Oxygen dependent pyruvate oxidase expression and production in Streptococcus sanguinis

Zheng, Lan Yan; Itzek, Andreas; Chen, Zhi Yun; Kreth, Jens

doi:10.4248/ijos11030

Cited by 50 publications

(44 citation statements)

References 26 publications

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“…S. oligofermentans also encodes a Pox enzyme, but there is evidence to suggest that these enzymes may not work synergistically because of the way the genes are regulated (100). Notably, in S. gordonii and S. sanguinis , expression of spxB is sensitive to carbon catabolite repression (CCR) by preferred carbohydrates like glucose (104). Thus, it remains to be determined to what degree H 2 O 2 production by Pox and other enzyme systems is active under conditions that are conducive to the formation of caries, i.e.…”

Section: The Good Streptococci: Commensal Oral Floramentioning

confidence: 99%

Biology of Oral Streptococci

et al. 2018

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Summary Bacteria belonging to the genus Streptococcus are the first inhabitants of the oral cavity which can be acquired right after birth and thus play an important role in the assembly of the oral microbiota. In this chapter, we will discuss the different oral environments inhabited by streptococci and the species that occupy each niche. Special attention is given to the taxonomy of Streptococcus as this genus is now divided into 8 distinct groups where oral species are found in 6 of them. Oral streptococci produce an arsenal of adhesive molecules that allow them to efficiently colonize different tissues in the mouth. Also, they have a remarkable ability to metabolize carbohydrates via fermentation thereby generating acids as byproducts. Excessive acidification of the oral environment by aciduric species such as Streptococcus mutans is directly associated with the development of dental caries. However, less acid-tolerant species such as Streptococcus salivarius and Streptococcus gordonii produce large amounts of alkali displaying and important role in the acid-base physiology of the oral cavity. Another important characteristic of certain oral streptococci is their ability to generate hydrogen peroxide that can inhibit the growth of S. mutans. Thus, oral streptococci can also be beneficial to the host by producing molecules that are inhibitory to pathogenic species. Lastly, commensal and pathogenic streptococci residing in the oral cavity can eventually gain access to the bloodstream and cause systemic infections such as infective endocarditis.

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Section: The Good Streptococci: Commensal Oral Floramentioning

confidence: 99%

Biology of Oral Streptococci

et al. 2018

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“…The peroxigenic oral streptococci, including Streptococcus sanguinis, S. gordonii, and S. oligofermentans, are major competitors of S. mutans. These early colonizers of dental plaque generate bactericidal levels of H 2 O 2 through enzymes such as pyruvate oxidase and lactate oxidase (10)(11)(12)(13)(14). Both O 2 and H 2 O 2 promote the formation of more-damaging reactive oxygen species (ROS), such as the hydroxyl radical and the superoxide anion radical (15).…”

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Loss of NADH Oxidase Activity in Streptococcus mutans Leads to Rex-Mediated Overcompensation in NAD ⁺ Regeneration by Lactate Dehydrogenase

et al. 2015

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Previous studies of the oral pathogen Streptococcus mutans have determined that this Gram-positive facultative anaerobe mounts robust responses to both acid and oxidative stresses. The water-forming NADH oxidase (Nox; encoded by nox) is thought to be critical for the regeneration of NAD ؉ , for use in glycolysis, and for the reduction of oxygen, thereby preventing the formation of damaging reactive oxygen species. In this study, the free NAD ؉ /NADH ratio in a nox deletion strain (⌬nox) was discovered to be remarkably higher than that in the parent strain, UA159, when the strains were grown in continuous culture. This unanticipated result was explained by significantly elevated lactate dehydrogenase (Ldh; encoded by ldh) activity and ldh transcription in the ⌬nox strain, which was mediated in part by the redox-sensing regulator Rex. cDNA microarray analysis of S. mutans cultures exposed to simultaneous acid stress (growth at a low pH) and oxidative stress (generated through the deletion of nox or the addition of exogenous oxygen) revealed a stress response synergistically heightened over that with either stress alone. In the ⌬nox strain, this elevated stress response included increased glucose phosphoenolpyruvate phosphotransferase system (PTS) activity, which appeared to be due to elevated manL transcription, mediated in part, like elevated ldh transcription, by Rex. While the ⌬nox strain does possess a membrane composition different from that of the parent strain, it did not appear to have defects in either membrane permeability or ATPase activity. However, the altered transcriptome and metabolome of the ⌬nox strain were sufficient to impair its ability to compete with commensal peroxigenic oral streptococci during growth under aerobic conditions. IMPORTANCEStreptococcus mutans is an oral pathogen whose ability to outcompete commensal oral streptococci is strongly linked to the formation of dental caries. Previous work has demonstrated that the S. mutans water-forming NADH oxidase is critical for both carbon metabolism and the prevention of oxidative stress. The results of this study show that upregulation of lactate dehydrogenase, mediated through the redox sensor Rex, overcompensates for the loss of nox. Additionally, nox deletion led to the upregulation of mannose and glucose transport, also mediated through Rex. Importantly, the loss of nox rendered S. mutans defective in its ability to compete directly with two species of commensal streptococci, suggesting a role for nox in the pathogenic potential of this organism. Streptococcus mutans, the major etiologic agent of dental caries, is an opportunistic oral pathogen that resides in the multispecies biofilm known as dental plaque. Microorganisms that live in the oral cavity must be equipped to survive feast-or-famine cycles of nutrient availability, rapid changes in pH and temperature, and a dynamic range of oxygen concentrations (1-3). Dental plaque is somewhat porous, allowing the movement of fluids and nutrients, the establishment of chemical grad...

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“…S. mutans has evolved several mechanisms to respond to acid stress, including upregulation of F-ATPase activity (7,8), reduced phosphotransferase activity (9,10), cytosolic alkalinization through the use of the agmatine deiminase system (5,11) or malolactic fermentation (12), and alteration of membrane fatty acid composition (13,14). In addition to acid stress, S. mutans must also cope with exposure to oxidative stress, created by diatomic environmental oxygen present in the oral cavity, as well as copious amounts of H 2 O 2 produced by competing oral microflora in an attempt to thwart persistence and proliferation of S. mutans and other cariogenic bacteria (15)(16)(17)(18)(19). S. mutans encodes several enzymes important in eliminating potentially dangerous reactive oxygen species (ROS) (20).…”

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Streptococcus mutans NADH Oxidase Lies at the Intersection of Overlapping Regulons Controlled by Oxygen and NAD ⁺ Levels

et al. 2014

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c NADH oxidase (Nox, encoded by nox) is a flavin-containing enzyme used by the oral pathogen Streptococcus mutans to reduce diatomic oxygen to water while oxidizing NADH to NAD ؉ . The critical nature of Nox is 2-fold: it serves to regenerate NAD ؉ , a carbon cycle metabolite, and to reduce intracellular oxygen, preventing formation of destructive reactive oxygen species (ROS). As oxygen and NAD؉ have been shown to modulate the activity of the global transcription factors Spx and Rex, respectively, Nox is potentially poised at a critical junction of two stress regulons. In this study, microarray data showed that either addition of oxygen or loss of nox resulted in altered expression of genes involved in energy metabolism and transport and the upregulation of genes encoding ROS-metabolizing enzymes. Loss of nox also resulted in upregulation of several genes encoding transcription factors and signaling molecules, including the redox-sensing regulator gene rex. Characterization of the nox promoter revealed that nox was regulated by oxygen, through SpxA, and by Rex. These data suggest a regulatory loop in which the roles of nox in reduction of oxygen and regeneration of NAD ؉ affect the activity levels of Spx and Rex, respectively, and their regulons, which control several genes, including nox, crucial to growth of S. mutans under conditions of oxidative stress.

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Oxygen dependent pyruvate oxidase expression and production in Streptococcus sanguinis

Cited by 50 publications

References 26 publications

Biology of Oral Streptococci

Biology of Oral Streptococci

Loss of NADH Oxidase Activity in Streptococcus mutans Leads to Rex-Mediated Overcompensation in NAD ⁺ Regeneration by Lactate Dehydrogenase

Streptococcus mutans NADH Oxidase Lies at the Intersection of Overlapping Regulons Controlled by Oxygen and NAD ⁺ Levels

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Oxygen dependent pyruvate oxidase expression and production in Streptococcus sanguinis

Cited by 50 publications

References 26 publications

Biology of Oral Streptococci

Biology of Oral Streptococci

Loss of NADH Oxidase Activity in Streptococcus mutans Leads to Rex-Mediated Overcompensation in NAD + Regeneration by Lactate Dehydrogenase

Streptococcus mutans NADH Oxidase Lies at the Intersection of Overlapping Regulons Controlled by Oxygen and NAD + Levels

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Loss of NADH Oxidase Activity in Streptococcus mutans Leads to Rex-Mediated Overcompensation in NAD ⁺ Regeneration by Lactate Dehydrogenase

Streptococcus mutans NADH Oxidase Lies at the Intersection of Overlapping Regulons Controlled by Oxygen and NAD ⁺ Levels