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      In vivo and In vitro Interactions between Pseudomonas aeruginosa and Staphylococcus spp.

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          Abstract

          The significance of polymicrobial infections is increasingly being recognized especially in a biofilm context wherein multiple bacterial species—including both potential pathogens and members of the commensal flora—communicate, cooperate, and compete with each other. Two important bacterial pathogens that have developed a complex network of evasion, counter-inhibition, and subjugation in their battle for space and nutrients are Pseudomonas aeruginosa and Staphylococcus aureus. Their strain- and environment-specific interactions, for instance in the cystic fibrosis lung or in wound infections, show severe competition that is generally linked to worse patient outcomes. For instance, the extracellular factors secreted by P. aeruginosa have been shown to subjugate S. aureus to persist as small colony variants (SCVs). On the other hand, data also exist where S. aureus inhibits biofilm formation by P. aeruginosa but also protects the pathogen by inhibiting its phagocytosis. Interestingly, such interspecies interactions differ between the planktonic and biofilm phenotype, with the extracellular matrix components of the latter likely being a key, and largely underexplored, influence. This review attempts to understand the complex relationship between P. aeruginosa and Staphylococcus spp., focusing on S. aureus, that not only is interesting from the bacterial evolution point of view, but also has important consequences for our understanding of the disease pathogenesis for better patient management.

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          The multiple signaling systems regulating virulence in Pseudomonas aeruginosa.

          Cell-to-cell communication is a major process that allows bacteria to sense and coordinately react to the fluctuating conditions of the surrounding environment. In several pathogens, this process triggers the production of virulence factors and/or a switch in bacterial lifestyle that is a major determining factor in the outcome and severity of the infection. Understanding how bacteria control these signaling systems is crucial to the development of novel antimicrobial agents capable of reducing virulence while allowing the immune system of the host to clear bacterial infection, an approach likely to reduce the selective pressures for development of resistance. We provide here an up-to-date overview of the molecular basis and physiological implications of cell-to-cell signaling systems in Gram-negative bacteria, focusing on the well-studied bacterium Pseudomonas aeruginosa. All of the known cell-to-cell signaling systems in this bacterium are described, from the most-studied systems, i.e., N-acyl homoserine lactones (AHLs), the 4-quinolones, the global activator of antibiotic and cyanide synthesis (GAC), the cyclic di-GMP (c-di-GMP) and cyclic AMP (cAMP) systems, and the alarmones guanosine tetraphosphate (ppGpp) and guanosine pentaphosphate (pppGpp), to less-well-studied signaling molecules, including diketopiperazines, fatty acids (diffusible signal factor [DSF]-like factors), pyoverdine, and pyocyanin. This overview clearly illustrates that bacterial communication is far more complex than initially thought and delivers a clear distinction between signals that are quorum sensing dependent and those relying on alternative factors for their production.
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            Quorum sensing and environmental adaptation in Pseudomonas aeruginosa: a tale of regulatory networks and multifunctional signal molecules.

            Bacteria employ sophisticated cell-to-cell communication or 'quorum sensing' (QS) systems for promoting collective behaviours that depend on the actions of one or more chemically distinct diffusible signal molecules. As determinants of cell population density, multiple QS systems are often integrated with each other and within global regulatory networks and subject to the prevailing environmental conditions as well as the presence and activities of other organisms. QS signal molecules, although largely considered as effectors of QS-dependent gene expression are also emerging as multifunctional molecules that influence life, development and death in single and mixed microbial populations and impact significantly the outcome of host-pathogen interactions.
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              Analysis of Pseudomonas aeruginosa 4-hydroxy-2-alkylquinolines (HAQs) reveals a role for 4-hydroxy-2-heptylquinoline in cell-to-cell communication.

              Bacterial communities use "quorum sensing" (QS) to coordinate their population behavior through the action of extracellular signal molecules, such as the N-acyl-l-homoserine lactones (AHLs). The versatile and ubiquitous opportunistic pathogen Pseudomonas aeruginosa is a well-studied model for AHL-mediated QS. This species also produces an intercellular signal distinct from AHLs, 3,4-dihydroxy-2-heptylquinoline (PQS), which belongs to a family of poorly characterized 4-hydroxy-2-alkylquinolines (HAQs) previously identified for their antimicrobial activity. Here we use liquid chromatography (LC)/MS, genetics, and whole-genome expression to investigate the structure, biosynthesis, regulation, and activity of HAQs. We show that the pqsA-E operon encodes enzymes that catalyze the biosynthesis of five distinct classes of HAQs, and establish the sequence of synthesis of these compounds, which include potent cytochrome inhibitors and antibiotics active against human commensal and pathogenic bacteria. We find that anthranilic acid, the product of the PhnAB synthase, is the primary precursor of HAQs and that the HAQ congener 4-hydroxy-2-heptylquinoline (HHQ) is the direct precursor of the PQS signaling molecule. Significantly, whereas phnAB and pqsA-E are positively regulated by the virulence-associated transcription factor MvfR, which is also required for the expression of several QS-regulated genes, the conversion of HHQ to PQS is instead controlled by LasR. Finally, our results reveal that HHQ is itself both released from, and taken up by, bacterial cells where it is converted into PQS, suggesting that it functions as a messenger molecule in a cell-to-cell communication pathway. HAQ signaling represents a potential target for the pharmacological intervention of P. aeruginosa-mediated infections.
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                Author and article information

                Contributors
                Journal
                Front Cell Infect Microbiol
                Front Cell Infect Microbiol
                Front. Cell. Infect. Microbiol.
                Frontiers in Cellular and Infection Microbiology
                Frontiers Media S.A.
                2235-2988
                03 April 2017
                2017
                : 7
                : 106
                Affiliations
                [1] 1Laboratory of Medical Microbiology, Vaccine and Infectious Disease Institute, University of Antwerp Wilrijk, Belgium
                [2] 2Molecular Pathology Group, Cell Biology and Histology, University of Antwerp Wilrijk, Belgium
                Author notes

                Edited by: Ghassan M. Matar, American University of Beirut, Lebanon

                Reviewed by: Robert J. C. McLean, Texas State University, USA; Sarah Maddocks, Cardiff Metropolitan University, UK

                *Correspondence: Surbhi Malhotra-Kumar surbhi.malhotra@ 123456uantwerpen.be
                Article
                10.3389/fcimb.2017.00106
                5376567
                28421166
                e16c6ced-49c8-4f65-90a7-cd6e5acf318f
                Copyright © 2017 Hotterbeekx, Kumar-Singh, Goossens and Malhotra-Kumar.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 30 January 2017
                : 16 March 2017
                Page count
                Figures: 3, Tables: 0, Equations: 0, References: 86, Pages: 13, Words: 10166
                Funding
                Funded by: Fonds Wetenschappelijk Onderzoek 10.13039/501100003130
                Award ID: G.0513.12
                Funded by: IMI
                Award ID: 115737-2
                Categories
                Microbiology
                Review

                Infectious disease & Microbiology
                microbial interactions,s. aureus,quorum-sensing,cystic fibrosis,biofilm

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