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Mapping the Proteome of Streptococcus Gordonii

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Mapping the Proteome of Streptococcus Gordonii CHAPTER 1 CHAPTER 1. INTRODUCTION 1.1. THE ROLE OF STREPTOCOCCUS GORDONII IN HEALTH AND DISEASE Dental plaque consists of a diverse community of microorganisms including bacteria, fungi and protozoa (Burne, 1998; Chandra et al., 2001; Lyons et al., 1983; Webb et al., 1995). In these biofilm communities different microorganisms co-adhere to one another within a polysaccharide matrix (Kolenbrander, 1993), and cooperate in degrading and utilizing host and dietary nutrients such as glycoproteins (Bradshaw et al., 1994). Studies of oral ecology have led to an appreciation of the complexity of the interactions that oral microorganisms have with the host both in health and disease (Bowden and Li, 1997; Quirynen and Bollen, 1995; Rose, 2000). Despite this, diseases such as dental caries and periodontal diseases are still worldwide human aliments resulting in a high level of morbidity and economic burden to society. Proteomics offers a novel approach to understanding the holistic changes occurring to oral microorganisms as environmental changes impinge on their habitats. Streptococcus gordonii was originally classified among the taxonomically diverse species Streptococcus sanguis2 until its description as a new species in 1989 (Kilian et al., 1989). S. gordonii cells are Gram-positive cocci that grow in short chains in serum broth. They are nonmotile, aerobic and faculatively anaerobic, fermentative, catalase negative, show α-hemolysis on horse blood agar and pronounced greening on chocolate agar. The cell wall contains glycerol teichoic acid and rhamnose, and the peptidoglycan type is Lys-Ala1-3. The guanine-plus-cytosine 2 The currently accepted nomenclature of S. sanguis is “S. sanguinis”, and of S. parasanguis is “S. parasanguinis”. However, a compelling argument has been made for the conservation of the original names (Kilian, 2001). Kilian stated that “The changing of well established names of species of Streptococcus and other genera is not desirable as it will cause unnecessary confusion and frustration for those who use these names in their daily work”. In order to avoid confusion, throughout this thesis, the name stated for Streptococcus species is that used in the associated literature. 1 CHAPTER 1 (G + C) content of the DNA is 40 to 43 mol%. S. gordonii is differentiated from S. sanguis by several biochemical characteristics, including a lack of an IgA1 protease, and by a significantly different G + C content (Kilian et al., 1989). S. gordonii is one of the viridans group streptococci (VS), which are part of the normal microbial flora in dental plaque (Whiley and Beighton, 1998). Viridis is Latin for green, and viridans refers to the green colour of the halo that surrounds α-haemolytic streptococci on chocolate agar, which is thought to comprise the metabolic degradation products of haem. While most VS are commensals, an exception is Streptococcus mutans, which is associated with dental caries (Bowden, 1997). Although most are not considered pathogens in the oral cavity, many VS species are associated with infective endocarditis (Douglas et al., 1993). In a study examining the identities of 47 strains of oral streptococci collected from 42 confirmed cases of infective endocarditis, the most common species identified were S. sanguis sensu stricto (31.9%), Streptococcus oralis (29.8%) and S. gordonii (12.7%). Other related species including Streptococcus mitis and Streptococcus parasanguis were less commonly isolated (Douglas et al., 1993). As environmental factors change, organisms either adapt or perish. In the oral cavity, early colonizing Gram-positive bacteria, such as S. gordonii, form biofilms on tooth surfaces and ferment carbohydrate efficiently at pH levels above 6.0 (Loo et al., 2000) and produce antibacterial factors that prevent the overgrowth of dental pathogens such as S. mutans (van der Hoeven and Schaeken, 1995). The initiation of oral biofilms on tooth surfaces by bacteria, such as S. gordonii, depends on the differential expression of genes in response to unique environmental clues. For example, one study observed the involvement of the adc operon and manganese homeostasis in the formation of S. gordonii biofilms (Loo et al., 2003). The conclusion drawn from this study was that AdcR could be a regulator at high levels of extracellular manganese, which is usually found at low levels in its natural and opportunistic habitats, and that the adc operon is not only involved in manganese acquisition and manganese homeostasis in S. gordonii, but appears to modulate sessile growth in this bacterium (Loo et al., 2003). This illustrates how changes in environment can cause a developmental change in a bacterium. 2 CHAPTER 1 If the pH of dental plaque drops below pH 6.0, the environment becomes unfavourable, S. gordonii is unable to metabolise efficiently, and aciduric pathogens begin to proliferate and predominate in the oral biofilm, further lowering the pH. However, under certain conditions, including some dental procedures, S. gordonii along with other VS may enter the bloodstream. In the bloodstream the environmental pH is slightly higher (pH 7.3) than the slightly acidic value in dental plaque (pH 6.5). Both the growth rate and the production of extracellular protein of S. gordonii increase as pH increases (Knox et al., 1985). During the resulting transient bacteremia (Vriesema et al., 2000) it is possible to kill the planktonic organisms using antimicrobial treatments while the bacteria are still in the bloodstream (Donlan and Costerton, 2002). However, should a biofilm form, such as that in an infective endocarditis lesion, the condition becomes difficult to treat due to the mass transfer limitations and the inherent resistance of biofilm microorganisms to antibiotic treatment (Donlan and Costerton, 2002; Giebink et al., 1982). In infective endocarditis, the VS adhere to a cardiac vegetation, which is a meshwork of platelets and fibrin present at the site of the endocardial lesions (Durack and Beeson, 1972). A number of surface components such as the fimbrial protein, FimA, of S. parasanguis (Burnette-Curley et al., 1995; Viscount et al., 1997) and the extracellular polysaccharides of various VS species (Dall and Herndon, 1990; Ramirez-Ronda, 1978; Scheld et al., 1978), have been implicated in the adherence of these bacteria to cardiac vegetations. The fibrin in these vegetations is converted from fibrinogen in blood by the enzyme thrombin. Interestingly, thrombin-like activity produced by S. sanguis has been shown to be a potential virulence factor for infective endocarditis (Mayo et al., 1995). Furthermore, this activity is 5-fold higher at pH 7.5 than at pH 5.5, implicating a change in pH following bacteraemia from dental plaque as a trigger for the infectious process (Mayo et al., 1995). 1.2. BIOFILMS AND QUORUM SENSING Biofilms are formed in diverse environments, from surfboard wax in a marine environment (Dalton et al., 1994), to tooth surfaces in the human mouth (Marsh and 3 CHAPTER 1 Bradshaw, 1997). Researchers have estimated that 99% of all bacteria in natural environments exist in biofilms (Costerton et al., 1987). Bacteria in biofilms optimise population survival by differentiation into forms suitable for particular conditions and organising themselves into communal groups exhibiting characteristics not shown by individual planktonic cells (Costerton et al., 1999; Lawrence et al., 1991). In these communities bacterial populations coordinate their activities by quorum sensing. This is accomplished by secreting small diffusible signal molecules (autoinducers), thus allowing a single cell to obtain information about the status of other bacteria from the same (Batchelor et al., 1997; Davies et al., 1998) or even different species (Møller et al., 1998). Autoinduction is commonly activated when the autoinducer reaches a critical density, leading to a fast, population-wide response, and, as such, is believed to be a sensor of population density (Fuqua et al., 1996). 1.2.1. Biofilms and human health Biofilms have an innate resistance to antibiotics (Donlan and Costerton, 2002; Mah et al., 2003; Stewart, 2002), and present problems of significant economic importance in industry, health and agriculture. Biofilms are often associated with human disease accounting for approximately 60% of human infections and virtually all, chronic, recurrent and implanted device associated infections (Centers for Disease, Control and Prevention, 2000; http://www.cdc.gov/). Cystic fibrosis, native valve endocarditis, otitis media, periodontitis, and chronic prostatitis are all caused by biofilm-associated microorganisms (Donlan, 2002). Biofilms colonize medical devices such as prosthetic heart valves, central venous catheters, urinary catheters, contact lenses, intrauterine devices, and dental unit water lines (Donlan and Costerton, 2002). Medical ventilation systems also support biofilms and fragments of these biofilms can readily detach and colonise the lungs (Costerton et al., 2003). 4 CHAPTER 1 1.2.2. The formation of oral biofilms Previous studies in oral ecology have led to an understanding of many of the mechanisms by which biofilms form on teeth (Bowden and Hamilton, 1987; Quirynen and Bollen, 1995; Rose, 2000), but dental caries and periodontal disease are still widespread human aliments (Hobdell et al., 2003). Researchers are still investigating possible solutions using antiseptics, antibiotics, adhesion agonists, recombinant antibodies and vaccines (Dutton et al., 2000; Hanada, 2000; Jenkinson et al., 1997).
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