Expanding the genomes insight of Streptococcus thermophilus phages through a multifaceted approach

Authors

DOI:

https://doi.org/10.33448/rsd-v11i10.32693

Keywords:

Biodiversity; Core genome; Holin; Panvirome; Taxonomy; Signature genes; Starter culture.

Abstract

Viruses have complex evolutionary relationships, and several strategies have been used in an attempt to classify the phages that infect S. thermophilus. In this study, we used a wide range of complementary methods, including comparative genomics, core genome analysis, and signature genes phylogenetics, to show that the S. thermophilus phages are organized into 142 species and five genera (three of them new) and that due to their genetic diversity, the classification at family level varies according to the classification criteria used. No significantly conserved genes were identified among the 183 genomes evaluated. However, the genes encoding holin protein were conserved in more than 95% of genomes. The holins analysis suggests that at least two α-helix are required for protein function within S. thermophilus phages. This study expanded the of knowledge about the genetic diversity and evolution of streptococcal phages, both fundamental to promoting control strategies and minimizing failures in milk fermentation processes.

References

Accolas, J.-P., & Spillmann, H. (1979). The Morphology of Six Bacteriophages of Streptococcus thermophilus. Journal of Applied Bacteriology, 47(1), 135–144. https://doi.org/10.1111/j.1365-2672.1979.tb01177.x

Achigar, R., Magadán, A. H., Tremblay, D. M., Julia Pianzzola, M., & Moineau, S. (2017). Phage-host interactions in Streptococcus thermophilus: Genome analysis of phages isolated in Uruguay and ectopic spacer acquisition in CRISPR array. Scientific Reports, 7(1), 43438. https://doi.org/10.1038/srep43438

Ali, Y., Koberg, S., Heßner, S., Sun, X., Rabe, B., Back, A., Neve, H., & Heller, K. J. (2014). Temperate Streptococcus thermophilus phages expressing superinfection exclusion proteins of the Ltp type. Frontiers in Microbiology, 5. https://doi.org/10.3389/fmicb.2014.00098

Al-Shayeb, B., Sachdeva, R., Chen, L.-X., Ward, F., Munk, P., Devoto, A., Castelle, C. J., Olm, M. R., Bouma-Gregson, K., Amano, Y., He, C., Méheust, R., Brooks, B., Thomas, A., Lavy, A., Matheus-Carnevali, P., Sun, C., Goltsman, D. S. A., Borton, M. A., … Banfield, J. F. (2020). Clades of huge phages from across Earth’s ecosystems. Nature, 578(7795), 425–431. https://doi.org/10.1038/s41586-020-2007-4

Arioli, S., Eraclio, G., Della Scala, G., Neri, E., Colombo, S., Scaloni, A., Fortina, M. G., & Mora, D. (2018). Role of Temperate Bacteriophage ϕ20617 on Streptococcus thermophilus DSM 20617T Autolysis and Biology. Frontiers in Microbiology, 9. https://doi.org/10.3389/fmicb.2018.02719

Baek, M., DiMaio, F., Anishchenko, I., Dauparas, J., Ovchinnikov, S., Lee, G. R., Wang, J., Cong, Q., Kinch, L. N., Schaeffer, R. D., Millán, C., Park, H., Adams, C., Glassman, C. R., DeGiovanni, A., Pereira, J. H., Rodrigues, A. V., van Dijk, A. A., Ebrecht, A. C., … Baker, D. (2021). Accurate prediction of protein structures and interactions using a three-track neural network. Science, 373(6557), 871–876. https://doi.org/10.1126/science.abj8754

Benson, D. A., Cavanaugh, M., Clark, K., Karsch-Mizrachi, I., Lipman, D. J., Ostell, J., & Sayers, E. W. (2012). GenBank. Nucleic Acids Research, 41(D1), D36–D42. https://doi.org/10.1093/nar/gks1195

Binetti, A. G., Del Río, B., Martín, M. C., & Álvarez, M. A. (2005). Detection and Characterization of Streptococcus thermophilus Bacteriophages by Use of the Antireceptor Gene Sequence. Applied and Environmental Microbiology, 71(10), 6096–6103. https://doi.org/10.1128/AEM.71.10.6096-6103.2005

Brussow, H., & Desiere, F. (2001). Comparative phage genomics and the evolution of Siphoviridae: Insights from dairy phages. Molecular Microbiology, 39(2), 213–223. https://doi.org/10.1046/j.1365-2958.2001.02228.x

da Silva Duarte, V., Giaretta, S., Treu, L., Campanaro, S., Pereira Vidigal, P. M., Tarrah, A., Giacomini, A., & Corich, V. (2018). Draft Genome Sequences of Three Virulent Streptococcus thermophilus Bacteriophages Isolated from the Dairy Environment in the Veneto Region of Italy. Genome Announcements, 6(10), e00045-18, /ga/6/10/e00045-18.atom. https://doi.org/10.1128/genomeA.00045-18

de Melo, A. G., Levesque, S., & Moineau, S. (2018). Phages as friends and enemies in food processing. Current Opinion in Biotechnology, 49, 185–190. https://doi.org/10.1016/j.copbio.2017.09.004

Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., Dufayard, J.-F., Guindon, S., Lefort, V., Lescot, M., Claverie, J.-M., & Gascuel, O. (2008). Phylogeny.fr: Robust phylogenetic analysis for the non-specialist. Nucleic Acids Research, 36(Web Server issue), W465-469. https://doi.org/10.1093/nar/gkn180

Desiere, F., Lucchini, S., & Brüssow, H. (1998). Evolution ofStreptococcus thermophilusBacteriophage Genomes by Modular Exchanges Followed by Point Mutations and Small Deletions and Insertions. Virology, 241(2), 345–356. https://doi.org/10.1006/viro.1997.8959

Desiere, F., Lucchini, S., & Brüssow, H. (1999). Comparative Sequence Analysis of the DNA Packaging, Head, and Tail Morphogenesis Modules in the Temperate cos-Site Streptococcus thermophilus Bacteriophage Sfi21. Virology, 260(2), 244–253. https://doi.org/10.1006/viro.1999.9830

Deveau, H., Barrangou, R., Garneau, J. E., Labonté, J., Fremaux, C., Boyaval, P., Romero, D. A., Horvath, P., & Moineau, S. (2008). Phage Response to CRISPR-Encoded Resistance in Streptococcus thermophilus. Journal of Bacteriology, 190(4), 1390–1400. https://doi.org/10.1128/JB.01412-07

Dion, M. B., Oechslin, F., & Moineau, S. (2020). Phage diversity, genomics and phylogeny. Nature Reviews Microbiology, 18(3), 125–138. https://doi.org/10.1038/s41579-019-0311-5

Edgar, R. C. (2004). MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32(5), 1792–1797. https://doi.org/10.1093/nar/gkh340

Farris, J. S. (1972). Estimating Phylogenetic Trees from Distance Matrices. The American Naturalist, 106(951), 645–668. https://www.jstor.org/stable/2459725

Finn, R. D., Clements, J., & Eddy, S. R. (2011). HMMER web server: Interactive sequence similarity searching. Nucleic Acids Research, 39(suppl_2), W29–W37. https://doi.org/10.1093/nar/gkr367

Fujimoto, K., Kimura, Y., Shimohigoshi, M., Satoh, T., Sato, S., Tremmel, G., Uematsu, M., Kawaguchi, Y., Usui, Y., Nakano, Y., Hayashi, T., Kashima, K., Yuki, Y., Yamaguchi, K., Furukawa, Y., Kakuta, M., Akiyama, Y., Yamaguchi, R., Crowe, S. E., … Uematsu, S. (2020). Metagenome Data on Intestinal Phage-Bacteria Associations Aids the Development of Phage Therapy against Pathobionts. Cell Host & Microbe, 28(3), 380-389.e9. https://doi.org/10.1016/j.chom.2020.06.005

Gilchrist, C. L. M., & Chooi, Y.-H. (2020). clinker & clustermap.js: Automatic generation of gene cluster comparison figures. BioRxiv, 2020.11.08.370650. https://doi.org/10.1101/2020.11.08.370650

Göker, M., García-Blázquez, G., Voglmayr, H., Tellería, M. T., & Martín, M. P. (2009). Molecular Taxonomy of Phytopathogenic Fungi: A Case Study in Peronospora. PLOS ONE, 4(7), e6319. https://doi.org/10.1371/journal.pone.0006319

Gontijo, M. T. P., Teles, M. P., Vidigal, P. M. P., & Brocchi, M. (2022). Expanding the Database of Signal-Anchor-Release Domain Endolysins Through Metagenomics. Probiotics and Antimicrobial Proteins. https://doi.org/10.1007/s12602-022-09948-y

Guglielmotti, D. M., Deveau, H., Binetti, A. G., Reinheimer, J. A., Moineau, S., & Quiberoni, A. (2009). Genome analysis of two virulent Streptococcus thermophilus phages isolated in Argentina. International Journal of Food Microbiology, 136(1), 101–109. https://doi.org/10.1016/j.ijfoodmicro.2009.09.005

Hanemaaijer, L., Kelleher, P., Neve, H., Franz, C. M. A. P., de Waal, P. P., van Peij, N. N. M. E., van Sinderen, D., & Mahony, J. (2021). Biodiversity of Phages Infecting the Dairy Bacterium Streptococcus thermophilus. Microorganisms, 9(9), 1822. https://doi.org/10.3390/microorganisms9091822

Hendrix, R. W., Smith, M. C. M., Burns, R. N., Ford, M. E., & Hatfull, G. F. (1999). Evolutionary relationships among diverse bacteriophages and prophages: All the world’s a phage. Proceedings of the National Academy of Sciences of the United States of America, 96(5), 2192–2197. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC26759/

Hockenberry, A. J., & Wilke, C. O. (2021). BACPHLIP: Predicting bacteriophage lifestyle from conserved protein domains. PeerJ, 9, e11396. https://doi.org/10.7717/peerj.11396

Hynes, A. P., Rousseau, G. M., Agudelo, D., Goulet, A., Amigues, B., Loehr, J., Romero, D. A., Fremaux, C., Horvath, P., Doyon, Y., Cambillau, C., & Moineau, S. (2018). Widespread anti-CRISPR proteins in virulent bacteriophages inhibit a range of Cas9 proteins. Nature Communications, 9(1), 2919. https://doi.org/10.1038/s41467-018-05092-w

ICTV. (2020). The new scope of virus taxonomy: Partitioning the virosphere into 15 hierarchical ranks. Nature Microbiology, 5(5), 668–674. https://doi.org/10.1038/s41564-020-0709-x

Koonin, E. V., Dolja, V. V., Krupovic, M., Varsani, A., Wolf, Y. I., Yutin, N., Zerbini, F. M., & Kuhn, J. H. (2020). Global Organization and Proposed Megataxonomy of the Virus World. Microbiology and Molecular Biology Reviews, 84(2), e00061-19, /mmbr/84/2/MMBR.00061-19.atom. https://doi.org/10.1128/MMBR.00061-19

Labrie, S., Vukov, N., Loessner, M. J., & Moineau, S. (2004). Distribution and composition of the lysis cassette of Lactococcus lactis phages and functional analysis of bacteriophage ul36 holin. FEMS Microbiology Letters, 233(1), 37–43. https://doi.org/10.1016/j.femsle.2004.01.038

Lavelle, K., Martinez, I., Neve, H., Lugli, G., Franz, C., Ventura, M., Bello, F., Sinderen, D., & Mahony, J. (2018). Biodiversity of Streptococcus thermophilus Phages in Global Dairy Fermentations. Viruses, 10(10), 577. https://doi.org/10.3390/v10100577

Lavelle, K., Murphy, J., Fitzgerald, B., Lugli, G. A., Zomer, A., Neve, H., Ventura, M., Franz, C. M., Cambillau, C., van Sinderen, D., & Mahony, J. (2018). A Decade of Streptococcus thermophilus Phage Evolution in an Irish Dairy Plant. Applied and Environmental Microbiology, 84(10), e02855-17, /aem/84/10/e02855-17.atom. https://doi.org/10.1128/AEM.02855-17

Le Marrec, C., van Sinderen, D., Walsh, L., Stanley, E., Vlegels, E., Moineau, S., Heinze, P., Fitzgerald, G., & Fayard, B. (1997). Two groups of bacteriophages infecting Streptococcus thermophilus can be distinguished on the basis of mode of packaging and genetic determinants for major structural proteins. Applied and Environmental Microbiology, 63(8), 3246–3253. https://doi.org/10.1128/AEM.63.8.3246-3253.1997

Lefort, V., Desper, R., & Gascuel, O. (2015). FastME 2.0: A Comprehensive, Accurate, and Fast Distance-Based Phylogeny Inference Program. Molecular Biology and Evolution, 32(10), 2798–2800. https://doi.org/10.1093/molbev/msv150

Leroy, F., & De Vuyst, L. (2004). Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends in Food Science & Technology, 15(2), 67–78. https://doi.org/10.1016/j.tifs.2003.09.004

Letunic, I., & Bork, P. (2021). Interactive Tree Of Life (iTOL) v5: An online tool for phylogenetic tree display and annotation. Nucleic Acids Research, 49(W1), W293–W296. https://doi.org/10.1093/nar/gkab301

Levesque, C., Duplessis, M., Labonte, J., Labrie, S., Fremaux, C., Tremblay, D., & Moineau, S. (2005). Genomic Organization and Molecular Analysis of Virulent Bacteriophage 2972 Infecting an Exopolysaccharide-Producing Streptococcus thermophilus Strain. APPL. ENVIRON. MICROBIOL., 71, 12.

Li, Z., Jaroszewski, L., Iyer, M., Sedova, M., & Godzik, A. (2020). FATCAT 2.0: Towards a better understanding of the structural diversity of proteins. Nucleic Acids Research, 48(W1), W60–W64. https://doi.org/10.1093/nar/gkaa443

Lucchini, S., Desiere, F., & Brüssow, H. (1998). The Structural Gene Module inStreptococcus thermophilusBacteriophage φSfi11 Shows a Hierarchy of Relatedness to Siphoviridae from a Wide Range of Bacterial Hosts. Virology, 246(1), 63–73. https://doi.org/10.1006/viro.1998.9190

Lucchini, S., Desiere, F., & Brüssow, H. (1999a). The Genetic Relationship between Virulent and Temperate Streptococcus thermophilus Bacteriophages: Whole Genome Comparison of cos-Site Phages Sfi19 and Sfi21. Virology, 260(2), 232–243. https://doi.org/10.1006/viro.1999.9814

Lucchini, S., Desiere, F., & Brüssow, H. (1999b). Comparative Genomics of Streptococcus thermophilus Phage Species Supports a Modular Evolution Theory. Journal of Virology, 73(10), 8647–8656. https://doi.org/10.1128/JVI.73.10.8647-8656.1999

Mahony, J., Casey, E., & van Sinderen, D. (2020). The Impact and Applications of Phages in the Food Industry and Agriculture. Viruses, 12(2), 210. https://doi.org/10.3390/v12020210

Mahony, J., & van Sinderen, D. (2014). Current taxonomy of phages infecting lactic acid bacteria. Frontiers in Microbiology, 5. https://doi.org/10.3389/fmicb.2014.00007

McDonnell, B., Mahony, J., Hanemaaijer, L., Neve, H., Noben, J.-P., Lugli, G. A., Ventura, M., Kouwen, T. R., & van Sinderen, D. (2017a). Global Survey and Genome Exploration of Bacteriophages Infecting the Lactic Acid Bacterium Streptococcus thermophilus. Frontiers in Microbiology, 8, 1754. https://doi.org/10.3389/fmicb.2017.01754

McDonnell, B., Mahony, J., Hanemaaijer, L., Neve, H., Noben, J.-P., Lugli, G. A., Ventura, M., Kouwen, T. R., & van Sinderen, D. (2017b). Global Survey and Genome Exploration of Bacteriophages Infecting the Lactic Acid Bacterium Streptococcus thermophilus. Frontiers in Microbiology, 8, 1754. https://doi.org/10.3389/fmicb.2017.01754

McDonnell, B., Mahony, J., Neve, H., Hanemaaijer, L., Noben, J.-P., Kouwen, T., & Sinderen, D. van. (2016). Identification and Analysis of a Novel Group of Bacteriophages Infecting the Lactic Acid Bacterium Streptococcus thermophilus. Applied and Environmental Microbiology, 82(17), 5153–5165. https://doi.org/10.1128/AEM.00835-16

McDonnell, B., Mahony, J., Neve, H., Hanemaaijer, L., Noben, J.-P., Kouwen, T., & van Sinderen, D. (2016). Identification and Analysis of a Novel Group of Bacteriophages Infecting the Lactic Acid Bacterium Streptococcus thermophilus. Applied and Environmental Microbiology, 82(17), 5153–5165. https://doi.org/10.1128/AEM.00835-16

Meier-Kolthoff, J. P., Auch, A. F., Klenk, H.-P., & Göker, M. (2013). Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics, 14(1), 60. https://doi.org/10.1186/1471-2105-14-60

Meier-Kolthoff, J. P., & Göker, M. (2017). VICTOR: Genome-based phylogeny and classification of prokaryotic viruses. Bioinformatics, 33(21), 3396–3404. https://doi.org/10.1093/bioinformatics/btx440

Mills, S., Griffin, C., O’Sullivan, O., Coffey, A., McAuliffe, O. E., Meijer, W. C., Serrano, L. M., & Ross, R. P. (2011a). A new phage on the ‘Mozzarella’ block: Bacteriophage 5093 shares a low level of homology with other Streptococcus thermophilus phages. International Dairy Journal, 21(12), 963–969. https://doi.org/10.1016/j.idairyj.2011.06.003

Mills, S., Griffin, C., O’Sullivan, O., Coffey, A., McAuliffe, O. E., Meijer, W. C., Serrano, L. M., & Ross, R. P. (2011b). A new phage on the ‘Mozzarella’ block: Bacteriophage 5093 shares a low level of homology with other Streptococcus thermophilus phages. International Dairy Journal, 21(12), 963–969. https://doi.org/10.1016/j.idairyj.2011.06.003

Moraru, C. (2021). VirClust – a tool for hierarchical clustering, core gene detection and annotation of (prokaryotic) viruses. BioRxiv, 2021.06.14.448304. https://doi.org/10.1101/2021.06.14.448304

Moraru, C., Varsani, A., & Kropinski, A. M. (2020). VIRIDIC—A Novel Tool to Calculate the Intergenomic Similarities of Prokaryote-Infecting Viruses. Viruses, 12(11), 1268. https://doi.org/10.3390/v12111268

Neve, H., Zenz, K. I., Desiere, F., Koch, A., Heller, K. J., & Brüssow, H. (1998). Comparison of the Lysogeny Modules from the TemperateStreptococcus thermophilusBacteriophages TP-J34 and Sfi21: Implications for the Modular Theory of Phage Evolution. Virology, 241(1), 61–72. https://doi.org/10.1006/viro.1997.8960

Nishimura, Y., Yoshida, T., Kuronishi, M., Uehara, H., Ogata, H., & Goto, S. (2017). ViPTree: The viral proteomic tree server. Bioinformatics, 33(15), 2379–2380. https://doi.org/10.1093/bioinformatics/btx157

Page, A. J., Cummins, C. A., Hunt, M., Wong, V. K., Reuter, S., Holden, M. T. G., Fookes, M., Falush, D., Keane, J. A., & Parkhill, J. (2015). Roary: Rapid large-scale prokaryote pan genome analysis. Bioinformatics, 31(22), 3691–3693. https://doi.org/10.1093/bioinformatics/btv421

Philippe, C., Levesque, S., Dion, M. B., Tremblay, D. M., Horvath, P., Lüth, N., Cambillau, C., Franz, C., Neve, H., Fremaux, C., Heller, K. J., & Moineau, S. (2020). Novel Genus of Phages Infecting Streptococcus thermophilus: Genomic and Morphological Characterization. Applied and Environmental Microbiology, 86(13), e00227-20, /aem/86/13/AEM.00227-20.atom. https://doi.org/10.1128/AEM.00227-20

Pujato, S. A., Quiberoni, A., & Mercanti, D. J. (2019). Bacteriophages on dairy foods. Journal of Applied Microbiology, 126(1), 14–30. https://doi.org/10.1111/jam.14062

Quiberoni, A., Moineau, S., Rousseau, G. M., Reinheimer, J., & Ackermann, H.-W. (2010). Streptococcus thermophilus bacteriophages. International Dairy Journal, 20(10), 657–664. https://doi.org/10.1016/j.idairyj.2010.03.012

Rambaut, A. (2012). FigTree. http://tree.bio.ed.ac.uk/software/figtree/

Seemann, T. (2014). Prokka: Rapid prokaryotic genome annotation. Bioinformatics, 30(14), 2068–2069. https://doi.org/10.1093/bioinformatics/btu153

Sehnal, D., Bittrich, S., Deshpande, M., Svobodová, R., Berka, K., Bazgier, V., Velankar, S., Burley, S. K., Koča, J., & Rose, A. S. (2021). Mol* Viewer: Modern web app for 3D visualization and analysis of large biomolecular structures. Nucleic Acids Research, 49(W1), W431–W437. https://doi.org/10.1093/nar/gkab314

Simmonds, P., Adams, M. J., Benkő, M., Breitbart, M., Brister, J. R., Carstens, E. B., Davison, A. J., Delwart, E., Gorbalenya, A. E., Harrach, B., Hull, R., King, A. M. Q., Koonin, E. V., Krupovic, M., Kuhn, J. H., Lefkowitz, E. J., Nibert, M. L., Orton, R., Roossinck, M. J., … Zerbini, F. M. (2017). Virus taxonomy in the age of metagenomics. Nature Reviews Microbiology, 15(3), 161–168. https://doi.org/10.1038/nrmicro.2016.177

Somerville, V., Lutz, S., Schmid, M., Frei, D., Moser, A., Irmler, S., Frey, J. E., & Ahrens, C. H. (2019). Long-read based de novo assembly of low-complexity metagenome samples results in finished genomes and reveals insights into strain diversity and an active phage system. BMC Microbiology, 19(1), 143. https://doi.org/10.1186/s12866-019-1500-0

Stanley, E., Fitzgerald, G., Le Marrec, C., Fayard, B., & Van Sinderen, D. (1997). Sequence analysis and characterization of ∅O1205, a temperate bacteriophage infecting Streptococcus thermophilus CNRZ1205. Microbiology (Reading, England), 143 ( Pt 11), 3417–3429. https://doi.org/10.1099/00221287-143-11-3417

Szymczak, P., Janzen, T., Neves, A. R., Kot, W., Hansen, L. H., Lametsch, R., Neve, H., Franz, C. M. A. P., & Vogensen, F. K. (2017). Novel Variants of Streptococcus thermophilus Bacteriophages Are Indicative of Genetic Recombination among Phages from Different Bacterial Species. Applied and Environmental Microbiology, 83(5), e02748-16, e02748-16. https://doi.org/10.1128/AEM.02748-16

Szymczak, P., Rau, M. H., Monteiro, J. M., Pinho, M. G., Filipe, S. R., Vogensen, F. K., Zeidan, A. A., & Janzen, T. (2019). A comparative genomics approach for identifying host-range determinants in Streptococcus thermophilus bacteriophages. Scientific Reports, 9(1), 7991. https://doi.org/10.1038/s41598-019-44481-z

Szymczak, P., Vogensen, F. K., & Janzen, T. (2019). Novel isolates of Streptococcus thermophilus bacteriophages from group 5093 identified with an improved multiplex PCR typing method. International Dairy Journal, 91, 18–24. https://doi.org/10.1016/j.idairyj.2018.12.001

Tremblay, D. M., & Moineau, S. (1999). Complete Genomic Sequence of the Lytic Bacteriophage DT1 ofStreptococcus thermophilus. Virology, 255(1), 63–76. https://doi.org/10.1006/viro.1998.9525

Turner, D., Kropinski, A. M., & Adriaenssens, E. M. (2021). A Roadmap for Genome-Based Phage Taxonomy. Viruses, 13(3), 506. https://doi.org/10.3390/v13030506

Walker, P. J., Siddell, S. G., Lefkowitz, E. J., Mushegian, A. R., Adriaenssens, E. M., Alfenas-Zerbini, P., Davison, A. J., Dempsey, D. M., Dutilh, B. E., García, M. L., Harrach, B., Harrison, R. L., Hendrickson, R. C., Junglen, S., Knowles, N. J., Krupovic, M., Kuhn, J. H., Lambert, A. J., Łobocka, M., … Zerbini, F. M. (2021). Changes to virus taxonomy and to the International Code of Virus Classification and Nomenclature ratified by the International Committee on Taxonomy of Viruses (2021). Archives of Virology. https://doi.org/10.1007/s00705-021-05156-1

Zafar, N., Mazumder, R., & Seto, D. (2002). CoreGenes: A computational tool for identifying and cataloging “core” genes in a set of small genomes. BMC Bioinformatics, 3(1), 12. https://doi.org/10.1186/1471-2105-3-12

Zinno, P., Janzen, T., Bennedsen, M., Ercolini, D., & Mauriello, G. (2010). Characterization of Streptococcus thermophilus lytic bacteriophages from mozzarella cheese plants. International Journal of Food Microbiology, 138(1–2), 137–144. https://doi.org/10.1016/j.ijfoodmicro.2009.12.008

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30/07/2022

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BATALHA, L. S.; VIDIGAL, P. M. P.; GONTIJO, M. T. P.; ELLER, M. R. Expanding the genomes insight of Streptococcus thermophilus phages through a multifaceted approach. Research, Society and Development, [S. l.], v. 11, n. 10, p. e273111032693, 2022. DOI: 10.33448/rsd-v11i10.32693. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/32693. Acesso em: 16 nov. 2024.

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Agrarian and Biological Sciences