Pseudomonas aeruginosa alkyl quinolone response is dampened by Enterococcus faecalis

ABSTRACT The bacterium Pseudomonas aeruginosa is an opportunistic pathogen that can cause lung, skin, wound, joint, urinary tract, and eye infections. While P. aeruginosa is known to exhibit a robust competitive response toward other bacterial species, this bacterium is frequently identified in poly...

Full description

Saved in:
Bibliographic Details
Main Authors: Maggie M. Fink, Abigail A. Weaver, Dharmeshkumar Parmar, Jon E. Paczkowski, Lingyun Li, Maggie K. Klaers, Ella A. Junker, Elizabeth A. Jarocki, Jonathan V. Sweedler, Joshua D. Shrout
Format: Article
Language:English
Published: American Society for Microbiology 2025-02-01
Series:mBio
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/mbio.03320-24
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1832096548131962880
author Maggie M. Fink
Abigail A. Weaver
Dharmeshkumar Parmar
Jon E. Paczkowski
Lingyun Li
Maggie K. Klaers
Ella A. Junker
Elizabeth A. Jarocki
Jonathan V. Sweedler
Joshua D. Shrout
author_facet Maggie M. Fink
Abigail A. Weaver
Dharmeshkumar Parmar
Jon E. Paczkowski
Lingyun Li
Maggie K. Klaers
Ella A. Junker
Elizabeth A. Jarocki
Jonathan V. Sweedler
Joshua D. Shrout
author_sort Maggie M. Fink
collection DOAJ
description ABSTRACT The bacterium Pseudomonas aeruginosa is an opportunistic pathogen that can cause lung, skin, wound, joint, urinary tract, and eye infections. While P. aeruginosa is known to exhibit a robust competitive response toward other bacterial species, this bacterium is frequently identified in polymicrobial infections where multiple species survive. For example, in prosthetic joint infections, P. aeruginosa can be identified along with other pathogenic bacteria including Staphylococcus aureus, Enterococcus faecalis, and Corynebacterium striatum. Here, we have explored the survival and behavior of such microbes and find that E. faecalis readily survives culturing with P. aeruginosa while other tested species do not. In each of the tested conditions, E. faecalis growth remained unchanged by the presence of P. aeruginosa, indicating a unique mutualistic interaction between the two species. We find that E. faecalis proximity leads P. aeruginosa to attenuate competitive behaviors as exemplified by reduced production of Pseudomonas quinolone signal and pyocyanin. Reduced alkyl quinolones are important to E. faecalis as these will grow in supernatant from a quinolone mutant but not P. aeruginosa wild-type in planktonic culture. The reduced pyocyanin production of P. aeruginosa is attributable to production of ornithine by E. faecalis, which we recapitulate by adding exogenous ornithine to P. aeruginosa monocultures. Similarly, co-culture with an ornithine-deficient strain of E. faecalis leads P. aeruginosa to yield near monoculture amounts of pyocyanin. Here, we directly demonstrate how notorious pathogens such as P. aeruginosa might persist in polymicrobial infections under the influence of metabolites produced by other bacterial species.IMPORTANCEWhile we now appreciate that many infections are polymicrobial, we understand little of the specific actions between a given set of microbes to enable combinatorial survival and pathogenesis. The bacteria Pseudomonas aeruginosa and Enterococcus faecalis are both prevalent pathogens in wound, urinary tract, and bacteremic infections. While P. aeruginosa often kills other species in standard laboratory culture conditions, we present here that E. faecalis can be reliably co-cultured with P. aeruginosa. We specifically detail that ornithine produced by E. faecalis reduces the Pseudomonas quinolone signal response of P. aeruginosa. This reduction of the Pseudomonas quinolone signal response aids E. faecalis growth.
format Article
id doaj-art-e31bc6fe30b54178b18d5a2574f77867
institution Kabale University
issn 2150-7511
language English
publishDate 2025-02-01
publisher American Society for Microbiology
record_format Article
series mBio
spelling doaj-art-e31bc6fe30b54178b18d5a2574f778672025-02-05T14:00:48ZengAmerican Society for MicrobiologymBio2150-75112025-02-0116210.1128/mbio.03320-24Pseudomonas aeruginosa alkyl quinolone response is dampened by Enterococcus faecalisMaggie M. Fink0Abigail A. Weaver1Dharmeshkumar Parmar2Jon E. Paczkowski3Lingyun Li4Maggie K. Klaers5Ella A. Junker6Elizabeth A. Jarocki7Jonathan V. Sweedler8Joshua D. Shrout9Department of Biological Sciences, University of Notre Dame, Notre Dame, Indiana, USADepartment of Civil and Environmental Engineering and Earth Sciences, University of Notre Dame, Notre Dame, Indiana, USADepartment of Chemistry and Beckman Institute for Advanced Science and Technology, University of Illinois at Urbana-Champaign, Urbana, Illinois, USADepartment of Biomedical Sciences, University at Albany, School of Public Health, Albany, New York, USADivision of Environmental Health Sciences, Wadsworth Center, New York State Department of Health, Albany, New York, USADepartment of Biological Sciences, University of Notre Dame, Notre Dame, Indiana, USADepartment of Civil and Environmental Engineering and Earth Sciences, University of Notre Dame, Notre Dame, Indiana, USADepartment of Civil and Environmental Engineering and Earth Sciences, University of Notre Dame, Notre Dame, Indiana, USADepartment of Chemistry and Beckman Institute for Advanced Science and Technology, University of Illinois at Urbana-Champaign, Urbana, Illinois, USADepartment of Biological Sciences, University of Notre Dame, Notre Dame, Indiana, USAABSTRACT The bacterium Pseudomonas aeruginosa is an opportunistic pathogen that can cause lung, skin, wound, joint, urinary tract, and eye infections. While P. aeruginosa is known to exhibit a robust competitive response toward other bacterial species, this bacterium is frequently identified in polymicrobial infections where multiple species survive. For example, in prosthetic joint infections, P. aeruginosa can be identified along with other pathogenic bacteria including Staphylococcus aureus, Enterococcus faecalis, and Corynebacterium striatum. Here, we have explored the survival and behavior of such microbes and find that E. faecalis readily survives culturing with P. aeruginosa while other tested species do not. In each of the tested conditions, E. faecalis growth remained unchanged by the presence of P. aeruginosa, indicating a unique mutualistic interaction between the two species. We find that E. faecalis proximity leads P. aeruginosa to attenuate competitive behaviors as exemplified by reduced production of Pseudomonas quinolone signal and pyocyanin. Reduced alkyl quinolones are important to E. faecalis as these will grow in supernatant from a quinolone mutant but not P. aeruginosa wild-type in planktonic culture. The reduced pyocyanin production of P. aeruginosa is attributable to production of ornithine by E. faecalis, which we recapitulate by adding exogenous ornithine to P. aeruginosa monocultures. Similarly, co-culture with an ornithine-deficient strain of E. faecalis leads P. aeruginosa to yield near monoculture amounts of pyocyanin. Here, we directly demonstrate how notorious pathogens such as P. aeruginosa might persist in polymicrobial infections under the influence of metabolites produced by other bacterial species.IMPORTANCEWhile we now appreciate that many infections are polymicrobial, we understand little of the specific actions between a given set of microbes to enable combinatorial survival and pathogenesis. The bacteria Pseudomonas aeruginosa and Enterococcus faecalis are both prevalent pathogens in wound, urinary tract, and bacteremic infections. While P. aeruginosa often kills other species in standard laboratory culture conditions, we present here that E. faecalis can be reliably co-cultured with P. aeruginosa. We specifically detail that ornithine produced by E. faecalis reduces the Pseudomonas quinolone signal response of P. aeruginosa. This reduction of the Pseudomonas quinolone signal response aids E. faecalis growth.https://journals.asm.org/doi/10.1128/mbio.03320-24Pseudomonas aeruginosaEnterococcus faecalisPseudomonas quinolone signalpyocyaninornithine
spellingShingle Maggie M. Fink
Abigail A. Weaver
Dharmeshkumar Parmar
Jon E. Paczkowski
Lingyun Li
Maggie K. Klaers
Ella A. Junker
Elizabeth A. Jarocki
Jonathan V. Sweedler
Joshua D. Shrout
Pseudomonas aeruginosa alkyl quinolone response is dampened by Enterococcus faecalis
mBio
Pseudomonas aeruginosa
Enterococcus faecalis
Pseudomonas quinolone signal
pyocyanin
ornithine
title Pseudomonas aeruginosa alkyl quinolone response is dampened by Enterococcus faecalis
title_full Pseudomonas aeruginosa alkyl quinolone response is dampened by Enterococcus faecalis
title_fullStr Pseudomonas aeruginosa alkyl quinolone response is dampened by Enterococcus faecalis
title_full_unstemmed Pseudomonas aeruginosa alkyl quinolone response is dampened by Enterococcus faecalis
title_short Pseudomonas aeruginosa alkyl quinolone response is dampened by Enterococcus faecalis
title_sort pseudomonas aeruginosa alkyl quinolone response is dampened by enterococcus faecalis
topic Pseudomonas aeruginosa
Enterococcus faecalis
Pseudomonas quinolone signal
pyocyanin
ornithine
url https://journals.asm.org/doi/10.1128/mbio.03320-24
work_keys_str_mv AT maggiemfink pseudomonasaeruginosaalkylquinoloneresponseisdampenedbyenterococcusfaecalis
AT abigailaweaver pseudomonasaeruginosaalkylquinoloneresponseisdampenedbyenterococcusfaecalis
AT dharmeshkumarparmar pseudomonasaeruginosaalkylquinoloneresponseisdampenedbyenterococcusfaecalis
AT jonepaczkowski pseudomonasaeruginosaalkylquinoloneresponseisdampenedbyenterococcusfaecalis
AT lingyunli pseudomonasaeruginosaalkylquinoloneresponseisdampenedbyenterococcusfaecalis
AT maggiekklaers pseudomonasaeruginosaalkylquinoloneresponseisdampenedbyenterococcusfaecalis
AT ellaajunker pseudomonasaeruginosaalkylquinoloneresponseisdampenedbyenterococcusfaecalis
AT elizabethajarocki pseudomonasaeruginosaalkylquinoloneresponseisdampenedbyenterococcusfaecalis
AT jonathanvsweedler pseudomonasaeruginosaalkylquinoloneresponseisdampenedbyenterococcusfaecalis
AT joshuadshrout pseudomonasaeruginosaalkylquinoloneresponseisdampenedbyenterococcusfaecalis