Post-translational regulation of a <i>Porphyromonas gingivalis</i> regulator

Li, Yuqing; Krishnan, Karthik; Duncan, Marilyn J.

doi:10.1080/20002297.2018.1487743

Cited by 18 publications

(25 citation statements)

References 36 publications

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“…Similar results have also been reported for Prevotella bryantii (53). In the oral bacterium Porphyromonas gingivalis, the RprY response regulator positively activates NQR by interacting with the promoter upstream of the nqrA gene (54), and under conditions of oxidative stress, the production of RprY decreases, as does the expression of nqrA (55). In addition, the RprY regulator of P. gingivalis was shown to bind the promoter region of the nqr operon of Bacteroides fragilis, suggesting that the regulation of this operon is similar in these two bacteria.…”

supporting

confidence: 84%

Genetic and Biochemical Analysis of Anaerobic Respiration in Bacteroides fragilis and Its Importance In Vivo

Ito

Gallegos

Matano

et al. 2020

mBio

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In bacteria, the respiratory pathways that drive molecular transport and ATP synthesis include a variety of enzyme complexes that utilize different electron donors and acceptors. This property allows them to vary the efficiency of energy conservation and to generate different types of electrochemical gradients (H+ or Na+). We know little about the respiratory pathways in Bacteroides species, which are abundant in the human gut, and whether they have a simple or a branched pathway. Here, we combined genetics, enzyme activity measurements, and mammalian gut colonization assays to better understand the first committed step in respiration, the transfer of electrons from NADH to quinone. We found that a model gut Bacteroides species, Bacteroides fragilis, has all three types of putative NADH dehydrogenases that typically transfer electrons from the highly reducing molecule NADH to quinone. Analyses of NADH oxidation and quinone reduction in wild-type and deletion mutants showed that two of these enzymes, Na+-pumping NADH:quinone oxidoreductase (NQR) and NADH dehydrogenase II (NDH2), have NADH dehydrogenase activity, whereas H+-pumping NADH:ubiquinone oxidoreductase (NUO) does not. Under anaerobic conditions, NQR contributes more than 65% of the NADH:quinone oxidoreductase activity. When grown in rich medium, none of the single deletion mutants had a significant growth defect; however, the double Δnqr Δndh2 mutant, which lacked almost all NADH:quinone oxidoreductase activity, had a significantly increased doubling time. Despite unaltered in vitro growth, the single nqr deletion mutant was unable to competitively colonize the gnotobiotic mouse gut, confirming the importance of NQR to respiration in B. fragilis and the overall importance of respiration to this abundant gut symbiont. IMPORTANCE Bacteroides species are abundant in the human intestine and provide numerous beneficial properties to their hosts. The ability of Bacteroides species to convert host and dietary glycans and polysaccharides to energy is paramount to their success in the human gut. We know a great deal about the molecules that these bacteria extract from the human gut but much less about how they convert those molecules into energy. Here, we show that B. fragilis has a complex respiratory pathway with two different enzymes that transfer electrons from NADH to quinone and a third enzyme complex that may use an electron donor other than NADH. Although fermentation has generally been believed to be the main mechanism of energy generation in Bacteroides, we found that a mutant lacking one of the NADH:quinone oxidoreductases was unable to compete with the wild type in the mammalian gut, revealing the importance of respiration to these abundant gut symbionts.

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supporting

confidence: 84%

Genetic and Biochemical Analysis of Anaerobic Respiration in Bacteroides fragilis and Its Importance In Vivo

Ito

Gallegos

Matano

et al. 2020

mBio

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“…Recently, two novel proteins named 'internalin pro-Clptein (InlJ)' along with the 'expression of the short fimbriae and the universal stress protein UspA' have been linked with monospecies P. gingivalis biofilms formation and initial attachment [100][101][102][103][104][105][106]. Furthermore, the loss of several genes has been observed within the P. gingivalis colonies to regulate the growth of the biofilm and promotes its chance of survival.…”

Section: Mechanism Of P Gingivalis Invasion and Persistence Within Tmentioning

confidence: 99%

“…Furthermore, the loss of several genes has been observed within the P. gingivalis colonies to regulate the growth of the biofilm and promotes its chance of survival. Some of the inhibitors of homotypic biofilm accumulation include Caseinolytic Mitochondrial Matrix Peptidase Chaperone Subunit X (ClpXP) along with ClpC, and GalE (UDP-galactose 4-epimerase) have been found in P. gingivalis microcolonies [99,[103][104][105][106][107]. P. gingivalis is also observed to cause lysine acetylation in colonies, and this is considered as novel mechanism of metabolic regulation, adaptation, and survival during infection [105].…”

Section: Mechanism Of P Gingivalis Invasion and Persistence Within Tmentioning

confidence: 99%

Porphyromonas gingivalis adopts intricate and unique molecular mechanisms to survive and persist within the host: a critical update

Chopra

Bhat

Sivaraman

2020

Journal of Oral Microbiology

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Porphyromonas. gingivalis (P. gingivalis) is an obligate, asaccharolytic, gram-negative bacteria commonly associated with increased periodontal and systemic inflammation. P. gingivalis is known to survive and persist within the host tissues as it modulates the entire ecosystem by either engineering its environment or modifying the host's immune response. It interacts with various host receptors and alters signaling pathways of inflammation, complement system, cell cycle, and apoptosis. P. gingivalis is even known to induce suicidal cell death of the host and other microbes in its vicinity with the emergence of pathobiont species. Recently, new molecular and immunological mechanisms and virulence factors of P. gingivalis that increase its chance of survival and immune evasion within the host have been discovered. Thus, the present paper aims to provide a consolidated update on the new intricate and unique molecular mechanisms and virulence factors of P. gingivalis associated with its survival, persistence, and immune evasion within the host.

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“…Recently, lysine acetylation in P gingivalis has been proposed as an important mechanism of metabolic regulation, which is vital for P gingivalis and its adaptation and survival during infection . Specifically, acetylation of RprY, a response regulator of P gingivalis in the oxidative stress response, has been demonstrated to reduce the promoter DNA binding ability of RprY, which consequently may alter gene expression …”

Section: Introductionmentioning

confidence: 99%

Global analysis of lysine succinylome in the periodontal pathogen Porphyromonas gingivalis

Gong

Zhou

et al. 2019

Molecular Oral Microbiology

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The gram-negative anaerobe Porphyromonas gingivalis is not only a keystone periodontal pathogen but also an emerging systemic pathogen. Although the newly discovered protein post-translational modification (PTM), lysine succinylation (Ksuc), appears to play an important role in modulating metabolic processes in bacteria, this PTM has not been investigated in P gingivalis. In this study, we used a highly sensitive proteomics approach combining affinity enrichment with high-resolution liquid chromatography coupled with tandem mass spectrometry to examine Ksuc in P gingivalis.In total, 345 Ksuc sites in 233 proteins were identified and determined to be involved in a variety of cellular processes. In the region surrounding Ksuc sites, lysine residues were drastically overrepresented and sequence motifs with succinyl-lysine flanked by a lysine at the +3 or +6 positions appear to be unique to this pathogen. Additionally, our results suggest a crosstalk between Ksuc and glycosylation, but the overlap between Ksuc and acetylation in P gingivalis is quite different from that observed in other organisms. Notably, Ksuc was observed in proteins associated with established virulence factors, including gingipains, fimbriae, RagB, and PorR. Moreover, products of the factors necessary for P gingivalis in vitro survival (18.5%) were found to be succinylated at lysine sites and the same was observed in products of fitness factors for P gingivalis survival in both abscess and epithelial cell colonization environments (12%). Collectively, these results suggest that Ksuc may be a new mechanism in modulating the virulence, adaptation, and fitness of P gingivalis. K E Y W O R D S fitness factors, lysine succinylation, necessary factors, Porphyromonas gingivalis, proteomics | 75 WU et al.

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Post-translational regulation of a Porphyromonas gingivalis regulator

Cited by 18 publications

References 36 publications

Genetic and Biochemical Analysis of Anaerobic Respiration in Bacteroides fragilis and Its Importance In Vivo

Genetic and Biochemical Analysis of Anaerobic Respiration in Bacteroides fragilis and Its Importance In Vivo

Porphyromonas gingivalis adopts intricate and unique molecular mechanisms to survive and persist within the host: a critical update

Global analysis of lysine succinylome in the periodontal pathogen Porphyromonas gingivalis

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