Deletion of luxI increases luminescence of Vibrio fischeri
ABSTRACT Bioluminescence in Vibrio fischeri is regulated by a quorum-dependent signaling system composed of LuxI and LuxR. LuxI generates N-3-oxohexanoyl homoserine lactone (3OC6-HSL), which triggers LuxR to activate transcription of the luxICDABEG operon responsible for bioluminescence. Surprisingl...
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American Society for Microbiology
2024-10-01
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| Online Access: | https://journals.asm.org/doi/10.1128/mbio.02446-24 |
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| author | Kathryn A. Bellissimo Alecia N. Septer Cheryl A. Whistler Coralis Rodríguez Eric V. Stabb |
| author_facet | Kathryn A. Bellissimo Alecia N. Septer Cheryl A. Whistler Coralis Rodríguez Eric V. Stabb |
| author_sort | Kathryn A. Bellissimo |
| collection | DOAJ |
| description | ABSTRACT Bioluminescence in Vibrio fischeri is regulated by a quorum-dependent signaling system composed of LuxI and LuxR. LuxI generates N-3-oxohexanoyl homoserine lactone (3OC6-HSL), which triggers LuxR to activate transcription of the luxICDABEG operon responsible for bioluminescence. Surprisingly, a ∆luxI mutant produced more bioluminescence than the wild type in culture. In contrast, a 4 bp duplication within luxI, resulting in a frameshift mutation and null allele, decreased luminescence tenfold. A second signaling system encoded by ainSR affects bioluminescence by increasing levels of LuxR, via the transcriptional activator LitR, and the N-octanoyl homoserine lactone (C8-HSL) signal produced by AinS is considered only a weak activator of LuxR. However, ainS is required for the bright phenotype of the ∆luxI mutant in culture. When 3OC6-HSL was provided either in the medium or by expression of luxI in trans, all cultures were brighter, but the ∆luxI mutant remained significantly brighter than the luxI frameshift mutant. Taken together, these data suggest that the enhanced bioluminescence due to the LuxI product 3OC6-HSL counteracts a negative cis-acting regulatory element within the luxI gene and that when luxI is absent the C8-HSL signal is sufficient to induce luminescence.IMPORTANCEThe regulation of bioluminescence by Vibrio fischeri is a textbook example of bacterial quorum-dependent pheromone signaling. The canonical regulatory model is that an autoinducer pheromone produced by LuxI accumulates as cells achieve a high density, and this LuxI-generated signal stimulates LuxR to activate transcription of the lux operon that underlies bioluminescence. The surprising observation that LuxI is dispensable for inducing bioluminescence forces a re-evaluation of the role of luxI. More broadly, the results underscore the potential deceptiveness of complex regulatory circuits, particularly those in which bacteria produce multiple related signaling molecules. |
| format | Article |
| id | doaj-art-11fc4a3efbeb4508b9a3af7416d4f253 |
| institution | OA Journals |
| issn | 2150-7511 |
| language | English |
| publishDate | 2024-10-01 |
| publisher | American Society for Microbiology |
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| series | mBio |
| spelling | doaj-art-11fc4a3efbeb4508b9a3af7416d4f2532025-08-20T02:16:49ZengAmerican Society for MicrobiologymBio2150-75112024-10-01151010.1128/mbio.02446-24Deletion of luxI increases luminescence of Vibrio fischeriKathryn A. Bellissimo0Alecia N. Septer1Cheryl A. Whistler2Coralis Rodríguez3Eric V. Stabb4Department of Microbiology, University of Georgia, Athens, Georgia, USADepartment of Earth, Marine & Environmental Sciences, University of North Carolina, Chapel Hill, North Carolina, USADepartment of Molecular, Cellular, and Biomedical Sciences, University of New Hampshire, Durham, New Hampshire, USADepartment of Microbiology, University of Georgia, Athens, Georgia, USADepartment of Biological Sciences, University of Illinois at Chicago, Chicago, Illinois, USAABSTRACT Bioluminescence in Vibrio fischeri is regulated by a quorum-dependent signaling system composed of LuxI and LuxR. LuxI generates N-3-oxohexanoyl homoserine lactone (3OC6-HSL), which triggers LuxR to activate transcription of the luxICDABEG operon responsible for bioluminescence. Surprisingly, a ∆luxI mutant produced more bioluminescence than the wild type in culture. In contrast, a 4 bp duplication within luxI, resulting in a frameshift mutation and null allele, decreased luminescence tenfold. A second signaling system encoded by ainSR affects bioluminescence by increasing levels of LuxR, via the transcriptional activator LitR, and the N-octanoyl homoserine lactone (C8-HSL) signal produced by AinS is considered only a weak activator of LuxR. However, ainS is required for the bright phenotype of the ∆luxI mutant in culture. When 3OC6-HSL was provided either in the medium or by expression of luxI in trans, all cultures were brighter, but the ∆luxI mutant remained significantly brighter than the luxI frameshift mutant. Taken together, these data suggest that the enhanced bioluminescence due to the LuxI product 3OC6-HSL counteracts a negative cis-acting regulatory element within the luxI gene and that when luxI is absent the C8-HSL signal is sufficient to induce luminescence.IMPORTANCEThe regulation of bioluminescence by Vibrio fischeri is a textbook example of bacterial quorum-dependent pheromone signaling. The canonical regulatory model is that an autoinducer pheromone produced by LuxI accumulates as cells achieve a high density, and this LuxI-generated signal stimulates LuxR to activate transcription of the lux operon that underlies bioluminescence. The surprising observation that LuxI is dispensable for inducing bioluminescence forces a re-evaluation of the role of luxI. More broadly, the results underscore the potential deceptiveness of complex regulatory circuits, particularly those in which bacteria produce multiple related signaling molecules.https://journals.asm.org/doi/10.1128/mbio.02446-24PhotobacteriumAliivibrioquorum sensingbioluminescence |
| spellingShingle | Kathryn A. Bellissimo Alecia N. Septer Cheryl A. Whistler Coralis Rodríguez Eric V. Stabb Deletion of luxI increases luminescence of Vibrio fischeri mBio Photobacterium Aliivibrio quorum sensing bioluminescence |
| title | Deletion of luxI increases luminescence of Vibrio fischeri |
| title_full | Deletion of luxI increases luminescence of Vibrio fischeri |
| title_fullStr | Deletion of luxI increases luminescence of Vibrio fischeri |
| title_full_unstemmed | Deletion of luxI increases luminescence of Vibrio fischeri |
| title_short | Deletion of luxI increases luminescence of Vibrio fischeri |
| title_sort | deletion of luxi increases luminescence of vibrio fischeri |
| topic | Photobacterium Aliivibrio quorum sensing bioluminescence |
| url | https://journals.asm.org/doi/10.1128/mbio.02446-24 |
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