Involvement of Nitric Oxide in Biofilm Dispersal of Pseudomonas aeruginosa

Abstract

Bacterial biofilms at times undergo regulated and coordinated dispersal events where sessile biofilm cells convert to free-swimming, planktonic bacteria. In the opportunistic pathogen Pseudomonas aeruginosa, we previously observed that dispersal occurs concurrently with three interrelated processes within mature biofilms: (i) production of oxidative or nitrosative stress-inducing molecules inside biofilm structures, (ii) bacteriophage induction, and (iii) cell lysis. Here we examine whether specific reactive oxygen or nitrogen intermediates play a role in cell dispersal from P. aeruginosa biofilms. We demonstrate the involvement of anaerobic respiration processes in P. aeruginosa biofilm dispersal and show that nitric oxide (NO), used widely as a signaling molecule in biological systems, causes dispersal of P. aeruginosa biofilm bacteria. Dispersal was induced with low, sublethal concentrations (25 to 500 nM) of the NO donor sodium nitroprusside (SNP). Moreover, a P. aeruginosa mutant lacking the only enzyme capable of generating metabolic NO through anaerobic respiration (nitrite reductase, ⌬nirS) did not disperse, whereas a NO reductase mutant (⌬norCB) exhibited greatly enhanced dispersal. Strategies to induce biofilm dispersal are of interest due to their potential to prevent biofilms and biofilm-related infections. We observed that exposure to SNP (500 nM) greatly enhanced the efficacy of antimicrobial compounds (tobramycin, hydrogen peroxide, and sodium dodecyl sulfate) in the removal of established P. aeruginosa biofilms from a glass surface. Combined exposure to both NO and antimicrobial agents may therefore offer a novel strategy to control preestablished, persistent P. aeruginosa biofilms and biofilm-related infections.

Endogenous nitric oxide regulates the recovery of the radiation-resistant bacterium Deinococcus radiodurans from exposure to UV light

“…In mammals and other higher organisms, NO participates in a large number of processes, including protection against pathogens, regulation of vascular tension, hormone release, and neuronal signaling (3,4). In bacteria, NO is a key intermediate in nitrate respiration (denitrification), and has recently been shown to act as a regulatory signal for cell dispersal and nitrosative stress responses (5,6). In mammals, NO is produced from the oxidation of L-arginine (L-arg) to L-citrulline and is catalyzed by the heme-containing NO synthases (NOSs).…”

Dispersion by Pseudomonas aeruginosa requires an unusual posttranslational modification of BdlA

“…In contrast, dispersion is the terminal stage of biofilm development, during which bacteria evacuate a mature biofilm and transition to a planktonic state. Biofilm dispersion can be induced by a variety of environmental cues, including changes in growth medium composition, pH, oxygen, and carbon concentrations, exposure to heavy metals and nitric oxide, exposure to the polysaccharide degrading enzyme dispersin B, and self-synthesized signaling molecules such as cis-2-decenoic acid (1)(2)(3)(4)(5)(6)(7)(8)(9). Dispersed cells are characterized by distinct gene expression and protein production patterns and increased susceptibility to antimicrobial agents compared with their sessile counterparts (2,(10)(11)(12).…”

Antibiofilm activity substances derived from coral symbiotic bacterial extract inhibit biofouling by the model strainPseudomonas aeruginosaPAO1

“…The latter are being increasingly recognized for their important roles in the fouling process, and inhibitors of biofilm formation or interference with bacterial signalling processes can mitigate the development of biofilm or even lead to biofilm decline without any toxic effects on the microbes (Deziel et al ., 2001). For example, nitric oxide (NO), an intracellular signalling molecule, has been shown to induce a reduction in biofilm (Barraud et al ., 2006). …”