{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,12]],"date-time":"2025-10-12T02:05:46Z","timestamp":1760234746764,"version":"build-2065373602"},"reference-count":59,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2021,6,19]],"date-time":"2021-06-19T00:00:00Z","timestamp":1624060800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100002661","name":"Fonds De La Recherche Scientifique - FNRS","doi-asserted-by":"publisher","award":["J.0144.20","1.B208.16"],"award-info":[{"award-number":["J.0144.20","1.B208.16"]}],"id":[{"id":"10.13039\/501100002661","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003134","name":"Fonds pour la Formation \u00e0 la Recherche dans l\u2019Industrie et dans l\u2019Agriculture","doi-asserted-by":"publisher","award":["PhD scholarship to L.Hock"],"award-info":[{"award-number":["PhD scholarship to L.Hock"]}],"id":[{"id":"10.13039\/501100003134","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Research Department of the Communaut\u00e9 fran\u00e7aise de Belgique","award":["ARC 17\/22-084"],"award-info":[{"award-number":["ARC 17\/22-084"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Tectiviruses infecting the Bacillus cereus group represent part of the bacterial \u201cplasmid repertoire\u201d as they behave as linear plasmids during their lysogenic cycle. Several novel tectiviruses have been recently found infecting diverse strains belonging the B. cereus lineage. Here, we report and analyze the complete genome sequences of phages Sato and Sole. The linear dsDNA genome of Sato spans 14,852 bp with 32 coding DNA sequences (CDSs), whereas the one of Sole has 14,444 bp comprising 30 CDSs. Both phage genomes contain inverted terminal repeats and no tRNAs. Genomic comparisons and phylogenetic analyses placed these two phages within the genus Betatectivirus in the family Tectiviridae. Additional comparative genomic analyses indicated that the \u201cgene regulation-genome replication\u201d module of phages Sato and Sole is more diverse than previously observed among other fully sequenced betatectiviruses, displaying very low sequence similarities and containing some ORFans. Interestingly, the ssDNA binding protein encoded in this genomic module in phages Sato and Sole has very little amino acid similarity with those of reference betatectiviruses. Phylogenetic analyses showed that both Sato and Sole represent novel tectivirus species, thus we propose to include them as two novel species in the genus Betatectivirus.<\/jats:p>","DOI":"10.3390\/microorganisms9061335","type":"journal-article","created":{"date-parts":[[2021,6,20]],"date-time":"2021-06-20T21:50:15Z","timestamp":1624225815000},"page":"1335","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Comparative Genomics of Prophages Sato and Sole Expands the Genetic Diversity Found in the Genus Betatectivirus"],"prefix":"10.3390","volume":"9","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-6735-3359","authenticated-orcid":false,"given":"Annika","family":"Gillis","sequence":"first","affiliation":[{"name":"Laboratory of Food and Environmental Microbiology, Earth and Life Institute, UCLouvain, Croix du Sud 2, L7.05.12, B-1348 Louvain-la-Neuve, Belgium"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Louise","family":"Hock","sequence":"additional","affiliation":[{"name":"Laboratory of Food and Environmental Microbiology, Earth and Life Institute, UCLouvain, Croix du Sud 2, L7.05.12, B-1348 Louvain-la-Neuve, Belgium"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jacques","family":"Mahillon","sequence":"additional","affiliation":[{"name":"Laboratory of Food and Environmental Microbiology, Earth and Life Institute, UCLouvain, Croix du Sud 2, L7.05.12, B-1348 Louvain-la-Neuve, Belgium"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2021,6,19]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"2499","DOI":"10.1099\/ijsem.0.001821","article-title":"Proposal of nine novel species of the Bacillus cereus group","volume":"67","author":"Liu","year":"2017","journal-title":"Int. J. Syst. Evol. Microbiol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"e00034-20","DOI":"10.1128\/mBio.00034-20","article-title":"Proposal of a taxonomic nomenclature for the Bacillus cereus group which reconciles genomic definitions of bacterial species with clinical and industrial phenotypes","volume":"11","author":"Carroll","year":"2020","journal-title":"mBio"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"631","DOI":"10.1046\/j.1462-2920.2003.00461.x","article-title":"The hidden lifestyles of Bacillus cereus and relatives","volume":"5","author":"Jensen","year":"2003","journal-title":"Environ. Microbiol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"829","DOI":"10.1093\/femsre\/fuy034","article-title":"Role of plasmid plasticity and mobile genetic elements in the entomopathogen Bacillus thuringiensis serovar israelensis","volume":"42","author":"Gillis","year":"2018","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"2623","DOI":"10.3390\/v6072623","article-title":"Phages preying on Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis: Past, present and future","volume":"6","author":"Gillis","year":"2014","journal-title":"Viruses"},{"key":"ref_6","first-page":"303","article-title":"Genomics of the Bacillus cereus group of organisms","volume":"29","author":"Rasko","year":"2005","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1524","DOI":"10.1111\/mec.14546","article-title":"Lineage-specific plasmid acquisition and the evolution of specialized pathogens in Bacillus thuringiensis and the Bacillus cereus group","volume":"27","author":"Meric","year":"2018","journal-title":"Mol. Ecol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"560","DOI":"10.1128\/MMBR.68.3.560-602.2004","article-title":"Phages and the evolution of bacterial pathogens: From genomic rearrangements to lysogenic conversion","volume":"68","author":"Canchaya","year":"2004","journal-title":"Microbiol. Mol. Biol. Rev."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"298","DOI":"10.1016\/j.coviro.2011.06.009","article-title":"Bacteriophages and their genomes","volume":"1","author":"Hatfull","year":"2011","journal-title":"Curr. Opin. Virol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"4138","DOI":"10.1128\/AEM.00912-14","article-title":"Prevalence, genetic diversity and host range of tectiviruses among members of the Bacillus cereus group","volume":"80","author":"Gillis","year":"2014","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"136","DOI":"10.1016\/j.virol.2018.02.014","article-title":"Extending the hosts of Tectiviridae into four additional genera of gram-positive bacteria and more diverse Bacillus species","volume":"518","author":"Jalasvuori","year":"2018","journal-title":"Virology"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1125","DOI":"10.1007\/s00705-018-3723-z","article-title":"Taxonomy of prokaryotic viruses: 2017 update from the ICTV Bacterial and Archaeal Viruses Subcommittee","volume":"163","author":"Adriaenssens","year":"2018","journal-title":"Arch. Virol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"6985","DOI":"10.1128\/JB.185.23.6985-6989.2003","article-title":"The Bacillus thuringiensis linear double-stranded DNA phage Bam35, which is highly similar to the Bacillus cereus linear plasmid pBClin15, has a prophage state","volume":"185","author":"Benson","year":"2003","journal-title":"J. Bacteriol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"7620","DOI":"10.1128\/AEM.01869-14","article-title":"Influence of lysogeny of tectiviruses GIL01 and GIL16 on Bacillus thuringiensis growth, biofilm formation, and swarming motility","volume":"80","author":"Gillis","year":"2014","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"M\u00e4ntynen, S., Sundberg, L.-R., Oksanen, H.M., and Poranen, M.M. (2019). Half a century of research on membrane-containing bacteriophages: Bringing new concepts to modern virology. Viruses, 11.","DOI":"10.3390\/v11010076"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"10566","DOI":"10.1021\/bi000711+","article-title":"Assembly of bacteriophage PRD1 spike complex:\u2009 Role of the multidomain protein p5","volume":"39","author":"Caldentey","year":"2000","journal-title":"Biochemistry"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Peralta, B., Gil-Carton, D., Casta\u00f1o-D\u00edez, D., Bertin, A., Boulogne, C., Oksanen, H.M., Bamford, D.H., and Abrescia, N.G.A. (2013). Mechanism of membranous tunnelling nanotube formation in viral genome delivery. PLoS Biol., 11.","DOI":"10.1371\/journal.pbio.1001667"},{"key":"ref_18","first-page":"9733","article-title":"Disclosing early steps of protein-primed genome replication of the gram-positive tectivirus Bam35","volume":"44","author":"Villar","year":"2016","journal-title":"Nucleic Acids Res."},{"key":"ref_19","unstructured":"Gillis, A., Jang, H.B., Kuhn, J.H., Kropinski, A.M., Adriaenssens, E., and Lavigne, R. (2021, April 30). To Rename the Existing Genus Tectivirus (Proposed New Name Alphatectivirus) in the Family Tectiviridae, Create a New Genus, Betatectivirus, and Include Three (3) New Species; ICTV Taxonomic Proposal, 2017.013B. Available online: https:\/\/talk.ictvonline.org\/files\/ictv_official_taxonomy_updates_since_the_8th_report\/m\/prokaryote-official\/7109."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"2083","DOI":"10.1099\/mic.0.26307-0","article-title":"pGIL01, a linear tectiviral plasmid prophage originating from Bacillus thuringiensis serovar israelensis","volume":"149","author":"Verheust","year":"2003","journal-title":"Microbiology"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1016\/j.resmic.2016.10.008","article-title":"Comparative genomics of extrachromosomal elements in Bacillus thuringiensis subsp","volume":"168","author":"Bolotin","year":"2017","journal-title":"israelensis. Res. Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"118","DOI":"10.1016\/j.resmic.2012.10.011","article-title":"Identification of five novel tectiviruses in Bacillus strains: Analysis of a highly variable region generating genetic diversity","volume":"164","author":"Jalasvuori","year":"2013","journal-title":"Res. Microbiol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"6792","DOI":"10.1128\/AEM.01124-08","article-title":"Molecular characterization of a variant of Bacillus anthracis-specific phage AP50 with improved bacteriolytic activity","volume":"74","author":"Sozhamannan","year":"2008","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Caruso, S.M., deCarvalho, T.N., Huynh, A., Morcos, G., Kuo, N., Parsa, S., and Erill, I. (2019). A novel genus of actinobacterial Tectiviridae. Viruses, 11.","DOI":"10.3390\/v11121134"},{"key":"ref_25","unstructured":"Sambrook, J., and Russell, D.W. (2001). Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press. [3rd ed.]."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"2555","DOI":"10.1007\/s00705-018-3865-z","article-title":"Complete genome sequence of bacteriophage Deep-Purple, a novel member of the family Siphoviridae infecting Bacillus cereus","volume":"163","author":"Hock","year":"2018","journal-title":"Arch. Virol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"8365","DOI":"10.1038\/srep08365","article-title":"RASTtk: A modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes","volume":"5","author":"Brettin","year":"2015","journal-title":"Sci. Rep."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"673","DOI":"10.1093\/bioinformatics\/btm009","article-title":"Identifying bacterial genes and endosymbiont DNA with Glimmer","volume":"23","author":"Delcher","year":"2007","journal-title":"Bioinformatics"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"2607","DOI":"10.1093\/nar\/29.12.2607","article-title":"GeneMarkS: A self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions","volume":"29","author":"Besemer","year":"2001","journal-title":"Nucleic Acids Res."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"W16","DOI":"10.1093\/nar\/gkw387","article-title":"PHASTER: A better, faster version of the PHAST phage search tool","volume":"44","author":"Arndt","year":"2016","journal-title":"Nucleic Acids Res."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Chan, P.P., Lin, B.Y., Mak, A.J., and Lowe, T.M. (2019). tRNAscan-SE 2.0: Improved detection and functional classification of transfer RNA genes. bioRxiv.","DOI":"10.1101\/614032"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"567","DOI":"10.1006\/jmbi.2000.4315","article-title":"Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes","volume":"305","author":"Krogh","year":"2001","journal-title":"J. Mol. Biol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1009","DOI":"10.1093\/bioinformatics\/btr039","article-title":"Easyfig: A genome comparison visualizer","volume":"27","author":"Sullivan","year":"2011","journal-title":"Bioinformatics"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1792","DOI":"10.1093\/nar\/gkh340","article-title":"Muscle: Multiple sequence alignment with high accuracy and high throughput","volume":"32","author":"Edgar","year":"2004","journal-title":"Nucleic Acids Res."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Muhire, B.M., Varsani, A., and Martin, D.P. (2014). SDT: A virus classification tool based on pairwise sequence alignment and identity calculation. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0108277"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"2237","DOI":"10.1016\/j.jmb.2017.12.007","article-title":"A completely reimplemented MPI bioinformatics toolkit with a new HHpred server at its core","volume":"430","author":"Zimmermann","year":"2018","journal-title":"J. Mol. Biol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"845","DOI":"10.1038\/nprot.2015.053","article-title":"The Phyre2 web portal for protein modeling, prediction and analysis","volume":"10","author":"Kelley","year":"2015","journal-title":"Nat. Protoc."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"725","DOI":"10.1038\/nprot.2010.5","article-title":"I-TASSER: A unified platform for automated protein structure and function prediction","volume":"5","author":"Roy","year":"2010","journal-title":"Nat. Protoc."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"4673","DOI":"10.1093\/nar\/22.22.4673","article-title":"CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice","volume":"22","author":"Thompson","year":"1994","journal-title":"Nucleic Acids Res."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1016\/j.resmic.2016.10.004","article-title":"Detection of the cryptic prophage-like molecule pBtic235 in Bacillus thuringiensis subsp. israelensis","volume":"168","author":"Gillis","year":"2017","journal-title":"Res. Microbiol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1547","DOI":"10.1093\/molbev\/msy096","article-title":"MEGA X: Molecular evolutionary genetics analysis across computing platforms","volume":"35","author":"Kumar","year":"2018","journal-title":"Mol. Biol. Evol."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Moraru, C., Varsani, A., and Kropinski, A.M. (2020). VIRIDIC\u2014A novel tool to calculate the intergenomic similarities of prokaryote-infecting viruses. Viruses, 12.","DOI":"10.1101\/2020.07.05.188268"},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Turner, D., Kropinski, A.M., and Adriaenssens, E.M. (2021). A roadmap for genome-based phage taxonomy. Viruses, 13.","DOI":"10.3390\/v13030506"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"6008","DOI":"10.1128\/JB.05618-11","article-title":"Phage-borne factors and host LexA regulate the lytic switch in phage GIL01","volume":"193","author":"Fornelos","year":"2011","journal-title":"J. Bacteriol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"e00870-17","DOI":"10.1128\/JVI.00870-17","article-title":"Bam35 tectivirus intraviral interaction map unveils new function and localization of phage orfan proteins","volume":"91","author":"Lechuga","year":"2017","journal-title":"J. Virol."},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Lechuga, A., Kazlauskas, D., Salas, M., and Redrejo-Rodr\u00edguez, M. (2021). Unlimited cooperativity of Betatectivirus SSB, a novel DNA binding protein related to an atypical group of SSBs from protein-primed replicating bacterial viruses. bioRxiv.","DOI":"10.1101\/2021.03.25.437074"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"e00380-13","DOI":"10.1128\/genomeA.00380-13","article-title":"Whole-genome sequences of 94 environmental isolates of Bacillus cereus sensu lato","volume":"1","author":"Feldgarden","year":"2013","journal-title":"Genome Announc."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1111\/j.1472-765X.2008.02483.x","article-title":"Orf 2 from the Bacillus cereus linear plasmid pBClin15 encodes a DNA binding protein","volume":"48","author":"Stabell","year":"2009","journal-title":"Lett. Appl. Microbiol."},{"key":"ref_49","first-page":"E3476","article-title":"DNA polymerase from temperate phage Bam35 is endowed with processive polymerization and abasic sites translesion synthesis capacity","volume":"112","author":"Villar","year":"2015","journal-title":"Proc. Nat. Acad. Sci. USA."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"401","DOI":"10.1016\/S0042-6822(03)00295-2","article-title":"Comparative analysis of bacterial viruses Bam35, infecting a gram-positive host, and PRD1, infecting gram-negative hosts, demonstrates a viral lineage","volume":"313","author":"Ravantti","year":"2003","journal-title":"Virology"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"9432","DOI":"10.1093\/nar\/gky646","article-title":"Lytic gene expression in the temperate bacteriophage GIL01 is activated by a phage-encoded lexa homologue","volume":"46","author":"Fornelos","year":"2018","journal-title":"Nucleic Acids Res."},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Keck, J.L. (2012). Functions of single-strand DNA-binding proteins in DNA replication, recombination, and repair. Single-Stranded DNA Binding Proteins: Methods and Protocols, Humana Press.","DOI":"10.1007\/978-1-62703-032-8"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1146\/annurev.biophys.32.110601.142506","article-title":"Nucleic acid recognition by OB-fold proteins","volume":"32","author":"Theobald","year":"2003","journal-title":"Annu. Rev. Biophys. Biomol. Struct."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1146\/annurev.bi.60.070191.000351","article-title":"Protein-priming of DNA replication","volume":"60","author":"Salas","year":"1991","journal-title":"Annu. Rev. Biochem."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"37","DOI":"10.3389\/fmolb.2016.00037","article-title":"DNA-binding proteins essential for protein-primed bacteriophage \u03c629 DNA replication","volume":"3","author":"Salas","year":"2016","journal-title":"Front. Mol. Biosci."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"3725","DOI":"10.1093\/nar\/21.16.3725","article-title":"In vitro replication of bacteriophage PRD1 DNA. Characterization of the protein-primed initiation site","volume":"21","author":"Caldentey","year":"1993","journal-title":"Nucleic Acids Res."},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"Philippe, C., Krupovic, M., Jaomanjaka, F., Claisse, O., Petrel, M., and le Marrec, C. (2018). Bacteriophage GC1, a novel tectivirus infecting Gluconobacter cerinus, an acetic acid bacterium associated with wine-making. Viruses, 10.","DOI":"10.3390\/v10010039"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"1062","DOI":"10.1038\/s41598-018-19455-2","article-title":"Characterization of a novel tectivirus phage Toil and its potential as an agent for biolipid extraction","volume":"8","author":"Gill","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"1966","DOI":"10.1128\/JB.187.6.1966-1973.2005","article-title":"GIL16, a new gram-positive tectiviral phage related to the Bacillus thuringiensis GIL01 and the Bacillus cereus pBClin15 elements","volume":"187","author":"Verheust","year":"2005","journal-title":"J. Bacteriol."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/9\/6\/1335\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T06:19:27Z","timestamp":1760163567000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/9\/6\/1335"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,6,19]]},"references-count":59,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2021,6]]}},"alternative-id":["microorganisms9061335"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms9061335","relation":{},"ISSN":["2076-2607"],"issn-type":[{"type":"electronic","value":"2076-2607"}],"subject":[],"published":{"date-parts":[[2021,6,19]]}}}