A Commensal Streptococcus Dysregulates the Pseudomonas aeruginosa Nitrosative Stress Response
Chronic infections in the cystic fibrosis (CF) airway are composed of both pathogenic and commensal bacteria. However, chronic Pseudomonas aeruginosa infections are the leading cause of lung deterioration in individuals with CF. Interestingly, oral commensals can translocate to the CF lung and their...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-05-01
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| Series: | Frontiers in Cellular and Infection Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fcimb.2022.817336/full |
| _version_ | 1828345113750798336 |
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| author | Joshua J. Baty Joshua T. Huffines Sara N. Stoner Jessica A. Scoffield |
| author_facet | Joshua J. Baty Joshua T. Huffines Sara N. Stoner Jessica A. Scoffield |
| author_sort | Joshua J. Baty |
| collection | DOAJ |
| description | Chronic infections in the cystic fibrosis (CF) airway are composed of both pathogenic and commensal bacteria. However, chronic Pseudomonas aeruginosa infections are the leading cause of lung deterioration in individuals with CF. Interestingly, oral commensals can translocate to the CF lung and their presence is associated with improved lung function, presumably due to their ability to antagonize P. aeruginosa. We have previously shown that one commensal, Streptococcus parasanguinis, produces hydrogen peroxide that reacts with nitrite to generate reactive nitrogen intermediates (RNI) which inhibit P. aeruginosa growth. In this study, we sought to understand the global impact of commensal-mediated RNI on the P. aeruginosa transcriptome. RNA sequencing analysis revealed that S. parasanguinis and nitrite-mediated RNI dysregulated expression of denitrification genes in a CF isolate of P. aeruginosa compared to when this isolate was only exposed to S. parasanguinis. Further, loss of a nitric oxide reductase subunit (norB) rendered an acute P. aeruginosa isolate more susceptible to S. parasanguinis-mediated RNI. Additionally, S. parasanguinis-mediated RNI inactivated P. aeruginosa aconitase activity. Lastly, we report that P. aeruginosa isolates recovered from CF individuals are uniquely hypersensitive to S. parasanguinis-mediated RNI compared to acute infection or environmental P. aeruginosa isolates. These findings illustrate that S. parasanguinis hinders the ability of P. aeruginosa to respond to RNI, which potentially prevents P. aeruginosa CF isolates from resisting commensal and host-induced RNI in the CF airway. |
| first_indexed | 2024-04-14T00:06:54Z |
| format | Article |
| id | doaj.art-8f79b1b8fab240ff9091bca4e44906d2 |
| institution | Directory Open Access Journal |
| issn | 2235-2988 |
| language | English |
| last_indexed | 2024-04-14T00:06:54Z |
| publishDate | 2022-05-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cellular and Infection Microbiology |
| spelling | doaj.art-8f79b1b8fab240ff9091bca4e44906d22022-12-22T02:23:29ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882022-05-011210.3389/fcimb.2022.817336817336A Commensal Streptococcus Dysregulates the Pseudomonas aeruginosa Nitrosative Stress ResponseJoshua J. BatyJoshua T. HuffinesSara N. StonerJessica A. ScoffieldChronic infections in the cystic fibrosis (CF) airway are composed of both pathogenic and commensal bacteria. However, chronic Pseudomonas aeruginosa infections are the leading cause of lung deterioration in individuals with CF. Interestingly, oral commensals can translocate to the CF lung and their presence is associated with improved lung function, presumably due to their ability to antagonize P. aeruginosa. We have previously shown that one commensal, Streptococcus parasanguinis, produces hydrogen peroxide that reacts with nitrite to generate reactive nitrogen intermediates (RNI) which inhibit P. aeruginosa growth. In this study, we sought to understand the global impact of commensal-mediated RNI on the P. aeruginosa transcriptome. RNA sequencing analysis revealed that S. parasanguinis and nitrite-mediated RNI dysregulated expression of denitrification genes in a CF isolate of P. aeruginosa compared to when this isolate was only exposed to S. parasanguinis. Further, loss of a nitric oxide reductase subunit (norB) rendered an acute P. aeruginosa isolate more susceptible to S. parasanguinis-mediated RNI. Additionally, S. parasanguinis-mediated RNI inactivated P. aeruginosa aconitase activity. Lastly, we report that P. aeruginosa isolates recovered from CF individuals are uniquely hypersensitive to S. parasanguinis-mediated RNI compared to acute infection or environmental P. aeruginosa isolates. These findings illustrate that S. parasanguinis hinders the ability of P. aeruginosa to respond to RNI, which potentially prevents P. aeruginosa CF isolates from resisting commensal and host-induced RNI in the CF airway.https://www.frontiersin.org/articles/10.3389/fcimb.2022.817336/fullnitrosative stressPseudomonas aeruginosaStreptococcus parasanguinispolymicrobialdenitrification |
| spellingShingle | Joshua J. Baty Joshua T. Huffines Sara N. Stoner Jessica A. Scoffield A Commensal Streptococcus Dysregulates the Pseudomonas aeruginosa Nitrosative Stress Response Frontiers in Cellular and Infection Microbiology nitrosative stress Pseudomonas aeruginosa Streptococcus parasanguinis polymicrobial denitrification |
| title | A Commensal Streptococcus Dysregulates the Pseudomonas aeruginosa Nitrosative Stress Response |
| title_full | A Commensal Streptococcus Dysregulates the Pseudomonas aeruginosa Nitrosative Stress Response |
| title_fullStr | A Commensal Streptococcus Dysregulates the Pseudomonas aeruginosa Nitrosative Stress Response |
| title_full_unstemmed | A Commensal Streptococcus Dysregulates the Pseudomonas aeruginosa Nitrosative Stress Response |
| title_short | A Commensal Streptococcus Dysregulates the Pseudomonas aeruginosa Nitrosative Stress Response |
| title_sort | commensal streptococcus dysregulates the pseudomonas aeruginosa nitrosative stress response |
| topic | nitrosative stress Pseudomonas aeruginosa Streptococcus parasanguinis polymicrobial denitrification |
| url | https://www.frontiersin.org/articles/10.3389/fcimb.2022.817336/full |
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