Candida albicans quorum-sensing molecule farnesol modulates staphyloxanthin production and activates the thiol-based oxidative-stress response in Staphylococcus aureus

ABSTRACT Candida albicans, the most frequent fungal pathogen of humans, encounters high levels of oxidants following ingestion by professional phagocytes and through contact with hydrogen peroxide-producing bacteria. In this study, we provide evidence that C. albicans is able to coordinately regulate the oxidative stress response at the global cell population level by releasing protective molecules into the surrounding medium. We demonstrate that conditioned medium, which is defined as a filter-sterilized supernatant from a C. albicans stationary-phase culture, is able to protect yeast cells from both hydrogen peroxide and superoxide anion-generating agents. Exponential-phase yeast cells preexposed to conditioned medium were able to survive levels of oxidative stress that would normally kill actively growing yeast cells. Heat treatment, digestion with proteinase K, pH adjustment, or the addition of the oxidant scavenger alpha-tocopherol did not alter the ability of conditioned medium to induce a protective response. Farnesol, a heat-stable quorum-sensing molecule (QSM) that is insensitive to proteolytic enzymes and is unaffected by pH extremes, is partly responsible for this protective response. In contrast, the QSM tyrosol did not alter the sensitivity of C. albicans cells to oxidants. Relative reverse transcription-PCR analysis indicates that Candida-conditioned growth medium induces the expression of CAT1, SOD1, SOD2, and SOD4, suggesting that protection may be mediated through the transcriptional regulation of antioxidant-encoding genes. Together, these data suggest a link between the quorum-sensing molecule farnesol and the oxidative stress response in C. albicans.

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Autoinducer-2 Triggers the Oxidative Stress Response in Mycobacterium avium, Leading to Biofilm Formation

Applied and Environmental Microbiology ◽

10.1128/aem.02066-07 ◽

2008 ◽

Vol 74 (6) ◽

pp. 1798-1804 ◽

Cited By ~ 51

Author(s):

Henriette Geier ◽

Serge Mostowy ◽

Gerard A. Cangelosi ◽

Marcel A. Behr ◽

Timothy E. Ford

Keyword(s):

Oxidative Stress ◽

Stress Response ◽

Quorum Sensing ◽

Mycobacterium Avium ◽

Biofilm Formation ◽

Transcriptional Response ◽

Opportunistic Pathogen ◽

Environmental Stresses ◽

Oxidative Stress Response ◽

Autoinducer 2

ABSTRACT Mycobacterium avium is an environmental organism and opportunistic pathogen with inherent resistance to drugs, environmental stresses, and the host immune response. To adapt to these disparate conditions, M. avium must control its transcriptional response to environmental cues. M. avium forms biofilms in various environmental settings, including drinking water pipes and potable water reservoirs. In this study, we investigated the role of the universal signaling molecule autoinducer-2 (AI-2) in biofilm formation by M. avium. The addition of the compound to planktonic M. avium cultures resulted in increased biofilm formation. Microarray and reverse transcriptase PCR studies revealed an upregulation of the oxidative stress response upon addition of AI-2. This suggests that the response to AI-2 might be related to oxidative stress, rather than quorum sensing. Consistent with this model, addition of hydrogen peroxide, a known stimulus of the oxidative stress response, to M. avium cultures resulted in elevated biofilm formation. These results suggest that AI-2 does not act as a quorum-sensing signal in M. avium. Instead, biofilm formation is triggered by environmental stresses of biotic and abiotic origins and AI-2 may exert effects on that level.

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The AGXX® Antimicrobial Coating Causes a Thiol-Specific Oxidative Stress Response and Protein S-bacillithiolation in Staphylococcus aureus

Frontiers in Microbiology ◽

10.3389/fmicb.2018.03037 ◽

2018 ◽

Vol 9 ◽

Cited By ~ 12

Author(s):

Vu Van Loi ◽

Tobias Busche ◽

Thalia Preuß ◽

Jörn Kalinowski ◽

Jörg Bernhardt ◽

...

Keyword(s):

Oxidative Stress ◽

Staphylococcus Aureus ◽

Stress Response ◽

Protein S ◽

Oxidative Stress Response ◽

Antimicrobial Coating

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Trehalose accumulation induced during the oxidative stress response is independent of TPS1 mRNA levels in Candida albicans

International Microbiology ◽

10.1007/s10123-003-0119-y ◽

2003 ◽

Vol 6 (2) ◽

pp. 121-125 ◽

Cited By ~ 12

Author(s):

�scar Zaragoza ◽

Pilar Gonz�lez-P�rraga ◽

Yolanda Pedre�o ◽

Francisco J. Alvarez-Peral ◽

Juan-Carlos Arg�elles

Keyword(s):

Oxidative Stress ◽

Candida Albicans ◽

Stress Response ◽

Oxidative Stress Response ◽

Mrna Levels ◽

Trehalose Accumulation

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Global Regulatory Impact of ClpP Protease of Staphylococcus aureus on Regulons Involved in Virulence, Oxidative Stress Response, Autolysis, and DNA Repair

Journal of Bacteriology ◽

10.1128/jb.00074-06 ◽

2006 ◽

Vol 188 (16) ◽

pp. 5783-5796 ◽

Cited By ~ 128

Author(s):

Antje Michel ◽

Franziska Agerer ◽

Christof R. Hauck ◽

Mathias Herrmann ◽

Joachim Ullrich ◽

...

Keyword(s):

Oxidative Stress ◽

Staphylococcus Aureus ◽

Dna Repair ◽

Stress Response ◽

Oxidative Stress Response ◽

Transcriptional Analysis ◽

Expression Of Genes ◽

Wide Range ◽

Genes Encoding ◽

Regulatory Impact

ABSTRACT Staphylococcus aureus is an important pathogen, causing a wide range of infections including sepsis, wound infections, pneumonia, and catheter-related infections. In several pathogens ClpP proteases were identified by in vivo expression technologies to be important for virulence. Clp proteolytic complexes are responsible for adaptation to multiple stresses by degrading accumulated and misfolded proteins. In this report clpP, encoding the proteolytic subunit of the ATP-dependent Clp protease, was deleted, and gene expression of ΔclpP was determined by global transcriptional analysis using DNA-microarray technology. The transcriptional profile reveals a strong regulatory impact of ClpP on the expression of genes encoding proteins that are involved in the pathogenicity of S. aureus and adaptation of the pathogen to several stresses. Expression of the agr system and agr-dependent extracellular virulence factors was diminished. Moreover, the loss of clpP leads to a complete transcriptional derepression of genes of the CtsR- and HrcA-controlled heat shock regulon and a partial derepression of genes involved in oxidative stress response, metal homeostasis, and SOS DNA repair controlled by PerR, Fur, MntR, and LexA. The levels of transcription of genes encoding proteins involved in adaptation to anaerobic conditions potentially regulated by an Fnr-like regulator were decreased. Furthermore, the expression of genes whose products are involved in autolysis was deregulated, leading to enhanced autolysis in the mutant. Our results indicate a strong impact of ClpP proteolytic activity on virulence, stress response, and physiology in S. aureus.

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Oxidative stress response and adaptation to H2O2 in the model eukaryote Saccharomyces cerevisiae and its human pathogenic relatives Candida albicans and Candida glabrata

Fungal Biology Reviews ◽

10.1016/j.fbr.2014.12.001 ◽

2014 ◽

Vol 28 (4) ◽

pp. 126-136 ◽

Cited By ~ 3

Author(s):

Stephanie Diezmann

Keyword(s):

Oxidative Stress ◽

Saccharomyces Cerevisiae ◽

Candida Albicans ◽

Stress Response ◽

Candida Glabrata ◽

Oxidative Stress Response

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Multiple methionine sulfoxide reductase genes in Staphylococcus aureus: expression of activity and roles in tolerance of oxidative stress

Microbiology ◽

10.1099/mic.0.26442-0 ◽

2003 ◽

Vol 149 (10) ◽

pp. 2739-2747 ◽

Cited By ~ 63

Author(s):

Vineet K. Singh ◽

Jackob Moskovitz

Keyword(s):

Oxidative Stress ◽

Staphylococcus Aureus ◽

Stress Response ◽

Double Mutant ◽

Mutational Analysis ◽

Physiological Role ◽

Methionine Sulfoxide ◽

Oxidative Stress Response ◽

Methionine Sulfoxide Reductase ◽

Activity Data

Staphylococcus aureus contains three genes encoding MsrA-specific methionine sulfoxide reductase (Msr) activity (msrA1, msrA2 and msrA3) and an additional gene that encodes MsrB-specific Msr activity. Data presented here suggest that MsrA1 is the major contributor of the MsrA activity in S. aureus. In mutational analysis, while the total Msr activity in msrA2 mutant was comparable to that of the parent, Msr activity was significantly up-regulated in the msrA1 or msrA1 msrA2 double mutant. Assessment of substrate specificity together with increased reactivity of the cell-free protein extracts of the msrA1 mutants to anti-MsrB polyclonal antibodies in Western analysis provided evidence that increased Msr activity was due to elevated synthesis of MsrB in the MsrA1 mutants. Previously, it was reported that oxacillin treatment of S. aureus cells led to induced synthesis of MsrA1 and a mutation in msrA1 increased the susceptibility of the organism to H2O2. A mutation in the msrA2 gene, however, was not significant for the bacterial oxidative stress response. In complementation assays, while the msrA2 gene was unable to complement the msrA1 msrA2 double mutant for H2O2 resistance, the same gene restored H2O2 tolerance in the double mutant when placed under the control of the msrA1 promoter. However, msrA1 which was able to complement the oxidative stress response in msrA1 mutants could not restore the tolerance of the msrA1 msrA2 mutants to H2O2 when placed under the control of the msrA2 promoter. Additionally, although the oxacillin minimum inhibitory concentration of the msrA1 mutant was comparable to that of the wild-type parent, in shaking liquid culture, the msrA1 mutant responded more efficiently to sublethal doses of oxacillin. The data suggest complex regulation of Msr proteins and a more significant physiological role for msrA1/msrB in S. aureus.

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Nonthermal Plasma Induces the Viable-but-Nonculturable State in Staphylococcus aureus via Metabolic Suppression and the Oxidative Stress Response

Applied and Environmental Microbiology ◽

10.1128/aem.02216-19 ◽

2019 ◽

Vol 86 (5) ◽

Cited By ~ 2

Author(s):

Xinyu Liao ◽

Donghong Liu ◽

Tian Ding

Keyword(s):

Oxidative Stress ◽

Staphylococcus Aureus ◽

Stress Response ◽

Nonthermal Plasma ◽

Energy Allocation ◽

Oxidative Stress Response ◽

Vbnc State ◽

Viable But Nonculturable ◽

Content Type ◽

Energy Dependent

ABSTRACT As a novel nonthermal technology, nonthermal plasma (NTP) has attracted a lot of attention. However, it could induce microorganisms into a viable but nonculturable (VBNC) state, posing a potential risk to food safety and public health. In this study, the molecular mechanisms of VBNC Staphylococcus aureus induced by NTP were investigated. With the use of a propidium monoazide quantitative PCR (PMA-qPCR) technique combined with a plate count method, we confirmed that 8.1 to 24.3 kJ NTP induced S. aureus into a VBNC state at a level of 7.4 to 7.6 log10 CFU/ml. The transcriptomic analysis was conducted and revealed that most energy-dependent physiological activities (e.g., metabolism) were arrested in VBNC S. aureus, while the oxidative stress response-related genes (katA, dps, msrB, msrA, and trxA) were significantly upregulated. In addition, this study showed that the ATP depletion by carbonyl cyanide m-chlorophenyl hydrazone (CCCP) pretreatment could accelerate the formation of VBNC S. aureus. The NTP-generated oxidative stress triggers the staphylococcal oxidative stress response, which consumes part of cellular energy (e.g., ATP). The energy allocation is therefore changed, and the energy assigned for other energy-dependent physiological activities (cell growth and division, etc.) is reduced, subsequently forcing S. aureus into a VBNC state. Therefore, the alterations of energy allocation should be some of the major contributors to the induction of VBNC S. aureus with NTP exposure. This study provides valuable knowledge for controlling the formation of VBNC S. aureus during NTP treatment. IMPORTANCE In recent years, nonthermal plasma (NTP) technology has received a lot of attention as a promising alternative to thermal pasteurization in the food industry. However, little is known about the microbial stress response toward NTP, which could be a potential risk to food safety and impede the development of NTP. A viable but nonculturable (VBNC) state is one of the most common survival strategies employed by microorganisms against external stress. This study investigated the mechanisms of the formation of VBNC Staphylococcus aureus by NTP in a more comprehensive and systematic aspect than had been done before. Our work confirmed that the NTP-generated oxidative stress induced changes in energy allocation as a driving force for the formation of VBNC S. aureus. This study could provide better knowledge for controlling the occurrence of VBNC S. aureus induced by NTP, which could lead to more rational design and ensure the development of safe foods.

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