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...
| Main Authors: | , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2020-08-01
|
| Series: | mSphere |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mSphere.00426-20 |
| _version_ | 1819005592452202496 |
|---|---|
| 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 |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-20T23:55:14Z |
| format | Article |
| id | doaj.art-6bf1658522ff459eadfbfbad9137da65 |
| institution | Directory Open Access Journal |
| issn | 2379-5042 |
| language | English |
| last_indexed | 2024-12-20T23:55:14Z |
| publishDate | 2020-08-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSphere |
| spelling | doaj.art-6bf1658522ff459eadfbfbad9137da652022-12-21T19:22:44ZengAmerican Society for MicrobiologymSphere2379-50422020-08-015410.1128/mSphere.00426-20Spatiotemporal Distribution of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Alkyl Quinolones under Metabolic and Competitive StressTianyuan Cao0Jonathan V. Sweedler1Paul W. Bohn2Joshua D. Shrout3Department of Chemistry and Biochemistry, University of Notre Dame, Notre Dame, Indiana, USADepartment of Chemistry, University of Illinois at Urbana-Champaign, Urbana, Illinois, USADepartment of Chemistry and Biochemistry, University of Notre Dame, Notre Dame, Indiana, USAAdvanced Diagnostics and Therapeutics, University of Notre Dame, Notre Dame, Indiana, USAABSTRACT 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.https://journals.asm.org/doi/10.1128/mSphere.00426-20PQSHQNOStaphylococcus aureuspolymicrobialquorum sensingRaman spectroscopy |
| spellingShingle | 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 mSphere PQS HQNO Staphylococcus aureus polymicrobial quorum sensing Raman spectroscopy |
| title | 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_short | 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 |
| topic | PQS HQNO Staphylococcus aureus polymicrobial quorum sensing Raman spectroscopy |
| url | https://journals.asm.org/doi/10.1128/mSphere.00426-20 |
| work_keys_str_mv | AT tianyuancao spatiotemporaldistributionofnamedcontentcontenttypegenusspeciespseudomonasaeruginosanamedcontentalkylquinolonesundermetabolicandcompetitivestress AT jonathanvsweedler spatiotemporaldistributionofnamedcontentcontenttypegenusspeciespseudomonasaeruginosanamedcontentalkylquinolonesundermetabolicandcompetitivestress AT paulwbohn spatiotemporaldistributionofnamedcontentcontenttypegenusspeciespseudomonasaeruginosanamedcontentalkylquinolonesundermetabolicandcompetitivestress AT joshuadshrout spatiotemporaldistributionofnamedcontentcontenttypegenusspeciespseudomonasaeruginosanamedcontentalkylquinolonesundermetabolicandcompetitivestress |