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Infection and Immunity, December 2009, p. 5631-5639, Vol. 77, No. 12
0019-9567/09/$08.00+0     doi:10.1128/IAI.00755-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

Instantaneous Within-Patient Diversity of Pseudomonas aeruginosa Quorum-Sensing Populations from Cystic Fibrosis Lung Infections {triangledown} ,{dagger}

Cara N. Wilder,1 Gopal Allada,2 and Martin Schuster1*

Department of Microbiology, Oregon State University, Corvallis, Oregon 97331,1 Pulmonary & Critical Care, Oregon Health & Science University, Portland, Oregon 972392

Received 2 July 2009/ Returned for modification 20 August 2009/ Accepted 27 September 2009

In the opportunistic pathogen Pseudomonas aeruginosa, acyl-homoserine lactone (acyl-HSL) quorum sensing (QS) regulates biofilm formation and expression of many extracellular virulence factors. Curiously, QS-deficient variants, often carrying mutations in the central QS regulator LasR, are frequently isolated from infections, particularly from cystic fibrosis (CF) lung infections. Very little is known about the proportion and diversity of these QS variants in individual infections. Such information is desirable to better understand the selective forces that drive the evolution of QS phenotypes, including social cheating and innate (nonsocial) benefits. To obtain insight into the instantaneous within-patient diversity of QS, we assayed a panel of 135 concurrent P. aeruginosa isolates from eight different adult CF patients (9 to 20 isolates per patient) for various QS-controlled phenotypes. Most patients contained complex mixtures of QS-proficient and -deficient isolates. Among all patients, deficiency in individual phenotypes ranged from 0 to about 90%. Acyl-HSL, sequencing, and complementation analyses of variants with global loss-of-function phenotypes revealed dependency upon the central QS circuitry genes lasR, lasI, and rhlI. Deficient and proficient isolates were clonally related, implying evolution from a common ancestor in vivo. Our results show that the diversity of QS types is high within and among patients, suggesting diverse selection pressures in the CF lung. A single selective mechanism, be it of a social or nonsocial nature, is unlikely to account for such heterogeneity. The observed diversity also shows that conclusions about the properties of P. aeruginosa QS populations in individual CF infections cannot be drawn from the characterization of one or a few selected isolates.

* Corresponding author. Mailing address: Department of Microbiology, 220 Nash Hall, Oregon State University, Corvallis, OR 97331. Phone: (541) 737-3496. Fax: (541) 737-0796. E-mail: martin.schuster{at}oregonstate.edu

{triangledown} Published ahead of print on 5 October 2009.

{dagger} Supplemental material for this article may be found at http://iai.asm.org/.

Editor: F. C. Fang

Infection and Immunity, December 2009, p. 5631-5639, Vol. 77, No. 12
0019-9567/09/$08.00+0     doi:10.1128/IAI.00755-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.





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