ABSTRACT
          
            Streptococcus thermophilus
            , a very important dairy species, is constantly threatened by phage infection. We report the genome sequences of three
            S. thermophilus
            bacteriophages isolated from a dairy environment in the Veneto region of Italy. These sequences will be used for the development of new strategies to detect and control phages in dairy environments.
          </jats:p

Campanaro, Stefano

Corich, Viviana

da Silva Duarte, Vin\uedcius

Giacomini, Alessio

Giaretta, Sabrina

Pereira Vidigal, Pedro M.

Tarrah, Armin

Treu, Laura

English

Streptococcus thermophilus, a very important dairy species, is constantly threatened by phage infection. We report the genome sequences of three S. thermophilus bacteriophages isolated from a dairy environment in the Veneto region of Italy. These sequences will be used for the development of new strategies to detect and control phages in dairy environments

Duarte, Viní­cius da Silva

Vidigal, Pedro M.Pereira

Online Research Database In Technology

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Downloaded from orbit.dtu.dk on: Apr 10, 2018Draft genome sequences of three virulent Streptococcus thermophilus bacteriophagesisolated from the dairy environment in the Veneto region of ItalyDuarte, Viní-cius da Silva; Giaretta, Sabrina; Treu, Laura; Campanaro, Stefano; Vidigal, Pedro M.Pereira;Tarrah, Armin; Giacomini, Alessio; Corich, VivianaPublished in:Genome AnnouncementsLink to article, DOI:10.1128/genomeA.00045-18Publication date:2018Document VersionPublisher's PDF, also known as Version of recordLink back to DTU OrbitCitation (APA):Duarte, V. D. S., Giaretta, S., Treu, L., Campanaro, S., Vidigal, P. M. P., Tarrah, A., ... Corich, V. (2018). Draftgenome sequences of three virulent Streptococcus thermophilus bacteriophages isolated from the dairyenvironment in the Veneto region of Italy. Genome Announcements, 6(10), [e00045-18]. DOI:10.1128/genomeA.00045-18Draft Genome Sequences of Three Virulent Streptococcusthermophilus Bacteriophages Isolated from the DairyEnvironment in the Veneto Region of ItalyVinícius da Silva Duarte,a Sabrina Giaretta,b Laura Treu,b,d Stefano Campanaro,c Pedro M. Pereira Vidigal,e Armin Tarrah,bAlessio Giacomini,b Viviana CorichbaDepartment of Microbiology, Federal University of Viçosa, Viçosa, Minas Gerais, BrazilbDepartment of Agronomy, Food, Natural Resources, Animals and the Environment, University of Padova,Legnaro, ItalycDepartment of Biology, University of Padova, Padua, ItalydDepartment of Environmental Engineering, Technical University of Denmark, Lyngby, DenmarkeNúcleo de Análise de Biomoléculas (NuBioMol), Center of Biological Sciences, Federal University of Viçosa,Viçosa, Minas Gerais, BrazilABSTRACT Streptococcus thermophilus, a very important dairy species, is constantlythreatened by phage infection. We report the genome sequences of three S. thermo-philus bacteriophages isolated from a dairy environment in the Veneto region ofItaly. These sequences will be used for the development of new strategies to detectand control phages in dairy environments.Streptococcus thermophilus is a low-GC Gram-positive bacterium considered the secondmost important dairy species (1) and is commonly used to produce cheese and yogurts(2, 3). Currently, its statuses of generally recognized as safe (GRAS) and of qualiﬁedpresumption of safety (QPS) (4) make it reach a market value of $40 billion (5, 6).Ubiquitous in the dairy environment, bacterial viruses or bacteriophages are aconstant threat to S. thermophilus starter cultures (7, 8). Overall, economic losses due tophage infection in dairy products are related to low fermentation activity and reducedproduct quality that may lead to total process failure (9, 10).Here, we report the genome sequences of three S. thermophilus bacteriophagesisolated from a dairy environment in Northeast Italy, vB_SthS_VA214, vB_SthS_VA460,and the partial genome sequence of vB_SthS_VA698 (VA214, VA460, and VA698,respectively).Bacteriophages were concentrated and puriﬁed using polyethylene glycol 8,000,and their genomic DNA was extracted following the method described by Binetti et al.(11). Sequencing was performed with the Illumina MiSeq platform using paired-end (PE)reads (2 250 bp) and a Nextera library at the Ramaciotti Centre for Genomics (Sydney,Australia). After quality ﬁltering and merging of the overlapping PE reads, a total of56,194, 57,208, and 68,210 sequences were obtained. Raw reads were assembled denovo using CLC Genomic Workbench software (version 9.5). Coverage values obtainedfor VA214, VA460, and VA698 were approximately 367-, 308-, and 122-fold, respectively.Total genomes sizes of 38.2, 41.2, and 33.3 Kb were estimated for VA214, VA460, andVA698, respectively, with an average GC content of 38.6%.The Rapid Annotations using Subsystems Technology (RAST) server (12) was usedfor gene ﬁnding and annotation. In total, 53, 56, and 38 coding sequences (CDS) werepredicted for VA214, VA460, and VA698, respectively. For phage VA214 only, a genecluster encoding seven tRNAs (Gly, Ala, Val, Lys, Leu, Thr, and Gly) and without intronsor pseudogenes was identiﬁed using the tRNAscan-SE program (13).Received 15 January 2018 Accepted 8February 2018 Published 8 March 2018Citation da Silva Duarte V, Giaretta S, Treu L,Campanaro S, Pereira Vidigal PM, Tarrah A,Giacomini A, Corich V. 2018. Draft genomesequences of three virulent Streptococcusthermophilus bacteriophages isolated from thedairy environment in the Veneto region of Italy.Genome Announc 6:e00045-18. https://doi.org/10.1128/genomeA.00045-18.Copyright © 2018 da Silva Duarte et al. This isan open-access article distributed under theterms of the Creative Commons Attribution 4.0International license.Address correspondence to Alessio Giacomini,alessio.giacomini@unipd.it.VIRUSEScrossmVolume 6 Issue 10 e00045-18 genomea.asm.org 1 on March 27, 2018 by DTU Libraryhttp://genomea.asm.org/Downloaded from A BLASTn similarity search revealed that the genome of VA214 is related toStreptococcus phage P0091, whereas VA460 and VA698 are closely related to Strepto-coccus phage P9851 and Streptococcus phage P7132, respectively.In this work, we present the complete genome sequences of three S. thermophilusbacteriophages, which will serve as the basis for developing new strategies useful todetect and control phages in dairy environments. In the future, we will also conductstudies of bacterial immunity against phages using S. thermophilus M17PTZA496 (14)and S. thermophilus TH1435/1436 (15).Accession number(s). This whole-genome shotgun project has been depositedat DDBJ/ENA/GenBank under the accession numbers MG708274, MG708275, andMG708273 for vB_SthS_VA214, vB_SthS_VA460, and vB_SthS_VA698, respectively. Theversions described in this paper are the ﬁrst versions, MG708274.1, MG708275.1,and MG708273.1, respectively.ACKNOWLEDGMENTSWe are grateful to the Núcleo de Análise de Biomoléculas and Núcleo de Microsco-pia e Microanálise of the Universidade Federal de Viçosa for providing the facilities forthe conduction of the experiments.We acknowledge ﬁnancial support by the following Brazilian agencies: Fundação deAmparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), Coordenacão de Aperfeiçoa-mento de Pessoal de Nível Superior (CAPES), Conselho Nacional de DesenvolvimentoCientíﬁco e Tecnológico (CNPq), and Financiadora de Estudos e Projetos (Finep).We thank Cristian Andrighetto and Veneto Agricoltura for providing the viruses.REFERENCES1. Hols P, Hancy F, Fontaine L, Grossiord B, Prozzi D, Leblond-Bourget N,Decaris B, Bolotin A, Delorme C, Dusko Ehrlich S, Guédon E, Monnet V,Renault P, Kleerebezem M. 2005. New insights in the molecular biologyand physiology of Streptococcus thermophilus revealed by comparativegenomics. FEMS Microbiol Rev 29:435–463. https://doi.org/10.1016/j.fmrre.2005.04.008.2. Calasso M, Ercolini D, Mancini L, Stellato G, Minervini F, Di Cagno R, DeAngelis M, Gobbetti M. 2016. Relationships among house, rind and coremicrobiotas during manufacture of traditional Italian cheeses at thesame dairy plant. Food Microbiol 54:115–126. https://doi.org/10.1016/j.fm.2015.10.008.3. Marco ML, Heeney D, Binda S, Cifelli CJ, Cotter PD, Foligné B, Gänzle M,Kort R, Pasin G, Pihlanto A, Smid EJ, Hutkins R. 2017. Health beneﬁts offermented foods: microbiota and beyond. Curr Opin Biotechnol 44:94–102. https://doi.org/10.1016/j.copbio.2016.11.010.4. Vendramin V, Treu L, Campanaro S, Lombardi A, Corich V, Giacomini A.2017. Genome comparison and physiological characterization of eightStreptococcus thermophilus strains isolated from Italian dairy products.Food Microbiol 63:47–57. https://doi.org/10.1016/j.fm.2016.11.002.5. Bolotin A, Quinquis B, Renault P, Sorokin A, Ehrlich SD, Kulakauskas S,Lapidus A, Goltsman E, Mazur M, Pusch GD, Fonstein M, Overbeek R,Kyprides N, Purnelle B, Prozzi D, Ngui K, Masuy D, Hancy F, Burteau S, BoutryM, Delcour J, Goffeau A, Hols P. 2004. Complete sequence and comparativegenome analysis of the dairy bacterium Streptococcus thermophilus. NatBiotechnol 22:1554–1558. https://doi.org/10.1038/nbt1034.6. Hutkins RW. 2007. Microbiology and technology of fermented foodsmicrobiology and technology of fermented foods John Wiley & Sons,Hoboken, NJ.7. Clokie MR, Millard AD, Letarov AV, Heaphy S. 2011. Phages in nature.Bacteriophage 1:31–45. https://doi.org/10.4161/bact.1.1.14942.8. Marcó MB, Moineau S, Quiberoni A. 2012. Bacteriophages and dairyfermentations. Bacteriophage 2:149–158. https://doi.org/10.4161/bact.21868.9. Bruttin A, Desiere F, D’amico N, Guérin JP, Sidoti J, Huni B, Lucchini S,Brüssow H. 1997. Molecular ecology of Streptococcus thermophilus bac-teriophage infections in a cheese factory. Appl Environ Microbiol 63:3144–3150.10. Moineau S, Lévesque C. 2004. Control of Bacteriophages in IndustrialFermentations, p. 285–296. In Bacteriophages CRC Press, Boca Raton, FL.11. Binetti AG, Del Rio B, Martin MC, Alvarez MA. 2005. Detection and charac-terization of Streptococcus thermophilus bacteriophages by use of theantireceptor gene sequence. Appl Environ Microbiol 71:6096–6103.https://doi.org/10.1128/AEM.71.10.6096-6103.2005.12. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, Edwards RA,Gerdes S, Parrello B, Shukla M, Vonstein V, Wattam AR, Xia F, Stevens R.2014. The SEED and the rapid annotation of microbial genomes usingsubsystems technology (RAST). Nucleic Acids Res 42:D206–D214. https://doi.org/10.1093/nar/gkt1226.13. Lowe TM, Eddy SR. 1996. TRNAscan-SE: a program for improved detec-tion of transfer RNA genes in genomic sequence. Nucleic Acids Res25:955–964.14. Treu L, Vendramin V, Bovo B, Campanaro S, Corich V, Giacomini A. 2014.Genome sequences of Streptococcus thermophilus strains MTH17CL396and M17PTZA496 from Fontina, an Italian PDO cheese. Genome An-nounc 2:e00067-14. https://doi.org/10.1128/genomeA.00067-14.15. Treu L, Vendramin V, Bovo B, Campanaro S, Corich V, Giacomini A. 2014.Whole-genome sequences of Streptococcus thermophilus strains TH1435and TH1436, isolated from raw goat milk. Genome Announc 2:e01129-13. https://doi.org/10.1128/genomeA.01129-13.da Silva Duarte et al.Volume 6 Issue 10 e00045-18 genomea.asm.org 2 on March 27, 2018 by DTU Libraryhttp://genomea.asm.org/Downloaded from 

Draft genome sequences of three virulent Streptococcus thermophilus bacteriophages isolated from the dairy environment in the Veneto region of Italy

Vinícius da Silva Duarte

Sabrina Giaretta

Laura Treu

Stefano Campanaro

Pedro M. Pereira Vidigal

Armin Tarrah

Alessio Giacomini

Viviana Corich

Crossref

Genome Announcements

Draft Genome Sequences of Three Virulent Streptococcus thermophilus Bacteriophages Isolated from the Dairy Environment in the Veneto Region of Italy

da Silva Duarte, Vinícius

TARRAH, ARMIN

Archivio istituzionale della ricerca - Università di Padova

Draft Genome Sequences of Three Virulent Streptococcusthermophilus Bacteriophages Isolated from the DairyEnvironment in the Veneto Region of ItalyVinícius da Silva Duarte,a Sabrina Giaretta,b Laura Treu,b,d Stefano Campanaro,c Pedro M. Pereira Vidigal,e Armin Tarrah,bAlessio Giacomini,b Viviana CorichbaDepartment of Microbiology, Federal University of Viçosa, Viçosa, Minas Gerais, BrazilbDepartment of Agronomy, Food, Natural Resources, Animals and the Environment, University of Padova,Legnaro, ItalycDepartment of Biology, University of Padova, Padua, ItalydDepartment of Environmental Engineering, Technical University of Denmark, Lyngby, DenmarkeNúcleo de Análise de Biomoléculas (NuBioMol), Center of Biological Sciences, Federal University of Viçosa,Viçosa, Minas Gerais, BrazilABSTRACT Streptococcus thermophilus, a very important dairy species, is constantlythreatened by phage infection. We report the genome sequences of three S. thermo-philus bacteriophages isolated from a dairy environment in the Veneto region ofItaly. These sequences will be used for the development of new strategies to detectand control phages in dairy environments.Streptococcus thermophilus is a low-GC Gram-positive bacterium considered the secondmost important dairy species (1) and is commonly used to produce cheese and yogurts(2, 3). Currently, its statuses of generally recognized as safe (GRAS) and of qualiﬁedpresumption of safety (QPS) (4) make it reach a market value of $40 billion (5, 6).Ubiquitous in the dairy environment, bacterial viruses or bacteriophages are aconstant threat to S. thermophilus starter cultures (7, 8). Overall, economic losses due tophage infection in dairy products are related to low fermentation activity and reducedproduct quality that may lead to total process failure (9, 10).Here, we report the genome sequences of three S. thermophilus bacteriophagesisolated from a dairy environment in Northeast Italy, vB_SthS_VA214, vB_SthS_VA460,and the partial genome sequence of vB_SthS_VA698 (VA214, VA460, and VA698,respectively).Bacteriophages were concentrated and puriﬁed using polyethylene glycol 8,000,and their genomic DNA was extracted following the method described by Binetti et al.(11). Sequencing was performed with the Illumina MiSeq platform using paired-end (PE)reads (2 250 bp) and a Nextera library at the Ramaciotti Centre for Genomics (Sydney,Australia). After quality ﬁltering and merging of the overlapping PE reads, a total of56,194, 57,208, and 68,210 sequences were obtained. Raw reads were assembled denovo using CLC Genomic Workbench software (version 9.5). Coverage values obtainedfor VA214, VA460, and VA698 were approximately 367-, 308-, and 122-fold, respectively.Total genomes sizes of 38.2, 41.2, and 33.3 Kb were estimated for VA214, VA460, andVA698, respectively, with an average GC content of 38.6%.The Rapid Annotations using Subsystems Technology (RAST) server (12) was usedfor gene ﬁnding and annotation. In total, 53, 56, and 38 coding sequences (CDS) werepredicted for VA214, VA460, and VA698, respectively. For phage VA214 only, a genecluster encoding seven tRNAs (Gly, Ala, Val, Lys, Leu, Thr, and Gly) and without intronsor pseudogenes was identiﬁed using the tRNAscan-SE program (13).Received 15 January 2018 Accepted 8February 2018 Published 8 March 2018Citation da Silva Duarte V, Giaretta S, Treu L,Campanaro S, Pereira Vidigal PM, Tarrah A,Giacomini A, Corich V. 2018. Draft genomesequences of three virulent Streptococcusthermophilus bacteriophages isolated from thedairy environment in the Veneto region of Italy.Genome Announc 6:e00045-18. https://doi.org/10.1128/genomeA.00045-18.Copyright © 2018 da Silva Duarte et al. This isan open-access article distributed under theterms of the Creative Commons Attribution 4.0International license.Address correspondence to Alessio Giacomini,alessio.giacomini@unipd.it.VIRUSEScrossmVolume 6 Issue 10 e00045-18 genomea.asm.org 1 on March 8, 2018 by BIBLIOTECA CENTRALE AGRIPOLIShttp://genomea.asm.org/Downloaded from A BLASTn similarity search revealed that the genome of VA214 is related toStreptococcus phage P0091, whereas VA460 and VA698 are closely related to Strepto-coccus phage P9851 and Streptococcus phage P7132, respectively.In this work, we present the complete genome sequences of three S. thermophilusbacteriophages, which will serve as the basis for developing new strategies useful todetect and control phages in dairy environments. In the future, we will also conductstudies of bacterial immunity against phages using S. thermophilus M17PTZA496 (14)and S. thermophilus TH1435/1436 (15).Accession number(s). This whole-genome shotgun project has been depositedat DDBJ/ENA/GenBank under the accession numbers MG708274, MG708275, andMG708273 for vB_SthS_VA214, vB_SthS_VA460, and vB_SthS_VA698, respectively. Theversions described in this paper are the ﬁrst versions, MG708274.1, MG708275.1,and MG708273.1, respectively.ACKNOWLEDGMENTSWe are grateful to the Núcleo de Análise de Biomoléculas and Núcleo de Microsco-pia e Microanálise of the Universidade Federal de Viçosa for providing the facilities forthe conduction of the experiments.We acknowledge ﬁnancial support by the following Brazilian agencies: Fundação deAmparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), Coordenacão de Aperfeiçoa-mento de Pessoal de Nível Superior (CAPES), Conselho Nacional de DesenvolvimentoCientíﬁco e Tecnológico (CNPq), and Financiadora de Estudos e Projetos (Finep).We thank Cristian Andrighetto and Veneto Agricoltura for providing the viruses.REFERENCES1. Hols P, Hancy F, Fontaine L, Grossiord B, Prozzi D, Leblond-Bourget N,Decaris B, Bolotin A, Delorme C, Dusko Ehrlich S, Guédon E, Monnet V,Renault P, Kleerebezem M. 2005. New insights in the molecular biologyand physiology of Streptococcus thermophilus revealed by comparativegenomics. FEMS Microbiol Rev 29:435–463. https://doi.org/10.1016/j.fmrre.2005.04.008.2. Calasso M, Ercolini D, Mancini L, Stellato G, Minervini F, Di Cagno R, DeAngelis M, Gobbetti M. 2016. Relationships among house, rind and coremicrobiotas during manufacture of traditional Italian cheeses at thesame dairy plant. Food Microbiol 54:115–126. https://doi.org/10.1016/j.fm.2015.10.008.3. Marco ML, Heeney D, Binda S, Cifelli CJ, Cotter PD, Foligné B, Gänzle M,Kort R, Pasin G, Pihlanto A, Smid EJ, Hutkins R. 2017. Health beneﬁts offermented foods: microbiota and beyond. Curr Opin Biotechnol 44:94–102. https://doi.org/10.1016/j.copbio.2016.11.010.4. Vendramin V, Treu L, Campanaro S, Lombardi A, Corich V, Giacomini A.2017. Genome comparison and physiological characterization of eightStreptococcus thermophilus strains isolated from Italian dairy products.Food Microbiol 63:47–57. https://doi.org/10.1016/j.fm.2016.11.002.5. Bolotin A, Quinquis B, Renault P, Sorokin A, Ehrlich SD, Kulakauskas S,Lapidus A, Goltsman E, Mazur M, Pusch GD, Fonstein M, Overbeek R,Kyprides N, Purnelle B, Prozzi D, Ngui K, Masuy D, Hancy F, Burteau S, BoutryM, Delcour J, Goffeau A, Hols P. 2004. Complete sequence and comparativegenome analysis of the dairy bacterium Streptococcus thermophilus. NatBiotechnol 22:1554–1558. https://doi.org/10.1038/nbt1034.6. Hutkins RW. 2007. Microbiology and technology of fermented foodsmicrobiology and technology of fermented foods John Wiley & Sons,Hoboken, NJ.7. Clokie MR, Millard AD, Letarov AV, Heaphy S. 2011. Phages in nature.Bacteriophage 1:31–45. https://doi.org/10.4161/bact.1.1.14942.8. Marcó MB, Moineau S, Quiberoni A. 2012. Bacteriophages and dairyfermentations. Bacteriophage 2:149–158. https://doi.org/10.4161/bact.21868.9. Bruttin A, Desiere F, D’amico N, Guérin JP, Sidoti J, Huni B, Lucchini S,Brüssow H. 1997. Molecular ecology of Streptococcus thermophilus bac-teriophage infections in a cheese factory. Appl Environ Microbiol 63:3144–3150.10. Moineau S, Lévesque C. 2004. Control of Bacteriophages in IndustrialFermentations, p. 285–296. In Bacteriophages CRC Press, Boca Raton, FL.11. Binetti AG, Del Rio B, Martin MC, Alvarez MA. 2005. Detection and charac-terization of Streptococcus thermophilus bacteriophages by use of theantireceptor gene sequence. Appl Environ Microbiol 71:6096–6103.https://doi.org/10.1128/AEM.71.10.6096-6103.2005.12. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, Edwards RA,Gerdes S, Parrello B, Shukla M, Vonstein V, Wattam AR, Xia F, Stevens R.2014. The SEED and the rapid annotation of microbial genomes usingsubsystems technology (RAST). Nucleic Acids Res 42:D206–D214. https://doi.org/10.1093/nar/gkt1226.13. Lowe TM, Eddy SR. 1996. TRNAscan-SE: a program for improved detec-tion of transfer RNA genes in genomic sequence. Nucleic Acids Res25:955–964.14. Treu L, Vendramin V, Bovo B, Campanaro S, Corich V, Giacomini A. 2014.Genome sequences of Streptococcus thermophilus strains MTH17CL396and M17PTZA496 from Fontina, an Italian PDO cheese. Genome An-nounc 2:e00067-14. https://doi.org/10.1128/genomeA.00067-14.15. Treu L, Vendramin V, Bovo B, Campanaro S, Corich V, Giacomini A. 2014.Whole-genome sequences of Streptococcus thermophilus strains TH1435and TH1436, isolated from raw goat milk. Genome Announc 2:e01129-13. https://doi.org/10.1128/genomeA.01129-13.da Silva Duarte et al.Volume 6 Issue 10 e00045-18 genomea.asm.org 2 on March 8, 2018 by BIBLIOTECA CENTRALE AGRIPOLIShttp://genomea.asm.org/Downloaded from 

https://www.research.unipd.it/bitstream/11577/3265133/1/2018_Genome%20Announc.Duarte.pdf

Draft Genome Sequences of Three Virulent Streptococcus thermophilus Bacteriophages Isolated from the Dairy Environment in the Veneto Region of Italy

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