Phosphorylating enzymes involved in glucose fermentation of Actinomyces naeslundii

Takahashi, Nobuhiro; Kalfas, Sotirios; Yamada, Tadashi

doi:10.1128/jb.177.20.5806-5811.1995

Cited by 30 publications

(42 citation statements)

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“…In contrast to streptococci, A. naeslundii has a unique glycolytic system in which the bacteria use phosphoryl donors instead of ATP for carbohydrate degradation (Takahashi et al, 1995). Actinomyces species can use lactate as a carbon source for growth (Takahashi & Yamada, 1996;van der Hoeven & van den Kieboom, 1990), whereby lactic acid is converted into weaker acids (Takahashi & Yamada, 1996).…”

Section: Discussionmentioning

confidence: 99%

“…Several culturebased studies indicated that Actinomyces species gain increased prominence at the expense of streptococci during maturation of the biofilm (Ritz, 1967; Socransky et al, 1977;Syed & Loesche, 1978;van Palenstein Helderman, 1981). Such population changes might reflect differences in growth rates (Nyvad & Kilian, 1987; Socransky et al, 1977) and/or differences in nutritional profiles of these genera (Takahashi et al, 1995;Takahashi & Yamada, 1996;van der Hoeven & van den Kieboom, 1990;Yaling et al, 2006). However, the spatial relationship of actinomycetes with other members of the dental biofilm microbiota was not disclosed by these culture-based studies.…”

Section: Introductionmentioning

confidence: 99%

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Actinomyces naeslundii in initial dental biofilm formation

et al. 2009

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The combined use of confocal laser scanning microscopy (CLSM) and fluorescent in situ hybridization (FISH) offers new opportunities for analysis of the spatial relationships and temporal changes of specific members of the microbiota of intact dental biofilms. The purpose of this study was to analyse the patterns of colonization and population dynamics of Actinomyces naeslundii compared to streptococci and other bacteria during the initial 48 h of biofilm formation in the oral cavity. Biofilms developed on standardized glass slabs mounted in intra-oral appliances worn by ten individuals for 6, 12, 24 and 48 h. The biofilms were subsequently labelled with probes against A. naeslundii (ACT476), streptococci (STR405) or all bacteria (EUB338), and were analysed by CLSM. Labelled bacteria were quantified by stereological tools. The results showed a notable increase in the number of streptococci and A. naeslundii over time, with a tendency towards a slower growth rate for A. naeslundii compared with streptococci. A. naeslundii was located mainly in the inner part of the multilayered biofilm, indicating that it is one of the species that attaches directly to the acquired pellicle. The participation of A. naeslundii in the initial stages of dental biofilm formation may have important ecological consequences. INTRODUCTIONDental biofilm is an archetypal example of a complex biofilm (Costerton et al., 1999;Davies, 2003;DuPont, 1997). Biofilm formation on tooth surfaces follows the same basic rules as biofilm formation elsewhere in nature. Dental biofilms develop readily because of the optimal temperature, the rich nutrient supply in the oral cavity, and the hard non-shedding surface. They are easily accessible for experimentation using intra-oral devices (Auschill et al., 2004;Kilian et al., 1979;Nyvad & Fejerskov, 1987a;Palmer et al., 2003), and therefore dental biofilms can be used to demonstrate colonization phenomena and ecological principles of universal interest. Concurrent with the increasing recognition of the significance of biofilms in infectious diseases, the development of techniques such as confocal laser scanning microscopy (CLSM), fluorescence in situ hybridization (FISH) and immunofluorescence has enabled visualization of bacteria in their natural undisturbed environment. This offers a substantial improvement upon previous microbiological studies of bacteria grown in planktonic settings (Anwar et al., 1992;Davies, 2003).Previous studies of dental biofilm that took advantage of these methods mainly focused on streptococci Dige et al., 2007; Hannig et al., 2007;Palmer et al., 2003) because culture-based studies suggested that this group of bacteria is prominent during the initial stages of biofilm formation on teeth (Li et al., 2004;Nyvad & Kilian, 1987. However, other genera such as Actinomyces are also among the earliest colonizers of dental surfaces and may constitute up to 27 % of the pioneer bacteria (Kilian et al., 1979;Li et al., 2004;Nyvad & Kilian, 1987). Several culturebased studies indicated that Ac...

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Actinomyces naeslundii in initial dental biofilm formation

et al. 2009

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“…Although these observations indicate that A. naeslundii cells could play a significant role in the initiation and progression of oral diseases, their carbohydrate metabolism, which provides the energy essential to their physiological activities, was not fully understood. Our recent studies (Takahashi et al, 1995) have revealed that strains of A. naeslundii have glycolytic enzymes different from those of Streptococcus, another predominant organism in plaque, and also the most intensively investigated bacterium, Escherichia coli. In addition, their metabolic properties can be modulated by several environmental factors in the oral ecosystem Takahashi et al, 1994).…”

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confidence: 99%

“…In addition, their metabolic properties can be modulated by several environmental factors in the oral ecosystem Takahashi et al, 1994). Therefore (Buchanan and Pine, 1967;Takahashi et al, 1995), which is widely distributed in saccharolytic bacteria. However, A. naeslundii cells operate this pathway in a manner different from that of the oral streptococci which comprise the other dominant part of the saccharolytic bacteria in dental plaque and whose glycolysis has been studied intensively (Yamada, 1987;Iwami, 1988 (Kulaev, 1979;Kulaev and Vagabov, 1983;Phillips et al, 1993).…”

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confidence: 99%

“…1, glucokinase; 2, PEP-glucose PTS; 3, phosphoglucose isomerase; 4, phosphofructokinase; 5, fructose-1,6-bisphosphate aldolase; 6, triosephosphate isomerase; 7, glyceraldehyde-phosphate dehydrogenase, 8, phosphoglycerate kinase; 9, phosphoglyceromutase; 10, enolase; 1 1, pyruvate kinase. (Based on ta from Takahashi and Yamada, 1992;Takahashi et al, 1994Takahashi et al, , 1995 and produce organic acids (Schaal, 1986). This characteristic, together with the capacity to accumulate glycogenlike intracellular polysaccharides (Komiyama et al, 1986), is considered to be related to the cariogenic potential of these bacteria.…”

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Glucose and Lactate Metabolism By Actinomyces Naeslundii

Takahashi

Yamada

1999

Critical Reviews in Oral Biology & Medicine

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Actinomyces are among the predominant bacteria in the oral microflora. This review discusses the glucose and lactate metabolism of Actinomyces naeslundii and its ecological significance in dental plaque. This bacterium has the EmbdenMeyerhof-Parnas (EMP) pathway as the main route to degrade glucose. The EMP pathway-derived metabolic intermediates, phosphoenolpyruvate (PEP) and pyruvate, are further converted into different end-products, depending on the environment. Under anaerobic conditions in the absence of bicarbonate, the pyruvate is converted into lactate by a lactate dehydrogenase. In the presence of bicarbonate, the PEP is combined with bicarbonate and then converted into succinate through the succinate pathway, while the pyruvate is converted into formate and acetate through the pyruvate formate-lyase pathway. Under aerobic conditions, the pyruvate liberates acetate and CO2 through a pathway initiated by a pyruvate dehydrogenase. A. naeslundii strains also degrade lactate, aerobically, to acetate and CO2 through the conversion of lactate into pyruvate by a NADindependent lactate dehydrogenase. These strains also synthesize glycogen from a glycolytic intermediate, glucose 6-phosphate. Besides atmospheric conditions and bicarbonate, the intracellular reduction-oxidation potential, carbohydrate concentration, and environmental pH also modulate the metabolism of A. naeslundii. Some of the phosphorylating enzymes involved in A. naeslundii metabolism-e.g., GTP/polyphosphate (PPn)-dependent glucokinase, pyrophosphate (PPi)-dependent phosphofructokinase, UDP-glucose pyrophosphorylase, and GDP/IDP-dependent PEP carboxykinase-are unique to A. naeslundii and have not been found in other oral bacteria. The utilization of PPn and PPi as phosphoryl donors, together with glycogen synthesis and lactate utilization, could contribute to the efficient energy metabolism found in A. naeslundii. Through this flexible and efficient metabolic capacity, A. naeslundii can adapt to fluctuating environments and compete with other bacteria in dental plaque. Further, this bacterium may modify the dental plaque environment and promote the microbial population shifts in dental plaque.

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Glucose metabolism in the antibiotic producing actinomycete Nonomuraea sp. ATCC 39727

Gunnarsson

Bruheim

Nielsen

2004

Biotech & Bioengineering

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The actinomycete Nonomuraea sp. ATCC 39727, producer of the glycopeptide A40926 that is used as precursor for the novel antibiotic dalbavancin, has an unusual carbon metabolism. Glucose is primarily metabolized via the Entner-Doudoroff (ED) pathway, although the energetically more favorable Embden-Meyerhof-Parnas (EMP) pathway is present in this organism. Moreover, Nonomuraea utilizes a PPi-dependent phosphofructokinase, an enzyme that has been connected with anaerobic metabolism in eukaryotes and higher plants, but recently has been recognized in several actinomycetes. In order to study its primary carbon metabolism in further detail, Nonomuraea was cultivated with [1-13C] glucose as the only carbon source and the 13C-labeling patterns of proteinogenic amino acids were determined by GC-MS analysis. Through this method, the fluxes in the central carbon metabolism during balanced growth were estimated. Moreover, a shift in the label incorporation pattern was observed in connection with phosphate limitation and increased antibiotic productivity in Nonomuraea. The shift indicated an increased flux through the EMP pathway at the expense of the flux through the ED pathway, a suggestion that was supported by alterations in intracellular metabolite levels during phosphate limitation. In contrast, expression levels of genes encoding enzymes in the ED and EMP pathways were not affected by phosphate limitation.

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Phosphorylating enzymes involved in glucose fermentation of Actinomyces naeslundii

Cited by 30 publications

References 53 publications

Actinomyces naeslundii in initial dental biofilm formation

Actinomyces naeslundii in initial dental biofilm formation

Glucose and Lactate Metabolism By Actinomyces Naeslundii

Glucose metabolism in the antibiotic producing actinomycete Nonomuraea sp. ATCC 39727

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