{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,15]],"date-time":"2026-09-15T18:15:48Z","timestamp":1789496148192,"version":"build-2803163510"},"reference-count":71,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2020,10,22]],"date-time":"2020-10-22T00:00:00Z","timestamp":1603324800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>Permafrost thaw lakes including thermokarst lakes and ponds are ubiquitous features of Subarctic and Arctic landscapes and are hotspots of microbial activity. Input of terrestrial organic matter into the planktonic microbial loop of these lakes may greatly amplify global greenhouse gas emissions. This microbial loop, dominated in the summer by aerobic microorganisms including phototrophs, is radically different in the winter, when metabolic processes shift to the anaerobic degradation of organic matter. Little is known about the viruses that infect these microbes, despite evidence that viruses can control microbial populations and influence biogeochemical cycling in other systems. Here, we present the results of a metagenomics-based study of viruses in the larger than 0.22 \u00b5m fraction across two seasons (summer and winter) in a permafrost thaw lake in Subarctic Canada. We uncovered 351 viral populations (vOTUs) in the surface waters of this lake, with diversity significantly greater during the summer. We also identified and characterized several phage genomes and prophages, which were mostly present in the summer. Finally, we compared the viral community of this waterbody to other habitats and found unexpected similarities with distant bog lakes in North America.<\/jats:p>","DOI":"10.3390\/v12111204","type":"journal-article","created":{"date-parts":[[2020,10,22]],"date-time":"2020-10-22T10:27:58Z","timestamp":1603362478000},"page":"1204","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Seasonal Regime Shift in the Viral Communities of a Permafrost Thaw Lake"],"prefix":"10.3390","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-3899-0180","authenticated-orcid":false,"given":"Catherine","family":"Girard","sequence":"first","affiliation":[{"name":"D\u00e9partement de Biochimie, de Microbiologie et de Bio-Informatique, Universit\u00e9 Laval, Qu\u00e9bec, QC G1V 0A6, Canada"},{"name":"Centre d\u2019\u00e9tudes Nordiques (CEN), Universit\u00e9 Laval, Qu\u00e9bec, QC G1V 0A6, Canada"},{"name":"Institut de Biologie Int\u00e9grative et des Syst\u00e8mes (IBIS), Universit\u00e9 Laval, Qu\u00e9bec, QC G1V 0A6, Canada"},{"name":"Takuvik Joint International Laboratory, Universit\u00e9 Laval, Qu\u00e9bec, QC G1V 0A6, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1326-7081","authenticated-orcid":false,"given":"Val\u00e9rie","family":"Langlois","sequence":"additional","affiliation":[{"name":"D\u00e9partement de Biochimie, de Microbiologie et de Bio-Informatique, Universit\u00e9 Laval, Qu\u00e9bec, QC G1V 0A6, Canada"},{"name":"Centre d\u2019\u00e9tudes Nordiques (CEN), Universit\u00e9 Laval, Qu\u00e9bec, QC G1V 0A6, Canada"},{"name":"Institut de Biologie Int\u00e9grative et des Syst\u00e8mes (IBIS), Universit\u00e9 Laval, Qu\u00e9bec, QC G1V 0A6, Canada"},{"name":"Takuvik Joint International Laboratory, Universit\u00e9 Laval, Qu\u00e9bec, QC G1V 0A6, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adrien","family":"Vigneron","sequence":"additional","affiliation":[{"name":"Centre d\u2019\u00e9tudes Nordiques (CEN), Universit\u00e9 Laval, Qu\u00e9bec, QC G1V 0A6, Canada"},{"name":"Institut de Biologie Int\u00e9grative et des Syst\u00e8mes (IBIS), Universit\u00e9 Laval, Qu\u00e9bec, QC G1V 0A6, Canada"},{"name":"Takuvik Joint International Laboratory, Universit\u00e9 Laval, Qu\u00e9bec, QC G1V 0A6, Canada"},{"name":"D\u00e9partement de Biologie, Universit\u00e9 Laval, Qu\u00e9bec, QC G1V 0A6, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9055-1938","authenticated-orcid":false,"given":"Warwick F.","family":"Vincent","sequence":"additional","affiliation":[{"name":"Centre d\u2019\u00e9tudes Nordiques (CEN), Universit\u00e9 Laval, Qu\u00e9bec, QC G1V 0A6, Canada"},{"name":"Institut de Biologie Int\u00e9grative et des Syst\u00e8mes (IBIS), Universit\u00e9 Laval, Qu\u00e9bec, QC G1V 0A6, Canada"},{"name":"Takuvik Joint International Laboratory, Universit\u00e9 Laval, Qu\u00e9bec, QC G1V 0A6, Canada"},{"name":"D\u00e9partement de Biologie, Universit\u00e9 Laval, Qu\u00e9bec, QC G1V 0A6, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6639-9112","authenticated-orcid":false,"given":"Alexander I.","family":"Culley","sequence":"additional","affiliation":[{"name":"D\u00e9partement de Biochimie, de Microbiologie et de Bio-Informatique, Universit\u00e9 Laval, Qu\u00e9bec, QC G1V 0A6, Canada"},{"name":"Centre d\u2019\u00e9tudes Nordiques (CEN), Universit\u00e9 Laval, Qu\u00e9bec, QC G1V 0A6, Canada"},{"name":"Institut de Biologie Int\u00e9grative et des Syst\u00e8mes (IBIS), Universit\u00e9 Laval, Qu\u00e9bec, QC G1V 0A6, Canada"},{"name":"Takuvik Joint International Laboratory, Universit\u00e9 Laval, Qu\u00e9bec, QC G1V 0A6, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,10,22]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"221","DOI":"10.5194\/tc-6-221-2012","article-title":"Derivation and analysis of a high-resolution estimate of global permafrost zonation","volume":"6","author":"Gruber","year":"2012","journal-title":"Cryosphere"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1038\/nature14338","article-title":"Climate change and the permafrost carbon feedback","volume":"520","author":"Schuur","year":"2015","journal-title":"Nature"},{"key":"ref_3","unstructured":"P\u00f6rtner, H.-O., Roberts, D.C., Masson-Delmotte, V., Zhai, P., Tignor, M., Poloczanska, E., Mintenbeck, K., Nicolai, M., Okem, A., and Petzold, J. (2019). IPCC. Summary for Policymakers. IPCC Special Report on the Ocean and Cryosphere in a Changing Climate, in press."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"264","DOI":"10.1038\/s41467-018-08240-4","article-title":"Permafrost is warming at a global scale","volume":"10","author":"Biskaborn","year":"2019","journal-title":"Nat. Commun."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"414","DOI":"10.1038\/nrmicro3262","article-title":"The microbial ecology of permafrost","volume":"12","author":"Jansson","year":"2014","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"7129","DOI":"10.5194\/bg-12-7129-2015","article-title":"Reviews and syntheses: Effects of permafrost thaw on Arctic aquatic ecosystems","volume":"12","author":"Vonk","year":"2015","journal-title":"Biogeosciences"},{"key":"ref_7","unstructured":"Vincent, W.F., and Laybourne-Parry, J. (2008). Origin and Geomorphology of Lakes in the Polar Regions in: Polar Lakes and Rivers: Limnology of Arctic and Antarctic Aquatic Ecosystems, Oxford University Press."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"116","DOI":"10.1016\/j.geomorph.2016.08.007","article-title":"Spatial distribution of thermokarst terrain in Arctic Alaska","volume":"273","author":"Farquharson","year":"2016","journal-title":"Geomorphology"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1002\/2013EO420002","article-title":"Adapting to permafrost change: A science framework","volume":"94","author":"Vincent","year":"2013","journal-title":"Eos Trans. Am. Geophys. Union"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"S150","DOI":"10.1002\/lno.10311","article-title":"High methane emissions from thermokarst lakes in subarctic peatlands: Methane emissions from peatland thermokarst takes","volume":"61","author":"Matveev","year":"2016","journal-title":"Limnol. Oceanogr."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Negandhi, K., Laurion, I., Whiticar, M.J., Galand, P.E., Xu, X., and Lovejoy, C. (2013). Small thaw ponds: An unaccounted source of methane in the Canadian High Arctic. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0078204"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"115","DOI":"10.4319\/lo.2010.55.1.0115","article-title":"Variability in greenhouse gas emissions from permafrost thaw ponds","volume":"55","author":"Laurion","year":"2010","journal-title":"Limnol. Oceanogr."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1038\/ngeo2578","article-title":"Climate-sensitive northern lakes and ponds are critical components of methane release","volume":"9","author":"Wik","year":"2016","journal-title":"Nat. Geosci."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"769","DOI":"10.1016\/j.tim.2020.04.002","article-title":"Roles of thermokarst lakes in a warming world","volume":"28","author":"Liebner","year":"2020","journal-title":"Trends Microbiol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"175","DOI":"10.5194\/bg-13-175-2016","article-title":"Co-occurrence patterns in aquatic bacterial communities across changing permafrost landscapes","volume":"13","author":"Comte","year":"2016","journal-title":"Biogeosciences"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"192","DOI":"10.3389\/fmicb.2015.00192","article-title":"Bacterial community structure across environmental gradients in permafrost thaw ponds: Methanotroph-rich ecosystems","volume":"6","author":"Crevecoeur","year":"2015","journal-title":"Front. Microbiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1656","DOI":"10.3389\/fmicb.2019.01656","article-title":"Contrasting winter versus summer microbial communities and metabolic functions in a permafrost thaw lake","volume":"10","author":"Vigneron","year":"2019","journal-title":"Front. Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1669","DOI":"10.1007\/s00300-014-1555-1","article-title":"Bacterial communities and greenhouse gas emissions of shallow ponds in the High Arctic","volume":"37","author":"Negandhi","year":"2014","journal-title":"Polar Biol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"31312","DOI":"10.1038\/srep31312","article-title":"Environmental selection of planktonic methanogens in permafrost thaw ponds","volume":"6","author":"Crevecoeur","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"fiw117","DOI":"10.1093\/femsec\/fiw117","article-title":"Temperature effects on net greenhouse gas production and bacterial communities in arctic thaw ponds","volume":"92","author":"Negandhi","year":"2016","journal-title":"FEMS Microbiol. Ecol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1038\/s41579-019-0270-x","article-title":"Metabolic and biogeochemical consequences of viral infection in aquatic ecosystems","volume":"18","author":"Zimmerman","year":"2020","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"16205","DOI":"10.1038\/nmicrobiol.2016.205","article-title":"Environmental microbiology: Viral diversity on the global stage","volume":"1","author":"Suttle","year":"2016","journal-title":"Nat. Microbiol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1016\/j.virusres.2017.11.008","article-title":"New insight into the RNA aquatic virosphere via viromics","volume":"244","author":"Culley","year":"2018","journal-title":"Virus Res."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1111\/j.1574-6976.2008.00132.x","article-title":"RNA viruses in the sea","volume":"33","author":"Lang","year":"2009","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1069","DOI":"10.1111\/j.1365-2427.2008.02014.x","article-title":"Viruses in freshwater ecosystems: An introduction to the exploration of viruses in new aquatic habitats","volume":"53","author":"Middelboe","year":"2008","journal-title":"Freshw. Biol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"e00667-16","DOI":"10.1128\/mBio.00667-16","article-title":"Viruses infecting a freshwater filamentous cyanobacterium (Nostoc sp.) encode a functional CRISPR array and a proteobacterial DNA polymerase B","volume":"7","author":"Wirth","year":"2016","journal-title":"mBio"},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Palermo, C.N., Fulthorpe, R.R., Saati, R., and Short, S.M. (2019). Metagenomic analysis of virus diversity and relative abundance in a eutrophic freshwater harbour. Viruses, 11.","DOI":"10.1101\/690891"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1016\/j.watres.2017.07.053","article-title":"Differential impact of lytic viruses on the taxonomical resolution of freshwater bacterioplankton community structure","volume":"124","author":"Keshri","year":"2017","journal-title":"Water Res."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1038\/nature08060","article-title":"Viruses manipulate the marine environment","volume":"459","author":"Rohwer","year":"2009","journal-title":"Nature"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"12166","DOI":"10.1073\/pnas.1310671110","article-title":"Insight into the unknown marine virus majority","volume":"110","author":"Culley","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"209","DOI":"10.3354\/ame01893","article-title":"Chlorovirus and myovirus diversity in permafrost thaw ponds","volume":"82","author":"Vincent","year":"2018","journal-title":"Aquat. Microb. Ecol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"3008","DOI":"10.1098\/rstb.2012.0243","article-title":"Warming shifts top-down and bottom-up control of pond food web structure and function","volume":"367","author":"Shurin","year":"2012","journal-title":"Philos. Trans. R. Soc. B Biol. Sci."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"870","DOI":"10.1038\/s41564-018-0190-y","article-title":"Host-linked soil viral ecology along a permafrost thaw gradient","volume":"3","author":"Emerson","year":"2018","journal-title":"Nat. Microbiol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1139\/as-2016-0027","article-title":"Arctic permafrost landscapes in transition: Towards an integrated Earth system approach","volume":"3","author":"Vincent","year":"2017","journal-title":"Arct. Sci."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1002\/lol2.10063","article-title":"Increasing dominance of terrigenous organic matter in circumpolar freshwaters due to permafrost thaw: Increasing allochthony in arctic freshwaters","volume":"3","author":"Wauthy","year":"2018","journal-title":"Limnol. Oceanogr. Lett."},{"key":"ref_36","unstructured":"Matveev, A., Laurion, I., Deshpande, B.N., and Vincent, W.F. (2020). Concentrations of dissolved methane, carbon dioxide and oxygen in thermokarst lakes and ponds in palsa peatlands, Northern Quebec, Canada, v. 1.100000 (2012\u20132017). Nordicana, D48."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1015","DOI":"10.1002\/lom3.10221","article-title":"Open the SterivexTM casing: An easy and effective way to improve DNA extraction yields: DNA extraction from SterivexTM filters","volume":"15","author":"Cruaud","year":"2017","journal-title":"Limnol. Oceanogr. Methods"},{"key":"ref_38","unstructured":"Andrews, S. (2020, October 21). FastQC: A Quality Control Tool for High Throughput Sequence Data, Available online: http:\/\/www.bioinformatics.babraham.ac.uk\/projects\/fastqc."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"2114","DOI":"10.1093\/bioinformatics\/btu170","article-title":"Trimmomatic: A flexible trimmer for Illumina sequence data","volume":"30","author":"Bolger","year":"2014","journal-title":"Bioinformatics"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1420","DOI":"10.1093\/bioinformatics\/bts174","article-title":"IDBA-UD: A de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth","volume":"28","author":"Peng","year":"2012","journal-title":"Bioinformatics"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"e985","DOI":"10.7717\/peerj.985","article-title":"VirSorter: Mining viral signal from microbial genomic data","volume":"3","author":"Roux","year":"2015","journal-title":"PeerJ"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1186\/s40168-017-0283-5","article-title":"VirFinder: A novel k-mer based tool for identifying viral sequences from assembled metagenomic data","volume":"5","author":"Ren","year":"2017","journal-title":"Microbiome"},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., and Madden, T.L. (2009). BLAST+: Architecture and applications. BMC Bioinf., 10.","DOI":"10.1186\/1471-2105-10-421"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1016\/S0022-2836(05)80360-2","article-title":"Basic Local Alignment Search Tool","volume":"215","author":"Altschu","year":"1990","journal-title":"J. Mol. Biol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1038\/ismej.2016.89","article-title":"iVirus: Facilitating new insights in viral ecology with software and community data sets imbedded in a cyberinfrastructure","volume":"11","author":"Bolduc","year":"2017","journal-title":"ISME J."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1038\/nmeth.1923","article-title":"Fast gapped-read alignment with Bowtie 2","volume":"9","author":"Langmead","year":"2012","journal-title":"Nat. Methods"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"2078","DOI":"10.1093\/bioinformatics\/btp352","article-title":"1000 Genome Project Data Processing Subgroup The Sequence Alignment\/Map format and SAMtools","volume":"25","author":"Li","year":"2009","journal-title":"Bioinformatics"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"e00039-18","DOI":"10.1128\/mSystems.00039-18","article-title":"Nonpareil 3: Fast Estimation of metagenomic coverage and sequence diversity","volume":"3","author":"Gunturu","year":"2018","journal-title":"MSystems"},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"R Core Team (2017). R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing. Version 3.6.1.","DOI":"10.1201\/9780203758212-1"},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Wickham, H. (2016). ggplot2: Elegant Graphics for Data Analysis, Springer.","DOI":"10.1007\/978-3-319-24277-4_9"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1200","DOI":"10.1038\/nmeth.2658","article-title":"Differential abundance analysis for microbial marker-gene surveys","volume":"10","author":"Paulson","year":"2013","journal-title":"Nat. Methods"},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"McMurdie, P.J., and Holmes, S. (2013). phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0061217"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"2068","DOI":"10.1093\/bioinformatics\/btu153","article-title":"Prokka: Rapid prokaryotic genome annotation","volume":"30","author":"Seemann","year":"2014","journal-title":"Bioinformatics"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"2379","DOI":"10.1093\/bioinformatics\/btx157","article-title":"ViPTree: The viral proteomic tree server","volume":"33","author":"Nishimura","year":"2017","journal-title":"Bioinformatics"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"W200","DOI":"10.1093\/nar\/gky448","article-title":"HMMER web server: 2018 update","volume":"46","author":"Potter","year":"2018","journal-title":"Nucleic Acids Res."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1038\/nature19094","article-title":"Uncovering Earth\u2019s virome","volume":"536","author":"Pavlopoulos","year":"2016","journal-title":"Nature"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"1673","DOI":"10.1038\/nprot.2017.063","article-title":"Nontargeted virus sequence discovery pipeline and virus clustering for metagenomic data","volume":"12","author":"Pavlopoulos","year":"2017","journal-title":"Nat. Protoc."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1038\/nbt.4306","article-title":"Minimum Information about an Uncultivated Virus Genome (MIUViG)","volume":"37","author":"Roux","year":"2019","journal-title":"Nat. Biotechnol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"1103","DOI":"10.1016\/j.cell.2016.08.007","article-title":"Toward accurate and quantitative comparative metagenomics","volume":"166","author":"Nayfach","year":"2016","journal-title":"Cell"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"13","DOI":"10.5194\/bg-13-13-2016","article-title":"Phototrophic pigment diversity and picophytoplankton in permafrost thaw lakes","volume":"13","author":"Przytulska","year":"2016","journal-title":"Biogeosciences"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1038\/ismej.2015.125","article-title":"Seasonal time bombs: Dominant temperate viruses affect Southern Ocean microbial dynamics","volume":"10","author":"Brum","year":"2016","journal-title":"ISME J."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"1605","DOI":"10.1016\/j.csbj.2020.06.019","article-title":"Computational approaches in viral ecology","volume":"18","author":"Khot","year":"2020","journal-title":"Comput. Struct. Biotechnol. J."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"gkw1030","DOI":"10.1093\/nar\/gkw1030","article-title":"IMG\/VR: A database of cultured and uncultured DNA Viruses and retroviruses","volume":"45","author":"Chen","year":"2016","journal-title":"Nucleic Acids Res."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1111\/j.1574-6968.2004.tb09654.x","article-title":"Global distribution of nearly identical phage-encoded DNA sequences","volume":"236","author":"Breitbart","year":"2004","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"278","DOI":"10.1016\/j.tim.2005.04.003","article-title":"Here a virus, there a virus, everywhere the same virus?","volume":"13","author":"Breitbart","year":"2005","journal-title":"Trends Microbiol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"858","DOI":"10.1038\/s41467-017-01086-2","article-title":"Ecogenomics of virophages and their giant virus hosts assessed through time series metagenomics","volume":"8","author":"Roux","year":"2017","journal-title":"Nat. Commun."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"4403","DOI":"10.1038\/s41467-020-18236-8","article-title":"Flexible genes establish widespread bacteriophage pan-genomes in cryoconite hole ecosystems","volume":"11","author":"Bellas","year":"2020","journal-title":"Nat. Commun."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"e00169-17","DOI":"10.1128\/mSphere.00169-17","article-title":"Bacterial community composition and dynamics spanning five years in freshwater bog lakes","volume":"2","author":"Linz","year":"2017","journal-title":"mSphere"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"6643","DOI":"10.1073\/pnas.1423667112","article-title":"Infection of phytoplankton by aerosolized marine viruses","volume":"112","author":"Sharoni","year":"2015","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"1154","DOI":"10.1038\/s41396-017-0042-4","article-title":"Deposition rates of viruses and bacteria above the atmospheric boundary layer","volume":"12","author":"Reche","year":"2018","journal-title":"ISME J."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"1109","DOI":"10.1016\/j.cell.2019.03.040","article-title":"Marine DNA viral macro- and microdiversity from pole to pole","volume":"177","author":"Gregory","year":"2019","journal-title":"Cell"}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/12\/11\/1204\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T10:26:08Z","timestamp":1760178368000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/12\/11\/1204"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,10,22]]},"references-count":71,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2020,11]]}},"alternative-id":["v12111204"],"URL":"https:\/\/doi.org\/10.3390\/v12111204","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,10,22]]}}}