Diversity, taxonomy, and evolution of archaeal viruses of the class Caudoviricetes

Liu, Ying; Demina, Tatiana A.; Roux, Simon; Aiewsakun, Pakorn; Kazlauskas, Darius; Simmonds, Peter; Prangishvili, David; Oksanen, Hanna M.; Krupovic, Mart; Suttle, ed., Curtis

doi:10.1371/journal.pbio.3001442

Diversity, taxonomy, and evolution of archaeal viruses of the class Caudoviricetes

Journal Article · Mon Nov 08 23:00:00 EST 2021 · PLoS Biology (Online)

DOI:https://doi.org/10.1371/journal.pbio.3001442· OSTI ID:1834437

; ; ; ; ; Simmonds, Peter; Prangishvili, David; ; ; Suttle, ed., Curtis

The archaeal tailed viruses (arTV), evolutionarily related to tailed double-stranded DNA (dsDNA) bacteriophages of the class Caudoviricetes , represent the most common isolates infecting halophilic archaea. Only a handful of these viruses have been genomically characterized, limiting our appreciation of their ecological impacts and evolution. Here, we present 37 new genomes of haloarchaeal tailed virus isolates, more than doubling the current number of sequenced arTVs. Analysis of all 63 available complete genomes of arTVs, which we propose to classify into 14 new families and 3 orders, suggests ancient divergence of archaeal and bacterial tailed viruses and points to an extensive sharing of genes involved in DNA metabolism and counterdefense mechanisms, illuminating common strategies of virus–host interactions with tailed bacteriophages. Coupling of the comparative genomics with the host range analysis on a broad panel of haloarchaeal species uncovered 4 distinct groups of viral tail fiber adhesins controlling the host range expansion. The survey of metagenomes using viral hallmark genes suggests that the global architecture of the arTV community is shaped through recurrent transfers between different biomes, including hypersaline, marine, and anoxic environments.

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Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1834437

Alternate ID(s):: OSTI ID: 1829546
OSTI ID: 1855197

Journal Information:: PLoS Biology (Online), Journal Name: PLoS Biology (Online) Journal Issue: 11 Vol. 19; ISSN 1545-7885

Publisher:: Public Library of Science (PLoS)Copyright Statement

Country of Publication:: United States

Language:: English

References (97)

Protein Sequence Analysis Using the MPI Bioinformatics Toolkit Gabler, Felix; Nam, Seung‐Zin; Till, Sebastian Current Protocols in Bioinformatics, Vol. 72, Issue 1 https://doi.org/10.1002/cpbi.108	journal	December 2020
Characterization of the lytic archaeal virus Drs3 infecting Methanobacterium formicicum Wolf, Sandro; Fischer, Martin A.; Kupczok, Anne Archives of Virology, Vol. 164, Issue 3 https://doi.org/10.1007/s00705-018-04120-w	journal	December 2018
Regulation of carbamoylphosphate synthesis in Escherichia coli: an amazing metabolite at the crossroad of arginine and pyrimidine biosynthesis Charlier, Daniel; Nguyen Le Minh, Phu; Roovers, Martine Amino Acids, Vol. 50, Issue 12 https://doi.org/10.1007/s00726-018-2654-z	journal	September 2018
A large-scale evaluation of algorithms to calculate average nucleotide identity Yoon, Seok-Hwan; Ha, Sung-min; Lim, Jeongmin Antonie van Leeuwenhoek, Vol. 110, Issue 10 https://doi.org/10.1007/s10482-017-0844-4	journal	February 2017
Extremely halophilic archaea and the issue of long-term microbial survival Fendrihan, Sergiu; Legat, Andrea; Pfaffenhuemer, Marion Reviews in Environmental Science and Bio/Technology, Vol. 5, Issue 2-3 https://doi.org/10.1007/s11157-006-0007-y	journal	July 2006
Marine DNA Viral Macro- and Microdiversity from Pole to Pole Gregory, Ann C.; Zayed, Ahmed A.; Conceição-Neto, Nádia Cell, Vol. 177, Issue 5 https://doi.org/10.1016/j.cell.2019.03.040	journal	May 2019
Massive expansion of human gut bacteriophage diversity Camarillo-Guerrero, Luis F.; Almeida, Alexandre; Rangel-Pineros, Guillermo Cell, Vol. 184, Issue 4 https://doi.org/10.1016/j.cell.2021.01.029	journal	February 2021
The Human Gut Virome Is Highly Diverse, Stable, and Individual Specific Shkoporov, Andrey N.; Clooney, Adam G.; Sutton, Thomas D. S. Cell Host & Microbe, Vol. 26, Issue 4 https://doi.org/10.1016/j.chom.2019.09.009	journal	October 2019
The Gut Virome Database Reveals Age-Dependent Patterns of Virome Diversity in the Human Gut Gregory, Ann C.; Zablocki, Olivier; Zayed, Ahmed A. Cell Host & Microbe, Vol. 28, Issue 5 https://doi.org/10.1016/j.chom.2020.08.003	journal	November 2020
The amazing HK97 fold: versatile results of modest differences Duda, Robert L.; Teschke, Carolyn M. Current Opinion in Virology, Vol. 36 https://doi.org/10.1016/j.coviro.2019.02.001	journal	June 2019
Novel Abundant Oceanic Viruses of Uncultured Marine Group II Euryarchaeota Philosof, Alon; Yutin, Natalya; Flores-Uribe, José Current Biology, Vol. 27, Issue 9 https://doi.org/10.1016/j.cub.2017.03.052	journal	May 2017
The Roles of Ribosomal Proteins in the Structure Assembly, and Evolution of the Large Ribosomal Subunit Klein, D. J.; Moore, P. B.; Steitz, T. A. Journal of Molecular Biology, Vol. 340, Issue 1 https://doi.org/10.1016/j.jmb.2004.03.076	journal	June 2004
Comparative Analysis of the Mosaic Genomes of Tailed Archaeal Viruses and Proviruses Suggests Common Themes for Virion Architecture and Assembly with Tailed Viruses of Bacteria Krupovič, Mart; Forterre, Patrick; Bamford, Dennis H. Journal of Molecular Biology, Vol. 397, Issue 1 https://doi.org/10.1016/j.jmb.2010.01.037	journal	March 2010
The AAA+ motor complex of subunits CobS and CobT of cobaltochelatase visualized by single particle electron microscopy Lundqvist, Joakim; Elmlund, Dominika; Heldt, Dana Journal of Structural Biology, Vol. 167, Issue 3 https://doi.org/10.1016/j.jsb.2009.06.013	journal	September 2009
Haloviruses of archaea, bacteria, and eukaryotes Atanasova, Nina S.; Oksanen, Hanna M.; Bamford, Dennis H. Current Opinion in Microbiology, Vol. 25 https://doi.org/10.1016/j.mib.2015.04.001	journal	June 2015
Salmonella Phage S16 Tail Fiber Adhesin Features a Rare Polyglycine Rich Domain for Host Recognition Dunne, Matthew; Denyes, Jenna M.; Arndt, Helena Structure, Vol. 26, Issue 12 https://doi.org/10.1016/j.str.2018.07.017	journal	December 2018
Archaeal viruses and bacteriophages: comparisons and contrasts Pietilä, Maija K.; Demina, Tatiana A.; Atanasova, Nina S. Trends in Microbiology, Vol. 22, Issue 6 https://doi.org/10.1016/j.tim.2014.02.007	journal	June 2014
Bacteriophage lambda: Early pioneer and still relevant Casjens, Sherwood R.; Hendrix, Roger W. Virology, Vol. 479-480 https://doi.org/10.1016/j.virol.2015.02.010	journal	May 2015
The genomic content and context of auxiliary metabolic genes in marine cyanomyoviruses Crummett, Lisa T.; Puxty, Richard J.; Weihe, Claudia Virology, Vol. 499 https://doi.org/10.1016/j.virol.2016.09.016	journal	December 2016
Uncovering Earth’s virome Paez-Espino, David; Eloe-Fadrosh, Emiley A.; Pavlopoulos, Georgios A. Nature, Vol. 536, Issue 7617 https://doi.org/10.1038/nature19094	journal	August 2016
Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses Roux, Simon; Brum, Jennifer R.; Dutilh, Bas E. Nature, Vol. 537, Issue 7622 https://doi.org/10.1038/nature19366	journal	September 2016
The enigmatic archaeal virosphere Prangishvili, David; Bamford, Dennis H.; Forterre, Patrick Nature Reviews Microbiology, Vol. 15, Issue 12 https://doi.org/10.1038/nrmicro.2017.125	journal	November 2017
The archaeal cell envelope Albers, Sonja-Verena; Meyer, Benjamin H. Nature Reviews Microbiology, Vol. 9, Issue 6 https://doi.org/10.1038/nrmicro2576	journal	May 2011
Discovery of several novel, widespread, and ecologically distinct marine Thaumarchaeota viruses that encode amoC nitrification genes Ahlgren, Nathan A.; Fuchsman, Clara A.; Rocap, Gabrielle The ISME Journal, Vol. 13, Issue 3 https://doi.org/10.1038/s41396-018-0289-4	journal	October 2018
New virus isolates from Italian hydrothermal environments underscore the biogeographic pattern in archaeal virus communities Baquero, Diana P.; Contursi, Patrizia; Piochi, Monica The ISME Journal, Vol. 14, Issue 7 https://doi.org/10.1038/s41396-020-0653-z	journal	April 2020
Numerous cultivated and uncultivated viruses encode ribosomal proteins Mizuno, Carolina M.; Guyomar, Charlotte; Roux, Simon Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-08672-6	journal	February 2019
7-Deazaguanine modifications protect phage DNA from host restriction systems Hutinet, Geoffrey; Kot, Witold; Cui, Liang Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13384-y	journal	November 2019
Phage puppet masters of the marine microbial realm Breitbart, Mya; Bonnain, Chelsea; Malki, Kema Nature Microbiology, Vol. 3, Issue 7 https://doi.org/10.1038/s41564-018-0166-y	journal	June 2018
Doubling of the known set of RNA viruses by metagenomic analysis of an aquatic virome Wolf, Yuri I.; Silas, Sukrit; Wang, Yongjie Nature Microbiology, Vol. 5, Issue 10 https://doi.org/10.1038/s41564-020-0755-4	journal	July 2020
Targeting mechanisms of tailed bacteriophages Nobrega, Franklin L.; Vlot, Marnix; de Jonge, Patrick A. Nature Reviews Microbiology, Vol. 16, Issue 12 https://doi.org/10.1038/s41579-018-0070-8	journal	August 2018
Phage diversity, genomics and phylogeny Dion, Moïra B.; Oechslin, Frank; Moineau, Sylvain Nature Reviews Microbiology, Vol. 18, Issue 3 https://doi.org/10.1038/s41579-019-0311-5	journal	February 2020
The LUCA and its complex virome Krupovic, Mart; Dolja, Valerian V.; Koonin, Eugene V. Nature Reviews Microbiology, Vol. 18, Issue 11 https://doi.org/10.1038/s41579-020-0408-x	journal	July 2020
Highly accurate protein structure prediction with AlphaFold Jumper, John; Evans, Richard; Pritzel, Alexander Nature https://doi.org/10.1038/s41586-021-03819-2	journal	July 2021
Taxonomic assignment of uncultivated prokaryotic virus genomes is enabled by gene-sharing networks Bin Jang, Ho; Bolduc, Benjamin; Zablocki, Olivier Nature Biotechnology, Vol. 37, Issue 6 https://doi.org/10.1038/s41587-019-0100-8	journal	May 2019
PhageTerm: a tool for fast and accurate determination of phage termini and packaging mechanism using next-generation sequencing data Garneau, Julian R.; Depardieu, Florence; Fortier, Louis-Charles Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-07910-5	journal	August 2017
A thaumarchaeal provirus testifies for an ancient association of tailed viruses with archaea Krupovic, Mart; Spang, Anja; Gribaldo, Simonetta Biochemical Society Transactions, Vol. 39, Issue 1 https://doi.org/10.1042/BST0390082	journal	January 2011
Molecular analysis of Methanobacterium phage ΨM2 Pfister, Peter; Wasserfallen, Alain; Stettler, Rolf Molecular Microbiology, Vol. 30, Issue 2 https://doi.org/10.1046/j.1365-2958.1998.01073.x	journal	October 1998
The archaeal halophilic virus-encoded Dam-like methyltransferase M.phiCh1-I methylates adenine residues and complements dam mutants in the low salt environment of Escherichia coli Baranyi, U.; Klein, R.; Lubitz, W. Molecular Microbiology, Vol. 35, Issue 5 https://doi.org/10.1046/j.1365-2958.2000.01786.x	journal	March 2000
Natrialba magadii virus φCh1: first complete nucleotide sequence and functional organization of a virus infecting a haloalkaliphilic archaeon: φ Ch1 genome Klein, R.; Baranyi, U.; Rössler, N. Molecular Microbiology, Vol. 45, Issue 3 https://doi.org/10.1046/j.1365-2958.2002.03064.x	journal	July 2002
Structure of the archaeal head-tailed virus HSTV-1 completes the HK97 fold story Pietila, M. K.; Laurinmaki, P.; Russell, D. A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 26 https://doi.org/10.1073/pnas.1303047110	journal	June 2013
Interrelations between substrate cycles and de novo synthesis of pyrimidine deoxyribonucleoside triphosphates in 3T6 cells. Bianchi, V.; Pontis, E.; Reichard, P. Proceedings of the National Academy of Sciences, Vol. 83, Issue 4 https://doi.org/10.1073/pnas.83.4.986	journal	February 1986
Comparative Genomics of the Vitamin B ₁₂ Metabolism and Regulation in Prokaryotes Rodionov, Dmitry A.; Vitreschak, Alexey G.; Mironov, Andrey A. Journal of Biological Chemistry, Vol. 278, Issue 42 https://doi.org/10.1074/jbc.M305837200	journal	July 2003
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T. Bioinformatics, Vol. 25, Issue 15 https://doi.org/10.1093/bioinformatics/btp348	journal	June 2009
Easyfig: a genome comparison visualizer Sullivan, M. J.; Petty, N. K.; Beatson, S. A. Bioinformatics, Vol. 27, Issue 7 https://doi.org/10.1093/bioinformatics/btr039	journal	January 2011
Application of the MAFFT sequence alignment program to large data—reexamination of the usefulness of chained guide trees Yamada, Kazunori D.; Tomii, Kentaro; Katoh, Kazutaka Bioinformatics, Vol. 32, Issue 21 https://doi.org/10.1093/bioinformatics/btw412	journal	July 2016
Strategies of adaptation of microorganisms of the three domains of life to high salt concentrations Gunde-Cimerman, Nina; Plemenitaš, Ana; Oren, Aharon FEMS Microbiology Reviews, Vol. 42, Issue 3 https://doi.org/10.1093/femsre/fuy009	journal	February 2018
The gp38 Adhesins of the T4 Superfamily: A Complex Modular Determinant of the Phage’s Host Specificity Trojet, Sabrina N.; Caumont-Sarcos, Anne; Perrody, Elsa Genome Biology and Evolution, Vol. 3 https://doi.org/10.1093/gbe/evr059	journal	January 2011
Two Cobalt Chelatase Subunits Can Be Generated from a Single chlD Gene via Programed Frameshifting Antonov, Ivan V. Molecular Biology and Evolution, Vol. 37, Issue 8 https://doi.org/10.1093/molbev/msaa081	journal	March 2020
FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix Price, M. N.; Dehal, P. S.; Arkin, A. P. Molecular Biology and Evolution, Vol. 26, Issue 7 https://doi.org/10.1093/molbev/msp077	journal	April 2009
Two Methods for Mapping and Visualizing Associated Data on Phylogeny Using Ggtree Yu, Guangchuang; Lam, Tommy Tsan-Yuk; Zhu, Huachen Molecular Biology and Evolution, Vol. 35, Issue 12 https://doi.org/10.1093/molbev/msy194	journal	October 2018
IMG/VR v3: an integrated ecological and evolutionary framework for interrogating genomes of uncultivated viruses Roux, Simon; Páez-Espino, David; Chen, I-Min A. Nucleic Acids Research, Vol. 49, Issue D1 https://doi.org/10.1093/nar/gkaa946	journal	November 2020
Genomes OnLine Database (GOLD) v.8: overview and updates Mukherjee, Supratim; Stamatis, Dimitri; Bertsch, Jon Nucleic Acids Research, Vol. 49, Issue D1 https://doi.org/10.1093/nar/gkaa983	journal	November 2020
PROMALS3D: a tool for multiple protein sequence and structure alignments Pei, Jimin; Kim, Bong-Hyun; Grishin, Nick V. Nucleic Acids Research, Vol. 36, Issue 7 https://doi.org/10.1093/nar/gkn072	journal	February 2008
The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST) Overbeek, Ross; Olson, Robert; Pusch, Gordon D. Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1226	journal	November 2013
Analysis Tool Web Services from the EMBL-EBI McWilliam, Hamish; Li, Weizhong; Uludag, Mahmut Nucleic Acids Research, Vol. 41, Issue W1 https://doi.org/10.1093/nar/gkt376	journal	May 2013
Insights into molecular plasticity in protein complexes from Trm9-Trm112 tRNA modifying enzyme crystal structure Létoquart, Juliette; van Tran, Nhan; Caroline, Vonny Nucleic Acids Research, Vol. 43, Issue 22 https://doi.org/10.1093/nar/gkv1009	journal	October 2015
Dali server update Holm, Liisa; Laakso, Laura M. Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw357	journal	April 2016
Evolutionary insights into Trm112-methyltransferase holoenzymes involved in translation between archaea and eukaryotes van Tran, Nhan; Muller, Leslie; Ross, Robert L. Nucleic Acids Research, Vol. 46, Issue 16 https://doi.org/10.1093/nar/gky638	journal	July 2018
New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0 Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent Systematic Biology, Vol. 59, Issue 3 https://doi.org/10.1093/sysbio/syq010	journal	March 2010
Analysis of Spounaviruses as a Case Study for the Overdue Reclassification of Tailed Phages Barylski, Jakub; Enault, François; Dutilh, Bas E. Systematic Biology https://doi.org/10.1093/sysbio/syz036	journal	May 2019
Evaluation of the genomic diversity of viruses infecting bacteria, archaea and eukaryotes using a common bioinformatic platform: steps towards a unified taxonomy Aiewsakun, Pakorn; Adriaenssens, Evelien M.; Lavigne, Rob Journal of General Virology, Vol. 99, Issue 9 https://doi.org/10.1099/jgv.0.001110	journal	September 2018
Circos: An information aesthetic for comparative genomics Krzywinski, M.; Schein, J.; Birol, I. Genome Research, Vol. 19, Issue 9 https://doi.org/10.1101/gr.092759.109	journal	June 2009
Analysis of metagenomic data reveals common features of halophilic viral communities across continents: Halovirus genomes are homogeneous across continents Roux, Simon; Enault, Francois; Ravet, Viviane Environmental Microbiology, Vol. 18, Issue 3 https://doi.org/10.1111/1462-2920.13084	journal	December 2015
Novel Caudovirales associated with Marine Group I Thaumarchaeota assembled from metagenomes López‐Pérez, Mario; Haro‐Moreno, Jose M.; de la Torre, José R. Environmental Microbiology, Vol. 21, Issue 6 https://doi.org/10.1111/1462-2920.14462	journal	December 2018
Integrated mobile genetic elements in Thaumarchaeota Krupovic, Mart; Makarova, Kira S.; Wolf, Yuri I. Environmental Microbiology, Vol. 21, Issue 6 https://doi.org/10.1111/1462-2920.14564	journal	March 2019
Novel haloarchaeal viruses from Lake Retba infecting Haloferax and Halorubrum species Mizuno, Carolina M.; Prajapati, Bina; Lucas‐Staat, Soizick Environmental Microbiology, Vol. 21, Issue 6 https://doi.org/10.1111/1462-2920.14604	journal	April 2019
The first head‐tailed virus, MFTV1 , infecting hyperthermophilic methanogenic deep‐sea archaea Thiroux, Sarah; Dupont, Samuel; Nesbø, Camilla L. Environmental Microbiology, Vol. 23, Issue 7 https://doi.org/10.1111/1462-2920.15271	journal	October 2020
MazG - a regulator of programmed cell death in Escherichia coli: MazG - PCD regulator in E. coli Gross, Miryam; Marianovsky, Irina; Glaser, Gad Molecular Microbiology, Vol. 59, Issue 2 https://doi.org/10.1111/j.1365-2958.2005.04956.x	journal	November 2005
Haloarchaeal myovirus φCh1 harbours a phase variation system for the production of protein variants with distinct cell surface adhesion specificities: φCh1 inversion Klein, R.; Rössler, N.; Iro, M. Molecular Microbiology, Vol. 83, Issue 1 https://doi.org/10.1111/j.1365-2958.2011.07921.x	journal	November 2011
Global network of specific virus-host interactions in hypersaline environments: Haloviruses are promiscuous Atanasova, Nina S.; Roine, Elina; Oren, Aharon Environmental Microbiology, Vol. 14, Issue 2 https://doi.org/10.1111/j.1462-2920.2011.02603.x	journal	October 2011
Phylogenomics of T4 cyanophages: lateral gene transfer in the ‘core’ and origins of host genes: Molecular evolution of T4 myoviruses Ignacio-Espinoza, J. Cesar; Sullivan, Matthew B. Environmental Microbiology, Vol. 14, Issue 8 https://doi.org/10.1111/j.1462-2920.2012.02704.x	journal	February 2012
The ecology of the extremely halophilic archaea Oren, Aharon FEMS Microbiology Reviews, Vol. 13, Issue 4 https://doi.org/10.1111/j.1574-6976.1994.tb00060.x	journal	April 1994
Marine viruses and global climate change Danovaro, Roberto; Corinaldesi, Cinzia; Dell'Anno, Antonio FEMS Microbiology Reviews, Vol. 35, Issue 6 https://doi.org/10.1111/j.1574-6976.2010.00258.x	journal	November 2011
Virus-mediated archaeal hecatomb in the deep seafloor Danovaro, Roberto; Dell’Anno, Antonio; Corinaldesi, Cinzia Science Advances, Vol. 2, Issue 10 https://doi.org/10.1126/sciadv.1600492	journal	October 2016
Expansion of known ssRNA phage genomes: From tens to over a thousand Callanan, J.; Stockdale, S. R.; Shkoporov, A. Science Advances, Vol. 6, Issue 6 https://doi.org/10.1126/sciadv.aay5981	journal	February 2020
Accurate prediction of protein structures and interactions using a three-track neural network Baek, Minkyung; DiMaio, Frank; Anishchenko, Ivan Science, Vol. 373, Issue 6557 https://doi.org/10.1126/science.abj8754	journal	July 2021
Expression and Characterization of (R)-Specific Enoyl Coenzyme A Hydratase Involved in Polyhydroxyalkanoate Biosynthesis by Aeromonas caviae Fukui, Toshiaki; Shiomi, Naofumi; Doi, Yoshiharu Journal of Bacteriology, Vol. 180, Issue 3 https://doi.org/10.1128/JB.180.3.667-673.1998	journal	February 1998
Insights into Head-Tailed Viruses Infecting Extremely Halophilic Archaea Pietilä, Maija K.; Laurinmäki, Pasi; Russell, Daniel A. Journal of Virology, Vol. 87, Issue 6 https://doi.org/10.1128/JVI.03397-12	journal	March 2013
Global Organization and Proposed Megataxonomy of the Virus World Koonin, Eugene V.; Dolja, Valerian V.; Krupovic, Mart Microbiology and Molecular Biology Reviews, Vol. 84, Issue 2 https://doi.org/10.1128/MMBR.00061-19	journal	March 2020
Environmental Viral Genomes Shed New Light on Virus-Host Interactions in the Ocean Nishimura, Yosuke; Watai, Hiroyasu; Honda, Takashi mSphere, Vol. 2, Issue 2 https://doi.org/10.1128/mSphere.00359-16	journal	March 2017
Abortive Infection: Bacterial Suicide as an Antiviral Immune Strategy Lopatina, Anna; Tal, Nitzan; Sorek, Rotem Annual Review of Virology, Vol. 7, Issue 1 https://doi.org/10.1146/annurev-virology-011620-040628	journal	September 2020
Biogeography of Viruses in the Sea Chow, Cheryl-Emiliane T.; Suttle, Curtis A. Annual Review of Virology, Vol. 2, Issue 1 https://doi.org/10.1146/annurev-virology-031413-085540	journal	November 2015
Portal Protein: The Orchestrator of Capsid Assembly for the dsDNA Tailed Bacteriophages and Herpesviruses Dedeo, Corynne L.; Cingolani, Gino; Teschke, Carolyn M. Annual Review of Virology, Vol. 6, Issue 1 https://doi.org/10.1146/annurev-virology-092818-015819	journal	September 2019
Sequence analysis of an Archaeal virus isolated from a hypersaline lake in Inner Mongolia, China Pagaling, Eulyn; Haigh, Richard D.; Grant, William D. BMC Genomics, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2164-8-410	journal	November 2007
Host-hijacking and planktonic piracy: how phages command the microbial high seas Warwick-Dugdale, Joanna; Buchholz, Holger H.; Allen, Michael J. Virology Journal, Vol. 16, Issue 1 https://doi.org/10.1186/s12985-019-1120-1	journal	February 2019
The genomic underpinnings of eukaryotic virus taxonomy: creating a sequence-based framework for family-level virus classification Aiewsakun, Pakorn; Simmonds, Peter Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0422-7	journal	February 2018
Next-Generation “-omics” Approaches Reveal a Massive Alteration of Host RNA Metabolism during Bacteriophage Infection of Pseudomonas aeruginosa Chevallereau, Anne; Blasdel, Bob G.; De Smet, Jeroen PLOS Genetics, Vol. 12, Issue 7 https://doi.org/10.1371/journal.pgen.1006134	journal	July 2016
Reconstructing Viral Genomes from the Environment Using Fosmid Clones: The Case of Haloviruses Garcia-Heredia, Inmaculada; Martin-Cuadrado, Ana-Belen; Mojica, Francisco J. M. PLoS ONE, Vol. 7, Issue 3 https://doi.org/10.1371/journal.pone.0033802	journal	March 2012
Candidatus Nitrosocaldus cavascurensis, an Ammonia Oxidizing, Extremely Thermophilic Archaeon with a Highly Mobile Genome Abby, Sophie S.; Melcher, Michael; Kerou, Melina Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00028	journal	January 2018
Halobacterium salinarum virus ChaoS9, a Novel Halovirus Related to PhiH1 and PhiCh1 Dyall-Smith, Mike; Palm, Peter; Wanner, Gerhard Genes, Vol. 10, Issue 3 https://doi.org/10.3390/genes10030194	journal	March 2019
Comparative Genomics of Two New HF1-like Haloviruses Dyall-Smith, Mike; Tang, Sen-Lin; Russ, Brendan Genes, Vol. 11, Issue 4 https://doi.org/10.3390/genes11040405	journal	April 2020
The Novel Halovirus Hardycor1, and the Presence of Active (Induced) Proviruses in Four Haloarchaea Dyall-Smith, Mike; Pfeiffer, Friedhelm; Chiang, Pei-Wen Genes, Vol. 12, Issue 2 https://doi.org/10.3390/genes12020149	journal	January 2021
Open Issues for Protein Function Assignment in Haloferax volcanii and Other Halophilic Archaea Pfeiffer, Friedhelm; Dyall-Smith, Mike Genes, Vol. 12, Issue 7 https://doi.org/10.3390/genes12070963	journal	June 2021
Complete Genome Sequence of the Model Halovirus PhiH1 (ΦH1) Dyall-Smith, Mike; Pfeifer, Felicitas; Witte, Angela Genes, Vol. 9, Issue 10 https://doi.org/10.3390/genes9100493	journal	October 2018
Archaeal Viruses Multiply: Temporal Screening in a Solar Saltern Atanasova, Nina; Demina, Tatiana; Buivydas, Andrius Viruses, Vol. 7, Issue 4 https://doi.org/10.3390/v7041902	journal	April 2015
Snapshot of haloarchaeal tailed virus genomes Senčilo, Ana; Jacobs-Sera, Deborah; Russell, Daniel A. RNA Biology, Vol. 10, Issue 5 https://doi.org/10.4161/rna.24045	journal	February 2013
Putative archaeal viruses from the mesopelagic ocean Vik, Dean R.; Roux, Simon; Brum, Jennifer R. PeerJ, Vol. 5 https://doi.org/10.7717/peerj.3428	journal	January 2017

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