Abstract
Streptococcus salivarius has an exclusive and intimate association with humans. We are its sole natural host, and its contribution to the relationship appears overwhelmingly benevolent. Beautifully adapted to its preferred habitat, the human tongue, it only rarely ventures far from this location in the healthy host and indeed appears ill-equipped to become invasive due to a scarcity of virulence attributes. We consider that its strategically advantageous lingual location and numerical predominance allow S. salivarius to carry out a population surveillance and modulation role within the oral microbiota. Some strains are armed with complex arrays of targeted antibiotic weaponry, much of which belongs to the lantibiotic class of bacteriocins and a key to their ability to assemble and utilize this armament is their possession of transmissible multi-bacteriocin-encoding megaplasmid DNA. This review traces the origins of research into S. salivarius bacteriocins and bacteriocin-like inhibitory substances, showcases some of the inhibitory activities that we currently have knowledge of, and speculates about potential directions for ongoing investigation and probiotic application of this previously under-rated human commensal.
Similar content being viewed by others
References
Andrews S (1997). Investigation of factors influencing the implantation of Streptococcus salivarius strain Min5 onto the human tongue. Department of Microbiology. Dunedin, University of Otago. BMedSci: 87
Asaduzzaman SM, Nagao J et al (2009) Nukacin ISK-1, a bacteriostatic lantibiotic. Antimicrob Agents Chemother 53(8):3595–3598
Balakrishnan M, Simmonds RS et al (2001) Diverse activity spectra of bacteriocin-like inhibitory substances having activity against mutans streptococci. Caries Res 35(1):75–80
Bishop CJ, Aanensen DM et al (2009) Assigning strains to bacterial species via the internet. BMC Biol 7:3
Bisno AL (1991) Group A streptococcal infections and acute rheumatic fever. N Engl J Med 325(11):783–793
Bouwer A (2006) Activation of natural killer cells by dendritic cells stimulated by gram-positive bacterial cell wall components. Department of Microbiology and Immunology. Dunedin, University of Otago. BSc (Hons): 41
Burton JP, Chilcott CN et al (2006) A preliminary study of the effect of probiotic Streptococcus salivarius K12 on oral malodour parameters. J Appl Microbiol 100(4):754–764
Burton JP, Wescombe PA et al (2006) Safety assessment of the oral cavity probiotic Streptococcus salivarius K12. Appl Environ Microbiol 72(4):3050–3053
Carapetis, J. R. (2004) Group A streptococcal vaccine development: current status and issues of relevance to less developed countries. WHO/FCH/CAH/05.09. Geneva:World Health Organization. Volume, DOI:
Carapetis JR (2007) Rheumatic heart disease in developing countries. N Engl J Med 357(5):439–441
Carapetis JR, Steer AC et al (2005) The global burden of group A streptococcal diseases. Lancet Infect Dis 5(11):685–694
Carlsson J, Grahnen H et al (1970) Early establishment of Streptococcus salivarius in the mouths of infants. J Dent Res 49:415–418
Chilcott CN, Crowley L et al (2005) Elevated levels of interferon gamma in human saliva following ingestion of Streptococcus salivarius K12. Joint meeting of New Zealand Microbiological Society and New Zealand Biochemistry and Molecular Biology, Dunedin
Chilcott CN and Tagg JR (2007) Antimicrobial composition. Patent. USA
Cosseau C, Devine DA et al (2008) The commensal Streptococcus salivarius K12 downregulates the innate immune responses of human epithelial cells and promotes host-microbe homeostasis. Infect Immun 76(9):4163–4175
Dale JB (2008) Current status of group A streptococcal vaccine development. Adv Exp Med Biol 609:53–63
Delorme C, Poyart C et al (2007) Extent of horizontal gene transfer in evolution of Streptococci of the salivarius group. J Bacteriol 189(4):1330–1341
Dempster RP, Tagg JR (1982) “The production of bacteriocin-like substances by the oral bacterium Streptococcus salivarius. Arch Oral Biol 27(2):151–157
Dierksen KP, Moore CJ et al (2007) “The effect of ingestion of milk supplemented with salivaricin A-producing Streptococcus salivarius on the bacteriocin-like inhibitory activity of streptococcal populations on the tongue. FEMS Microbiol Ecol 59(3):584–591
Dierksen KP and Tagg J (2000) The influence of indigenous bacteriocin-producing Streptococcus salivarius on the acquisition of Streptococcus pyogenes by primary school children in Dunedin, New Zealand. Streptococci and streptococcal diseases entering the new millennium. DR Martin and TJ Auckland, Securacopy: 81–85
Dodd SJ (1999) A saliva model to demonstrate Streptococcus salivarius BLIS production and characterisation of salivaricin MPS. University of Otago, Dunedin
Favier CF, Vaughan EE et al (2002) Molecular monitoring of succession of bacterial communities in human neonates. Appl Environ Microbiol 68(1):219–226
Georgalaki MD, Van Den Berghe E et al (2002) Macedocin, a food-grade lantibiotic produced by Streptococcus macedonicus ACA-DC 198. Appl Environ Microbiol 68(12):5891–5903
Hyink O, Wescombe PA et al (2007) Salivaricin A2 and the novel lantibiotic salivaricin B are encoded at adjacent loci on a 190-kilobase transmissible megaplasmid in the oral probiotic strain Streptococcus salivarius K12. Appl Environ Microbiol 73(4):1107–1113
Hynes WL, Friend VL et al (1994) Duplication of the lantibiotic structural gene in M-type 49 group A streptococcus strains producing streptococcin A-M49. Appl Environ Microbiol 60(11):4207–4209
Hynes WL, Tagg JR (1984) Bacteriocin-like activity of an M-type 25 group A Streptococcus. Proc Univ Otago Med Sch 62:109–110
Hynes WL, Tagg JR (1985) Production of broad-spectrum bacteriocin-like activity by group A streptococci of particular M-types. Zentralbl Bakteriol Mikrobiol Hyg [A] 259(2):155–164
Ivanova I, Miteva V et al (1998) Characterization of a bacteriocin produced by Streptococcus thermophilus 81. Int J Food Microbiol 42(3):147–158
Johnson DW, Tagg JR et al (1979) Production of a bacteriocin-like substance by group-A streptococci of M-type 4 and T-pattern 4. J Med Microbiol 12(4):413–427
Karaya K, Shimizu T et al (2001) New gene cluster for lantibiotic streptin possibly involved in streptolysin S formation. J Biochem (Tokyo) 129(5):769–775
Kazor CE, Mitchell PM et al (2003) Diversity of bacterial populations on the tongue dorsa of patients with halitosis and healthy patients. J Clin Microbiol 41(2):558–563
Kennedy KL (1995) Saliva-dependent autoinhibitory activity of Streptococcus salivarius strain 6. Department of Microbiology. Dunedin, University of Otago. BSc (Hons): 43
Lennon D (2004) Acute rheumatic fever in children: recognition and treatment. Paediatr Drugs 6(6):363–373
Lester H (2006) The relationship between β-haemolysis and bacteriocin-like inhibitory substance (BLIS) production of Streptococcus salivarius. Department of Microbiology. Dunedin, University of Otago. BSc (Hons): 43
Lewus CB, Sun S et al (1992) Production of an amylase-sensitive bacteriocin by an atypical Leuconostoc paramesenteroides strain. Appl Environ Microbiol 58(1):143–149
Liljemark WF, Gibbons RJ (1973) Suppression of Candida albicans by human oral streptococci in gnotobiotic mice. Infect Immun 8(5):846–849
Loesche WJ, Kazor C (2002) Microbiology and treatment of halitosis. Periodontol 28:256–279
MacFarlane TW (1984) The oral ecology of patients with severe Sjogren’s syndrome. Microbios 41(160):99–106
Papadelli M, Karsioti A et al (2007) Characterization of the gene cluster involved in the biosynthesis of macedocin, the lantibiotic produced by Streptococcus macedonicus. FEMS Microbiol Lett 272(1):75–82
Phelps HA, Neely MN (2007) SalY of the Streptococcus pyogenes lantibiotic locus is required for full virulence and intracellular survival in macrophages. Infect Immun 75(9):4541–4551
Power DA, Burton JP et al (2008) Preliminary investigations of the colonisation of upper respiratory tract tissues of infants using a paediatric formulation of the oral probiotic Streptococcus salivarius K12. Eur J Clin Microbiol Infect Dis 27(12):1261–1263
Robson CL, Wescombe PA et al (2007) Isolation and partial characterization of the Streptococcus mutans type AII lantibiotic mutacin K8. Microbiology 153(Pt 5):1631–1641
Ross KF, Ronson CW et al (1993) Isolation and characterization of the lantibiotic salivaricin A and its structural gene salA from Streptococcus salivarius 20P3. Appl Environ Microbiol 59(7):2014–2021
Russell C, Tagg JR (1981) Role of bacteriocin during plaque formation by Streptococcus salivarius and Streptococcus sanguis on a tooth in an artificial mouth. J Appl Bacteriol 50(2):305–313
Sanders CC, Sanders WE (1982) Enocin: an antibiotic produced by Streptococcus salivarius that may contribute to protection against infections due to Group A Streptococci. J Infect Dis 146:683–690
Simpson WJ, Ragland NL et al (1995) A lantibiotic gene family widely distributed in Streptococcus salivarius and Streptococcus pyogenes. Dev Biol Stand 85:639–643
Tagg JR (1991) Studies of “BLIS-ful” oral bacteria. N Z Dent J 87(387):14–16
Tagg JR, Bannister LV (1979) “Fingerprinting” beta-haemolytic streptococci by their production of and sensitivity to bacteriocin-like inhibitors. J Med Microbiol 12(4):397–411
Tagg JR, Pybus V et al (1983) Application of inhibitor typing in a study of the transmission and retention in the human mouth of the bacterium Streptococcus salivarius. Arch Oral Biol 28(10):911–915
Tagg JR, Ragland NL et al (1990) A longitudinal study of Lancefield group A streptococcus acquisitions by a group of young Dunedin schoolchildren. N Z Med J 103(897):429–431
Tagg JR, Russell C (1981) Bacteriocin production by Streptococcus salivarius strain P. Can J Microbiol 27(9):918–923
Tompkins GR, Tagg JR (1987) Bacteriocin-like inhibitory activity associated with beta-hemolytic strains of Streptococcus salivarius. J Dent Res 66(8):1321–1325
Tompkins GR, Tagg JR (1989) The ecology of bacteriocin-producing strains of Streptococcus salivarius. Microb Ecol Health Dis 2:19–28
Upton M, Tagg JR et al (2001) Intra- and interspecies signaling between Streptococcus salivarius and Streptococcus pyogenes mediated by SalA and SalA1 lantibiotic peptides. J Bacteriol 183(13):3931–3938
Walls T, Power D et al (2003) Bacteriocin-like inhibitory substance (BLIS) production by the normal flora of the nasopharynx: potential to protect against otitis media? J Med Microbiol 52(Pt 9):829–833
Wang Y (2007) Purification and characterisation of novel bacteriocin salivaricin MPS. Department of Biochemistry. Dunedin, University of Otago. PGDipSci: 39
Wescombe PA (2002) Characterisation of lantibiotics produced by Streptococcus salivarius and Streptococcus pyogenes. Department of Microbiology and Immunology. Dunedin, University of Otago: 324
Wescombe PA, Burton JP et al (2006) Megaplasmids encode differing combinations of lantibiotics in Streptococcus salivarius. Antonie Van Leeuwenhoek 90(3):269–280
Wescombe PA, Tagg JR (2003) Purification and characterization of streptin, a type A1 lantibiotic produced by Streptococcus pyogenes. Appl Environ Microbiol 69(5):2737–2747
Wescombe PA, Upton M et al (2006) Production of the lantibiotic salivaricin A and its variants by oral streptococci and use of a specific induction assay to detect their presence in human saliva. Appl Environ Microbiol 72(2):1459–1466
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wescombe, P.A., Heng, N.C.K., Burton, J.P. et al. Something Old and Something New: An Update on the Amazing Repertoire of Bacteriocins Produced by Streptococcus salivarius . Probiotics & Antimicro. Prot. 2, 37–45 (2010). https://doi.org/10.1007/s12602-009-9026-7
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12602-009-9026-7