Infections

African army ants at the forefront of virome surveillance in a remote tropical forest

10.24072/pcjournal.249 - Peer Community Journal, Volume 3 (2023), article no. e24.

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In this study, we used a predator-enabled metagenomics strategy to sample the virome of a remote and difficult-to-access densely forested African tropical region. Specifically, we focused our study on the use of army ants of the genus Dorylus that are obligate collective foragers and group predators that attack and overwhelm a broad array of animal prey. Using 209 army ant samples collected from 29 colonies and the virion-associated nucleic acid-based metagenomics approach, we showed that a broad diversity of bacterial, plant, invertebrate and vertebrate viral sequences were accumulated by army ants: including sequences from 157 different viral genera in 56 viral families. This suggests that using predators and scavengers such as army ants to sample broad swathes of tropical forest viromes can shed light on the composition and the structure of viral populations of these complex and inaccessible ecosystems.

Published online:
DOI: 10.24072/pcjournal.249
Keywords: Army ants, predator-enabled metagenomics, virus diversity, deep tropical forests
Fritz, Matthieu 1; Reggiardo, Bérénice 2, 3; Filloux, Denis 2, 3; Claude, Lisa 2, 3; Fernandez, Emmanuel 2, 3; Mahé, Frédéric 2, 3; Kraberger, Simona 4; Custer, Joy M. 4; Becquart, Pierre 1; Mebaley, Telstar Ndong 5; Kombila, Linda Bohou 5; Lenguiya, Léadisaelle H. 6, 7; Boundenga, Larson 5, 8; Mombo, Illich M. 5; Maganga, Gael D. 5, 9; Niama, Fabien R. 6, 7; Koumba, Jean-Sylvain 5; Ogliastro, Mylène 10; Yvon, Michel 3; Martin, Darren P. 11; Blanc, Stéphane 3; Varsani, Arvind 4, 12; Leroy, Eric 1; Roumagnac, Philippe 2, 3

1 Institut de Recherche pour le Développement (IRD), Maladies Infectieuses et Vecteurs, Ecologie, Génétique, Evolution et Contrôle (MIVEGEC) (Université de Montpellier-IRD 224–CNRS 5290), 34394 Montpellier, France
2 CIRAD, UMR PHIM, 34090 Montpellier, France
3 PHIM Plant Health Institute, Univ Montpellier, CIRAD, INRAE, Institut Agro, IRD, Montpellier, France
4 The Biodesign Center for Fundamental and Applied Microbiomics, Center for Evolution and Medicine, School of Life Sciences, Arizona State University, Tempe, AZ, USA
5 Centre Interdisciplinaire de Recherches Médicales de Franceville, Franceville, Gabon
6 Laboratoire National de Santé Publique, Brazzaville, Republic of Congo
7 Université Marien Ngouabi, Brazzaville, Republic of Congo
8 Department of Anthropology, Durham University, South Road, Durham DH1 3LE, UK
9 Université des Sciences et Technique de Masuku (USTM), Institut National Supérieur d’Agronomie et de Biotechnologies (INSAB), Franceville, Gabon
10 INRAE-Université de Montpellier UMR DGIMI 34095 Montpellier, France
11 Division of Computational Biology, Department of Integrative Biomedical Sciences, Institute of infectious Diseases and Molecular Medicine, University of Cape Town, Cape Town, South Africa
12 Structural Biology Research Unit, Department of Integrative Biomedical Sciences, University of Cape Town, Observatory, Cape Town, South Africa
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
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     author = {Fritz, Matthieu and Reggiardo, B\'er\'enice and Filloux, Denis and Claude, Lisa and Fernandez, Emmanuel and Mah\'e, Fr\'ed\'eric and Kraberger, Simona and Custer, Joy M. and Becquart, Pierre and Mebaley, Telstar Ndong and Kombila, Linda Bohou and Lenguiya, L\'eadisaelle H. and Boundenga, Larson and Mombo, Illich M. and Maganga, Gael D. and Niama, Fabien R. and Koumba, Jean-Sylvain and Ogliastro, Myl\`ene and Yvon, Michel and Martin, Darren P. and Blanc, St\'ephane and Varsani, Arvind and Leroy, Eric and Roumagnac, Philippe},
     title = {African army ants at the forefront of virome surveillance in a remote tropical forest},
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     volume = {3},
     year = {2023},
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}
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%A Claude, Lisa
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%A Mebaley, Telstar Ndong
%A Kombila, Linda Bohou
%A Lenguiya, Léadisaelle H.
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%A Mombo, Illich M.
%A Maganga, Gael D.
%A Niama, Fabien R.
%A Koumba, Jean-Sylvain
%A Ogliastro, Mylène
%A Yvon, Michel
%A Martin, Darren P.
%A Blanc, Stéphane
%A Varsani, Arvind
%A Leroy, Eric
%A Roumagnac, Philippe
%T African army ants at the forefront of virome surveillance in a remote tropical forest
%J Peer Community Journal
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Fritz, Matthieu; Reggiardo, Bérénice; Filloux, Denis; Claude, Lisa; Fernandez, Emmanuel; Mahé, Frédéric; Kraberger, Simona; Custer, Joy M.; Becquart, Pierre; Mebaley, Telstar Ndong; Kombila, Linda Bohou; Lenguiya, Léadisaelle H.; Boundenga, Larson; Mombo, Illich M.; Maganga, Gael D.; Niama, Fabien R.; Koumba, Jean-Sylvain; Ogliastro, Mylène; Yvon, Michel; Martin, Darren P.; Blanc, Stéphane; Varsani, Arvind; Leroy, Eric; Roumagnac, Philippe. African army ants at the forefront of virome surveillance in a remote tropical forest. Peer Community Journal, Volume 3 (2023), article  no. e24. doi : 10.24072/pcjournal.249. https://peercommunityjournal.org/articles/10.24072/pcjournal.249/

Peer reviewed and recommended by PCI : 10.24072/pci.infections.100077

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Altschul, S. F.; Gish, W.; Miller, W.; Myers, E. W.; Lipman, D. J. Basic local alignment search tool, Journal of Molecular Biology, Volume 215 (1990) no. 3, pp. 403-410 | DOI

[2] 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.; Pyshkin, A. V.; Sirotkin, A. V.; Vyahhi, N.; Tesler, G.; Alekseyev, M. A.; Pevzner, P. A. SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing, Journal of Computational Biology, Volume 19 (2012) no. 5, pp. 455-477 | DOI

[3] Brady, S. G.; Fisher, B. L.; Schultz, T. R.; Ward, P. S. The rise of army ants and their relatives: diversification of specialized predatory doryline ants, BMC Evolutionary Biology, Volume 14 (2014) no. 1 | DOI

[4] Brahma, A.; Leon, R. G.; Hernandez, G. L.; Wurm, Y. Larger, more connected societies of ants have a higher prevalence of viruses, Molecular Ecology, Volume 31 (2021) no. 3, pp. 859-865 | DOI

[5] Brinkmann, A.; Nitsche, A.; Kohl, C. Viral metagenomics on blood-feeding arthropods as a tool for human disease surveillance, International Journal of Molecular Sciences, Volume 17 (2016) no. 10 | DOI

[6] Buchfink, B.; Xie, C.; Huson, D. H. Fast and sensitive protein alignment using DIAMOND, Nature Methods, Volume 12 (2015) no. 1, pp. 59-60 | DOI

[7] Chandra, V.; Gal, A.; Kronauer, D. J. C. Colony expansions underlie the evolution of army ant mass raiding, Proceedings of the National Academy of Sciences, Volume 118 (2021) no. 22 | DOI

[8] Cotmore, S. F.; Agbandje-McKenna, M.; Chiorini, J. A.; Mukha, D. V.; Pintel, D. J.; Qiu, J.; Soderlund-Venermo, M.; Tattersall, P.; Tijssen, P.; Gatherer, D.; Davison, A. J. The family Parvoviridae, Archives of Virology, Volume 159 (2013) no. 5, pp. 1239-1247 | DOI

[9] Dayaram, A.; Galatowitsch, M. L.; Argüello-Astorga, G. R.; van Bysterveldt, K.; Kraberger, S.; Stainton, D.; Harding, J. S.; Roumagnac, P.; Martin, D. P.; Lefeuvre, P.; Varsani, A. Diverse circular replication-associated protein encoding viruses circulating in invertebrates within a lake ecosystem, Infection, Genetics and Evolution, Volume 39 (2016), pp. 304-316 | DOI

[10] De Coster, W.; D’Hert, S.; Schultz, D. T.; Cruts, M.; Van Broeckhoven, C. NanoPack: visualizing and processing long-read sequencing data, Bioinformatics, Volume 34 (2018) no. 15, pp. 2666-2669 | DOI

[11] Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput, Nucleic Acids Research, Volume 32 (2004) no. 5, pp. 1792-1797 | DOI

[12] Elena, S. F.; Fraile, A.; García-Arenal, F. Evolution and emergence of plant viruses, Advances in Virus Research, Elsevier, 2014, pp. 161-191 | DOI

[13] Fahsbender, E.; Altan, E.; Seguin, M. A.; Young, P.; Estrada, M.; Leutenegger, C.; Delwart, E. Chapparvovirus DNA found in 4% of dogs with diarrhea, Viruses, Volume 11 (2019) no. 5 | DOI

[14] Fauver, J. R.; Weger-Lucarelli, J.; Fakoli, L. S.; Bolay, K.; Bolay, F. K.; Diclaro, J. W.; Brackney, D. E.; Foy, B. D.; Stenglein, M. D.; Ebel, G. D. Xenosurveillance reflects traditional sampling techniques for the identification of human pathogens: A comparative study in West Africa, PLOS Neglected Tropical Diseases, Volume 12 (2018) no. 3 | DOI

[15] Fermin, G. Virion structure, genome organization, and taxonomy of viruses, Viruses, Elsevier, 2018, pp. 17-54 | DOI

[16] François, S.; Filloux, D.; Roumagnac, P.; Bigot, D.; Gayral, P.; Martin, D. P.; Froissart, R.; Ogliastro, M. Discovery of parvovirus-related sequences in an unexpected broad range of animals, Scientific Reports, Volume 6 (2016) no. 1 | DOI

[17] François, S.; Filloux, D.; Fernandez, E.; Ogliastro, M.; Roumagnac, P. Viral metagenomics approaches for high-resolution screening of multiplexed arthropod and plant viral communities, Methods in Molecular Biology, Springer New York, New York, NY, 2018, pp. 77-95 | DOI

[18] French, R. K.; Holmes, E. C. An ecosystems perspective on virus evolution and emergence, Trends in Microbiology, Volume 28 (2020) no. 3, pp. 165-175 | DOI

[19] Fritz, M.; Reggiardo, B.; Filloux, D.; Claude, L.; Fernandez, E.; Mahé, F.; Kraberger, S.; Custer, J. M.; Becquart, P.; Mebaley, T. N.; Kombila, L. B.; Lenguiya, L. H.; Boundenga, L.; Mombo, I. M.; Maganga, G. D.; Niama, F. R.; Koumba, J.-S.; Ogliastro, M.; Yvon, M.; Martin, D. P.; Blanc, S.; Varsani, A.; Leroy, E.; Roumagnac, P. African army ants at the forefront of virome surveillance in a remote tropical forest [Data Set]., Zenodo, 2023 | DOI

[20] Geoghegan, J. L.; Holmes, E. C. Predicting virus emergence amid evolutionary noise, Open Biology, Volume 7 (2017) no. 10 | DOI

[21] Greninger, A. L. A decade of RNA virus metagenomics is (not) enough, Virus Research, Volume 244 (2018), pp. 218-229 | DOI

[22] Grubaugh, N. D.; Sharma, S.; Krajacich, B. J.; Fakoli III, L. S.; Bolay, F. K.; Diclaro II, J. W.; Johnson, W. E.; Ebel, G. D.; Foy, B. D.; Brackney, D. E. Xenosurveillance: A novel mosquito-based approach for examining the human-pathogen landscape, PLOS Neglected Tropical Diseases, Volume 9 (2015) no. 3 | DOI

[23] 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, Systematic Biology, Volume 59 (2010) no. 3, pp. 307-321 | DOI

[24] Harvey, E.; Holmes, E. C. Diversity and evolution of the animal virome, Nature Reviews Microbiology, Volume 20 (2022) no. 6, pp. 321-334 | DOI

[25] Jones, P.; Binns, D.; Chang, H.-Y.; Fraser, M.; Li, W.; McAnulla, C.; McWilliam, H.; Maslen, J.; Mitchell, A.; Nuka, G.; Pesseat, S.; Quinn, A. F.; Sangrador-Vegas, A.; Scheremetjew, M.; Yong, S.-Y.; Lopez, R.; Hunter, S. InterProScan 5: Genome-scale protein function classification, Bioinformatics, Volume 30 (2014) no. 9, pp. 1236-1240 | DOI

[26] Kamiya, T.; O'Dwyer, K.; Nakagawa, S.; Poulin, R. What determines species richness of parasitic organisms? A meta-analysis across animal, plant and fungal hosts, Biological Reviews, Volume 89 (2013) no. 1, pp. 123-134 | DOI

[27] Krishnamurthy, S. R.; Wang, D. Extensive conservation of prokaryotic ribosomal binding sites in known and novel picobirnaviruses, Virology, Volume 516 (2018), pp. 108-114 | DOI

[28] Kronauer, D. J. Recent advances in army ant biology (Hymenoptera: Formicidae), Myrmecological News, Volume 12, pp. 51-65

[29] Kronauer, D. J.; Schöning, C.; Vilhelmsen, L. B.; Boomsma, J. J. A molecular phylogeny of Dorylus army ants provides evidence for multiple evolutionary transitions in foraging niche, BMC Evolutionary Biology, Volume 7 (2007) no. 1 | DOI

[30] Krupovic, M.; Koonin, E. V. Multiple origins of viral capsid proteins from cellular ancestors, Proceedings of the National Academy of Sciences, Volume 114 (2017) no. 12 | DOI

[31] Krupovic, M.; Koonin, E. V. Evolution of eukaryotic single-stranded DNA viruses of the Bidnaviridae family from genes of four other groups of widely different viruses, Scientific Reports, Volume 4 (2014) no. 1 | DOI

[32] Kumar, S.; Stecher, G.; Li, M.; Knyaz, C.; Tamura, K. MEGA X: Molecular evolutionary genetics analysis across computing platforms, Molecular Biology and Evolution, Volume 35 (2018) no. 6, pp. 1547-1549 | DOI

[33] Lefeuvre, P.; Martin, D. P.; Elena, S. F.; Shepherd, D. N.; Roumagnac, P.; Varsani, A. Evolution and ecology of plant viruses, Nature Reviews Microbiology, Volume 17 (2019) no. 10, pp. 632-644 | DOI

[34] Maclot, F.; Candresse, T.; Filloux, D.; Malmstrom, C. M.; Roumagnac, P.; van der Vlugt, R.; Massart, S. Illuminating an ecological blackbox: Using high throughput sequencing to characterize the plant virome across scales, Frontiers in Microbiology, Volume 11 (2020) | DOI

[35] Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads, EMBnet, Volume 17 (2011) no. 1 | DOI

[36] Mokili, J. L.; Rohwer, F.; Dutilh, B. E. Metagenomics and future perspectives in virus discovery, Current Opinion in Virology, Volume 2 (2012) no. 1, pp. 63-77 | DOI

[37] Moubset, O.; François, S.; Maclot, F.; Palanga, E.; Julian, C.; Claude, L.; Fernandez, E.; Rott, P.; Daugrois, J.-H.; Antoine-Lorquin, A.; Bernardo, P.; Blouin, A. G.; Temple, C.; Kraberger, S.; Fontenele, R. S.; Harkins, G. W.; Ma, Y.; Marais, A.; Candresse, T.; Chéhida, S. B.; Lefeuvre, P.; Lett, J.-M.; Varsani, A.; Massart, S.; Ogliastro, M.; Martin, D. P.; Filloux, D.; Roumagnac, P. Virion-associated nucleic acid-based metagenomics: A decade of advances in molecular characterization of plant viruses, Phytopathology®, Volume 112 (2022) no. 11, pp. 2253-2272 | DOI

[38] Neo, J. P. S.; Tan, B. H. The use of animals as a surveillance tool for monitoring environmental health hazards, human health hazards and bioterrorism, Veterinary Microbiology, Volume 203 (2017), pp. 40-48 | DOI

[39] Ng, T. F. F.; Duffy, S.; Polston, J. E.; Bixby, E.; Vallad, G. E.; Breitbart, M. Exploring the diversity of plant DNA viruses and their satellites using vector-enabled metagenomics on whiteflies, PLoS ONE, Volume 6 (2011) no. 4 | DOI

[40] Olendraite, I.; Brown, K.; Valles, S. M.; Firth, A. E.; Chen, Y.; Guérin, D. M. A.; Hashimoto, Y.; Herrero, S.; de Miranda, J. R.; Ryabov, E. ICTV virus taxonomy profile: Polycipiviridae, Journal of General Virology, Volume 100 (2019) no. 4, pp. 554-555 | DOI

[41] Phan, T. G.; Mori, D.; Deng, X.; Rajindrajith, S.; Ranawaka, U.; Fan Ng, T. F.; Bucardo-Rivera, F.; Orlandi, P.; Ahmed, K.; Delwart, E. Small circular single stranded DNA viral genomes in unexplained cases of human encephalitis, diarrhea, and in untreated sewage, Virology, Volume 482 (2015), pp. 98-104 | DOI

[42] Poker, J.; MacDicken, K. Tropical Forest Resources: Facts and Tables, Tropical Forestry Handbook, Springer Berlin Heidelberg, Berlin, Heidelberg, 2016, pp. 3-45 | DOI

[43] Poulin, R. Phylogeny, ecology, and the richness of parasite communities in vertebrates, Ecological Monographs, Volume 65 (1995) no. 3, pp. 283-302 | DOI

[44] Powell, S. How much do army ants eat? On the prey intake of a neotropical top-predator, Insectes Sociaux, Volume 58 (2011) no. 3, pp. 317-324 | DOI

[45] Purdy, M. A.; Harrison, T. J.; Jameel, S.; Meng, X.-J.; Okamoto, H.; Van der Poel, W. H. M.; Smith, D. B. ICTV virus taxonomy profile: Hepeviridae, Journal of General Virology, Volume 98 (2017) no. 11, pp. 2645-2646 | DOI

[46] Pénzes, J. J.; Söderlund-Venermo, M.; Canuti, M.; Eis-Hübinger, A. M.; Hughes, J.; Cotmore, S. F.; Harrach, B. Reorganizing the family Parvoviridae: a revised taxonomy independent of the canonical approach based on host association, Archives of Virology, Volume 165 (2020) no. 9, pp. 2133-2146 | DOI

[47] Pénzes, J. J.; de Souza, W. M.; Agbandje-McKenna, M.; Gifford, R. J. An ancient lineage of highly divergent parvoviruses infects both vertebrate and invertebrate hosts, Viruses, Volume 11 (2019) no. 6 | DOI

[48] Quaiser, A.; Dufresne, A.; Ballaud, F.; Roux, S.; Zivanovic, Y.; Colombet, J.; Sime-Ngando, T.; Francez, A.-J. Diversity and comparative genomics of Microviridae in Sphagnum- dominated peatlands, Frontiers in Microbiology, Volume 6 (2015) | DOI

[49] Roediger, B.; Lee, Q.; Tikoo, S.; Cobbin, J. C.; Henderson, J. M.; Jormakka, M.; O’Rourke, M. B.; Padula, M. P.; Pinello, N.; Henry, M.; Wynne, M.; Santagostino, S. F.; Brayton, C. F.; Rasmussen, L.; Lisowski, L.; Tay, S. S.; Harris, D. C.; Bertram, J. F.; Dowling, J. P.; Bertolino, P.; Lai, J. H.; Wu, W.; Bachovchin, W. W.; Wong, J. J.-L.; Gorrell, M. D.; Shaban, B.; Holmes, E. C.; Jolly, C. J.; Monette, S.; Weninger, W. An atypical parvovirus drives chronic tubulointerstitial nephropathy and kidney fibrosis, Cell, Volume 175 (2018) no. 2 | DOI

[50] Rosario, K.; Breitbart, M.; Harrach, B.; Segalés, J.; Delwart, E.; Biagini, P.; Varsani, A. Revisiting the taxonomy of the family Circoviridae: establishment of the genus Cyclovirus and removal of the genus Gyrovirus, Archives of Virology, Volume 162 (2017) no. 5, pp. 1447-1463 | DOI

[51] Rosario, K.; Dayaram, A.; Marinov, M.; Ware, J.; Kraberger, S.; Stainton, D.; Breitbart, M.; Varsani, A. Diverse circular ssDNA viruses discovered in dragonflies (Odonata: Epiprocta), Journal of General Virology, Volume 93 (2012) no. 12, pp. 2668-2681 | DOI

[52] Sasaki, M.; Orba, Y.; Ueno, K.; Ishii, A.; Moonga, L.; Hang’ombe, B. M.; Mweene, A. S.; Ito, K.; Sawa, H. Metagenomic analysis of the shrew enteric virome reveals novel viruses related to human stool-associated viruses, Journal of General Virology, Volume 96 (2015) no. 2, pp. 440-452 | DOI

[53] Schöning, C.; Njagi, W.; Kinuthia, W. Prey spectra of two swarm‐raiding army ant species in East Africa, Journal of Zoology, Volume 274 (2007) no. 1, pp. 85-93 | DOI

[54] Schöning, C.; Shepard, L.; Sen, A.; Kinuthia, W.; Ogutu, J. O. Should I stay or should I go now? Patch use by African army ant colonies in relation to food availability and predation, Insectes Sociaux, Volume 58 (2011) no. 3, pp. 335-343 | DOI

[55] Smits, S. L.; Zijlstra, E. E.; van Hellemond, J. J.; Schapendonk, C. M.; Bodewes, R.; Schürch, A. C.; Haagmans, B. L.; Osterhaus, A. D. Novel cyclovirus in human cerebrospinal fluid, Malawi, 2010–2011, Emerging Infectious Diseases, Volume 19 (2013) no. 9 | DOI

[56] Sommers, P.; Chatterjee, A.; Varsani, A.; Trubl, G. Integrating viral metagenomics into an ecological framework, Annual Review of Virology, Volume 8 (2021) no. 1, pp. 133-158 | DOI

[57] Souza, W. M. d.; Romeiro, M. F.; Fumagalli, M. J.; Modha, S.; de Araujo, J.; Queiroz, L. H.; Durigon, E. L.; Figueiredo, L. T. M.; Murcia, P. R.; Gifford, R. J. Chapparvoviruses occur in at least three vertebrate classes and have a broad biogeographic distribution, Journal of General Virology, Volume 98 (2017) no. 2, pp. 225-229 | DOI

[58] Stöver, B. C.; Müller, K. F. TreeGraph 2: Combining and visualizing evidence from different phylogenetic analyses, BMC Bioinformatics, Volume 11 (2010) no. 1 | DOI

[59] Tan, L. V.; van Doorn, H. R.; Nghia, H. D. T.; Chau, T. T. H.; Tu, L. T. P.; de Vries, M.; Canuti, M.; Deijs, M.; Jebbink, M. F.; Baker, S.; Bryant, J. E.; Tham, N. T.; BKrong, N. T. T. C.; Boni, M. F.; Loi, T. Q.; Phuong, L. T.; Verhoeven, J. T. P.; Crusat, M.; Jeeninga, R. E.; Schultsz, C.; Chau, N. V. V.; Hien, T. T.; van der Hoek, L.; Farrar, J.; de Jong, M. D. Identification of a new cyclovirus in cerebrospinal fluid of patients with acute central nervous system infections, mBio, Volume 4 (2013) no. 3 | DOI

[60] Temmam, S.; Davoust, B.; Berenger, J.-M.; Raoult, D.; Desnues, C. Viral metagenomics on animals as a tool for the detection of zoonoses prior to human infection?, International Journal of Molecular Sciences, Volume 15 (2014) no. 6, pp. 10377-10397 | DOI

[61] Walker, P. J.; Siddell, S. G.; Lefkowitz, E. J.; Mushegian, A. R.; Adriaenssens, E. M.; Alfenas-Zerbini, P.; Dempsey, D. M.; Dutilh, B. E.; García, M. L.; Curtis Hendrickson, R.; Junglen, S.; Krupovic, M.; Kuhn, J. H.; Lambert, A. J.; Łobocka, M.; Oksanen, H. M.; Orton, R. J.; Robertson, D. L.; Rubino, L.; Sabanadzovic, S.; Simmonds, P.; Smith, D. B.; Suzuki, N.; Van Doorslaer, K.; Vandamme, A.-M.; Varsani, A.; Zerbini, F. M. Recent changes to virus taxonomy ratified by the International Committee on Taxonomy of Viruses (2022), Archives of Virology, Volume 167 (2022) no. 11, pp. 2429-2440 | DOI

[62] Wang, J.; Moore, N. E.; Murray, Z. L.; McInnes, K.; White, D. J.; Tompkins, D. M.; Hall, R. J. Discovery of novel virus sequences in an isolated and threatened bat species, the New Zealand lesser short-tailed bat (Mystacina tuberculata), Journal of General Virology, Volume 96 (2015) no. 8, pp. 2442-2452 | DOI

[63] Wasik, B. R.; Turner, P. E. On the biological success of viruses, Annual Review of Microbiology, Volume 67 (2013) no. 1, pp. 519-541 | DOI

[64] Wren, J. D.; Roossinck, M. J.; Nelson, R. S.; Scheets, K.; Palmer, M. W.; Melcher, U. Plant virus biodiversity and ecology, PLoS Biology, Volume 4 (2006) no. 3 | DOI

[65] Wu S; Manber U A fast approximate pattern-matching tool, Usenix Winter 1992 Technical Conference, San Francisco, 1992, pp. 153-162

[66] Yinda, C. K.; Ghogomu, S. M.; Conceição-Neto, N.; Beller, L.; Deboutte, W.; Vanhulle, E.; Maes, P.; Van Ranst, M.; Matthijnssens, J. Cameroonian fruit bats harbor divergent viruses, including rotavirus H, bastroviruses, and picobirnaviruses using an alternative genetic code, Virus Evolution, Volume 4 (2018) no. 1 | DOI

[67] Zhang, Y.-Z.; Chen, Y.-M.; Wang, W.; Qin, X.-C.; Holmes, E. C. Expanding the RNA virosphere by unbiased metagenomics, Annual Review of Virology, Volume 6 (2019) no. 1, pp. 119-139 | DOI

[68] de la Higuera, I.; Kasun, G. W.; Torrance, E. L.; Pratt, A. A.; Maluenda, A.; Colombet, J.; Bisseux, M.; Ravet, V.; Dayaram, A.; Stainton, D.; Kraberger, S.; Zawar-Reza, P.; Goldstien, S.; Briskie, J. V.; White, R.; Taylor, H.; Gomez, C.; Ainley, D. G.; Harding, J. S.; Fontenele, R. S.; Schreck, J.; Ribeiro, S. G.; Oswald, S. A.; Arnold, J. M.; Enault, F.; Varsani, A.; Stedman, K. M. Unveiling Crucivirus Diversity by Mining Metagenomic Data, mBio, Volume 11 (2020) no. 5 | DOI

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