A library preparation optimized for metagenomics of RNA viruses.
insects
library preparation
metagenomics
shotgun sequencing
virome
virus
Journal
Molecular ecology resources
ISSN: 1755-0998
Titre abrégé: Mol Ecol Resour
Pays: England
ID NLM: 101465604
Informations de publication
Date de publication:
Aug 2021
Aug 2021
Historique:
revised:
23
02
2021
received:
09
12
2019
accepted:
25
02
2021
pubmed:
14
3
2021
medline:
20
8
2021
entrez:
13
3
2021
Statut:
ppublish
Résumé
Our understanding of the viral communities associated to animals has not yet reached the level attained on the bacteriome. This situation is due to, among others, technical challenges in adapting metagenomics using high-throughput sequencing to the study of RNA viromes in animals. Although important developments have been achieved in most steps of viral metagenomics, there is yet a key step that has received little attention: the library preparation. This situation differs from bacteriome studies in which developments in library preparation have largely contributed to the democratisation of metagenomics. Here, we present a library preparation optimized for metagenomics of RNA viruses from insect vectors of viral diseases. The library design allows a simple PCR-based preparation, such as those routinely used in bacterial metabarcoding, that is adapted to shotgun sequencing as required in viral metagenomics. We first optimized our library preparation using mock viral communities and then validated a full metagenomic approach incorporating our preparation in two pilot studies with field-caught insect vectors; one including a comparison with a published metagenomic protocol. Our approach provided a fold increase in virus-like sequences compared to other studies, and nearly-full genomes from new virus species. Moreover, our results suggested conserved trends in virome composition within a population of a mosquito species. Finally, the sensitivity of our approach was compared to a commercial diagnostic PCR for the detection of an arbovirus in field-caught insect vectors. Our approach could facilitate studies on viral communities from animals and the democratization of metagenomics in community ecology of viruses.
Identifiants
pubmed: 33713395
doi: 10.1111/1755-0998.13378
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1788-1807Subventions
Organisme : Seventh Framework Programme
ID : CuliOme/291815
Organisme : Seventh Framework Programme
ID : Vmerge/613996
Organisme : Direction Générale de l'Alimentation
Informations de copyright
© 2021 John Wiley & Sons Ltd.
Références
Adriaenssens, E. M., Kramer, R., Van Goethem, M. W., Makhalanyane, T. P., Hogg, I., & Cowan, D. A. (2017). Environmental drivers of viral community composition in Antarctic soils identified by viromics. Microbiome, 5(1), 83. https://doi.org/10.1186/s40168-017-0301-7.
Aguirre de Carcer, D., Angly, F. E., & Alcami, A. (2014). Evaluation of viral genome assembly and diversity estimation in deep metagenomes. BMC Genomics, 15, 989. https://doi.org/10.1186/1471-2164-15-989.
Ambrose, H. E., & Clewley, J. P. (2006). Virus discovery by sequence-independent genome amplification. Reviews in Medical Virology, 16(6), 365-383. https://doi.org/10.1002/rmv.515.
Angly, F. E., Felts, B., Breitbart, M., Salamon, P., Edwards, R. A., Carlson, C., Chan, A. M., Haynes, M., Kelley, S., Liu, H., Mahaffy, J. M., Mueller, J. E., Nulton, J., Olson, R., Parsons, R., Rayhawk, S., Suttle, C. A., & Rohwer, F. (2006). The marine viromes of four oceanic regions. Plos Biology, 4(11), 2121-2131. https://doi.org/10.1371/journal.pbio.0040368.
Anthony, S. J., Islam, A., Johnson, C., Navarrete-Macias, I., Liang, E., Jain, K., Hitchens, P. L., Che, X., Soloyvov, A., Hicks, A. L., Ojeda-Flores, R., Zambrana-Torrelio, C., Ulrich, W., Rostal, M. K., Petrosov, A., Garcia, J., Haider, N., Wolfe, N., Goldstein, T., … Lipkin, W. I. (2015). Non-random patterns in viral diversity. Nature Communications, 6, 8147. https://doi.org/10.1038/ncomms9147.
Baidaliuk, A., Miot, E. F., Lequime, S., Moltini-Conclois, I., Delaigue, F., Dabo, S., & Lambrechts, L. (2019). Cell-fusing agent virus reduces arbovirus dissemination in Aedes aegypti mosquitoes in vivo. Journal of Virology, 93(18), e00705-00719. https://doi.org/10.1128/jvi.00705-19.
Bergner, L. M., Orton, R. J., da Silva Filipe, A., Shaw, A. E., Becker, D. J., Tello, C., Biek, R., & Streicker, D. G. (2019). Using noninvasive metagenomics to characterize viral communities from wildlife. Molecular Ecology Resources, 19(1), 128-143. https://doi.org/10.1111/1755-0998.12946.
Bigot, D., Dalmon, A., Roy, B., Hou, C., Germain, M., Romary, M., Deng, S., Diao, Q., Weinert, L. A., Cook, J. M., Herniou, E. A., & Gayral, P. (2017). The discovery of Halictivirus resolves the Sinaivirus phylogeny. Journal of General Virology, 98(11), 2864-2875. https://doi.org/10.1099/jgv.0.000957.
Binladen, J., Gilbert, M. T., Bollback, J. P., Panitz, F., Bendixen, C., Nielsen, R., & Willerslev, E. (2007). The use of coded PCR primers enables high-throughput sequencing of multiple homolog amplification products by 454 parallel sequencing. PLoS One, 2(2), e197. https://doi.org/10.1371/journal.pone.0000197.
Biteye, B., Fall, A. G., Ciss, M., Seck, M. T., Apolloni, A., Fall, M., Tran, A., & Gimonneau, G. (2018). Ecological distribution and population dynamics of Rift Valley fever virus mosquito vectors (Diptera, Culicidae) in Senegal. Parasit Vectors, 11(1), 27. https://doi.org/10.1186/s13071-017-2591-9.
Bolduc, B., Youens-Clark, K., Roux, S., Hurwitz, B. L., & Sullivan, M. B. (2017). iVirus: facilitating new insights in viral ecology with software and community data sets imbedded in a cyberinfrastructure. ISME Journal, 11(1), 7-14. https://doi.org/10.1038/ismej.2016.89.
Breitbart, M., Hewson, I., Felts, B., Mahaffy, J. M., Nulton, J., Salamon, P., & Rohwer, F. (2003). Metagenomic analyses of an uncultured viral community from human feces. Journal of Bacteriology, 185(20), 6220-6223. https://doi.org/10.1128/jb.185.20.6220-6223.2003.
Breitbart, M., Salamon, P., Andresen, B., Mahaffy, J. M., Segall, A. M., Mead, D., Azam, F., & Rohwer, F. (2002). Genomic analysis of uncultured marine viral communities. Proceedings of the National Academy of Sciences of the United States of America, 99(22), 14250-14255. https://doi.org/10.1073/pnas.202488399.
Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., & Madden, T. L. (2009). BLAST+: architecture and applications. BMC Bioinformatics, 10, 421. https://doi.org/10.1186/1471-2105-10-421.
Cann, A. J., Fandrich, S. E., & Heaphy, S. (2005). Analysis of the virus population present in equine faeces indicates the presence of hundreds of uncharacterized virus genomes. Virus Genes, 30(2), 151-156. https://doi.org/10.1007/s11262-004-5624-3.
Caporaso, J. G., Lauber, C. L., Walters, W. A., Berg-Lyons, D., Lozupone, C. A., Turnbaugh, P. J., Fierer, N., & Knight, R. (2011). Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proceedings of the National Academy of Sciences, USA, 108(Suppl 1), 4516-4522. https://doi.org/10.1073/pnas.1000080107.
Carissimo, G., Eiglmeier, K., Reveillaud, J., Holm, I., Diallo, M., Diallo, D., Vantaux, A., Kim, S., Ménard, D., Siv, S., Belda, E., Bischoff, E., Antoniewski, C., & Vernick, K. D. (2016). Identification and characterization of two novel RNA viruses from Anopheles gambiae species complex mosquitoes. PLoS One, 11(5), e0153881. https://doi.org/10.1371/journal.pone.0153881.
Chandler, J. A., Liu, R. M., & Bennett, S. N. (2015). RNA shotgun metagenomic sequencing of northern California (USA) mosquitoes uncovers viruses, bacteria, and fungi. Frontiers in Microbiology, 6, 185. https://doi.org/10.3389/fmicb.2015.00185.
Charbonneau, M. R., Blanton, L. V., DiGiulio, D. B., Relman, D. A., Lebrilla, C. B., Mills, D. A., & Gordon, J. I. (2016). A microbial perspective of human developmental biology. Nature, 535(7610), 48-55. https://doi.org/10.1038/nature18845.
Cheval, J., Sauvage, V., Frangeul, L., Dacheux, L., Guigon, G., Dumey, N., Pariente, K., Rousseaux, C., Dorange, F., Berthet, N., Brisse, S., Moszer, I., Bourhy, H., Manuguerra, C. J., Lecuit, M., Burguiere, A., Caro, V., & Eloit, M. (2011). Evaluation of high-throughput sequencing for identifying known and unknown viruses in biological samples. Journal of Clinical Microbiology, 49(9), 3268-3275. https://doi.org/10.1128/JCM.00850-11.
Conceição-Neto, N., Zeller, M., Lefrère, H., De Bruyn, P., Beller, L., Deboutte, W., Yinda, C. K., Lavigne, R., Maes, P., Ranst, M. V., Heylen, E., & Matthijnssens, J. (2015). Modular approach to customise sample preparation procedures for viral metagenomics: a reproducible protocol for virome analysis. Scientific Reports, 5, 16532. https://doi.org/10.1038/srep16532.
Cox-Foster, D. L., Conlan, S., Holmes, E. C., Palacios, G., Evans, J. D., Moran, N. A., Quan, P.-L., Briese, T., Hornig, M., Geiser, D. M., Martinson, V., vanEngelsdorp, D., Kalkstein, A. L., Drysdale, A., Hui, J., Zhai, J., Cui, L., Hutchison, S. K., Simons, J. F., … Lipkin, W. I. (2007). A metagenomic survey of microbes in honey bee colony collapse disorder. Science, 318(5848), 283-287. https://doi.org/10.1126/science.1146498.
Culley, A. I., Lang, A. S., & Suttle, C. A. (2006). Metagenomic analysis of coastal RNA virus communities. Science, 312(5781), 1795-1798. https://doi.org/10.1126/science.1127404.
D’Amore, R., Ijaz, U. Z., Schirmer, M., Kenny, J. G., Gregory, R., Darby, A. C., Shakya, M., Podar, M., Quince, C., & Hall, N. (2016). A comprehensive benchmarking study of protocols and sequencing platforms for 16S rRNA community profiling. BMC Genomics, 17, 55. https://doi.org/10.1186/s12864-015-2194-9.
Daly, G. M., Bexfield, N., Heaney, J., Stubbs, S., Mayer, A. P., Palser, A., Kellam, P., Drou, N., Caccamo, M., Tiley, L., Alexander, G. J. M., Bernal, W., & Heeney, J. L. (2011). A viral discovery methodology for clinical biopsy samples utilising massively parallel next generation sequencing. PLoS One, 6(12), e28879. https://doi.org/10.1371/journal.pone.0028879.
de Vries, M., Deijs, M., Canuti, M., van Schaik, B. D. C., Faria, N. R., van de Garde, M. D. B., Jachimowski, L. C. M., Jebbink, M. F., Jakobs, M., Luyf, A. C. M., Coenjaerts, F. E. J., Claas, E. C. J., Molenkamp, R., Koekkoek, S. M., Lammens, C., Leus, F., Goossens, H., Ieven, M., Baas, F., & van der Hoek, L. (2011). A sensitive assay for virus discovery in respiratory clinical samples. PLoS One, 6(1), e16118. https://doi.org/10.1371/journal.pone.0016118.
Dean, F. B., Nelson, J. R., Giesler, T. L., & Lasken, R. S. (2001). Rapid amplification of plasmid and phage DNA using Phi 29 DNA polymerase and multiply-primed rolling circle amplification. Genome Research, 11(6), 1095-1099. https://doi.org/10.1101/gr.180501.
Delwart, E. L. (2007). Viral metagenomics. Reviews in Medical Virology, 17(2), 115-131. https://doi.org/10.1002/rmv.532.
Desnues, C., Rodriguez-Brito, B., Rayhawk, S., Kelley, S., Tran, T., Haynes, M., Liu, H., Furlan, M., Wegley, L., Chau, B., Ruan, Y., Hall, D., Angly, F. E., Edwards, R. A., Li, L., Thurber, R. V., Reid, R. P., Siefert, J., Souza, V., … Rohwer, F. (2008). Biodiversity and biogeography of phages in modern stromatolites and thrombolites. Nature, 452(7185), 340-343. https://doi.org/10.1038/nature06735.
Djikeng, A., Halpin, R., Kuzmickas, R., DePasse, J., Feldblyum, J., Sengamalay, N., Afonso, C., Zhang, X., Anderson, N. G., Ghedin, E., & Spiro, D. J. (2008). Viral genome sequencing by random priming methods. BMC Genomics, 9(1), 5. https://doi.org/10.1186/1471-2164-9-5.
Eiden, M., Gil, P., Ziegler, U., Rakotoarivony, I., Marie, A., Frances, B., L'Ambert, G., Simonin, Y., Foulongne, V., Groschup, M. H., Gutierrez, S., & Eloit, M. (2018). Emergence of two Usutu virus lineages in Culex pipiens mosquitoes in the Camargue, France, 2015. Infection, Genetics and Evolution, 61, 151-154. https://doi.org/10.1016/j.meegid.2018.03.020.
Ezenwa, V. O., Gerardo, N. M., Inouye, D. W., Medina, M., & Xavier, J. B. (2012). Animal behavior and the microbiome. Science, 338(6104), 198-199. https://doi.org/10.1126/science.1227412.
Fancello, L., Raoult, D., & Desnues, C. (2012). Computational tools for viral metagenomics and their application in clinical research. Virology, 434(2), 162-174. https://doi.org/10.1016/j.virol.2012.09.025.
Fauver, J. R., Grubaugh, N. D., Krajacich, B. J., Weger-Lucarelli, J., Lakin, S. M., Fakoli, L. S., Bolay, F. K., Diclaro, J. W., Dabiré, K. R., Foy, B. D., Brackney, D. E., Ebel, G. D., & Stenglein, M. D. (2016). West African Anopheles gambiae mosquitoes harbor a taxonomically diverse virome including new insect-specific flaviviruses, mononegaviruses, and totiviruses. Virology, 498, 288-299. https://doi.org/10.1016/j.virol.2016.07.031.
Filloux, D., Dallot, S., Delaunay, A., Galzi, S., Jacquot, E., & Roumagnac, P. (2015). Metagenomics approaches based on Virion-associated nucleic acids (VANA): An innovative tool for assessing without a priori viral diversity of plants. Methods in Molecular Biology, 1302, 249-257. https://doi.org/10.1007/978-1-4939-2620-6_18.
Fontenille, D., Traore-Lamizana, M., Diallo, M., Thonnon, J., Digoutte, J. P., & Zeller, H. G. (1998). New vectors of Rift Valley fever in West Africa. Emerging Infectious Diseases, 4(2), 289-293. https://doi.org/10.3201/eid0402.980218.
Froussard, P. (1992). A random-PCR method (rPCR) to construct whole cDNA library from low amounts of RNA. Nucleic Acids Research, 20(11), 2900. https://doi.org/10.1093/nar/20.11.2900.
Galiez, C., Magnan, C. N., Coste, F., & Baldi, P. (2016). VIRALpro: a tool to identify viral capsid and tail sequences. Bioinformatics, 32(9), 1405-1407. https://doi.org/10.1093/bioinformatics/btv727.
Gentile, C. L., & Weir, T. L. (2018). The gut microbiota at the intersection of diet and human health. Science, 362(6416), 776-780. https://doi.org/10.1126/science.aau5812.
Gloor, G. B., Hummelen, R., Macklaim, J. M., Dickson, R. J., Fernandes, A. D., MacPhee, R., & Reid, G. (2010). Microbiome profiling by illumina sequencing of combinatorial sequence-tagged PCR products. PLoS One, 5(10), e15406. https://doi.org/10.1371/journal.pone.0015406.
Goenaga, S., Kenney, J., Duggal, N., Delorey, M., Ebel, G., Zhang, B. O., Levis, S., Enria, D., & Brault, A. (2015). Potential for co-infection of a mosquito-specific Flavivirus, Nhumirim virus, to block west Nile virus transmission in mosquitoes. Viruses, 7(11), 5801-5812.
Graf, E. H., Simmon, K. E., Tardif, K. D., Hymas, W., Flygare, S., Eilbeck, K., Yandell, M., & Schlaberg, R. (2016). Unbiased detection of respiratory viruses by use of RNA sequencing-based metagenomics: a systematic comparison to a commercial PCR panel. Journal of Clinical Microbiology, 54(4), 1000-1007. https://doi.org/10.1128/jcm.03060-15.
Greninger, A. L. (2018). A decade of RNA virus metagenomics is (not) enough. Virus Research, 244, 218-229. https://doi.org/10.1016/j.virusres.2017.10.014.
Greninger, A. L., Waghmare, A., Adler, A., Qin, X., Crowley, J. L., Englund, J. A., Kuypers, J. M., Jerome, K. R., & Zerr, D. M. (2017). Rule-out outbreak: 24-hour metagenomic next-generation sequencing for characterizing respiratory virus source for infection prevention. Journal of the Pediatric Infectious Diseases Society, 6(2), 168-172. https://doi.org/10.1093/jpids/pix019.
Greninger, A. L., Zerr, D. M., Qin, X., Adler, A. L., Sampoleo, R., Kuypers, J. M., Englund, J. A., & Jerome, K. R. (2017). Rapid metagenomic next-generation sequencing during an investigation of hospital-acquired human parainfluenza virus 3 infections. Journal of Clinical Microbiology, 55(1), 177-182. https://doi.org/10.1128/jcm.01881-16.
Hall, R. J., Wang, J., Todd, A. K., Bissielo, A. B., Yen, S., Strydom, H., Moore, N. E., Ren, X., Huang, Q. S., Carter, P. E., & Peacey, M. (2014). Evaluation of rapid and simple techniques for the enrichment of viruses prior to metagenomic virus discovery. Journal of Virological Methods, 195, 194-204. https://doi.org/10.1016/j.jviromet.2013.08.035.
Hall-Mendelin, S., McLean, B. J., Bielefeldt-Ohmann, H., Hobson-Peters, J., Hall, R. A., & van den Hurk, A. F. (2016). The insect-specific Palm Creek virus modulates West Nile virus infection in and transmission by Australian mosquitoes. Parasites & Vectors, 9(1), 414. https://doi.org/10.1186/s13071-016-1683-2.
Hamady, M., Walker, J. J., Harris, J. K., Gold, N. J., & Knight, R. (2008). Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex. Nature Methods, 5(3), 235-237. https://doi.org/10.1038/nmeth.1184.
Handelsman, J. (2004). Metagenomics: Application of genomics to uncultured microorganisms. Microbiology and Molecular Biology Reviews, 68(4), 669-+. https://doi.org/10.1128/mmbr.68.4.669-685.2004.
Head, S. R., Komori, H. K., LaMere, S. A., Whisenant, T., Van Nieuwerburgh, F., Salomon, D. R., & Ordoukhanian, P. (2014). Library construction for next-generation sequencing: overviews and challenges. BioTechniques, 56(2), 61-64. https://doi.org/10.2144/000114133.
Hoffmann, B., Scheuch, M., Höper, D., Jungblut, R., Holsteg, M., Schirrmeier, H., Eschbaumer, M., Goller, K. V., Wernike, K., Fischer, M., Breithaupt, A., Mettenleiter, T. C., & Beer, M. (2012). Novel orthobunyavirus in Cattle, Europe, 2011. Emerging Infectious Diseases, 18(3), 469-472. https://doi.org/10.3201/eid1803.111905.
Illumina (2013). Illumina 16S metagenomic sequencing library preparation (Illumina Technical Note 15044223). Retrieved from https://support.illumina.com/documents/documentation/chemistry_documentation/16s/16s-metagenomic-library-prep-guide-15044223-b.pdf
Illumina. Specifications for the MiSeq System. Retrieved from https://www.illumina.com/systems/sequencing-platforms/miseq/specifications.html
Illumina (2020). Illumina adapter portfolio. Illumina bulletin. Retrieved from https://support.illumina.com/bulletins/2020/06/illumina-adapter-portfolio.html
Kallies, R., Hölzer, M., Brizola Toscan, R., Nunes da Rocha, U., Anders, J., Marz, M., & Chatzinotas, A. (2019). Evaluation of sequencing library preparation protocols for viral metagenomic analysis from pristine aquifer groundwaters. Viruses, 11(6), 484. https://doi.org/10.3390/v11060484.
Keller, M., & Zengler, K. (2004). Tapping into microbial diversity. Nature Reviews Microbiology, 2(2), 141-150. https://doi.org/10.1038/nrmicro819.
Kircher, M., Sawyer, S., & Meyer, M. (2012). Double indexing overcomes inaccuracies in multiplex sequencing on the Illumina platform. Nucleic Acids Research, 40(1), e3. https://doi.org/10.1093/nar/gkr771.
Kluge, M., Campos, F. S., Tavares, M., de Amorim, D. B., Valdez, F. P., Giongo, A., Roehe, P. M., & Franco, A. C. (2016). Metagenomic survey of viral diversity obtained from feces of subantarctic and South American fur seals. PLoS One, 11(3), e0151921. https://doi.org/10.1371/journal.pone.0151921.
Kohl, C., Brinkmann, A., Dabrowski, P. W., Radonic, A., Nitsche, A., & Kurth, A. (2015). Protocol for metagenomic virus detection in clinical specimens. Emerging Infectious Diseases, 21(1), 48-57. https://doi.org/10.3201/eid2101.140766.
Koonin, E. V., Dolja, V. V., Krupovic, M., Varsani, A., Wolf, Y. I., Yutin, N., Zerbini, F. M., & Kuhn, J. H. (2020). Global organization and proposed megataxonomy of the virus world. Microbiology and Molecular Biology Reviews, 84(2), https://doi.org/10.1128/mmbr.00061-19.
Kozich, J. J., Westcott, S. L., Baxter, N. T., Highlander, S. K., & Schloss, P. D. (2013). Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Applied and Environment Microbiology, 79(17), 5112-5120. https://doi.org/10.1128/aem.01043-13.
Kuhn, J. H., Wolf, Y. I., Krupovic, M., Zhang, Y. Z., Maes, P., Dolja, V. V., & Koonin, E. V. (2019). Classify viruses - the gain is worth the pain. Nature, 566(7744), 318-320. https://doi.org/10.1038/d41586-019-00599-8.
Kumar, S., Stecher, G., & Tamura, K. (2016). MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33(7), 1870-1874. https://doi.org/10.1093/molbev/msw054.
Lewandowska, D. W., Schreiber, P. W., Schuurmans, M. M., Ruehe, B., Zagordi, O., Bayard, C., Greiner, M., Geissberger, F. D., Capaul, R., Zbinden, A., Böni, J., Benden, C., Mueller, N. J., Trkola, A., & Huber, M. (2017). Metagenomic sequencing complements routine diagnostics in identifying viral pathogens in lung transplant recipients with unknown etiology of respiratory infection. PLoS One, 12(5), e0177340. https://doi.org/10.1371/journal.pone.0177340.
Li, D., Liu, C.-M., Luo, R., Sadakane, K., & Lam, T.-W. (2015). MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics, 31(10), 1674-1676. https://doi.org/10.1093/bioinformatics/btv033.
Li, H., & Durbin, R. (2009). Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25(14), 1754-1760. https://doi.org/10.1093/bioinformatics/btp324.
Lott, S. E., Villalta, J. E., Schroth, G. P., Luo, S., Tonkin, L. A., & Eisen, M. B. (2011). Noncanonical compensation of Zygotic X transcription in early Drosophila melanogaster development revealed through single-embryo RNA-Seq. PLoS Biology, 9(2), e1000590. https://doi.org/10.1371/journal.pbio.1000590.
Magoc, T., & Salzberg, S. L. (2011). FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics, 27(21), 2957-2963. https://doi.org/10.1093/bioinformatics/btr507.
Manso, C. F., Bibby, D. F., & Mbisa, J. L. (2017). Efficient and unbiased metagenomic recovery of RNA virus genomes from human plasma samples. Scientific Reports, 7(1), 4173. https://doi.org/10.1038/s41598-017-02239-5.
Mardis, E. R. (2008). The impact of next-generation sequencing technology on genetics. Trends in Genetics, 24(3), 133-141. https://doi.org/10.1016/j.tig.2007.12.007.
McKnight, D. T., Huerlimann, R., Bower, D. S., Schwarzkopf, L., Alford, R. A., & Zenger, K. R. (2019). Methods for normalizing microbiome data: An ecological perspective. Methods in Ecology and Evolution, 10(3), 389-400. https://doi.org/10.1111/2041-210x.13115.
Mihara, T., Nishimura, Y., Shimizu, Y., Nishiyama, H., Yoshikawa, G., Uehara, H., Hingamp, P., Goto, S., & Ogata, H. (2016). Linking virus genomes with host taxonomy. Viruses-Basel, 8(3), https://doi.org/10.3390/v8030066.
Mokili, J. L., Rohwer, F., & Dutilh, B. E. (2012). Metagenomics and future perspectives in virus discovery. Current Opinion in Virology, 2(1), 63-77. https://doi.org/10.1016/j.coviro.2011.12.004.
Moreno, P. S., Wagner, J., Mansfield, C. S., Stevens, M., Gilkerson, J. R., & Kirkwood, C. D. (2017). Characterisation of the canine faecal virome in healthy dogs and dogs with acute diarrhoea using shotgun metagenomics. PLoS One, 12(6), e0178433. https://doi.org/10.1371/journal.pone.0178433.
Moutailler, S., Popovici, I., Devillers, E., Vayssier-Taussat, M., & Eloit, M. (2016). Diversity of viruses in Ixodes ricinus, and characterization of a neurotropic strain of Eyach virus. New Microbes and New Infections, 11, 71-81. https://doi.org/10.1016/j.nmni.2016.02.012.
Ng, S., Braxton, C., Eloit, M., Feng, S., Fragnoud, R., Mallet, L., Mee, E., Sathiamoorthy, S., Vandeputte, O., & Khan, A. (2018). Current Perspectives on High-Throughput Sequencing (HTS) for adventitious virus detection: upstream sample processing and library preparation. Viruses, 10(10) , 566. https://doi.org/10.3390/v10100566.
Norling, M., Karlsson-Lindsjo, O. E., Gourle, H., Bongcam-Rudloff, E., & Hayer, J. (2016). MetLab: An in silico experimental design, simulation and analysis tool for viral metagenomics studies. PLoS One, 11(8), e0160334. https://doi.org/10.1371/journal.pone.0160334.
Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Wagner, H. (2019). vegan: Community Ecology Package. R package version 2.5-6. Retrieved from https://CRAN.R-project.org/package=vegan
Oristo, S., Lee, H.-J., & Maunula, L. (2018). Performance of pre-RT-qPCR treatments to discriminate infectious human rotaviruses and noroviruses from heat-inactivated viruses: applications of PMA/PMAxx, benzonase and RNase. Journal of Applied Microbiology, 124(4), 1008-1016. https://doi.org/10.1111/jam.13737.
Paez-Espino, D., Eloe-Fadrosh, E. A., Pavlopoulos, G. A., Thomas, A. D., Huntemann, M., Mikhailova, N., Rubin, E., Ivanova, N. N., & Kyrpides, N. C. (2016). Uncovering Earth's virome. Nature, 536(7617), 425-430. https://doi.org/10.1038/nature19094.
Rampelli, S., Soverini, M., Turroni, S., Quercia, S., Biagi, E., Brigidi, P., & Candela, M. (2016). ViromeScan: a new tool for metagenomic viral community profiling. BMC Genomics, 17, 165. https://doi.org/10.1186/s12864-016-2446-3.
Ren, J., Ahlgren, N. A., Lu, Y. Y., Fuhrman, J. A., & Sun, F. (2017). VirFinder: a novel k-mer based tool for identifying viral sequences from assembled metagenomic data. Microbiome, 5(1), 69. https://doi.org/10.1186/s40168-017-0283-5.
Riesenfeld, C. S., Schloss, P. D., & Handelsman, J. (2004). Metagenomics: Genomic analysis of microbial communities. Annual Review of Genetics, 38, 525-552. https://doi.org/10.1146/annurev.genet.38.072902.091216.
Romo, H., Kenney, J. L., Blitvich, B. J., & Brault, A. C. (2018). Restriction of Zika virus infection and transmission in Aedes aegypti mediated by an insect-specific flavivirus. Emerging Microbes & Infections, 7(1), 1-13. https://doi.org/10.1038/s41426-018-0180-4.
Roossinck, M. J., Martin, D. P., & Roumagnac, P. (2015). Plant Virus metagenomics: Advances in virus discovery. Phytopathology, 105(6), 716-727. https://doi.org/10.1094/phyto-12-14-0356-rvw.
Rosseel, T., Ozhelvaci, O., Freimanis, G., & Van Borm, S. (2015). Evaluation of convenient pretreatment protocols for RNA virus metagenomics in serum and tissue samples. Journal of Virological Methods, 222, 72-80. https://doi.org/10.1016/j.jviromet.2015.05.010.
Rosseel, T., Van Borm, S., Vandenbussche, F., Hoffmann, B., van den Berg, T., Beer, M., & Hoper, D. (2013). The origin of biased sequence depth in sequence-independent nucleic acid amplification and optimization for efficient massive parallel sequencing. PLoS One, 8(9), https://doi.org/10.1371/journal.pone.0076144.
Roux, S., Enault, F., Hurwitz, B. L., & Sullivan, M. B. (2015). VirSorter: mining viral signal from microbial genomic data. PeerJ, 3, e985. https://doi.org/10.7717/peerj.985.
Roux, S., Faubladier, M., Mahul, A., Paulhe, N., Bernard, A., Debroas, D., & Enault, F. (2011). Metavir: a web server dedicated to virome analysis. Bioinformatics, 27(21), 3074-3075. https://doi.org/10.1093/bioinformatics/btr519.
Roux, S., Krupovic, M., Daly, R. A., Borges, A. L., Nayfach, S., Schulz, F., Sharrar, A., Matheus Carnevali, P. B., Cheng, J.-F., Ivanova, N. N., Bondy-Denomy, J., Wrighton, K. C., Woyke, T., Visel, A., Kyrpides, N. C., & Eloe-Fadrosh, E. A. (2019). Cryptic inoviruses revealed as pervasive in bacteria and archaea across Earth's biomes. Nat Microbiol, 4(11), 1895-1906. https://doi.org/10.1038/s41564-019-0510-x.
Roux, S., Solonenko, N. E., Dang, V. T., Poulos, B. T., Schwenck, S. M., Goldsmith, D. B., Coleman, M. L., Breitbart, M., & Sullivan, M. B. (2016). Towards quantitative viromics for both double-stranded and single-stranded DNA viruses. PeerJ, 4, e2777. https://doi.org/10.7717/peerj.2777.
Runckel, C., Flenniken, M. L., Engel, J. C., Ruby, J. G., Ganem, D., Andino, R., & DeRisi, J. L. (2011). Temporal analysis of the honey bee microbiome reveals four novel viruses and seasonal prevalence of known viruses, Nosema, and Crithidia. PLoS One, 6(6), e20656. https://doi.org/10.1371/journal.pone.0020656.
Sauvage, V., Laperche, S., Cheval, J., Muth, E., Dubois, M., Boizeau, L., & Eloit, M. (2016). Viral metagenomics applied to blood donors and recipients at high risk for blood-borne infections. Blood Transfusion = Trasfusione Del Sangue, 14(5), 400-407. https://doi.org/10.2450/2016.0160-15.
Segard, A., Gardes, L., Jacquier, E., Grillet, C., Mathieu, B., Rakotoarivony, I., & Garros, C. (2018). Schmallenberg virus in Culicoides Latreille (Diptera: Ceratopogonidae) populations in France during 2011-2012 outbreak. Transbound Emerg Dis, 65(1), e94-e103. https://doi.org/10.1111/tbed.12686.
Shi, C., Beller, L., Deboutte, W., Yinda, K. C., Delang, L., Vega-Rúa, A., Failloux, A.-B., & Matthijnssens, J. (2019). Stable distinct core eukaryotic viromes in different mosquito species from Guadeloupe, using single mosquito viral metagenomics. Microbiome, 7(1), 121. https://doi.org/10.1186/s40168-019-0734-2.
Shi, M., Lin, X.-D., Tian, J.-H., Chen, L.-J., Chen, X., Li, C.-X., Qin, X.-C., Li, J., Cao, J.-P., Eden, J.-S., Buchmann, J., Wang, W., Xu, J., Holmes, E. C., & Zhang, Y.-Z. (2016). Redefining the invertebrate RNA virosphere. Nature, 540(7634), 539-543. https://doi.org/10.1038/nature20167.
Shi, M., Zhang, Y.-Z., & Holmes, E. C. (2018). Meta-transcriptomics and the evolutionary biology of RNA viruses. Virus Research, 243, 83-90. https://doi.org/10.1016/j.virusres.2017.10.016.
Simmonds, P., Adams, M. J., Benkő, M., Breitbart, M., Brister, J. R., Carstens, E. B., Davison, A. J., Delwart, E., Gorbalenya, A. E., Harrach, B., Hull, R., King, A. M. Q., Koonin, E. V., Krupovic, M., Kuhn, J. H., Lefkowitz, E. J., Nibert, M. L., Orton, R., Roossinck, M. J., … Zerbini, F. M. (2017). Virus taxonomy in the age of metagenomics. Nature Reviews Microbiology, 15, 161. https://doi.org/10.1038/nrmicro.2016.177.
Solonenko, S. A., Ignacio-Espinoza, J., Alberti, A., Cruaud, C., Hallam, S., Konstantinidis, K., Tyson, G., Wincker, P., & Sullivan, M. B. (2013). Sequencing platform and library preparation choices impact viral metagenomes. BMC Genomics, 14, 320. https://doi.org/10.1186/1471-2164-14-320.
Stang, A., Korn, K., Wildner, O., & Überla, K. (2005). Characterization of virus isolates by particle-associated nucleic acid PCR. Journal of Clinical Microbiology, 43(2), 716-720. https://doi.org/10.1128/jcm.43.2.716-720.2005.
Stern, J., Miller, G., Li, X., & Saxena, D. (2019). Virome and bacteriome: two sides of the same coin. Current Opinion in Virology, 37, 37-43. https://doi.org/10.1016/j.coviro.2019.05.007.
Temmam, S., Davoust, B., Berenger, J.-M., Raoult, D., & Desnues, C. (2014). Viral metagenomics on animals as a tool for the detection of zoonoses prior to human infection? International Journal of Molecular Sciences, 15(6), 10377-10397. https://doi.org/10.3390/ijms150610377.
Temmam, S., Monteil-Bouchard, S., Robert, C., Pascalis, H., Michelle, C., Jardot, P., Charrel, R., Raoult, D., & Desnues, C. (2015). Host-associated metagenomics: A guide to generating infectious RNA viromes. PLoS One, 10(10), e0139810. https://doi.org/10.1371/journal.pone.0139810.
Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994). Clustal-W - Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22(22), 4673-4680. https://doi.org/10.1093/nar/22.22.4673.
Trubl, G., Roux, S., Solonenko, N., Li, Y.-F., Bolduc, B., Rodríguez-Ramos, J., Eloe-Fadrosh, E. A., Rich, V. I., & Sullivan, M. B. (2019). Towards optimized viral metagenomes for double-stranded and single-stranded DNA viruses from challenging soils. PeerJ, 7, e7265. https://doi.org/10.7717/peerj.7265.
Venail, R., Lhoir, J., Fall, M., del Río, R., Talavera, S., Labuschagne, K., Miranda, M., Pagès, N., Venter, G., Rakotoarivony, I., Allène, X., Scheid, B., Gardès, L., Gimonneau, G., Lancelot, R., Garros, C., Cêtre-Sossah, C., Balenghien, T., Carpenter, S., & Baldet, T. (2015). How do species, population and active ingredient influence insecticide susceptibility in Culicoides biting midges (Diptera: Ceratopogonidae) of veterinary importance? Parasites & Vectors, 8(1), 439. https://doi.org/10.1186/s13071-015-1042-8.
Verhoeven, J. T. P., Canuti, M., Munro, H. J., Dufour, S. C., & Lang, A. S. (2018). ViDiT-CACTUS: an inexpensive and versatile library preparation and sequence analysis method for virus discovery and other microbiology applications. Canadian Journal of Microbiology, 64(10), 761-773. https://doi.org/10.1139/cjm-2018-0097.
Victoria, J. G., Kapoor, A., Li, L., Blinkova, O., Slikas, B., Wang, C., Naeem, A., Zaidi, S., & Delwart, E. (2009). Metagenomic analyses of viruses in stool samples from children with acute flaccid paralysis. Journal of Virology, 83(9), 4642-4651. https://doi.org/10.1128/jvi.02301-08.
Warwick-Dugdale, J., Solonenko, N., Moore, K., Chittick, L., Gregory, A. C., Allen, M. J., Sullivan, M. B., & Temperton, B. (2019). Long-read viral metagenomics captures abundant and microdiverse viral populations and their niche-defining genomic islands. PeerJ, 7, https://doi.org/10.7717/peerj.6800.
Wolf, Y. I., Kazlauskas, D., Iranzo, J., Lucía-Sanz, A., Kuhn, J. H., Krupovic, M., Dolja, V. V., & Koonin, E. V. (2018). Origins and evolution of the global RNA virome. mBio, 9(6), https://doi.org/10.1128/mBio.02329-18.
Wylezich, C., Papa, A., Beer, M., & Hoper, D. (2018). A versatile sample processing workflow for metagenomic pathogen detection. Scientific Reports, 8(1), 13108. https://doi.org/10.1038/s41598-018-31496-1.
Yilmaz, P., Parfrey, L. W., Yarza, P., Gerken, J., Pruesse, E., Quast, C., Schweer, T., Peplies, J., Ludwig, W., & Glöckner, F. O. (2013). The SILVA and “All-species Living Tree Project (LTP)” taxonomic frameworks. Nucleic Acids Research, 42(D1), D643-D648. https://doi.org/10.1093/nar/gkt1209.
Zhang, Y. Z., Shi, M., & Holmes, E. C. (2018). Using metagenomics to characterize an expanding virosphere. Cell, 172(6), 1168-1172. https://doi.org/10.1016/j.cell.2018.02.043.