In Streptococcus thermophilus, Ammonia from Urea Hydrolysis Paradoxically Boosts Acidification and Reveals a New Regulatory Mechanism of Glycolysis

Arioli, Stefania; Scala, Giulia Della; Martinović, Anđela; Scaglioni, Leonardo; Mazzini, Stefania; Volontè, Federica; Pedersen, Martin Bastian; Mora, Diego

doi:10.1128/spectrum.02760-21

Cited by 7 publications

(7 citation statements)

References 43 publications

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“…In our experiments, we observed that adding ammonium citrate or ammonium chloride to CDM hindered cell growth; similarly, it is reported that ammonium chloride was much less effective than urea or ammonia at promoting acidification in S. thermophilus. 15 This is because directly added NH 4 + cannot combine with protons and achieve cytoplasmic alkalinization.…”

Section: Discussionmentioning

confidence: 99%

“…14 Nevertheless, a novel study has proposed that NH 4 + may enhance glycolysis and lactic acid fermentation by acting as an activator of phosphofructokinase. 15 These findings have prompted a reassessment of the role of urease in S. thermophilus. The unfavorable impact of urease on fermentation processes is attributed to unpredictable acidification rates, resulting from variable urea concentrations in different milk batches.…”

Section: Introductionmentioning

confidence: 99%

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Genome‐scale reconstruction of the metabolic network in Streptococcus thermophilus S‐3 and assess urea metabolism

Hou,

Song,

Xiong

et al. 2023

J Sci Food Agric

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BACKGROUNDStreptococcus thermophilus is an important strain widely used in dairy fermentation, with distinct urea metabolism characteristics compared to other lactic acid bacteria. The conversion of urea by S. thermophilus has been shown to affect the flavor and acidification characteristics of milk. Additionally, urea metabolism has been found to significantly increase the number of cells and reduce cell damage under acidic pH conditions, resulting in higher activity. However, the physiological role of urea metabolism in S. thermophilus has not been fully evaluated. A deep understanding of this metabolic feature is of great significance for its production and application. Genome‐scale metabolic network models (GEMs) are effective tools for investigating the metabolic network of organisms using computational biology methods. Constructing an organism‐specific GEM can assist us in comprehending its characteristic metabolism at a systemic level.RESULTSIn the present study, we reconstructed a high‐quality GEM of S. thermophilus S‐3 (iCH492), which contains 492 genes, 608 metabolites and 642 reactions. Growth phenotyping experiments were employed to validate the model both qualitatively and quantitatively, yielding satisfactory predictive accuracy (95.83%), sensitivity (93.33%) and specificity (100%). Subsequently, a systematic evaluation of urea metabolism in S. thermophilus was performed using iCH492. The results showed that urea metabolism reduces intracellular hydrogen ions and creates membrane potential by producing and transporting ammonium ions. This activation of glycolytic fluxes and ATP synthase produces more ATP for biomass synthesis. The regulation of fluxes of reactions involving NAD(P)H by urea metabolism improves redox balance.CONCLUSIONModel iCH492 represents the most comprehensive knowledge‐base of S. thermophilus to date, serving as a potent tool. The evaluation of urea metabolism led to novel insights regarding the role of urease. © 2023 Society of Chemical Industry.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Genome‐scale reconstruction of the metabolic network in Streptococcus thermophilus S‐3 and assess urea metabolism

Hou,

Song,

Xiong

et al. 2023

J Sci Food Agric

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“…Notably, the partitioning between lactate and mixed-acid products was likely regulated at the metabolic level instead of at the transcriptional level ( Paixao et al., 2015 ). Correspondingly, the additional NADH in vivo synthesized by the fragmentary TCA cycle is used for homolactic fermentation of pyruvate and contributes to a balanced NAD + /NADH ratio that controls the shift from homolactic to mixed-acid fermentation in Lactococcus lactis , S. pneumoniae , Streptococcus thermophilus , and perhaps in S. suis ( Willenborg et al., 2015 ; Arioli et al., 2022 ). We speculated that the inhibited fragmentary TCA cycle reduces the yield of NADH and leads to the imbalance of the ratio and the transformation of fermentation manner in glycogen cultures.…”

Section: Discussionmentioning

confidence: 99%

Exogenous glycogen utilization effects the transcriptome and pathogenicity of Streptococcus suis serotype 2

Tan

Tan²,

Zhang³

et al. 2022

Front. Cell. Infect. Microbiol.

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Streptococcus suis serotype 2 (SS2) is an important zoonotic pathogen that causes severe infections in humans and the swine industry. Acquisition and utilization of available carbon sources from challenging host environments is necessary for bacterial pathogens to ensure growth and proliferation. Glycogen is abundant in mammalian body and may support the growth of SS2 during infection in hosts. However, limited information is known about the mechanism between the glycogen utilization and host adaptation of SS2. Here, the pleiotropic effects of exogenous glycogen on SS2 were investigated through transcriptome sequencing. Analysis of transcriptome data showed that the main basic metabolic pathways, especially the core carbon metabolism pathways and virulence-associated factors, of SS2 responded actively to glycogen induction. Glycogen induction led to the perturbation of the glycolysis pathway and citrate cycle, but promoted the pentose phosphate pathway and carbohydrate transport systems. Extracellular glycogen utilization also promoted the mixed-acid fermentation in SS2 rather than homolactic fermentation. Subsequently, apuA, a gene encoding the unique bifunctional amylopullulanase for glycogen degradation, was deleted from the wild type and generated the mutant strain ΔapuA. The pathogenicity details of the wild type and ΔapuA cultured in glucose and glycogen were investigated and compared. Results revealed that the capsule synthesis or bacterial morphology were not affected by glycogen incubation or apuA deletion. However, extracellular glycogen utilization significantly enhanced the hemolytic activity, adhesion and invasion ability, and lethality of SS2. The deletion of apuA also impaired the pathogenicity of bacteria cultured in glucose, indicating that ApuA is indeed an important virulence factor. Our results revealed that exogenous glycogen utilization extensively influenced the expression profile of the S. suis genome. Based on the transcriptome response, exogenous glycogen utilization promoted the carbon adaption and pathogenicity of SS2.

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“…Urease rather has a key role in streamlining the energetic metabolism of S. thermophilus and specifically by acting on glycolysis regulation. [ 20–22 ]…”

Section: Introductionmentioning

confidence: 99%

“…Urease rather has a key role in streamlining the energetic metabolism of S. thermophilus and specifically by acting on glycolysis regulation. [20][21][22] In human microbiota, since the discovery of Helicobacter pylori, microbial ureases have been found to play a key role in the pathogenetic traits of several bacteria. [23] Several studies showed through a metagenomic approach that microbial ureases led to dysbiosis of the gut microbiota and that urease-genes are enriched in patients with irritable bowel syndrome (IBS) and depression.…”

Section: Introductionmentioning

confidence: 99%

The Ability of Streptococcus thermophilus BT01 to Modulate Urease Activity in Healthy Subjects’ Fecal Samples Depends on the Biomass Production Process

Martinović

Marco

Mora

et al. 2023

Molecular Nutrition Food Res

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Scope: This study evaluates how manufacturing conditions of probiotic biomass production, using two different cryoprotectants, Cryo-A and Cryo-B, can affect Streptococcus thermophilus BT01 in vivo gastrointestinal tract survival and its ability to modulate the level of urease activity in fecal samples of healthy subjects. Methods and results: A randomized controlled cross-over study is carried out on 20 adult healthy subjects to evaluate total and viable loads, persistence of S. thermophilus BT01, and urease activity in fecal samples. Strain-specific quantification by using developed culture-based method and molecular qPCR tool allows to quantify viable S. thermophilus BT01 strain in 90% of the subjects. The quantification of both total DNA and recovered viable S. thermophilus BT01 in fecal samples does not reveal significant differences between Cryo-A or Cryo-B treated biomass. However, the administration of S. thermophilus BT01 produced with Cryo-A results in a decreased urease activity in fecal samples compared to Cryo-B protected cells. Conclusion: This study i) highlights how the manufacturing conditions can play a role in influencing the probiotic functionality in vivo and ii) represents the first evidence that links S. thermophilus to a specific probiotic mechanism, the reduction of urease activity in fecal samples.

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In Streptococcus thermophilus, Ammonia from Urea Hydrolysis Paradoxically Boosts Acidification and Reveals a New Regulatory Mechanism of Glycolysis

Cited by 7 publications

References 43 publications

Genome‐scale reconstruction of the metabolic network in Streptococcus thermophilus S‐3 and assess urea metabolism

Genome‐scale reconstruction of the metabolic network in Streptococcus thermophilus S‐3 and assess urea metabolism

Exogenous glycogen utilization effects the transcriptome and pathogenicity of Streptococcus suis serotype 2

The Ability of Streptococcus thermophilus BT01 to Modulate Urease Activity in Healthy Subjects’ Fecal Samples Depends on the Biomass Production Process

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