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Research Article

Static Growth Promotes PrrF and 2-Alkyl-4(1H)-Quinolone Regulation of Type VI Secretion Protein Expression in Pseudomonas aeruginosa

Luke K. Brewer, Weiliang Huang, Brandy J. Hackert, Maureen A. Kane, Amanda G. Oglesby
Laurie E. Comstock, Editor
Luke K. Brewer
aUniversity of Maryland, Baltimore, School of Pharmacy, Department of Pharmaceutical Sciences, Baltimore, Maryland, USA
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Weiliang Huang
aUniversity of Maryland, Baltimore, School of Pharmacy, Department of Pharmaceutical Sciences, Baltimore, Maryland, USA
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Brandy J. Hackert
aUniversity of Maryland, Baltimore, School of Pharmacy, Department of Pharmaceutical Sciences, Baltimore, Maryland, USA
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Maureen A. Kane
aUniversity of Maryland, Baltimore, School of Pharmacy, Department of Pharmaceutical Sciences, Baltimore, Maryland, USA
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Amanda G. Oglesby
aUniversity of Maryland, Baltimore, School of Pharmacy, Department of Pharmaceutical Sciences, Baltimore, Maryland, USA
bUniversity of Maryland, School of Medicine, Department of Microbiology and Immunology, Baltimore, Maryland, USA
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Laurie E. Comstock
Brigham and Women’s Hospital/Harvard Medical School
Roles: Editor
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DOI: 10.1128/JB.00416-20
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ABSTRACT

Pseudomonas aeruginosa is an opportunistic pathogen that is frequently associated with both acute and chronic infections. P. aeruginosa possesses a complex regulatory network that modulates nutrient acquisition and virulence, but our knowledge of these networks is largely based on studies with shaking cultures, which are not likely representative of conditions during infection. Here, we provide proteomic, metabolic, and genetic evidence that regulation by iron, a critical metallonutrient, is altered in static P. aeruginosa cultures. Specifically, we observed a loss of iron-induced expression of proteins for oxidative phosphorylation, tricarboxylic acid (TCA) cycle metabolism under static conditions. Moreover, we identified type VI secretion as a target of iron regulation in P. aeruginosa cells under static but not shaking conditions, and we present evidence that this regulation occurs via PrrF small regulatory RNA (sRNA)-dependent production of 2-alkyl-4(1H)-quinolone metabolites. These results yield new iron regulation paradigms in an important opportunistic pathogen and highlight the need to redefine iron homeostasis in static microbial communities.

IMPORTANCE Host-mediated iron starvation is a broadly conserved signal for microbial pathogens to upregulate expression of virulence traits required for successful infection. Historically, global iron regulatory studies in microorganisms have been conducted in shaking cultures to ensure culture homogeneity, yet these conditions are likely not reflective of growth during infection. Pseudomonas aeruginosa is a well-studied opportunistic pathogen and model organism for iron regulatory studies. Iron homeostasis is maintained through the Fur protein and PrrF small regulatory sRNAs, the functions of which are highly conserved in many other bacterial species. In the current study, we examined how static growth affects the known iron and PrrF regulons of P. aeruginosa, leading to the discovery of novel PrrF-regulated virulence processes. This study demonstrates how the utilization of distinct growth models can enhance our understanding of basic physiological processes that may also affect pathogenesis.

FOOTNOTES

    • Received 21 July 2020.
    • Accepted 29 September 2020.
    • Accepted manuscript posted online 5 October 2020.
  • Supplemental material is available online only.

  • Copyright © 2020 American Society for Microbiology.

All Rights Reserved.

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Static Growth Promotes PrrF and 2-Alkyl-4(1H)-Quinolone Regulation of Type VI Secretion Protein Expression in Pseudomonas aeruginosa
Luke K. Brewer, Weiliang Huang, Brandy J. Hackert, Maureen A. Kane, Amanda G. Oglesby
Journal of Bacteriology Nov 2020, 202 (24) e00416-20; DOI: 10.1128/JB.00416-20

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Static Growth Promotes PrrF and 2-Alkyl-4(1H)-Quinolone Regulation of Type VI Secretion Protein Expression in Pseudomonas aeruginosa
Luke K. Brewer, Weiliang Huang, Brandy J. Hackert, Maureen A. Kane, Amanda G. Oglesby
Journal of Bacteriology Nov 2020, 202 (24) e00416-20; DOI: 10.1128/JB.00416-20
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KEYWORDS

PrrF
Pseudomonas aeruginosa
type 6 secretion
alkyl-quinolones
iron regulation

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