Spatiotemporal Distribution of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Alkyl Quinolones under Metabolic and Competitive Stress

ABSTRACT Pseudomonas aeruginosa is an opportunistic human pathogen important to diseases such as cystic fibrosis. P. aeruginosa has multiple quorum-sensing (QS) systems, one of which utilizes the signaling molecule 2-heptyl-3-hydroxy-4-quinolone (Pseudomonas quinolone signal [PQS]). Here, we use hyp...

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Autores principales:	Tianyuan Cao, Jonathan V. Sweedler, Paul W. Bohn, Joshua D. Shrout
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	PQS HQNO Staphylococcus aureus polymicrobial quorum sensing Raman spectroscopy Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/6bf1658522ff459eadfbfbad9137da65
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spelling	oai:doaj.org-article:6bf1658522ff459eadfbfbad9137da652021-11-15T15:30:50ZSpatiotemporal Distribution of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Alkyl Quinolones under Metabolic and Competitive Stress10.1128/mSphere.00426-202379-5042https://doaj.org/article/6bf1658522ff459eadfbfbad9137da652020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00426-20https://doaj.org/toc/2379-5042ABSTRACT Pseudomonas aeruginosa is an opportunistic human pathogen important to diseases such as cystic fibrosis. P. aeruginosa has multiple quorum-sensing (QS) systems, one of which utilizes the signaling molecule 2-heptyl-3-hydroxy-4-quinolone (Pseudomonas quinolone signal [PQS]). Here, we use hyperspectral Raman imaging to elucidate the spatiotemporal PQS distributions that determine how P. aeruginosa regulates surface colonization and its response to both metabolic stress and competition from other bacterial strains. These chemical imaging experiments illustrate the strong link between environmental challenges, such as metabolic stress caused by nutritional limitations or the presence of another bacterial species, and PQS signaling. Metabolic stress elicits a complex response in which limited nutrients induce the bacteria to produce PQS earlier, but the bacteria may also pause PQS production entirely if the nutrient concentration is too low. Separately, coculturing P. aeruginosa in the proximity of another bacterial species, or its culture supernatant, results in earlier production of PQS. However, these differences in PQS appearance are not observed for all alkyl quinolones (AQs) measured; the spatiotemporal response of 2-heptyl-4-hydroxyquinoline N-oxide (HQNO) is highly uniform for most conditions. These insights on the spatiotemporal distributions of quinolones provide additional perspective on the behavior of P. aeruginosa in response to different environmental cues. IMPORTANCE Alkyl quinolones (AQs), including Pseudomonas quinolone signal (PQS), made by the opportunistic pathogen Pseudomonas aeruginosa have been associated with both population density and stress. The regulation of AQ production is known to be complex, and the stimuli that modulate AQ responses are not fully clear. Here, we have used hyperspectral Raman chemical imaging to examine the temporal and spatial profiles of AQs exhibited by P. aeruginosa under several potentially stressful conditions. We found that metabolic stress, effected by carbon limitation, or competition stress, effected by proximity to other species, resulted in accelerated PQS production. This competition effect did not require cell-to-cell interaction, as evidenced by the fact that the addition of supernatants from either Escherichia coli or Staphylococcus aureus led to early appearance of PQS. Lastly, the fact that these modulations were observed for PQS but not for all AQs suggests a high level of complexity in AQ regulation that remains to be discerned.Tianyuan CaoJonathan V. SweedlerPaul W. BohnJoshua D. ShroutAmerican Society for MicrobiologyarticlePQSHQNOStaphylococcus aureuspolymicrobialquorum sensingRaman spectroscopyMicrobiologyQR1-502ENmSphere, Vol 5, Iss 4 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	PQS HQNO Staphylococcus aureus polymicrobial quorum sensing Raman spectroscopy Microbiology QR1-502
spellingShingle	PQS HQNO Staphylococcus aureus polymicrobial quorum sensing Raman spectroscopy Microbiology QR1-502 Tianyuan Cao Jonathan V. Sweedler Paul W. Bohn Joshua D. Shrout Spatiotemporal Distribution of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Alkyl Quinolones under Metabolic and Competitive Stress
description	ABSTRACT Pseudomonas aeruginosa is an opportunistic human pathogen important to diseases such as cystic fibrosis. P. aeruginosa has multiple quorum-sensing (QS) systems, one of which utilizes the signaling molecule 2-heptyl-3-hydroxy-4-quinolone (Pseudomonas quinolone signal [PQS]). Here, we use hyperspectral Raman imaging to elucidate the spatiotemporal PQS distributions that determine how P. aeruginosa regulates surface colonization and its response to both metabolic stress and competition from other bacterial strains. These chemical imaging experiments illustrate the strong link between environmental challenges, such as metabolic stress caused by nutritional limitations or the presence of another bacterial species, and PQS signaling. Metabolic stress elicits a complex response in which limited nutrients induce the bacteria to produce PQS earlier, but the bacteria may also pause PQS production entirely if the nutrient concentration is too low. Separately, coculturing P. aeruginosa in the proximity of another bacterial species, or its culture supernatant, results in earlier production of PQS. However, these differences in PQS appearance are not observed for all alkyl quinolones (AQs) measured; the spatiotemporal response of 2-heptyl-4-hydroxyquinoline N-oxide (HQNO) is highly uniform for most conditions. These insights on the spatiotemporal distributions of quinolones provide additional perspective on the behavior of P. aeruginosa in response to different environmental cues. IMPORTANCE Alkyl quinolones (AQs), including Pseudomonas quinolone signal (PQS), made by the opportunistic pathogen Pseudomonas aeruginosa have been associated with both population density and stress. The regulation of AQ production is known to be complex, and the stimuli that modulate AQ responses are not fully clear. Here, we have used hyperspectral Raman chemical imaging to examine the temporal and spatial profiles of AQs exhibited by P. aeruginosa under several potentially stressful conditions. We found that metabolic stress, effected by carbon limitation, or competition stress, effected by proximity to other species, resulted in accelerated PQS production. This competition effect did not require cell-to-cell interaction, as evidenced by the fact that the addition of supernatants from either Escherichia coli or Staphylococcus aureus led to early appearance of PQS. Lastly, the fact that these modulations were observed for PQS but not for all AQs suggests a high level of complexity in AQ regulation that remains to be discerned.
format	article
author	Tianyuan Cao Jonathan V. Sweedler Paul W. Bohn Joshua D. Shrout
author_facet	Tianyuan Cao Jonathan V. Sweedler Paul W. Bohn Joshua D. Shrout
author_sort	Tianyuan Cao
title	Spatiotemporal Distribution of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Alkyl Quinolones under Metabolic and Competitive Stress
title_short	Spatiotemporal Distribution of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Alkyl Quinolones under Metabolic and Competitive Stress
title_full	Spatiotemporal Distribution of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Alkyl Quinolones under Metabolic and Competitive Stress
title_fullStr	Spatiotemporal Distribution of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Alkyl Quinolones under Metabolic and Competitive Stress
title_full_unstemmed	Spatiotemporal Distribution of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Alkyl Quinolones under Metabolic and Competitive Stress
title_sort	spatiotemporal distribution of <named-content content-type="genus-species">pseudomonas aeruginosa</named-content> alkyl quinolones under metabolic and competitive stress
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/6bf1658522ff459eadfbfbad9137da65
work_keys_str_mv	AT tianyuancao spatiotemporaldistributionofnamedcontentcontenttypegenusspeciespseudomonasaeruginosanamedcontentalkylquinolonesundermetabolicandcompetitivestress AT jonathanvsweedler spatiotemporaldistributionofnamedcontentcontenttypegenusspeciespseudomonasaeruginosanamedcontentalkylquinolonesundermetabolicandcompetitivestress AT paulwbohn spatiotemporaldistributionofnamedcontentcontenttypegenusspeciespseudomonasaeruginosanamedcontentalkylquinolonesundermetabolicandcompetitivestress AT joshuadshrout spatiotemporaldistributionofnamedcontentcontenttypegenusspeciespseudomonasaeruginosanamedcontentalkylquinolonesundermetabolicandcompetitivestress
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Spatiotemporal Distribution of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Alkyl Quinolones under Metabolic and Competitive Stress

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