Abstract
Bovine mastitis is an important disease in dairy cows, and Staphylococcus aureus is the most prevalent microorganism. Bacteriophages are considered an alternative to treat bacterial infections due to antimicrobial resistance crisis. In this study, we isolated and characterized novel S. aureus temperate phages, namely B_UFSM4 and B_UFSM5, from bovine milk. The complete genomes of B_UFSM4 and B_UFSM5 have 41.396 bp and 41.829 bp, respectively. The viruses have double-stranded DNA and linear architecture. Phylogenic similarity was observed by proteome with Staphylococcus phage phiPV83, CN125 and JS01. Therefore, the phages were classified into the family Siphoviridae, genus Biseptimavirus and order Caudovirales. In the host range, the B_UFSM4 and B_UFSM5 had lytic activity of 45.8% and 54.16%, respectively, inclusive on isolates from Staphylococcus sciuri and Rothia terrae. Thus, in this study, species novel of S. aureus temperate phages was isolated and characterized, these phages reveal similarities to each other; however, they are distinct from other species of S. aureus phages of the family Siphoviridae.
Similar content being viewed by others
Data availability
Nucleotide sequence data reported are available in the GenBank database under the accession number MW147366 for phage B_UFSM4 and MW192778 for B_UFSM5.
References
Ackermann H-W (2009) Phage classification and characterization. Methods Mol Biol 501:127–140. https://doi.org/10.1007/978-1-60327-164-6_13
Adams M (1959) Bacteriophages. Interscience Publishers Inc, Nova york
Alluwaimi AM (2004) The cytokines of bovine mammary gland: prospects for diagnosis and therapy. Res Vet Sci 77:211–222. https://doi.org/10.1016/j.rvsc.2004.04.006
Andrews S, Bittencourt S (2010) FastQC: a quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc. Accessed 21 Jan 2021
Anisimova M, Gascuel O (2006) Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst Biol 55:539–552. https://doi.org/10.1080/10635150600755453
Arndt D, Grant JR, Marcu A et al (2016) PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res 44:W16–W21. https://doi.org/10.1093/nar/gkw387
Barkema HW, Schukken YH, Lam TJGM et al (1999) Management practices associated with the incidence rate of clinical mastitis. J Dairy Sci 82:1643–1654. https://doi.org/10.3168/jds.S0022-0302(99)75393-2
Barkema HW, Schukken YH, Zadoks RN (2006) Invited review: the role of cow, pathogen, and treatment regimen in the therapeutic success of bovine Staphylococcus aureus mastitis. J Dairy Sci 89:1877–1895. https://doi.org/10.3168/jds.S0022-0302(06)72256-1
Bebeacua C, Lorenzo Fajardo JC, Blangy S et al (2013) X-ray structure of a superinfection exclusion lipoprotein from phage TP-J34 and identification of the tape measure protein as its target. Mol Microbiol 89:152–165. https://doi.org/10.1111/mmi.12267
Boeckel TPV, Pires J, Silvester R et al (2019) Global trends in antimicrobial resistance in animals in low—and middle-income countries. Science. https://doi.org/10.1126/science.aaw1944
Bohannan BJM, Lenski RE (1997) Effect of resource enrichment on a chemostat community of bacteria and bacteriophage. Ecology 78:2303–2315
Bortolaia V, Kaas RS, Ruppe E et al (2020) ResFinder 4.0 for predictions of phenotypes from genotypes. J Antimicrob Chemother. https://doi.org/10.1093/jac/dkaa345
Boyd EF, Carpenter MR, Chowdhury N (2012) Mobile effector proteins on phage genomes. Bacteriophage 2:139–148. https://doi.org/10.4161/bact.21658
Bradley DE (1967) Ultrastructure of bacteriophage and bacteriocins. Bacteriol Rev 31:230–314. https://doi.org/10.1128/mmbr.31.4.230-314.1967
Chang H, Chen C, Lin J et al (2005) Isolation and characterization of novel giant. Society 71:1387–1393
D’Herelle F (1931) Bacteriophage as a treatment in acute medical and surgical infections. New York Acad Med 7:329–348
de Jong A, Garch FE, Simjee S et al (2018) Monitoring of antimicrobial susceptibility of udder pathogens recovered from cases of clinical mastitis in dairy cows across Europe: VetPath results. Vet Microbiol 213:73–81. https://doi.org/10.1016/j.vetmic.2017.11.021
Dehkordi SH, Hosseinpour F, Kahrizangi AE (2011) An in vitro evaluation of antibacterial effect of silver nanoparticles on Staphylococcus aureus isolated from bovine subclinical mastitis. Afr J Biotechnol 10:10795–10797. https://doi.org/10.5897/ajb11.1499
Del Sol CM, Molina-Santiago C, Gómez-García MR, Ramos JL (2016) A Pseudomonas putida double mutant deficient in butanol assimilation: a promising step for engineering a biological biofuel production platform. FEMS Microbiol Lett 363:1–7. https://doi.org/10.1093/femsle/fnw018
Dunne M, Hupfeld M, Klumpp J, Loessner MJ (2018) Molecular basis of bacterial host interactions by gram-positive targeting bacteriophages. Viruses. https://doi.org/10.3390/v10080397
Gill J, Hyman P (2010) Phage choice, isolation, and preparation for phage therapy. Curr Pharm Biotechnol 11:2–14. https://doi.org/10.2174/138920110790725311
Girardini LK, Paim DS, Ausani TC et al (2016) Antimicrobial resistance profiles of Staphylococcus aureus clusters on small dairy farms in southern Brazil. Pesqui Vet Bras 36:951–956. https://doi.org/10.1590/S0100-736X2016001000006
Goerke C, Pantucek R, Holtfreter S et al (2009) Diversity of prophages in dominant Staphylococcus aureus clonal lineages. J Bacteriol 191:3462–3468. https://doi.org/10.1128/JB.01804-08
Gomes F, Henriques M (2016) Control of bovine mastitis: old and recent therapeutic approaches. Curr Microbiol 72:377–382. https://doi.org/10.1007/s00284-015-0958-8
Guindon S, Dufayard JF, Lefort V et al (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. https://doi.org/10.1093/sysbio/syq010
Halasa T, Huijps K, Østerås O, Hogeveen H (2007) Economic effects of bovine mastitis and mastitis management: a review. Vet Q 29:18–31. https://doi.org/10.1080/01652176.2007.9695224
Howard-Varona C, Hargreaves KR, Abedon ST, Sullivan MB (2017) Lysogeny in nature: mechanisms, impact and ecology of temperate phages. ISME J 11:1511–1520. https://doi.org/10.1038/ismej.2017.16
Jia H, Bai Q, Yang Y, Yao H (2013) Complete genome sequence of Staphylococcus aureus siphovirus phage JS01. Genome Announc 1:2–3. https://doi.org/10.1128/genomeA.00797-13
Jia H, Dong W, Yuan L et al (2015) Characterization and complete genome sequence analysis of Staphylococcus aureus bacteriophage JS01. Virus Genes 50:345–348. https://doi.org/10.1007/s11262-015-1168-y
Joensen KG, Scheutz F, Lund O et al (2014) Real-time whole-genome sequencing for routine typing, surveillance, and outbreak detection of verotoxigenic Escherichia coli. J Clin Microbiol 52:1501–1510. https://doi.org/10.1128/JCM.03617-13
Kwiatek M, Parasion S, Mizak L et al (2012) Characterization of a bacteriophage, isolated from a cow with mastitis, that is lytic against Staphylococcus aureus strains. Arch Virol 157:225–234. https://doi.org/10.1007/s00705-011-1160-3
Lane L (1991) 16S/23S rRNA sequencing. Nucleic acid techniques in bacterial systematic. Wiley, New york, pp 115–175
Li L, Zhang Z (2014) Isolation and characterization of a virulent bacteriophage SPW specific for Staphylococcus aureus isolated from bovine mastitis of lactating dairy cattle. Mol Biol Rep 41:5829–5838. https://doi.org/10.1007/s11033-014-3457-2
Malik DJ, Sokolov IJ, Vinner GK et al (2017) Formulation, stabilisation and encapsulation of bacteriophage for phage therapy. Adv Colloid Interface Sci 249:100–133. https://doi.org/10.1016/j.cis.2017.05.014
Melo LDR, Sillankorva S, Ackermann H et al (2014) Isolation and characterization of a new Staphylococcus epidermidis broad-spectrum bacteriophage. J Gen Virol 95:506–515. https://doi.org/10.1099/vir.0.060590-0
Monteiro R, Pires DP, Costa AR, Azeredo J (2019) Phage therapy: going temperate? Trends Microbiol 27:368–378. https://doi.org/10.1016/j.tim.2018.10.008
Owens WE (1987) Isolation of Staphylococcus aureus L forms from experimentally induced bovine mastitis. J Clin Microbiol 25:1956–1961
Pastagia M, Schuch R, Fischetti VA, Huang DB (2013) Lysins: the arrival of pathogen-directed anti-infectives. J Med Microbiol 62:1506–1516. https://doi.org/10.1099/jmm.0.061028-0
Prevelige PE, Cortines JR (2018) Phage assembly and the special role of the portal protein. Curr Opin Virol 31:66–73. https://doi.org/10.1016/j.coviro.2018.09.004
Rohde C, Wittmann J, Kutter E (2018) Bacteriophages: a therapy concept against multi-drug-resistant bacteria. Surg Infect (Larchmt) 19:737–744. https://doi.org/10.1089/sur.2018.184
Rozewicki J, Li S, Amada KM et al (2019) MAFFT-DASH: integrated protein sequence and structural alignment. Nucleic Acids Res 47:W5–W10. https://doi.org/10.1093/nar/gkz342
Sambrook J, Fritsch ER, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New york
Seegers H, Fourichon C, Beaudeau F (2003) Production effects related to mastitis and mastitis economics in dairy cattle herds Henri. Vet Res 34:475–491. https://doi.org/10.1051/vetres:2003027
Seyoum B, Kefyalew H, Abera B, Abdela N (2017) Prevalence, risk factors and antimicrobial susceptibility test of Staphylococcus aureus in Bovine cross breed mastitic milk in and around Asella town, Oromia regional state, southern Ethiopia. Acta Trop 177:32–36. https://doi.org/10.1016/j.actatropica.2017.09.012
Shao Y, Wang IN (2008) Bacteriophage adsorption rate and optimal lysis time. Genetics 180:471–482. https://doi.org/10.1534/genetics.108.090100
Sillankorva S, Neubauer P, Azeredo J (2008) Isolation and characterization of a T7-like lytic phage for Pseudomonas fluorescens. BMC Biotechnol 8:1–11. https://doi.org/10.1186/1472-6750-8-80
Sompolinsky D, Samra Z, Karakawa WW et al (1985) Encapsulation and capsular types in isolates of Staphylococcus aureus from different sources and relationship to phage types. J Clin Microbiol 22:828–834. https://doi.org/10.1128/jcm.22.5.828-834.1985
Steele N, McDougall S (2014) Effect of prolonged duration therapy of subclinical mastitis in lactating dairy cows using penethamate hydriodide. N Z Vet J 62:38–46. https://doi.org/10.1080/00480169.2013.830350
Suleiman TS, Karimuribo ED, Mdegela RH (2018) Prevalence of bovine subclinical mastitis and antibiotic susceptibility patterns of major mastitis pathogens isolated in Unguja island of Zanzibar, Tanzania. Trop Anim Health Prod 50:259–266. https://doi.org/10.1007/s11250-017-1424-3
Tahir A, Asif M, Abbas Z, Rehman SU (2017) Three bacteriophages SA, SA2 and SNAF can control growth of milk isolated staphylococcal species. Pak J Zool 49:529–533. https://doi.org/10.17582/journal.pjz/2017.49.2.529.533
Titze I, Lehnherr T, Lehnherr H, Krömker V (2020) Efficacy of bacteriophages against Staphylococcus aureus isolates from bovine mastitis. Pharmaceuticals. https://doi.org/10.3390/ph13030035
Torres-Barceló C (2018) Phage therapy faces evolutionary challenges. Viruses. https://doi.org/10.3390/v10060323
Vakkamäki J, Taponen S, Heikkilä AM, Pyörälä S (2017) Bacteriological etiology and treatment of mastitis in Finnish dairy herds. Acta Vet Scand 59:1–9. https://doi.org/10.1186/s13028-017-0301-4
Weinbauer MG (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28:127–181. https://doi.org/10.1016/j.femsre.2003.08.001
Zhang L, Bao H, Wei C et al (2014) Characterization and partial genomic analysis of a lytic Myoviridae bacteriophage against Staphylococcus aureus isolated from dairy cows with mastitis in Mid-east of China. Virus Genes 50:111–117. https://doi.org/10.1007/s11262-014-1130-4
Zou D, Kaneko J, Narita S, Kamio Y (2000) Prophage, φpv83-pro, carrying panton-valentine leukocidin genes, on the staphylococcus aureus p83 chromosome: comparative analysis of the genome structures of φpv83-pro, φpvl, φ11, and other phages. Biosci Biotechnol Biochem 64:2631–2643. https://doi.org/10.1271/bbb.64.2631
Acknowledgements
The authors acknowledge the support received from: Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq); Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul (FAPERGS); Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) (financial code 001); Setor de Virologia at Universidade Federal de Santa Maria (SV/UFSM); Centro de Microscopia da Zona Sul—FURG (CEME-SUL) at Universidade Federal de Rio Grande (FURG); and Prof Dr. Daniel Mendes Pereira Ardisson de Araújo of Departamento de Bioquimica e Biologia Molecular at UFSM that contributed to the development of this research. This research was also partially supported by Financiadora de Estudos e Projetos (FINEP, grant number 0112.0113).
Funding
Not applicable.
Author information
Authors and Affiliations
Contributions
Conceptualization: BMB; SAB. Methodology: BMB; ESP; DIBP; JFC; SAB. Formal analysis and investigation: BMB; GFG; DIBP; SC; APMV; FQM; SAB. Writing—original draft preparation: BMB; SAB. Writing—review and editing: BMB; ESP; DIBP; SC; APMV; FQM; GFG; LAS; JFC; SAB. Funding acquisition: SAB. Resources: FQM; JFC; SAB. Supervision: SAB.
Corresponding author
Ethics declarations
Conflict of interest
Authors declare no conflicts of interest.
Ethical approval
Not applicable.
Additional information
Communicated by Erko Stackebrandt.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Barasuol, B.M., Cargnelutti, J.F., Sangioni, L.A. et al. Characterization of novel of temperate phages of Staphylococcus aureus isolated from bovine milk. Arch Microbiol 204, 680 (2022). https://doi.org/10.1007/s00203-022-03296-9
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00203-022-03296-9