]
Runckel, C.; Flenniken, M.L.; Engel, J.C.; Ruby, J.G.; Ganem, D.; Andino, R.; DeRisi, J.L. Temporal analysis of the honey bee microbiome reveals four novel viruses and seasonal prevalence of known viruses, Nosema, and Crithidia. PLoS ONE 2011, 6, e20656. [CrossRef] [PubMed]
Shi, C.; Liu, Y.; Hu, X.; Xiong, J.; Zhang, B.; Yuan, Z. A metagenomic survey of viral abundance and diversity in mosquitoes from hubei province. PLoS ONE 2015, 10, e0129845. [CrossRef] [PubMed]
Duraisamy, R.; Akiana, J.; Davoust, B.; Mediannikov, O.; Michelle, C.; Robert, C.; Parra, H.J.; Raoult, D.; Biagini, P.; Desnues, C. Detection of novel RNA viruses from free-living gorillas, Republic of the Congo: Genetic diversity of picobirnaviruses. Virus Genes 2018, 54, 256-271. [CrossRef] [PubMed]
Ge, X.; Li, Y.; Yang, X.; Zhang, H.; Zhou, P.; Zhang, Y.; Shi, Z. Metagenomic analysis of viruses from bat fecal samples reveals many novel viruses in insectivorous bats in China. J. Virol. 2012, 86, 4620-4630. [CrossRef]
Krumbholz, A.; Groth, M.; Esefeld, J.; Peter, H.-U.; Zelld, R. Genome sequence of a novel picorna- like RNA virus from feces of the antarctic fur seal (Arctocephalus gazella). Genome Annouc. 2017, 5, 17-18. [CrossRef]
Li, L.; Victoria, J.G.; Wang, C.; Jones, M.; Fellers, G.M.; Kunz, T.H.; Delwart, E. Bat guano virome: Predominance of dietary viruses from insects and plants plus novel mammalian viruses. J. Virol. 2010, 84, 6955-6965. [CrossRef]
Bennett, A.J.; Bushmaker, T.; Cameron, K.; Ondzie, A.; Niama, F.R.; Parra, H.-J.; Mombouli, J.-V.; Olson, S.H.; Munster, V.J.; Goldberg, T.L. Diverse RNA viruses of arthropod origin in the blood of fruit bats suggest a link between bat and arthropod viromes. Virology 2019, 528, 64-72. [CrossRef]
Cordey, S.; Laubscher, F.; Hartley, M.-A.; Junier, T.; Pérez-Rodriguez, F.J.; Keitel, K.; Vieille, G.; Samaka, J.; Mlaganile, T.; Kagoro, F.; et al. Detection of dicistroviruses RNA in blood of febrile Tanzanian children. Emerg. Microbes Infect. 2019, 8, 613-623. [CrossRef]
Phan, T.G.; Del Valle Mendoza, J.; Sadeghi, M.; Altan, E.; Deng, X.; Delwart, E. Sera of Peruvians with fever of unknown origins include viral nucleic acids from non-vertebrate hosts. Virus Genes 2015, 20, 163-178. [CrossRef] [PubMed]
Bourgarel, M.; Pfukenyi, D.M.; Boué, V.; Talignani, L.; Chiweshe, N.; Diop, F.; Caron, A.; Matope, G.; Missé, D.; Liégeois, F. Circulation of Alphacoronavirus, Betacoronavirus and Paramyxovirus in Hipposideros bat species in Zimbabwe. Infect. Genet. Evol. 2018, 58, 253-257. [CrossRef] [PubMed]
Kocher, T.D.; Thomas, W.K.; Meyer, A.; Edwards, S.V.; Paabo, S.; Villablanca, F.X.; Wilson, A.C. Dynamics of mitochondrialDNAevolution in animals: Amplification and sequencing with conserved primers (cytochrome b/12S ribosomal DNA/control region/evolutionary genetics/molecular phylogenies). Evolution (N. Y.) 1989, 86, 6196-6200.
Monadjem, A.; Taylor, P.J.; Cotterill, F.P.D.; Schoeman, M.C. Bats of Southern and Central Africa: A Biogeographic and Taxonomic Synthesis; Wits University Press: Johannesburg, South Africa, 2010; ISBN 978-1-86814-508-9.
Gillet, F.; Tiouchichine, M.-L.; Galan, M.; Blanc, F.; Némoz, M.; Aulagnier, S.; Michaux, J.R. A new method to identify the endangered Pyrenean desman (Galemys pyrenaicus) and to study its diet, using next generation sequencing from faeces. Mamm. Biol. 2015, 80, 505-509. [CrossRef]
Andriollo, T.; Gillet, F.; Michaux, J.R.; Ruedi, M. The menu varies with metabarcoding practices: A case study with the bat Plecotus auritus. PLoS ONE 2019, 14, e0219135. [CrossRef]
Goodacre, N.; Aljanahi, A.; Nandakumar, S.; Mikailov, M.; Khan, A.S. A Reference Viral Database (RVDB) to enhane bioinformatics analysis of high-throughput sequencing for novel virus detection. mSphere 2018, 3, e00069-18. [CrossRef]
Kumar, S.; Stecher, G.; Tamura, K. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 2016, 33, 1870-1874. [CrossRef]
Guindon, S.; Dufayard, J.F.; Lefort, V.; Anisimova, M.; Hordijk, W.; Gascuel, O. New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst. Biol. 2010, 59, 307-321. [CrossRef]
Milne, I.; Lindner, D.; Bayer, M.; Husmeier, D.; Mcguire, G.; Marshall, D.F.; Wright, F. TOPALi v2: A rich graphical interface for evolutionary analyses of multiple alignments on HPC clusters and multi-core desktops. Bioinformatics 2009, 25, 126-127. [CrossRef]
Larkin, M.A.; Blackshields, G.; Brown, N.P.; Chenna, R.; Mcgettigan, P.A.; McWilliam, H.; Valentin, F.; Wallace, I.M.; Wilm, A.; Lopez, R.; et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23, 2947-2948. [CrossRef] [PubMed]
Ratnasingham, S.; Hebert, P.D.N. BOLD: The barcode of life data system (www.barcodinglife.org). Mol. Ecol. Notes 2007, 7, 355-364. [CrossRef] [PubMed]
Valles, S.M.; Rivers, A.R. Nine new RNA viruses associated with the fire ant Solenopsis invicta from its native range. Virus Genes 2019, 55, 368-380. [CrossRef] [PubMed]
Haddad, N.; Horth, L.; Al-Shagour, B.; Adjlane, N.; Loucif-Ayad, W. Next-generation sequence data demonstrate several pathogenic bee viruses in Middle East and African honey bee subspecies (Apis mellifera syriaca, Apis mellifera intermissa) as well as their cohabiting pathogenic mites (Varroa destructor). Virus Genes 2018, 54, 694-705. [CrossRef] [PubMed]
Kajobe, R.; Marris, G.; Budge, G.; Laurenson, L.; Cordoni, G.; Jones, B.; Wilkins, S.; Cuthbertson, A.G.S.; Brown, M.A. First molecular detection of a viral pathogen in Ugandan honey bees. J. Invertebr. Pathol. 2010, 104, 153-156. [CrossRef]
Benjeddou, M.; Leat, N.; Allsopp, M.; Davison, S. Detection of acute bee paralysis virus and black queen cell virus from honeybees by reverse transcriptase PCR. Appl. Environ. Microbiol. 2001, 67, 2384-2387. [CrossRef]
Van Munster, M.; Dullemans, A.M.; Verbeek, M.; Van Den Heuvel, J.F.; Clérivet, A.; Van Der Wilk, F. Sequence analysis and genomic organization of Aphid lethal paralysis virus: A new member of the family Dicistroviridae. J. Gen. Virol. 2002, 83 Pt 12, 3131-3138. [CrossRef]
Govan, V.A.; Leat, N.; Allsopp, M.; Davison, S. Analysis of the complete genome sequence of acute bee paralysis virus shows that it belongs to the novel group of insect-infecting RNA viruses. Virology 2000, 277, 457-463. [CrossRef]
Bakonyi, T.; Grabensteiner, E.; Kolodziejek, J.; Rusvai, M.; Topolska, G.; Ritter, W.; Nowotny, N. Phylogenetic analysis of acute bee paralysis virus strains. Appl. Environ. Microbiol. 2002, 68, 6446-6450. [CrossRef]
Hilmi, M.; Bradbear, N.; Mejia, D. Beekeeping and Sustainable Livelihoods; Rural Infrastructure and Agro-Industries Division Food and Agriculture Organization of the United Nations: Rome, Italy, 2011; ISBN 9789251070628.
McMenamin, A.J.; Flenniken, M.L. Recently identified bee viruses and their impact on bee pollinators. Curr. Opin. Insect Sci. 2018, 26, 120-129. [CrossRef]
Van Emdem, H.F.; Harrington, R. (Eds.) Aphids as Crop Pests, 2nd ed.; CABI: Wallingfor, UK, 2017; ISBN 9788578110796.
Williamson, C.; Rybicki, E.P.; Kasdorf, G.G.F.; VonWechmar, M.B. Characterization of a new picorna-like virus isolated from Aphids. J. Gen. Virol. 1988, 69, 787-795. [CrossRef]
Rhoda, M.; Upenyu, M.; Peter, C.; Susan, D. The response of the red morph of the Tobacco aphid, myzus persicae nicotianae, to insecticides applied under laboratory and field conditions. Asian J. Agric. Rural Dev. 2013, 3, 141-147.
Belwood, J.J.; Fenton, M.B. Variation in the diet of Myotis lucifiugus (Chiroptera: Vespertilionidae). Can. J. Zool. 1976, 54, 1674-1678. [CrossRef]
Barclay, R.M.R.; Brigham, R.M. Constraints on optimal foraging: A field test ofprey discrimination by echolocating insectivorous bats. Anim. Behav. 1994, 48, 1013-1021. [CrossRef]
Whitaker, J.O.; Clem, P. Food of the evening bat Nycticeius humeralis from Indiana. Am. Midl. Nat. 1992, 127, 211-217. [CrossRef]
Spanjer-Wright, G. Hipposideros caffer (Chiroptera: Hipposideridae). Mamm. Species 2009, 845, 1-9. [CrossRef]