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Metaviromics coupled with phage-host identification to open the viral ‘black box’

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  • Omics in Microbial Ecology
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Abstract

Viruses are found in almost all biomes on Earth, with bacteriophages (phages) accounting for the majority of viral particles in most ecosystems. Phages have been isolated from natural environments using the plaque assay and liquid medium-based dilution culturing. However, phage cultivation is restricted by the current limitations in the number of culturable bacterial strains. Unlike prokaryotes, which possess universally conserved 16S rRNA genes, phages lack universal marker genes for viral taxonomy, thus restricting cultureindependent analyses of viral diversity. To circumvent these limitations, shotgun viral metagenome sequencing (i.e., metaviromics) has been developed to enable the extensive sequencing of a variety of viral particles present in the environment and is now widely used. Using metaviromics, numerous studies on viral communities have been conducted in oceans, lakes, rivers, and soils, resulting in many novel phage sequences. Furthermore, auxiliary metabolic genes such as ammonic monooxygenase C and β-lactamase have been discovered in viral contigs assembled from viral metagenomes. Current attempts to identify putative bacterial hosts of viral metagenome sequences based on sequence homology have been limited due to viral sequence variations. Therefore, culture-independent approaches have been developed to predict bacterial hosts using single-cell genomics and fluorescentlabeling. This review focuses on recent viral metagenome studies conducted in natural environments, especially in aquatic ecosystems, and their contributions to phage ecology. Here, we concluded that although metaviromics is a key tool for the study of viral ecology, this approach must be supplemented with phage-host identification, which in turn requires the cultivation of phage-bacteria systems.

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References

  • Ahlgren, N.A., Ren, J., Lu, Y.Y., Fuhrman, J.A., and Sun, F. 2017. Alignment-free oligonucleotide frequency dissimilarity measure improves prediction of hosts from metagenomically-derived viral sequences. Nucleic Acids Res. 45, 39–53.

    Article  CAS  PubMed  Google Scholar 

  • Amgarten, D., Braga, L.P.P., da Silva, A.M., and Setubal, J.C. 2018. MARVEL, a tool for prediction of bacteriophage sequences in metagenomic bins. Front. Genet. 9, 304.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Amgarten, D., Iha, B.K., Piroupo, C.M., da Silva, A.M., and Setubal, J.C. 2020. vHULK, a new tool for bacteriophage host prediction based on annotated genomic features and deep neural networks. bioRxiv 413476. doi: https://doi.org/10.1101/2020.12.06.413476.

  • Antipov, D., Raiko, M., Lapidus, A., and Pevzner, P.A. 2020. Metaviral SPAdes: assembly of viruses from metagenomic data. Bioinformatics 36, 4126–4129.

    Article  CAS  PubMed  Google Scholar 

  • Arkhipova, K., Skvortsov, T., Quinn, J.P., McGrath, J.W., Allen, C.C.R., Dutilh, B.E., McElarney, Y., and Kulakov, L.A. 2018. Temporal dynamics of uncultured viruses: A new dimension in viral diversity. ISME J. 12, 199–211.

    Article  PubMed  Google Scholar 

  • Aylward, F.O., Boeuf, D., Mende, D.R., Wood-Charlson, E.M., Vislova, A., Eppley, J.M., Romano, A.E., and DeLong, E.F. 2017. Diel cycling and long-term persistence of viruses in the ocean’s euphotic zone. Proc. Natl. Acad. Sci. USA 114, 11446–11451.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Balogh, B., Jones, J.B., Iriarte, F.B., and Momol, M.T. 2010. Phage therapy for plant disease control. Curr. Pharm. Biotechnol. 11, 48–57.

    Article  CAS  PubMed  Google Scholar 

  • Bergh, Ø., BØrsheim, K.Y., Bratbak, G., and Heldal, M. 1989. High abundance of viruses found in aquatic environments. Nature 340, 467–468.

    Article  CAS  PubMed  Google Scholar 

  • Bland, C., Ramsey, T.L., Sabree, F., Lowe, M., Brown, K., Kyrpides, N.C., and Hugenholtz, P. 2007. CRISPR Recognition Tool (CRT): a tool for automatic detection of clustered regularly interspaced palindromic repeats. BMC Bioinformatics 8, 209.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Breitbart, M., Bonnain, C., Malki, K., and Sawaya, N.A. 2018. Phage puppet masters of the marine microbial realm. Nat. Microbiol. 3, 754–766.

    Article  CAS  PubMed  Google Scholar 

  • Breitbart, M., Salamon, P., Andresen, B., Mahaffy, J.M., Segall, A.M., Mead, D., Azam, F., and Rohwer, F. 2002. Genomic analysis of uncultured marine viral communities. Proc. Natl. Acad. Sci. USA 99, 14250–14255.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brum, J.R., Hurwitz, B.L., Schofield, O., Ducklow, H.W., and Sullivan, M.B. 2015a. Seasonal time bombs: dominant temperate viruses affect Southern Ocean microbial dynamics. ISME J. 10, 437–449.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Brum, J.R., Ignacio-Espinoza, J.C., Roux, S., Doulcier, G., Acinas, S.G., Alberti, A., Chaffron, S., Cruaud, C., de Vargas, C., Gasol, J.M., et al. 2015b. Patterns and ecological drivers of ocean viral communities. Science 348, 1261498.

    Article  PubMed  CAS  Google Scholar 

  • Buchholz, H.H., Michelsen, M.L., Bolaños, L.M., Browne, E., Allen, M.J., and Temperton, B. 2021. Efficient dilution-to-extinction isolation of novel virus-host model systems for fastidious heterotrophic bacteria. ISME J. doi: https://doi.org/10.1038/s41396-020-00872-z.

  • Casas, V. and Rohwer, F. 2007. Phage metagenomics. Methods Enzymol. 421, 259–268.

    Article  CAS  PubMed  Google Scholar 

  • Chen, L.X., Méheust, R., Crits-Christoph, A., McMahon, K.D., Nelson, T.C., Slater, G.F., Warren, L.A., and Banfield, J.F. 2020. Large freshwater phages with the potential to augment aerobic methane oxidation. Nat. Microbiol. 12, 1504–1515.

    Article  CAS  Google Scholar 

  • Chen, L.X, Zhao, Y., McMahon, K.D., Mori, J.F., Jessen, G.L., Nelson, T.C., Warren, L.A., and Banfield, J.F. 2019. Wide distribution of phage that infect freshwater SAR11 bacteria. mSystems 4, e00410–19.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Choi, A., Kang, I., Yang, S.J., and Cho, J.C. 2015. Complete genome sequence of bacteriophage P8625, the first lytic phage that infects Verrucomicrobia. Stand. Genomic Sci. 10, 96.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Clokie, M.R.J., Shan, J., Bailey, S., Jia, Y., Krisch, H.M., West, S., and Mann, N.H. 2006. Transcription of a ‘photosynthetic’ T4-type phage during infection of a marine cyanobacterium. Environ. Microbiol. 8, 827–835.

    Article  CAS  PubMed  Google Scholar 

  • Cobián Güemes, A.G., Youle, M., Cantú, V.A., Felts, B., Nulton, J., and Rohwer, F. 2016. Viruses as winners in the game of life. Annu. Rev. Virol. 3, 197–214.

    Article  PubMed  CAS  Google Scholar 

  • Conceiçào-Neto, N., Zeller, M., Lefrère, H., De Bruyn, P., Beller, L., Deboutte, W., Yinda, C.K., Lavigne, R., Maes, P., Van Ranst, M., et al. 2015. Modular approach to customise sample preparation procedures for viral metagenomics: a reproducible protocol for virome analysis. Sci. Rep. 5, 16532.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Coutinho, F.H., Cabello-Yeves, P.J., Gonzalez-Serrano, R., Rosselli, R., López-Pérez, M., Zemskaya, T.I., Zakharenko, A.S., Ivanov, V.G., and Rodriguez-Valera, F. 2020. New viral biogeochemical roles revealed through metagenomic analysis of Lake Baikal. Microbiome 8, 163.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coutinho, F.H., Gregoracci, G.B., Walter, J.M., Thompson, C.C., and Thompson, F.L. 2018. Metagenomics sheds light on the ecology of marine microbes and their viruses. Trends Microbiol. 26, 955–965.

    Article  CAS  PubMed  Google Scholar 

  • Culley, A.I. 2013. Insight into the unknown marine virus majority. Proc. Natl. Acad. Sci. USA 110, 12166–12167.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dávila-Ramos, S., Castelán-Sánchez, H.G., Martínez-Ávila, L., Sánchez-Carbente, M.D.R., Peralta, R., Hernández-Mendoza, A., Dobson, A.D.W., Gonzalez, R.A., Pastor, N., and Batista-García, R.A. 2019. A review on viral metagenomics in extreme environments. Front. Microbiol. 10, 2403.

    Article  PubMed  PubMed Central  Google Scholar 

  • de Cárcer, D.A., López-Bueno, A., Pearce, D.A., and Alcamí, A. 2015. Biodiversity and distribution of polar freshwater DNA viruses. Sci. Adv. 1, e1400127.

    Article  CAS  Google Scholar 

  • De Corte, D., Martínez, J.M., Cretoiu, M.S., Takaki, Y., Nunoura, T., Sintes, E., Herndl, G.J., and Yokokawa, T. 2019. Viral communities in the global deep ocean conveyor belt assessed by targeted viromics. Front. Microbiol. 10, 1801.

    Article  PubMed  PubMed Central  Google Scholar 

  • de Jonge, P.A., von Meijenfeldt, F.A.B., Costa, A.R., Nobrega, F.L., Brouns, S.J.J., and Dutilh, B.E. 2020. Adsorption sequencing as a rapid method to link environmental bacteriophages to hosts. iScience 23, 101439.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Smet, J., Zimmermann, M., Kogadeeva, M., Ceyssens, P.J., Vermaelen, W., Blasdel, B., Jang, H.B., Sauer, U., and Lavigne, R. 2016. High coverage metabolomics analysis reveals phage-specific alterations to Pseudomonas aeruginosa physiology during infection. ISME J. 10, 1823–1835.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deng, L., Gregory, A., Yilmaz, S., Poulos, B.T., Hugenholtz, P., and Sullivan, M.B. 2012. Contrasting life strategies of viruses that infect photo- and heterotrophic bacteria, as revealed by viral tagging. mBio 3, e00373–12.

    Article  PubMed  PubMed Central  Google Scholar 

  • Deng, L., Ignacio-Espinoza, J.C., Gregory, A.C., Poulos, B.T., Weitz, J.S., Hugenholtz, P., and Sullivan, M.B. 2014. Viral tagging reveals discrete populations in Synechococcus viral genome sequence space. Nature 513, 242–245.

    Article  CAS  PubMed  Google Scholar 

  • Dinsdale, E.A., Edwards, R.A., Hall, D., Angly, F., Breitbart, M., Brulc, J.M., Furlan, M., Desnues, C., Haynes, M., Li, L., et al. 2008. Functional metagenomic profiling of nine biomes. Nature 452, 629–632.

    Article  CAS  PubMed  Google Scholar 

  • Dion, M.B., Oechslin, F., and Moineau, S. 2020. Phage diversity, genomics and phylogeny. Nat. Rev. Microbiol. 18, 125–138.

    Article  CAS  PubMed  Google Scholar 

  • Djikeng, A., Kuzmickas, R., Anderson, N.G., and Spiro, D.J. 2009. Metagenomic analysis of RNA viruses in a fresh water lake. PLoS ONE 4, e7264.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Doss, J., Culbertson, K., Hahn, D., Camacho, J., and Barekzi, N. 2017. A review of phage therapy against bacterial pathogens of aquatic and terrestrial organisms. Viruses 9, 50.

    Article  PubMed Central  CAS  Google Scholar 

  • Dutilh, B.E., Cassman, N., McNair, K., Sanchez, S.E., Silva, G.G.Z., Boling, L., Barr, J.J., Speth, D.R., Seguritan, V., Aziz, R.K., et al. 2014. A highly abundant bacteriophage discovered in the unknown sequences of human faecal metagenomes. Nat. Commun. 5, 4498.

    Article  CAS  PubMed  Google Scholar 

  • Dřunková, M., Low, S.J., Daly, J.N., Deng, L., Rinke, C., and Hugenholtz, P. 2019. Defining the human gut host-phage network through single-cell viral tagging. Nat. Microbiol. 4, 2192–2203.

    Article  CAS  Google Scholar 

  • Edwards, R.A., McNair, K., Faust, K., Raes, J., and Dutilh, B.E. 2016. Computational approaches to predict bacteriophage-host relationships. FEMS Microbiol. Rev. 40, 258–272.

    Article  CAS  PubMed  Google Scholar 

  • Edwards, R.A., Vega, A.A., Norman, H.M., Ohaeri, M., Levi, K., Dinsdale, E.A., Cinek, O., Aziz, R.K., McNair, K., Barr, J.J., et al. 2019. Global phylogeography and ancient evolution of the widespread human gut virus crAssphage. Nat. Microbiol. 4, 1727–1736.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Enault, F., Briet, A., Bouteille, L., Roux, S., Sullivan, M.B., and Petit, M.A. 2017. Phages rarely encode antibiotic resistance genes: a cautionary tale for virome analysis. ISME J. 11, 237–247.

    Article  CAS  PubMed  Google Scholar 

  • Fridman, S., Flores-Uribe, J., Larom, S., Alalouf, O., Liran, O., Yacoby, I., Salama, F., Bailleul, B., Rappaport, F., Ziv, T., et al. 2017. A myovirus encoding both photosystem I and II proteins enhances cyclic electron flow in infected Prochlorococcus cells. Nat. Microbiol. 2, 1350–1357.

    Article  CAS  PubMed  Google Scholar 

  • Galiez, C., Siebert, M., Enault, F., Vincent, J., and Söding, J. 2017. WIsH: who is the host? Predicting prokaryotic hosts from metagenomic phage contigs. Bioinformatics 33, 3113–3114.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghai, R., Mehrshad, M., Mizuno, C.M., and Rodriguez-Valera, F. 2017. Metagenomic recovery of phage genomes of uncultured freshwater actinobacteria. ISME J. 11, 304–308.

    Article  CAS  PubMed  Google Scholar 

  • Ghylin, T.W., Garcia, S.L., Moya, F., Oyserman, B.O., Schwientek, P., Forest, K.T., Mutschler, J., Dwulit-Smith, J., Chan, L.K., and Martinez-Garcia, M. 2014. Comparative single-cell genomics reveals potential ecological niches for the freshwater acI Actinobacteria lineage. ISME J. 8, 2503–2516.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Green, J.C., Rahman, F., Saxton, M.A., and Williamson, K.E. 2015. Metagenomic assessment of viral diversity in Lake Matoaka, a temperate, eutrophic freshwater lake in southeastern Virginia, USA. Aquat. Microb. Ecol. 75, 117–128.

    Article  Google Scholar 

  • Gregory, A.C., Zayed, A.A., Conceição-Neto, N., Temperton, B., Bolduc, B., Alberti, A., Ardyna, M., Arkhipova, K., Carmichael, M., Cruaud, C., et al. 2019. Marine DNA viral macro- and microdiversity from pole to pole. Cell 177, 1109–1123.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Greninger, A.L. 2018. A decade of RNA virus metagenomics is (not) enough. Virus Res. 244, 218–229.

    Article  CAS  PubMed  Google Scholar 

  • Guerin, E. and Hill, C. 2020. Shining light on human gut bacteriophages. Front. Cell. Infect. Microbiol. 10, 481.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guerin, E., Shkoporov, A., Stockdale, S.R., Clooney, A.G., Ryan, F.J., Sutton, T.D.S., Draper, L.A., Gonzalez-Tortuero, E., Ross, R.P., and Hill, C. 2018. Biology and taxonomy of crAss-like bacteriophages, the most abundant virus in the human gut. Cell Host Microbe 24, 653–664.

    Article  CAS  PubMed  Google Scholar 

  • Hatfull, G.F. 2008. Bacteriophage genomics. Curr. Opin. Microbiol. 11, 447–453.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayes, S., Mahony, J., Nauta, A., and Van Sinderen, D. 2017. Metagenomic approaches to assess bacteriophages in various environmental niches. Viruses 9, 127.

    Article  PubMed Central  CAS  Google Scholar 

  • Hendrix, H., Kogadeeva, M., Zimmermann, M., Sauer, U., De Smet, J., Muchez, L., Lissens, M., Staes, I., Voet, M., Wagemans, J., et al. 2019. Host metabolic reprogramming of Pseudomonas aeruginosa by phage-based quorum sensing modulation. bioRxiv, 577908. doi: https://doi.org/10.1101/577908.

  • Hesse, U., van Heusden, P., Kirby, B.M., Olonade, I., van Zyl, L.J., and Trindade, M. 2017. Virome assembly and annotation: a surprise in the Namib Desert. Front. Microbiol. 8, 13.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hewson, I., Barbosa, J.G., Brown, J.M., Donelan, R.P., Eaglesham, J.B., Eggleston, E.M., and LaBarre, B.A. 2012. Temporal dynamics and decay of putatively allochthonous and autochthonous viral genotypes in contrasting freshwater lakes. Appl. Environ. Microbiol. 78, 6583–6591.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holmfeldt, K., Middelboe, M., Nybroe, O., and Riemann, L. 2007. Large variabilities in host strain susceptibility and phage host range govern interactions between lytic marine phages and their Flavobacterium hosts. Appl. Environ. Microbiol. 73, 6730–6739.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Howard-Varona, C., Lindback, M.M., Bastien, G.E., Solonenko, N., Zayed, A.A., Jang, H.B., Andreopoulos, B., Brewer, H.M., Glavina del Rio, T., Adkins, J.N., et al. 2020. Phage-specific metabolic reprogramming of virocells. ISME J. 14, 881–895.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hurwitz, B.L., Brum, J.R., and Sullivan, M.B. 2015. Depth-stratified functional and taxonomic niche specialization in the ‘core’ and ‘flexible’ Pacific Ocean Virome. ISME J. 9, 472–484.

    Article  CAS  PubMed  Google Scholar 

  • Hurwitz, B.L. and Sullivan, M.B. 2013. The Pacific Ocean Virome (POV): a marine viral metagenomic dataset and associated protein clusters for quantitative viral ecology. PLoS ONE 8, e57355.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hurwitz, B.L. and U’Ren, J.M. 2016. Viral metabolic reprogramming in marine ecosystems. Curr. Opin. Microbiol. 31, 161–168.

    Article  CAS  PubMed  Google Scholar 

  • Hwang, J., Park, S.Y., Park, M., Lee, S., Jo, Y., Cho, W.K., and Lee, T.K. 2016. Metagenomic characterization of viral communities in Goseong Bay, Korea. Ocean Sci. J. 51, 599–612.

    Article  CAS  Google Scholar 

  • Ignacio-Espinoza, J.C., Laperriere, S.M., Yeh, Y.C., Weissman, J., Hou, S., Long, A.M., and Fuhrman, J.A. 2020. Ribosome-linked mRNA-rRNA chimeras reveal active novel virus host associations. bioRxiv, 332502. doi: https://doi.org/10.1101/2020.10.30.332502.

  • Jang, H.B., Bolduc, B., Zablocki, O., Kuhn, J.H., Roux, S., Adriaenssens, E.M., Brister, J.R., Kropinski, A.M., Krupovic, M., Lavigne, R., et al. 2019. Taxonomic assignment of uncultivated prokaryotic virus genomes is enabled by gene-sharing networks. Nat. Biotechnol. 37, 632–639.

    Article  CAS  Google Scholar 

  • Ji, P., Aw, T.G., Van Bonn, W., and Rose, J.B. 2020. Evaluation of a portable nanopore-based sequencer for detection of viruses in water. J. Virol. Methods 278, 113805.

    Article  CAS  PubMed  Google Scholar 

  • Jin, M., Cai, L., Ma, R., Zeng, R., Jiao, N., and Zhang, R. 2020. Prevalence of temperate viruses in deep South China Sea and western Pacific Ocean. Deep Sea Res. 1 Oceanogr. Res. Pap. 166, 103403.

    Article  CAS  Google Scholar 

  • John, S.G., Mendez, C.B., Deng, L., Poulos, B., Kauffman, A.K., Kern, S., Brum, J., Polz, M.F., Boyle, E.A., and Sullivan, M.B. 2011. A simple and efficient method for concentration of ocean viruses by chemical flocculation. Environ. Microbiol. Rep. 3, 195–202.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kang, I., Jang, H., and Cho, J.C. 2015. Complete genome sequences of bacteriophages P12002L and P12002S, two lytic phages that infect a marine Polaribacter strain. Stand. Genomic Sci. 10, 82.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kang, I., Jang, H., Oh, H.M., and Cho, J.C. 2012. Complete genome sequence of Celeribacter bacteriophage P12053L. J. Virol. 86, 8339–8340.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kang, I., Oh, H.M., Kang, D., and Cho, J.C. 2013. Genome of a SAR116 bacteriophage shows the prevalence of this phage type in the oceans. Proc. Natl. Acad. Sci. USA 110, 12343–12348.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan Mirzaei, M., Xue, J., Costa, R., Ru, J., Schulz, S., Taranu, Z.E., and Deng, L. 2020. Challenges of studying the human virome — relevant emerging technologies. Trends Microbiol. 29, 171–181.

    Article  PubMed  CAS  Google Scholar 

  • Kim, K.H. and Bae, J.W. 2011. Amplification methods bias metagenomic libraries of uncultured single-stranded and double-stranded DNA viruses. Appl. Environ. Microbiol. 77, 7663–7668.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim, K.H., Chang, H.W., Nam, Y.D., Roh, S.W., Kim, M.S., Sung, Y., Jeon, C.O., Oh, H.M., and Bae, J.W. 2008. Amplification of uncultured single-stranded DNA viruses from rice paddy soil. Appl. Environ. Microbiol. 74, 5975–5985.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim, S., Park, M.S., Song, J., Kang, I., and Cho, J.C. 2020. High-throughput cultivation based on dilution-to-extinction with catalase supplementation and a case study of cultivating acI bacteria from Lake Soyang. J. Microbiol. 58, 893–905.

    Article  CAS  PubMed  Google Scholar 

  • Kropinski, A.M., Mazzocco, A., Waddell, T.E., Lingohr, E., and Johnson, R.P. 2009. Enumeration of bacteriophages by double agar overlay plaque assay. In Clokie, M.R. and Kropinski, A.M. (eds.), Bacteriophages: Methods and Protocols, Volume 1: Isolation, Characterization, and Interactions, pp. 69–76. Humana Press, Totowa, New Jersey, USA.

    Google Scholar 

  • Krupovic, M., Prangishvili, D., Hendrix, R.W., and Bamford, D.H. 2011. Genomics of bacterial and archaeal viruses: Dynamics within the prokaryotic virosphere. Microbiol. Mol. Biol. Rev. 75, 610–635.

    Article  PubMed  PubMed Central  Google Scholar 

  • Labbé, M., Girard, C., Vincent, W.F., and Culley, A.I. 2020. Extreme viral partitioning in a marine-derived High Arctic Lake. mSphere 5, e00334–20.

    Article  PubMed  PubMed Central  Google Scholar 

  • Labonté, J.M., Pachiadaki, M., Fergusson, E., McNichol, J., Grosche, A., Gulmann, L.K., Vetriani, C., Sievert, S.M., and Stepanauskas, R. 2019. Single cell genomics-based analysis of gene content and expression of prophages in a diffuse-flow deep-sea hydrothermal system. Front. Microbiol. 10, 1262.

    Article  PubMed  PubMed Central  Google Scholar 

  • Labonté, J.M., Swan, B.K., Poulos, B., Luo, H., Koren, S., Hallam, S.J., Sullivan, M.B., Woyke, T., Wommack, K.E., and Stepanauskas, R. 2015. Single-cell genomics-based analysis of virus-host interactions in marine surface bacterioplankton. ISME J. 9, 2386–2399.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Langenfeld, K., Chin, K., Wigginton, K.R., and Duhaime, M.B. 2020. Comparison of ultrafiltration and iron chloride flocculation in the preparation of aquatic viromes from contrasting sample types. bioRxiv, 356501. doi: https://doi.org/10.1101/2020.10.26.356501.

  • Li, D., Liu, C.M., Luo, R., Sadakane, K., and Lam, T.W. 2015. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics 31, 1674–1676.

    Article  CAS  PubMed  Google Scholar 

  • Lin, D.M., Koskella, B., and Lin, H.C. 2017. Phage therapy: An alternative to antibiotics in the age of multi-drug resistance. World J. Gastrointest Pharmacol. Ther. 8, 162–173.

    Article  PubMed  PubMed Central  Google Scholar 

  • López-Bueno, A., Rastrojo, A., Peiró, R., Arenas, M., and Alcamí, A. 2015. Ecological connectivity shapes quasispecies structure of RNA viruses in an Antarctic lake. Mol. Ecol. 24, 4812–4825.

    Article  PubMed  CAS  Google Scholar 

  • López-Bueno, A., Tamames, J., Velázquez, D., Moya, A., Quesada, A., and Alcamí, A. 2009. High diversity of the viral community from an Antarctic lake. Science 326, 858–861.

    Article  PubMed  CAS  Google Scholar 

  • Low, S.J., Džunková, M., Chaumeil, P.A., Parks, D.H., and Hugenholtz, P. 2019. Evaluation of a concatenated protein phylogeny for classification of tailed double-stranded DNA viruses belonging to the order Caudovirales. Nat. Microbiol. 4, 1306–1315.

    Article  CAS  PubMed  Google Scholar 

  • Malki, K., Rosario, K., Sawaya, N.A., Székely, A.J., Tisza, M.J., and Breitbart, M. 2020. Prokaryotic and viral community composition of freshwater springs in Florida, USA. mBio 11, e00436–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mann, N.H., Cook, A., Millard, A., Bailey, S., and Clokie, M. 2003. Marine ecosystems: bacterial photosynthesis genes in a virus. Nature 424, 741.

    Article  CAS  PubMed  Google Scholar 

  • Meier-Kolthoff, J.P. and Göker, M. 2017. VICTOR: genome-based phylogeny and classification of prokaryotic viruses. Bioinformatics 33, 3396–3404.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miranda, J.A., Culley, A.I., Schvarcz, C.R., and Steward, G.F. 2016. RNA viruses as major contributors to Antarctic virioplankton. Environ. Microbiol. 18, 3714–3727.

    Article  CAS  PubMed  Google Scholar 

  • Mohiuddin, M. and Schellhorn, H.E. 2015. Spatial and temporal dynamics of virus occurrence in two freshwater lakes captured through metagenomic analysis. Front. Microbiol. 6, 950.

    Article  Google Scholar 

  • Moon, K., Jeon, J.H., Kang, I., Park, K.S., Lee, K., Cha, C.J., Lee, S.H., and Cho, J.C. 2020a. Freshwater viral metagenome reveals novel and functional phage-borne antibiotic resistance genes. Microbiome 8, 75.

    Article  PubMed  PubMed Central  Google Scholar 

  • Moon, K., Kang, I., Kim, S., Kim, S.J., and Cho, J.C. 2017. Genome characteristics and environmental distribution of the first phage that infects the LD28 clade, a freshwater methylotrophic bacterial group. Environ. Microbiol. 19, 4714–4727.

    Article  CAS  PubMed  Google Scholar 

  • Moon, K., Kim, S., Kang, I., and Cho, J.C. 2020b. Viral metagenomes of Lake Soyang, the largest freshwater lake in South Korea. Sci. Data 7, 349.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mougari, S., Sahmi-Bounsiar, D., Levasseur, A., Colson, P., and La Scola, B. 2019. Virophages of giant viruses: an update at eleven. Viruses 11, 733.

    Article  CAS  PubMed Central  Google Scholar 

  • Nishimura, Y., Yoshida, T., Kuronishi, M., Uehara, H., Ogata, H., and Goto, S. 2017. ViPTree: the viral proteomic tree server. Bioinformatics 33, 2379–2380.

    Article  CAS  PubMed  Google Scholar 

  • Okazaki, Y., Nishimura, Y., Yoshida, T., Ogata, H., and Nakano, S.I. 2019. Genome-resolved viral and cellular metagenomes revealed potential key virus-host interactions in a deep freshwater lake. Environ. Microbiol. 21, 4740–4754.

    Article  CAS  PubMed  Google Scholar 

  • Overholt, W.A., Hölzer, M., Geesink, P., Diezel, C., Marz, M., and Küsel, K. 2020. Inclusion of Oxford Nanopore long reads improves all microbial and viral metagenome-assembled genomes from a complex aquifer system. Environ. Microbiol. 22, 4000–4013.

    Article  CAS  PubMed  Google Scholar 

  • Páez-Espino, D., Eloe-Fadrosh, E.A., Pavlopoulos, G.A., Thomas, A.D., Huntemann, M., Mikhailova, N., Rubin, E., Ivanova, N.N., and Kyrpides, N.C. 2016. Uncovering Earth’s virome. Nature 536, 425–430.

    Article  PubMed  CAS  Google Scholar 

  • Páez-Espino, D., Zhou, J., Roux, S., Nayfach, S., Pavlopoulos, G.A., Schulz, F., McMahon, K.D., Walsh, D., Woyke, T., Ivanova, N.N., et al. 2019. Diversity, evolution, and classification of virophages uncovered through global metagenomics. Microbiome 7, 157.

    Article  PubMed  PubMed Central  Google Scholar 

  • Peng, Y., Leung, H.C., Yiu, S.M., and Chin, F.Y. 2012. IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics 28, 1420–1428.

    Article  CAS  PubMed  Google Scholar 

  • Pesant, S., Not, F., Picheral, M., Kandels-Lewis, S., Le Bescot, N., Gorsky, G., Iudicone, D., Karsenti, E., Speich, S., Troublé, R., et al. 2015. Open science resources for the discovery and analysis of Tara Oceans data. Sci. Data 2, 150023.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramos-Barbero, M.D., Martínez, J.M., Almansa, C., Rodríguez, N., Villamor, J., Gomariz, M., Escudero, C., Rubin, S.D., Antón, J., Martínez-García, M., et al. 2019. Prokaryotic and viral community structure in the singular chaotropic salt lake Salar de Uyuni. Environ. Microbiol. 21, 2029–2042.

    Article  PubMed  Google Scholar 

  • Rastrojo, A. and Alcamí, A. 2017. Aquatic viral metagenomics: Lights and shadows. Virus Res. 239, 87–96.

    Article  CAS  PubMed  Google Scholar 

  • Ren, J., Ahlgren, N.A., Lu, Y.Y., Fuhrman, J.A., and Sun, F. 2017. VirFinder: a novel k-mer based tool for identifying viral sequences from assembled metagenomic data. Microbiome 5, 69.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ren, J., Song, K., Deng, C., Ahlgren, N.A., Fuhrman, J.A., Li, Y., Xie, X., Poplin, R., and Sun, F. 2020. Identifying viruses from metagenomic data using deep learning. Quant. Biol. 1, 64–77.

    Article  CAS  Google Scholar 

  • Rohwer, F., Segall, A., Steward, G., Seguritan, V., Breitbart, M., Wolven, F., and Farooq Azam, F. 2000. The complete genomic sequence of the marine phage Roseophage SIO1 shares homology with nonmarine phages. Limnol. Oceanogr. 45, 408–418.

    Article  CAS  Google Scholar 

  • Ronner, A.B. and Cliver, D.O. 1990. Isolation and characterization of a coliphage specific for Escherichia coli 0157:H7. J. Food Prot. 53, 944–947.

    Article  PubMed  Google Scholar 

  • Roux, S., Brum, J.R., Dutilh, B.E., Sunagawa, S., Duhaime, M.B., Loy, A., Poulos, B.T., Solonenko, N., Lara, E., Poulain, J., et al. 2016a. Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses. Nature 537, 689–693.

    Article  CAS  PubMed  Google Scholar 

  • Roux, S., Chan, L.K., Egan, R., Malmstrom, R.R., McMahon, K.D., and Sullivan, M.B. 2017. Ecogenomics of virophages and their giant virus hosts assessed through time series metagenomics. Nat. Commun. 8, 858.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Roux, S., Enault, F., Hurwitz, B.L., and Sullivan, M.B. 2015. VirSorter: mining viral signal from microbial genomic data. PeerJ 3, e985.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Roux, S., Enault, F., Ravet, V., Colombet, J., Bettarel, Y., Auguet, J.C., Bouvier, T., Lucas-Staat, S., Vellet, A., Prangishvili, D., et al. 2016b. Analysis of metagenomic data reveals common features of halophilic viral communities across continents. Environ. Microbiol. 3, 889–903.

    Article  Google Scholar 

  • Roux, S., Enault, F., Robin, A., Ravet, V., Personnic, S., Theil, S., Colombet, J., Sime-Ngando, T., and Debroas, D. 2012. Assessing the diversity and specificity of two freshwater viral communities through metagenomics. PLoS ONE 7, e33641.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santiago-Rodriguez, T.M., Fornaciari, G., Luciani, S., Dowd, S.E., Toranzos, G.A., Marota, I., and Cano, R.J. 2016. Taxonomic and predicted metabolic profiles of the human gut microbiome in pre-Columbian mummies. FEMS Microbiol. Ecol. 92, fiw182.

    Article  PubMed  CAS  Google Scholar 

  • Schneider, C.L. 2017. Bacteriophage-mediated horizontal gene transfer: transduction. In Harper, D., Abedon, S., Burrowes, B., and McConville, M. (eds.), Bacteriophages, pp. 1–42. Springer, Cham, Switzerland.

    Google Scholar 

  • Sharon, I., Alperovitch, A., Rohwer, F., Haynes, M., Glaser, F., Atamna-Ismaeel, N., Pinter, R.Y., Partensky, F., Koonin, E.V., Wolf, Y.I., et al. 2009. Photosystem I gene cassettes are present in marine virus genomes. Nature 461, 258–262.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simmonds, P., Adams, M.J., Benkõ, M., Breitbart, M., Brister, J.R., Carstens, E.B., Davison, A.J., Delwart, E., Gorbalenya, A.E., Harrach, B., et al. 2017. Consensus statement: virus taxonomy in the age of metagenomics. Nat. Rev. Microbiol. 15, 161–168.

    Article  CAS  PubMed  Google Scholar 

  • Skennerton, C.T., Imelfort, M., and Tyson, G.W. 2013. Crass: identification and reconstruction of CRISPR from unassembled metagenomic data. Nucleic Acids Res. 41, e105.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Skvortsov, T., de Leeuwe, C., Quinn, J.P., McGrath, J.W., Allen, C.C., McElarney, Y., Watson, C., Arkhipova, K., Lavigne, R., and Kulakov, L.A. 2016. Metagenomic characterisation of the viral community of Lough Neagh, the largest freshwater lake in Ireland. PLoS ONE 11, e0150361.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Solonenko, S.A., Ignacio-Espinoza, J.C., Alberti, A., Cruaud, C., Hallam, S., Konstantinidis, K., Tyson, G., Wincker, P., and Sullivan, M.B. 2013. Sequencing platform and library preparation choices impact viral metagenomes. BMC Genomics 14, 320.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Solonenko, S.A. and Sullivan, M.B. 2013. Preparation of metagenomic libraries from naturally occurring marine viruses. Methods Enzymol. 531, 143–165.

    Article  CAS  PubMed  Google Scholar 

  • Steen, A.D., Crits-Christoph, A., Carini, P., DeAngelis, K.M., Fierer, N., Lloyd, K.G., and Thrash, C.J. 2019. High proportions of bacteria and archaea across most biomes remain uncultured. ISME J. 13, 3126–3130.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sullivan, M.B., Waterbury, J.B., and Chisholm, S.W. 2003. Cyanophages infecting the oceanic cyanobacterium Prochlorococcus. Nature 424, 1047–1051.

    Article  CAS  PubMed  Google Scholar 

  • Sunagawa, S., Acinas, S.G., Bork, P., Bowler, C., Tara Oceans Coordinators, Eveillard, D., Gorsky, G., Guidi, L., Iudicone, D., Karsenti, E., et al. 2020. Tara Oceans: towards global ocean ecosystems biology. Nat. Rev. Microbiol. 18, 428–445.

    Article  CAS  PubMed  Google Scholar 

  • Suttle, C.A. 2005. Viruses in the sea. Nature 437, 356–361.

    Article  CAS  PubMed  Google Scholar 

  • Sutton, T.D.S., Clooney, A.G., Ryan, F.J., Ross, R.P., and Hill, C. 2019. Choice of assembly software has a critical impact on virome characterisation. Microbiome 7, 12.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tadmor, A.D., Ottesen, E.A., Leadbetter, J.R., and Phillips, R. 2011. Probing individual environmental bacteria for viruses by using microfluidic digital PCR. Science 333, 58–62.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thammatinna, K., Egan, M.E., Htoo, H.H., Khanna, K., Sugie, J., Nideffer, J.F., Villa, E., Tassanakajon, A., Pogliano, J., Nonejuie, P., et al. 2020. A novel vibriophage exhibits inhibitory activity against host protein synthesis machinery. Sci. Rep. 10, 2347.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomas, J.A., Rolando, M.R., Carroll, C.A., Shen, P.S., Belnap, D.M., Weintraub, S.T., Serwer, P., and Hardies, S.C. 2008. Characterization of Pseudomonas chlororaphis myovirus 201ϕ2-1 via genomic sequencing, mass spectrometry, and electron microscopy. Virology 376, 330–338.

    Article  CAS  PubMed  Google Scholar 

  • Thurber, R.V., Haynes, M., Breitbart, M., Wegley, L., and Rohwer, F. 2009. Laboratory procedures to generate viral metagenomes. Nat. Protoc. 4, 470–483.

    Article  CAS  PubMed  Google Scholar 

  • Van Etten, J.L., Lane, L.C., and Dunigan, D.D. 2010. DNA viruses: the really big ones (Giruses). Annu. Rev. Microbiol. 64, 83–99.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vandeputte, D., Kathagen, G., D’hoe, K., Vieira-Silva, S., Valles-Colomer, M., Sabino, J., Wang, J., Tito, R.Y., De Commer, L., Darzi, Y., et al. 2017. Quantitative microbiome profiling links gut community variation to microbial load. Nature 551, 507–511.

    Article  CAS  PubMed  Google Scholar 

  • Villarroel, J., Kleinheinz, K.A., Jurtz, V.I., Zschach, H., Lund, O., Nielsen, M., and Larsen, M.V. 2016. HostPhinder: a phage host prediction tool. Viruses 8, 116.

    Article  PubMed Central  CAS  Google Scholar 

  • Watkins, S.C., Kuehnle, N., Ruggeri, C.A., Malki, K., Bruder, K., Elayyan, J., Damisch, K., Vahora, N., O’Malley, P., Ruggles-Sage, B., et al. 2015. Assessment of a metaviromic dataset generated from nearshore Lake Michigan. Mar. Freshw. Res. 67, 1700–1708.

    Article  Google Scholar 

  • Williamson, S.J., Rusch, D.B., Yooseph, S., Halpern, A.L., Heidelberg, K.B., Glass, J.I., Andrews-Pfannkoch, C., Fadrosh, D., Miller, C.S., Sutton, G., et al. 2008. The Sorcerer II Global Ocean Sampling Expedition: metagenomic characterization of viruses within aquatic microbial samples. PLoS ONE 3, e1456.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wolf, Y.I., Silas, S., Wang, Y., Wu, S., Bocek, M., Kazlauskas, D., Krupovic, M., Fire, A., Dolja, V.V., and Koonin, E.V. 2020. Doubling of the known set of RNA viruses by metagenomic analysis of an aquatic virome. Nat. Microbiol. 5, 1262–1270.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wommack, K.E. and Colwell, R.R. 2000. Viroplankton: viruses in aquatic ecosystems. Microbiol. Mol. Biol. Rev. 64, 69–114.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wommack, K.E., Williamson, K.E., Helton, R.R., Bench, S.R., and Winget, D.M. 2009. Methods for the isolation of viruses from environmental samples. In Clokie, M.R. and Kropinski, A.M. (eds.), Bacteriophages. Methods in Molecular Biology, pp. 3–14. Homana press, Totowa, New Jersey, USA.

    Chapter  Google Scholar 

  • Wong, H.C., Wang, T.Y., Yang, C.W., Tang, C.T., Ying, C., Wang, C.H., and Chang, W.H. 2019. Characaterization of a lytic vibriophage VP06 of Vibrio parahaemolyticus. Res. Microbiol. 170, 13–23.

    Article  CAS  PubMed  Google Scholar 

  • Yang, M., Liang, Y., Huang, S., Zhang, J., Wang, J., Chen, H., Ye, Y., Gao, X., Wu, Q., and Tan, Z. 2020. Isolation and characterization of the novel phages vB_VpS_BA3 and vB_VpS_CA8 for lysing Vibrio parahaemolyticus. Front. Microbiol. 11, 259.

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang, Y., Lu, S., Shen, W., Zhao, X., Shen, M., Tan, Y., Li, G., Li, M., Wang, J., Hu, F., et al. 2016. Characterization of the first doublestranded RNA bacteriophage infecting Pseudomonas aeruginosa. Sci. Rep. 6, 38795.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshida, M., Mochizuki, T., Urayama, S.I., Yoshida-Takashima, Y., Nishi, S., Hirai, M., Nomaki, H., Takaki, Y., Nunoura, T., and Takai, K. 2018. Quantitative viral community DNA analysis reveals the dominance of single-stranded DNA viruses in offshore upper bathyal sediment from Tohoku, Japan. Front. Microbiol. 9, 75.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zaragoza-Solas, A., Rodriguez-Valera, F., and López-Pérez, M. 2020. Metagenome mining reveals hidden genomic diversity of pelagimyophages in aquatic environments. mSystems 5, e00905–19.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zeidner, G., Bielawski, J.P., Shmoish, M., Scanlan, D.J., Sabehi, G., and Béjà, O. 2005. Potential photosynthesis gene recombination between Prochlorococcus and Synechococcus via viral intermediates. Environ. Microbiol. 7, 1505–1513.

    Article  CAS  PubMed  Google Scholar 

  • Zeigler Allen, L., McCrow, J.P., Ininbergs, K., Dupont, C.L., Badger, J.H., Hoffman, J.M., Ekman, M., Allen, A.E., Bergman, B., and Venter, J.C. 2017. The Baltic Sea Virome: diversity and transcriptional activity of DNA and RNA viruses. mSystems 2, e00125–16.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang, Z., Chen, F., Chu, X., Zhang, H., Luo, H., Qin, F., Zhai, Z., Yang, M., Sun, J., and Zhao, Y. 2019. Diverse, abundant, and novel viruses infecting the marine Roseobacter RCA lineage. mSystems 4, e00494–19.

    PubMed  PubMed Central  Google Scholar 

  • Zhang, F., Zhao, S., Ren, C., Zhu, Y., Zhou, H., Lai, Y., Zhou, F., Jia, Y., Zheng, K., and Huang, Z. 2018. CRISPRminer is a knowledge base for exploring CRISPR-Cas systems in microbe and phage interactions. Commun. Biol. 1, 180.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhao, Y., Qin, F., Zhang, R., Giovannoni, S.J., Zhang, Z., Sun, J., Du, S., and Rensing, C. 2019. Pelagiphages in the Podoviridae family integrate into host genomes. Environ. Microbiol. 21, 1989–2001.

    Article  CAS  PubMed  Google Scholar 

  • Zhao, Y., Temperton, B., Thrash, J.C., Schwalbach, M.S., Vergin, K.L., Landry, Z.C., Ellisman, M., Deerinck, T., Sullivan, M.B., and Giovannoni, S.J. 2013. Abundant SAR11 viruses in the ocean. Nature 494, 357–360.

    Article  CAS  PubMed  Google Scholar 

  • Zhong, Z.P., Rapp, J.Z., Wainaina, J.M., Solonenko, N.E., Maughan, H., Carpenter, S.D., Cooper, Z.S., Jang, H.B., Bolduc, B., Deming, J.W., et al. 2020. Viral ecogenomics of arctic cryopeg brine and sea ice. mSystems 5, e00246–20.

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This study was supported by the Mid-Career Research Program through the National Research Foundation (NRF) funded by the Ministry of Sciences and ICT (NRF-2019R1A2B5B02070538 to J-CC), the Science Research Center grant of the NRF (NRF-2018R1A5A1025077 to J-CC), and the Research Staff Program (RF-2019R1I1A1A01062072 to KM).

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  1. Biological Resources Utilization Division, Honam National Institute of Biological Resources, Mokpo, 58762, Republic of Korea

    Kira Moon

  2. Department of Biological Sciences and Bioengineering, Inha University, Incheon, 22212, Republic of Korea

    Jang-Cheon Cho

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Moon, K., Cho, JC. Metaviromics coupled with phage-host identification to open the viral ‘black box’. J Microbiol. 59, 311–323 (2021). https://doi.org/10.1007/s12275-021-1016-9

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