Occurrence of virulence-associated genes in Streptococcus uberis and Streptococcus parauberis isolated from bovine mastitis


Zouharova M, Nedbalcova K, Slama P, Bzdil J, Masarikova M, Matiasovic J (2022): Occurrence of virulence-associated genes in Streptococcus uberis and Streptococcus parauberis isolated from bovine mastitis. Vet Med-Czech 67, 123–130.

download PDF

Streptococcus uberis is one of the most important mastitis-causing pathogens. Although the pathogenesis and virulence factors required for the intramammary infection development are not yet well established, several putative virulence-associated genes have been described. This work aimed to investigate the presence of ten known and putative virulence-associated genes in S. uberis isolated from subclinical or clinical mastitis and its closely related species Streptococcus parauberis in 135 dairy farms in the Czech Republic. The PCR analysis detected that all the examined isolates possessed at least four virulence genes and most isolates carried eight out of ten virulence genes. All S. uberis isolates were positive for the oppF, gapC and sua genes. Among the most prevalent virulence-associated genes skc (98%) and pauA (97%) were also found. The hasA and hasB genes were always present together in 94% of the isolates. The genes cfu and lbp were detected in 6% and 2%, respectively. In the S. uberis isolates, 14 different virulence gene profiles were observed. The most frequent profile was hasA+ hasB+ sua+ skc+ pauA+ gapC+ oppF with variable hasC, observed in 86% of the tested isolates, occurring in 127 out of 135 farms. S. parauberis was identified very sporadically and, although it is closely related to S. uberis, only a rare occurrence of the examined virulence-associated genes was found.

Almeida RA, Luther DA, Patel D, Oliver SP. Predicted antigenic regions of Streptococcus uberis adhesion molecule (SUAM) are involved in adherence to and internalization into mammary epithelial cells. Vet Microbiol. 2011 Mar 24;148(2-4):323-8. https://doi.org/10.1016/j.vetmic.2010.09.017
Almeida RA, Kerro-Dego O, Prado ME, Headrick SI, Lewis MJ, Siebert LJ, Pighetti GM, Oliver SP. Protective effect of anti-SUAM antibodies on Streptococcus uberis mastitis. Vet Res. 2015 Nov;46:133. https://doi.org/10.1186/s13567-015-0271-3
Bentley RW, Leigh JA, Collins MD. Development and use of species-specific oligonucleotide probes for differentiation of Streptococcus uberis and Streptococcus parauberis. J Clin Microbiol. 1993 Jan;31(1):57-60. https://doi.org/10.1128/jcm.31.1.57-60.1993
Boonyayatra S, Tharavichitkul P, Oliver SP. Virulence-associated genes and molecular typing of Streptococcus uberis associated with bovine mastitis in northern Thailand. Turk J Vet Anim Sci. 2018 Nov;42(1):73-81. https://doi.org/10.3906/vet-1704-75
Bradley AJ, Leach KA, Breen JE, Green LE, Green MJ. Survey of the incidence and aetiology of mastitis on dairy farms in England and Wales. Vet Rec. 2007 Feb 24;160(8):253-7. https://doi.org/10.1136/vr.160.8.253
Davies PL, Leigh JA, Bradley AJ, Archer SC, Emes RD, Green MJ. Molecular epidemiology of Streptococcus uberis clinical mastitis in dairy herds: Strain heterogeneity and transmission. J Clin Microbiol. 2016 Jan;54(1):68-74. https://doi.org/10.1128/JCM.01583-15
Field TR, Ward PN, Pedersen LH, Leigh JA. The hyaluronic acid capsule of Streptococcus uberis is not required for the development of infection and clinical mastitis. Infect Immun. 2003 Jan;71(1):132-9. https://doi.org/10.1128/IAI.71.1.132-139.2003
Fontaine MC, Perez-Casal J, Song XM, Shelford J, Willson PJ, Potter AA. Immunisation of dairy cattle with recombinant Streptococcus uberis GapC or a chimeric CAMP antigen confers protection against heterologous bacterial challenge. Vaccine. 2002 May 22;20(17-18):2278-86. https://doi.org/10.1016/S0264-410X(02)00114-7
Hassan AA, Khan IU, Abdulmawjood A, Lammler C. Evaluation of PCR methods for rapid identification and differentiation of Streptococcus uberis and Streptococcus parauberis. J Clin Microbiol. 2001 Apr;39(4):1618-21. https://doi.org/10.1128/JCM.39.4.1618-1621.2001
Jayarao BM, Dore JJ Jr, Baumbach GA, Matthews KR, Oliver SP. Differentiation of Streptococcus uberis from Streptococcus parauberis by polymerase chain reaction and restriction fragment length polymorphism analysis of 16S ribosomal DNA. J Clin Microbiol. 1991 Dec;29(12):2774-8. https://doi.org/10.1128/jcm.29.12.2774-2778.1991
Jiang M, Babiuk LA, Potter AA. Cloning, sequencing and expression of the CAMP factor gene of Streptococcus uberis. Microb Pathog. 1996 May;20(5):297-307. https://doi.org/10.1006/mpat.1996.0028
Johnsen LB, Poulsen K, Kilian M, Petersen TE. Purification and cloning of a streptokinase from Streptococcus uberis. Infect Immun. 1999 Mar;67(3):1072-8. https://doi.org/10.1128/IAI.67.3.1072-1078.1999
Kaczorek E, Malaczewska J, Wojcik R, Siwicki AK. Biofilm production and other virulence factors in Streptococcus spp. isolated from clinical cases of bovine mastitis in Poland. BMC Vet Res. 2017 Dec;13(1):398. https://doi.org/10.1186/s12917-017-1322-y
Khan IU, Hassan AA, Abdulmawjood A, Lammler C, Wolter W, Zschock M. Identification and epidemiological characterization of Streptococcus uberis isolated from bovine mastitis using conventional and molecular methods. J Vet Sci. 2003 Dec;4(3):213-24. Erratum in: J Vet Sci. 2004 Mar;5(1):85. https://doi.org/10.4142/jvs.2003.4.3.213
Kromker V, Reinecke F, Paduch JH, Grabowski N. Bovine Streptococcus uberis intramammary infections and mastitis. Clin Microbial. 2014 Jun;3(4):157. https://doi.org/10.4172/2327-5073.1000157
Leigh JA. Activation of bovine plasminogen by Streptococcus uberis. FEMS Microbiol Lett. 1993 Nov 15;114(1):67-71. https://doi.org/10.1111/j.1574-6968.1993.tb06552.x
McVey DS, Shi J, Leigh JA, Rosey EL, Ward PN, Field TR, Yancey RJ. Identification of multiple linear epitopes of the plasminogen activator A (PauA) of Streptococcus uberis with murine monoclonal antibodies. Vet Immunol Immunopathol. 2005 Apr 8;104(3-4):155-62. https://doi.org/10.1016/j.vetimm.2004.11.005
Moshynskyy I, Jiang M, Fontaine MC, Perez-Casal J, Babiuk LA, Potter AA. Characterization of a bovine lactoferrin binding protein of Streptococcus uberis. Microb Pathog. 2003 Nov;35(5):203-15. https://doi.org/10.1016/S0882-4010(03)00150-5
Pancholi V, Fischetti VA. A major surface protein on group A streptococci is a glyceraldehyde-3-phosphate-dehydrogenase with multiple binding activity. J Exp Med. 1992 Aug 1;176(2):415-26. https://doi.org/10.1084/jem.176.2.415
Pancholi V, Fischetti VA. Glyceraldehyde-3-phosphate dehydrogenase on the surface of group A streptococci is also an ADP-ribosylating enzyme. Proc Natl Acad Sci U S A. 1993 Sep;90(17):8154-8. https://doi.org/10.1073/pnas.90.17.8154
Perrig MS, Ambroggio MB, Buzzola FR, Marcipar IS, Calvinho LF, Veaute CM, Barbagelata MS. Genotyping and study of the pauA and sua genes of Streptococcus uberis isolates from bovine mastitis. Rev Argent Microbiol. 2015 Oct-Dec;47(4):282-94. https://doi.org/10.1016/j.ram.2015.06.007
Phuektes P, Mansell PD, Dyson RS, Hooper ND, Dick JS, Browning GF. Molecular epidemiology of Streptococcus uberis isolates from dairy cows with mastitis. J Clin Microbiol. 2001 Apr;39(4):1460-6. https://doi.org/10.1128/JCM.39.4.1460-1466.2001
Pitkala A, Koort J, Bjorkroth J. Identification and antimicrobial resistance of Streptococcus uberis and Streptococcus parauberis isolated from bovine milk samples. J Dairy Sci. 2008 Oct;91(10):4075-81. https://doi.org/10.3168/jds.2008-1040
Reinoso EB, Lasagno MC, Dieser SA, Odierno LM. Distribution of virulence-associated genes in Streptococcus uberis isolated from bovine mastitis. FEMS Microbiol Lett. 2011 May;318(2):183-8. https://doi.org/10.1111/j.1574-6968.2011.02258.x
Rosey EL, Lincoln RA, Ward PN, Yancey RJ Jr, Leigh JA. PauA: A novel plasminogen activator from Streptococcus uberis. FEMS Microbiol Lett. 1999 Sep 1;178(1):27-33. Erratum in: FEMS Microbiol Lett 1999 Nov 15;180(2):353. https://doi.org/10.1016/S0378-1097(99)00464-4
Smith AJ, Kitt AJ, Ward PN, Leigh JA. Isolation and characterization of a mutant strain of Streptococcus uberis, which fails to utilize a plasmin derived beta-casein peptide for the acquisition of methionine. J Appl Microbiol. 2002 Sep;93(4):631-9. https://doi.org/10.1046/j.1365-2672.2002.01723.x
Tassi R, Mcneilly TN, Fitzpatrick JL, Fontaine MC, Reddick D, Ramage C. Strain-specific pathogenicity of putative host-adapted and nonadapted strains of Streptococcus uberis in dairy cattle. J Dairy Sci. 2013 Aug;96(8):5129-45. https://doi.org/10.3168/jds.2013-6741
Vezina B, Al-Harbi H, Ramay HR, Soust M, Moore RJ, Olchowy TWJ, Alawneh JI. Sequence characterisation and novel insights into bovine mastitis-associated Streptococcus uberis in dairy herds. Sci Rep. 2021 Feb 4;11(1):3046. https://doi.org/10.1038/s41598-021-82357-3
Ward PN, Field TR, Ditcham WG, Maguin E, Leigh JA. Identification and disruption of two discrete loci encoding hyaluronic acid capsule biosynthesis genes hasA, hasB, and hasC in Streptococcus uberis. Infect Immun. 2001 Jan;69(1):392-9. https://doi.org/10.1128/IAI.69.1.392-399.2001
Ward PN, Holden MT, Leigh JA, Lennard N, Bignell A, Barron A, Clark L, Quail MA, Woodward J, Barrell BG, Egan SA, Field TR, Maskell D, Kehoe M, Dowson CG, Chanter N, Whatmore AM, Bentley SD, Parkhill J. Evidence for niche adaptation in the genome of the bovine pathogen Streptococcus uberis. BMC Genomics. 2009 Jan 28;10(1):1-17. https://doi.org/10.1186/1471-2164-10-54
Zadoks RN, Schukken YH, Wiedmann M. Multilocus sequence typing of Streptococcus uberis provides sensitive and epidemiologically relevant subtype information and reveals positive selection in the virulence gene pauA. J Clin Microbiol. 2005 May;43(5):2407-17. https://doi.org/10.1128/JCM.43.5.2407-2417.2005
download PDF

© 2022 Czech Academy of Agricultural Sciences | Prohlášení o přístupnosti