The Two-Component System 09 of Streptococcus pneumoniae Is Important for Metabolic Fitness and Resistance during Dissemination in the Host

Hirschmann, Stephanie; Gómez-Mejía, Alejandro; Kohler, Thomas P.; Voß, Franziska; Rohde, Manfred; Brendel, Max; Hammerschmidt, Sven

doi:10.3390/microorganisms9071365

Cited by 4 publications

(3 citation statements)

References 57 publications

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“…The maximum density was calculated from the mean of the three replicates of the highest OD 600nm values. For the calculation of the maximal growth rate, time points were chosen during maximal growth (steepest slope) and the following formula was then used as described ( Hirschmann et al., 2021 ):…”

Section: Methodsmentioning

confidence: 99%

Carbon source–dependent capsule thickness regulation in Streptococcus pneumoniae

Werren,

Mostacci,

Gjuroski

et al. 2023

Front. Cell. Infect. Microbiol.

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BackgroundThe polysaccharide capsule of Streptococcus pneumoniae plays a major role in virulence, adherence to epithelial cells, and overall survival of the bacterium in the human host. Galactose, mannose, and N-acetylglucosamine (GlcNAc) are likely to be relevant for metabolization in the nasopharynx, while glucose is the primary carbon source in the blood. In this study, we aim to further the understanding of the influence of carbon sources on pneumococcal growth, capsule biosynthesis, and subsequent adherence potential.MethodsWe tested the growth behavior of clinical wild-type and capsule knockout S. pneumoniae strains, using galactose, GlcNAc, mannose, and glucose as carbon source for growth. We measured capsule thickness and quantified capsule precursors by fluorescein isothiocyanate (FITC)–dextran exclusion assays and 31P-nuclear magnetic resonance measurements, respectively. We also performed epithelial adherence assays using Detroit 562 cells and performed a transcriptome analysis (RNA sequencing).ResultsWe observed a reduced growth in galactose, mannose, and GlcNAc compared to growth in glucose and found capsular size reductions in mannose and GlcNAc compared to galactose and glucose. Additionally, capsular precursor measurements of uridine diphosphate-(UDP)-glucose and UDP-galactose showed less accumulation of precursors in GlcNAc or mannose than in glucose and galactose, indicating a possible link with the received capsular thickness measurements. Epithelial adherence assays showed an increase in adherence potential for a pneumococcal strain, when grown in mannose compared to glucose. Finally, transcriptome analysis of four clinical isolates revealed not only strain specific but also common carbon source-specific gene expression.ConclusionOur findings may indicate a careful adaption of the lifestyle of S. pneumoniae according to the monosaccharides encountered in the respective human niche.

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Section: Methodsmentioning

confidence: 99%

Carbon source–dependent capsule thickness regulation in Streptococcus pneumoniae

Werren,

Mostacci,

Gjuroski

et al. 2023

Front. Cell. Infect. Microbiol.

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“…Capsule or EPS production is often controlled by TCSs, such as S. pneumoniae ZmpRS, linking carbon metabolism, capsule production, and infection (Hirschmann et al 2021a , b ). Other examples are A. baumannii BfmRS involved in production of capsular EPS upon bacterial exposure to low concentrations of antibiotics (Geisinger and Isberg 2015 ) and ExPEC TCS Rcs, which controls EPS colanic acid production (Miajlovic and Smith 2014 ).…”

Section: Bacterial Factors Mediating Adaptive Response To Bloodmentioning

confidence: 99%

Determinants of bacterial survival and proliferation in blood

Lê-Bury,

Echenique-Rivera,

Pizarro-Cerdá

et al. 2024

FEMS Microbiology Reviews

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Bloodstream infection is a major public health concern associated with high mortality and high healthcare costs worldwide. Bacteremia can trigger fatal sepsis whose prevention, diagnosis and management have been recognized as a global health priority by the World Health Organization. Additionally, infection control is increasingly threatened by antimicrobial resistance, which is the focus of global action plans in the framework of a One Health response. In-depth knowledge of the infection process is needed to develop efficient preventive and therapeutic measures. The pathogenesis of bloodstream infection is a dynamic process resulting from the invasion of the vascular system by bacteria, which finely regulate their metabolic pathways and virulence factors to overcome the blood immune defenses and proliferate. In this review, we highlight our current understanding of determinants of bacterial survival and proliferation in the bloodstream and discuss their interactions with the molecular and cellular components of blood.

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“…The same phenotype was displayed by mutants in the tcs09 genes, which encode TCS09. The probable mechanism by which TCS09 is involved in resistance against oxidative stress is mediating the regulation of carbohydrate metabolism, cell wall integrity and amount of capsular polysaccharide ( Hirschmann et al, 2021 ; Figure 3 ).…”

Section: Gene Regulation Mechanismsmentioning

confidence: 99%

The oxidative stress response of Streptococcus pneumoniae: its contribution to both extracellular and intracellular survival

Hernandez-Morfa,

Olivero,

Zappia

et al. 2023

Front. Microbiol.

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Streptococcus pneumoniae is a gram-positive, aerotolerant bacterium that naturally colonizes the human nasopharynx, but also causes invasive infections and is a major cause of morbidity and mortality worldwide. This pathogen produces high levels of H2O2 to eliminate other microorganisms that belong to the microbiota of the respiratory tract. However, it also induces an oxidative stress response to survive under this stressful condition. Furthermore, this self-defense mechanism is advantageous in tolerating oxidative stress imposed by the host’s immune response. This review provides a comprehensive overview of the strategies employed by the pneumococcus to survive oxidative stress. These strategies encompass the utilization of H2O2 scavengers and thioredoxins, the adaptive response to antimicrobial host oxidants, the regulation of manganese and iron homeostasis, and the intricate regulatory networks that control the stress response. Here, we have also summarized less explored aspects such as the involvement of reparation systems and polyamine metabolism. A particular emphasis is put on the role of the oxidative stress response during the transient intracellular life of Streptococcus pneumoniae, including coinfection with influenza A and the induction of antibiotic persistence in host cells.

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The Two-Component System 09 of Streptococcus pneumoniae Is Important for Metabolic Fitness and Resistance during Dissemination in the Host

Cited by 4 publications

References 57 publications

Carbon source–dependent capsule thickness regulation in Streptococcus pneumoniae

Carbon source–dependent capsule thickness regulation in Streptococcus pneumoniae

Determinants of bacterial survival and proliferation in blood

The oxidative stress response of Streptococcus pneumoniae: its contribution to both extracellular and intracellular survival

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