<i>Pseudomonas aeruginosa</i> RoxR, a response regulator related to <i>Rhodobacter sphaeroides</i> PrrA, activates expression of the cyanide‐insensitive terminal oxidase

Comolli, James C.; Donohue, Timothy J.

doi:10.1046/j.1365-2958.2002.03046.x

Cited by 67 publications

(95 citation statements)

References 65 publications

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“…Thus, these results suggest that PQS affect aerobic and anaerobic respiration in P. aeruginosa PAO1 differently. Therefore, the target of PQS in the respiratory chain may not be a component such as NADH-dehydrogenase that is common to both aerobic and anaerobic respiration (6). Alternatively, PQS may induce production of some factors under aerobic conditions that inhibit the effect of PQS observed under anaerobic conditions.…”

Section: Discussionmentioning

confidence: 99%

The Effect of a Cell-to-Cell Communication Molecule, Pseudomonas Quinolone Signal (PQS), Produced by P. aeruginosa on Other Bacterial Species

et al. 2010

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One of the most important factors in the development of a bacterial community is whether the bacteria are able to grow in that habitat. The regulation of bacterial growth is generally studied in relation to physicochemical conditions, however, how bacterial communities regulate themselves remains unclear. In our previous study, it was demonstrated that a cell-to-cell communication molecule, 2-heptyl-3-hydroxy-4-quinolone, referred to as the Pseudomonas quinolone signal (PQS), affects respiring-activity in Pseudomonas aeruginosa without requiring its cognate receptor PqsR. The results suggested that PQS may affect other bacterial species, which was further examined in this study. PQS repressed the growth of several species including both Gram-negative and Gram-positive bacteria. In most cases, this effect differed from the bacteriostatic or bacteriolytic actions of antibiotics. The growth repression by PQS was inhibited when iron was added to the medium, indicating iron-chelating activity to be involved. In addition, PQS affected oxygen consumption in some species tested, and may have other underlying effects. Thus, this cell-to-cell communication molecule may influence the development of bacterial communities by regulating bacterial growth, and physicochemical factors such as iron would be important in determining its effect. Key words: Pseudomonas quinolone signal, cell-to-cell communication, interspecies interactionStudies of natural samples using techniques such as PCRdenaturing gradient gel electrophoresis (DGGE) and terminal-restriction fragment length polymorphism have provided information about the kinds of bacteria inhabiting different environments. However, why bacteria live where they do is still unclear. The regulation of growth is important when considering the habitats of bacteria, and many factors that regulate energy production have been studied, such as the presence of electron acceptors or electron donors and pH.Besides physicochemical factors, extracellular bacterial metabolites are also reported to control the growth of bacteria. For example, indole derivatives were isolated as growth inhibitors in Symbiobacterium thermophilum (35). Antibiotic reactions are another example of an interaction where bacterial growth is inhibited by extracellular bacterial metabolites. Recently, it has been proposed that antibiotics work as signals, regulating gene expression (8). Moreover, numerous bacteria utilize cell-to-cell communication signaling molecules, enabling them to coordinate diverse biological responses (27). In Gram-negative bacteria, these signaling molecules are typically N-acyl-L-homoserine lactones (AHLs). Pseudomonas aeruginosa is a well-studied bacterium possessing at least two AHL-dependent quorum-sensing systems, the LasR-LasI (las) and the RhlR-RhlI (rhl) systems (24). In addition, a non-AHL quorum-sensing signal, 2-heptyl-3-hydroxy-4-quinolone, referred to as the Pseudomonas quinolone signal (PQS), was found in P. aeruginosa (25). PQS regulates the production of virulence factors such as...

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Section: Discussionmentioning

confidence: 99%

The Effect of a Cell-to-Cell Communication Molecule, Pseudomonas Quinolone Signal (PQS), Produced by P. aeruginosa on Other Bacterial Species

et al. 2010

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“…However, in Rhodobacter sphaeroides a two-component regulatory system PrrAB is proposed to regulate electron-transfer components by sensing the redox flux through the cytochrome c oxidizing pathway, specifically through a component of the cytochrome cbb 3 (Oh & Kaplan, 2000. Very interesting, in this context, is the recent report of P. aeruginosa RoxR, a response regulator that is related to PrrA, with a role in regulating cioAB (Comolli & Donohue, 2002). The authors showed that mutation of roxR leads to the loss of cyanide and azide resistance in P. aeruginosa PAK, and provided evidence to support the idea that this resulted from CIO deficiency.…”

Section: Discussionmentioning

confidence: 99%

“…In this paper, we have clearly shown that CIO is not induced by endogenously generated cyanide. It is important to note that Comolli & Donohue (2002) performed their experiments on exponential-phase cultures, that is, conditions under which the CIO expression is at a minimum and during which the endogenous stationary-phase inducing signal either is absent or has its effects repressed. So, while an attractive model, it is premature to suggest that RoxR is responsible for the stationaryphase induction of CIO.…”

Section: Discussionmentioning

confidence: 99%

Regulation of expression of the cyanide-insensitive terminal oxidase in Pseudomonas aeruginosa

2003

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The regulation of the cyanide-insensitive oxidase (CIO) in Pseudomonas aeruginosa, a bacterium that can synthesize HCN, is reported. The expression of a cioA-lacZ transcriptional fusion, CioA protein levels and CIO activity were low in exponential phase but induced about fivefold upon entry into stationary phase. Varying the O 2 transfer coefficient from 11?5 h 21 to 87?4 h 21 had no effect on CIO expression and no correlation was observed between CIO induction and the dissolved O 2 levels in the growth medium. However, a mutant deleted for the O 2 -sensitive transcriptional regulator ANR derepressed CIO expression in an O 2 -sensitive manner, with the highest induction occurring under low-O 2 conditions. Therefore, CIO expression can respond to a signal generated by low O 2 levels, but this response is normally kept in check by ANR repression. ANR may play an important role in preventing overexpression of the CIO in relation to other terminal oxidases. A component present in spent culture medium was able to induce CIO expression. However, experiments with purified N-butanoyl-L-homoserine lactone or N-(3-oxododecanoyl)homoserine lactone ruled out a role for these quorum-sensing molecules in the control of CIO expression. Cyanide was a potent inducer of the CIO at physiologically relevant concentrations and experiments using spent culture medium from a DhcnB mutant, which is unable to synthesize cyanide, showed that cyanide was the inducing factor present in P. aeruginosa spent culture medium. However, the finding that in a DhcnB mutant cioA-lacZ expression was induced normally upon entry into stationary phase indicated that cyanide was not the endogenous inducer of the terminal oxidase. The authors suggest that the failure of O 2 to have an effect on CIO expression in the wild-type can be explained either by the requirement for an additional, stationary-phase-specific inducing signal or by the loss of an exponential-phase-specific repressing signal. INTRODUCTIONPseudomonas aeruginosa is an opportunistic pathogen that causes a variety of nosocomial infections, including pneumonia, urinary tract infections, surgical wound infections, and bloodstream infections (for a review see Deretic, 2000). It causes life-threatening illness in patients with cystic fibrosis. Initially, P. aeruginosa colonizes the airways with other pathogens such as Haemophilus influenzae and Staphylococcus aureus. However, in most of these patients chronic lung disease develops in which the bacterial population consists almost exclusively of P. aeruginosa in the form of biofilms (Govan & Deretic, 1996). P. aeruginosa is a facultative anaerobe that preferentially obtains its energy via aerobic respiration, but it is well adapted to conditions of limited O 2 supply (Palleroni, 1984;Davies et al., 1989). It is capable of anaerobic growth with nitrate as a terminal electron acceptor and in the absence of nitrate it is able to ferment arginine, generating ATP by substrate-level phosphorylation (Palleroni, 1984;Davies et al., 1989;Van der Wauven et ...

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“…Inactivation of the other terminal oxidases by respiratory inhibitors or gene disruption also leads to significant upregulation of the cio genes (15)(16)(17)(18)(19)(20)(21). The upregulation of CIO in the stationary phase is probably because P. aeruginosa produces cyanide, which inhibits heme-copper oxidases, in the stationary phase.…”

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confidence: 99%

Enzymatic Characterization and In Vivo Function of Five Terminal Oxidases in Pseudomonas aeruginosa

et al. 2014

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The ubiquitous opportunistic pathogen Pseudomonas aeruginosa has five aerobic terminal oxidases: bo 3 -type quinol oxidase (Cyo), cyanide-insensitive oxidase (CIO), aa 3 -type cytochrome c oxidase (aa 3 ), and two cbb 3 -type cytochrome c oxidases (cbb 3 -1 and cbb 3 -2). These terminal oxidases are differentially regulated under various growth conditions and are thought to contribute to the survival of this microorganism in a wide variety of environmental niches. Here, we constructed multiple mutant strains of P. aeruginosa that express only one aerobic terminal oxidase to investigate the enzymatic characteristics and in vivo function of each enzyme. The K m values of Cyo, CIO, and aa 3 for oxygen were similar and were 1 order of magnitude higher than those of cbb 3 -1 and cbb 3 -2, indicating that Cyo, CIO, and aa 3 are low-affinity enzymes and that cbb 3 -1 and cbb 3 -2 are high-affinity enzymes. Although cbb 3 -1 and cbb 3 -2 exhibited different expression patterns in response to oxygen concentration, they had similar K m values for oxygen. Both cbb 3 -1 and cbb 3 -2 utilized cytochrome c 4 as the main electron donor under normal growth conditions. The electron transport chains terminated by cbb 3 -1 and cbb 3 -2 generate a proton gradient across the cell membrane with similar efficiencies. The electron transport chain of aa 3 had the highest proton translocation efficiency, whereas that of CIO had the lowest efficiency. The enzymatic properties of the terminal oxidases reported here are partially in agreement with their regulatory patterns and may explain the environmental adaptability and versatility of P. aeruginosa.

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Pseudomonas aeruginosa RoxR, a response regulator related to Rhodobacter sphaeroides PrrA, activates expression of the cyanide‐insensitive terminal oxidase

Cited by 67 publications

References 65 publications

The Effect of a Cell-to-Cell Communication Molecule, Pseudomonas Quinolone Signal (PQS), Produced by P. aeruginosa on Other Bacterial Species

The Effect of a Cell-to-Cell Communication Molecule, Pseudomonas Quinolone Signal (PQS), Produced by P. aeruginosa on Other Bacterial Species

Regulation of expression of the cyanide-insensitive terminal oxidase in Pseudomonas aeruginosa

Enzymatic Characterization and In Vivo Function of Five Terminal Oxidases in Pseudomonas aeruginosa

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