<italic toggle="yes">Pseudomonas aeruginosa</italic> Alginate Overproduction Promotes Coexistence with <italic toggle="yes">Staphylococcus aureus</italic> in a Model of Cystic Fibrosis Respiratory Infection

ABSTRACT While complex intra- and interspecies microbial community dynamics are apparent during chronic infections and likely alter patient health outcomes, our understanding of these interactions is currently limited. For example, Pseudomonas aeruginosa and Staphylococcus aureus are often found to...

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Autores principales:	Dominique H. Limoli, Gregory B. Whitfield, Tomoe Kitao, Melissa L. Ivey, Michael R. Davis, Nora Grahl, Deborah A. Hogan, Laurence G. Rahme, P. Lynne Howell, George A. O’Toole, Joanna B. Goldberg
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	Pseudomonas aeruginosa Staphylococcus aureus biofilm cystic fibrosis mucoid polymicrobial Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/c38afdeb9d90436fab29b532827b078f
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spelling	oai:doaj.org-article:c38afdeb9d90436fab29b532827b078f2021-11-15T15:50:59Z<italic toggle="yes">Pseudomonas aeruginosa</italic> Alginate Overproduction Promotes Coexistence with <italic toggle="yes">Staphylococcus aureus</italic> in a Model of Cystic Fibrosis Respiratory Infection10.1128/mBio.00186-172150-7511https://doaj.org/article/c38afdeb9d90436fab29b532827b078f2017-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00186-17https://doaj.org/toc/2150-7511ABSTRACT While complex intra- and interspecies microbial community dynamics are apparent during chronic infections and likely alter patient health outcomes, our understanding of these interactions is currently limited. For example, Pseudomonas aeruginosa and Staphylococcus aureus are often found to coinfect the lungs of patients with cystic fibrosis (CF), yet these organisms compete under laboratory conditions. Recent observations that coinfection correlates with decreased health outcomes necessitate we develop a greater understanding of these interbacterial interactions. In this study, we tested the hypothesis that P. aeruginosa and/or S. aureus adopts phenotypes that allow coexistence during infection. We compared competitive interactions of P. aeruginosa and S. aureus isolates from mono- or coinfected CF patients employing in vitro coculture models. P. aeruginosa isolates from monoinfected patients were more competitive toward S. aureus than P. aeruginosa isolates from coinfected patients. We also observed that the least competitive P. aeruginosa isolates possessed a mucoid phenotype. Mucoidy occurs upon constitutive activation of the sigma factor AlgT/U, which regulates synthesis of the polysaccharide alginate and dozens of other secreted factors, including some previously described to kill S. aureus. Here, we show that production of alginate in mucoid strains is sufficient to inhibit anti-S. aureus activity independent of activation of the AlgT regulon. Alginate reduces production of siderophores, 2-heptyl-4-hydroxyquinolone-N-oxide (HQNO), and rhamnolipids—each required for efficient killing of S. aureus. These studies demonstrate alginate overproduction may be an important factor driving P. aeruginosa coinfection with S. aureus. IMPORTANCE Numerous deep-sequencing studies have revealed the microbial communities present during respiratory infections in cystic fibrosis (CF) patients are diverse, complex, and dynamic. We now face the challenge of determining the influence of these community dynamics on patient health outcomes and identifying candidate targets to modulate these interactions. We make progress toward this goal by determining that the polysaccharide alginate produced by mucoid strains of P. aeruginosa is sufficient to inhibit multiple secreted antimicrobial agents produced by this organism. Importantly, these secreted factors are required to outcompete S. aureus, when the microbes are grown in coculture; thus we propose a mechanism whereby mucoid P. aeruginosa can coexist with S. aureus. Finally, the approach used here can serve as a platform to investigate the interactions among other CF pathogens.Dominique H. LimoliGregory B. WhitfieldTomoe KitaoMelissa L. IveyMichael R. DavisNora GrahlDeborah A. HoganLaurence G. RahmeP. Lynne HowellGeorge A. O’TooleJoanna B. GoldbergAmerican Society for MicrobiologyarticlePseudomonas aeruginosaStaphylococcus aureusbiofilmcystic fibrosismucoidpolymicrobialMicrobiologyQR1-502ENmBio, Vol 8, Iss 2 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	Pseudomonas aeruginosa Staphylococcus aureus biofilm cystic fibrosis mucoid polymicrobial Microbiology QR1-502
spellingShingle	Pseudomonas aeruginosa Staphylococcus aureus biofilm cystic fibrosis mucoid polymicrobial Microbiology QR1-502 Dominique H. Limoli Gregory B. Whitfield Tomoe Kitao Melissa L. Ivey Michael R. Davis Nora Grahl Deborah A. Hogan Laurence G. Rahme P. Lynne Howell George A. O’Toole Joanna B. Goldberg <italic toggle="yes">Pseudomonas aeruginosa</italic> Alginate Overproduction Promotes Coexistence with <italic toggle="yes">Staphylococcus aureus</italic> in a Model of Cystic Fibrosis Respiratory Infection
description	ABSTRACT While complex intra- and interspecies microbial community dynamics are apparent during chronic infections and likely alter patient health outcomes, our understanding of these interactions is currently limited. For example, Pseudomonas aeruginosa and Staphylococcus aureus are often found to coinfect the lungs of patients with cystic fibrosis (CF), yet these organisms compete under laboratory conditions. Recent observations that coinfection correlates with decreased health outcomes necessitate we develop a greater understanding of these interbacterial interactions. In this study, we tested the hypothesis that P. aeruginosa and/or S. aureus adopts phenotypes that allow coexistence during infection. We compared competitive interactions of P. aeruginosa and S. aureus isolates from mono- or coinfected CF patients employing in vitro coculture models. P. aeruginosa isolates from monoinfected patients were more competitive toward S. aureus than P. aeruginosa isolates from coinfected patients. We also observed that the least competitive P. aeruginosa isolates possessed a mucoid phenotype. Mucoidy occurs upon constitutive activation of the sigma factor AlgT/U, which regulates synthesis of the polysaccharide alginate and dozens of other secreted factors, including some previously described to kill S. aureus. Here, we show that production of alginate in mucoid strains is sufficient to inhibit anti-S. aureus activity independent of activation of the AlgT regulon. Alginate reduces production of siderophores, 2-heptyl-4-hydroxyquinolone-N-oxide (HQNO), and rhamnolipids—each required for efficient killing of S. aureus. These studies demonstrate alginate overproduction may be an important factor driving P. aeruginosa coinfection with S. aureus. IMPORTANCE Numerous deep-sequencing studies have revealed the microbial communities present during respiratory infections in cystic fibrosis (CF) patients are diverse, complex, and dynamic. We now face the challenge of determining the influence of these community dynamics on patient health outcomes and identifying candidate targets to modulate these interactions. We make progress toward this goal by determining that the polysaccharide alginate produced by mucoid strains of P. aeruginosa is sufficient to inhibit multiple secreted antimicrobial agents produced by this organism. Importantly, these secreted factors are required to outcompete S. aureus, when the microbes are grown in coculture; thus we propose a mechanism whereby mucoid P. aeruginosa can coexist with S. aureus. Finally, the approach used here can serve as a platform to investigate the interactions among other CF pathogens.
format	article
author	Dominique H. Limoli Gregory B. Whitfield Tomoe Kitao Melissa L. Ivey Michael R. Davis Nora Grahl Deborah A. Hogan Laurence G. Rahme P. Lynne Howell George A. O’Toole Joanna B. Goldberg
author_facet	Dominique H. Limoli Gregory B. Whitfield Tomoe Kitao Melissa L. Ivey Michael R. Davis Nora Grahl Deborah A. Hogan Laurence G. Rahme P. Lynne Howell George A. O’Toole Joanna B. Goldberg
author_sort	Dominique H. Limoli
title	<italic toggle="yes">Pseudomonas aeruginosa</italic> Alginate Overproduction Promotes Coexistence with <italic toggle="yes">Staphylococcus aureus</italic> in a Model of Cystic Fibrosis Respiratory Infection
title_short	<italic toggle="yes">Pseudomonas aeruginosa</italic> Alginate Overproduction Promotes Coexistence with <italic toggle="yes">Staphylococcus aureus</italic> in a Model of Cystic Fibrosis Respiratory Infection
title_full	<italic toggle="yes">Pseudomonas aeruginosa</italic> Alginate Overproduction Promotes Coexistence with <italic toggle="yes">Staphylococcus aureus</italic> in a Model of Cystic Fibrosis Respiratory Infection
title_fullStr	<italic toggle="yes">Pseudomonas aeruginosa</italic> Alginate Overproduction Promotes Coexistence with <italic toggle="yes">Staphylococcus aureus</italic> in a Model of Cystic Fibrosis Respiratory Infection
title_full_unstemmed	<italic toggle="yes">Pseudomonas aeruginosa</italic> Alginate Overproduction Promotes Coexistence with <italic toggle="yes">Staphylococcus aureus</italic> in a Model of Cystic Fibrosis Respiratory Infection
title_sort	<italic toggle="yes">pseudomonas aeruginosa</italic> alginate overproduction promotes coexistence with <italic toggle="yes">staphylococcus aureus</italic> in a model of cystic fibrosis respiratory infection
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/c38afdeb9d90436fab29b532827b078f
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<italic toggle="yes">Pseudomonas aeruginosa</italic> Alginate Overproduction Promotes Coexistence with <italic toggle="yes">Staphylococcus aureus</italic> in a Model of Cystic Fibrosis Respiratory Infection

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