Influence of a model human defensive peroxidase system on oral streptococcal antagonism

Abstract

Streptococcus is a dominant genus in the human oral cavity, making up about 20 % of the more than 800 species of bacteria that have been identified, and about 80 % of the early biofilm colonizers. Oral streptococci include both health-compatible (e.g. Streptococcus gordonii and Streptococcus sanguinis) and pathogenic strains (e.g. the cariogenic Streptococcus mutans). Because the streptococci have similar metabolic requirements, they have developed defence strategies that lead to antagonism (also known as bacterial interference). S. mutans expresses bacteriocins that are cytotoxic toward S. gordonii and S. sanguinis, whereas S. gordonii and S. sanguinis differentially produce H 2 O 2 (under aerobic growth conditions), which is relatively toxic toward S. mutans. Superimposed on the inter-bacterial combat are the effects of the host defensive mechanisms. We report here on the multifarious effects of bovine lactoperoxidase (bLPO) on the antagonism between S. gordonii and S. sanguinis versus S. mutans. Some of the effects are apparently counterproductive with respect to maintaining a health-compatible population of streptococci. For example, the bLPO system (comprised of bLPO+SCN " +H 2 O 2 ) destroys H 2 O 2 , thereby abolishing the ability of S. gordonii and S. sanguinis to inhibit the growth of S. mutans. Furthermore, bLPO protein (with or without its substrate) inhibits bacterial growth in a biofilm assay, but sucrose negates the inhibitory effects of the bLPO protein, thereby facilitating adherence of S. mutans in lieu of S. gordonii and S. sanguinis. Our findings may be relevant to environmental pressures that select early supragingival colonizers. INTRODUCTIONThe term 'microbial ecosystem' has been defined as an organization of micro-organisms that live in a particular niche, while subject to the environmental pressures of the niche (Raes & Bork, 2008). These pressures may be biotic (e.g. self, other microbial species, plants and animals) and abiotic (e.g. temperature, pH, nutrients, etc.) in origin. Dental plaques are examples of dynamic and exceedingly complex microbial ecosystems that are thought to comprise at least 800 bacterial species (Kroes et al., 1999;Paster et al., 2006;Aas et al., 2005Aas et al., , 2008Preza et al., 2008;Becker et al., 2002;Paster et al., 2001;Dethlefsen et al., 2007). Many of the environmental factors that influence the speciation of oral biofilms have been reviewed in other articles (Marsh, 2005;Overman, 2000;Rosan & Lamont, 2000;Sissons, 1997;Socransky & Haffajee, 2005;ten Cate, 2006), including the effects of pH (Burne & Marquis, 2000), nutrients (Sissons et al., 2007), fluoride (Bowden, 1990) and various antimicrobials (Dashper et al., 2007;Fine et al., 2001;Leung et al., 2005;Yang et al., 2006;Zaura-Arite et al., 2001). The effects of the host immune system on oral biofilms are less well understood. This paper focuses on the influence of defensive peroxidases on interstreptococcal interactions.There are two host-derived defensive peroxidases in the human oral cavity, salivar...

Genomic Island TnSmu2 of Streptococcus mutans Harbors a Nonribosomal Peptide Synthetase-Polyketide Synthase Gene Cluster Responsible for the Biosynthesis of Pigments Involved in Oxygen and H 2 O 2 Tolerance

“…In addition, the supragingival plaque is bathed in saliva, which contains H 2 O 2 produced by salivary enzymes and innate immune cells (4). Likewise, the pioneer colonizers, such as the mitis group streptococci, produce copious amounts of H 2 O 2 as a defense mechanism to ward off competitors (4,22,23 (26), and its pyruvate formate-lyase is more sensitive to oxygen than that of S. sanguinis (37). Therefore, alternative strategies must be employed to cope with the oxygen and H 2 O 2 challenges imposed by the host and the competing species of mitis group streptococci.…”

Pt-Decorated MWCNTs–Ionic Liquid Composite-Based Hydrogen Peroxide Sensor To Study Microbial Metabolism Using Scanning Electrochemical Microscopy

“…In recent study Kreth et al, were unable to detect any H 2 O 2 produced by Sg in the presence of salivary LPO and thiocyanate (SCN‾). 22 Typically, these assays require the collection of an aliquot of samples at a certain time point and thus lack temporal and spatial resolution. This becomes more evident when attempting to measure H 2 O 2 close to the biofilm before it is decomposed by relevant H 2 O 2 -decomposing agents including salivary LPO and thiocyanate SCN ‒ .…”

Thiocyanate supplementation decreases atherosclerotic plaque in mice expressing human myeloperoxidase

“…A number of studies have reported beneficial effects, such in the oral cavity [12], in the lungs [13,14]) and in subjects who have suffered a myocardial infarction [15], whereas others have reported that exposure to HOSCN induces detrimental effects by, for example, increasing lipoprotein modification [16,17], damaging key cellular enzymes [18-20] and altering plasma thiol status [10]). It is well established that lactoperoxidase (LPO) and salivary peroxidase (SPO) use the high (millimolar) concentrations of SCN − present in milk, tears and saliva to produce HOSCN as an antibacterial defense (reviewed [21]).…”