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      The role of multispecies social interactions in shaping Pseudomonas aeruginosa pathogenicity in the cystic fibrosis lung

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          Abstract

          Pseudomonas aeruginosa is a major pathogen in the lungs of cystic fibrosis (CF) patients. However, it is now recognised that a diverse microbial community exists in the airways comprising aerobic and anaerobic bacteria as well as fungi and viruses. This rich soup of microorganisms provides ample opportunity for interspecies interactions, particularly when considering secreted compounds. Here, we discuss how P. aeruginosa-secreted products can have community-wide effects, with the potential to ultimately shape microbial community dynamics within the lung. We focus on three well-studied traits associated with worsening clinical outcome in CF: phenazines, siderophores and biofilm formation, and discuss how secretions can shape interactions between P. aeruginosa and other commonly encountered members of the lung microbiome: Staphylococcus aureus, the Burkholderia cepacia complex, Candida albicans and Aspergillus fumigatus. These interactions may shape the evolutionary trajectory of P. aeruginosa while providing new opportunities for therapeutic exploitation of the CF lung microbiome.

          Abstract

          How social interactions among microbes living in the cystic fibrosis lung may be influencing patient health.

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          Most cited references118

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          Pseudomonas aeruginosa Evolutionary Adaptation and Diversification in Cystic Fibrosis Chronic Lung Infections

          Pseudomonas aeruginosa populations undergo a characteristic evolutionary adaptation during chronic infection of the cystic fibrosis (CF) lung, including reduced production of virulence factors, transition to a biofilm-associated lifestyle, and evolution of high-level antibiotic resistance. Populations of P. aeruginosa in chronic CF lung infections typically exhibit high phenotypic diversity, including for clinically important traits such as antibiotic resistance and toxin production, and this diversity is dynamic over time, making accurate diagnosis and treatment challenging. Population genomics studies reveal extensive genetic diversity within patients, including for transmissible strains the coexistence of highly divergent lineages acquired by patient-to-patient transmission. The inherent spatial structure and spatial heterogeneity of selection in the CF lung appears to play a key role in driving P. aeruginosa diversification.
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            Adaptation of Pseudomonas aeruginosa to the cystic fibrosis airway: an evolutionary perspective.

            The airways of patients with cystic fibrosis (CF) are nearly always infected with many different microorganisms. This environment offers warm, humid and nutrient-rich conditions, but is also stressful owing to frequent antibiotic therapy and the host immune response. Pseudomonas aeruginosa is commonly isolated from the airways of patients with CF, where it most often establishes chronic infections that usually persist for the rest of the lives of the patients. This bacterium is a major cause of mortality and morbidity and has therefore been studied intensely. Here, we discuss how P. aeruginosa evolves from a state of early, recurrent intermittent colonization of the airways of patients with CF to a chronic infection state, and how this process offers opportunities to study bacterial evolution in natural environments. We believe that such studies are valuable not only for our understanding of bacterial evolution but also for the future development of new therapeutic strategies to treat severe chronic infections.
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              Biofilm infections, their resilience to therapy and innovative treatment strategies.

              Biofilm formation of microorganisms causes persistent tissue and foreign body infections resistant to treatment with antimicrobial agents. Up to 80% of human bacterial infections are biofilm associated; such infections are most frequently caused by Staphylococcus epidermidis, Pseudomonas aeruginosa, Staphylococcus aureus and Enterobacteria such as Escherichia coli. The accurate diagnosis of biofilm infections is often difficult, which prevents the appropriate choice of treatment. As biofilm infections significantly contribute to patient morbidity and substantial healthcare costs, novel strategies to treat these infections are urgently required. Nucleotide second messengers, c-di-GMP, (p)ppGpp and potentially c-di-AMP, are major regulators of biofilm formation and associated antibiotic tolerance. Consequently, different components of these signalling networks might be appropriate targets for antibiofilm therapy in combination with antibiotic treatment strategies. In addition, cyclic di-nucleotides are microbial-associated molecular patterns with an almost universal presence. Their conserved structures sensed by the eukaryotic host have a widespread effect on the immune system. Thus, cyclic di-nucleotides are also potential immunotherapeutic agents to treat antibiotic-resistant bacterial infections. © 2012 The Association for the Publication of the Journal of Internal Medicine.
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                Author and article information

                Journal
                FEMS Microbiol Lett
                FEMS Microbiol. Lett
                femsle
                FEMS Microbiology Letters
                Oxford University Press
                0378-1097
                1574-6968
                13 July 2017
                August 2017
                13 July 2017
                : 364
                : 15
                : fnx128
                Affiliations
                [1 ]Center for Adaptation to a Changing Environment (ACE), ETH Zürich, 8092 Zürich, Switzerland
                [2 ]Department of Biology, University of York, Wentworth Way, York YO10 5DD, UK
                [3 ]Institute of Infection and Global Health, University of Liverpool, 8 West Derby Street, Liverpool L69 7B3, UK
                Author notes
                [* ] Corresponding author: Center for Adaptation to a Changing Environment (ACE), ETH Zürich, CHN G35.1, Universitätstrasse 16, 8092 Zürich, Switzerland. Tel: +41 44 632 8494; E-mail: siobhan.obrien@ 123456env.ethz.ch
                Article
                fnx128
                10.1093/femsle/fnx128
                5812498
                28859314
                42947cd2-4ec0-423a-b565-fb1e91dcfde1
                © FEMS 2017.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 31 March 2017
                : 11 July 2017
                Page count
                Pages: 10
                Categories
                Minireview
                Pathogens & Pathogenicity
                Editor's Choice
                Minireview

                Microbiology & Virology
                interspecific interactions: multispecies interactions,microbiome,cystic fibrosis,pseudomonas aeruginosa,microbial communities

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