Perturbation of Quorum Sensing after the Acquisition of Bacteriophage Resistance Could Contribute to Novel Traits in <i>Vibrio alginolyticus</i>
Bacteria employ a wide range of molecular mechanisms to confer resistance to bacteriophages, and these mechanisms are continuously being discovered and characterized. However, there are instances where certain bacterial species, despite lacking these known mechanisms, can still develop bacteriophage...
| Main Authors: | , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2023-09-01
|
| Series: | Microorganisms |
| Subjects: | |
| Online Access: | https://www.mdpi.com/2076-2607/11/9/2273 |
| _version_ | 1827725209542590464 |
|---|---|
| author | Dimitrios Skliros Stavros Droubogiannis Chrysanthi Kalloniati Pantelis Katharios Emmanouil Flemetakis |
| author_facet | Dimitrios Skliros Stavros Droubogiannis Chrysanthi Kalloniati Pantelis Katharios Emmanouil Flemetakis |
| author_sort | Dimitrios Skliros |
| collection | DOAJ |
| description | Bacteria employ a wide range of molecular mechanisms to confer resistance to bacteriophages, and these mechanisms are continuously being discovered and characterized. However, there are instances where certain bacterial species, despite lacking these known mechanisms, can still develop bacteriophage resistance through intricate metabolic adaptation strategies, potentially involving mutations in transcriptional regulators or phage receptors. <i>Vibrio</i> species have been particularly useful for studying the orchestrated metabolic responses of Gram-negative marine bacteria in various challenges. In a previous study, we demonstrated that <i>Vibrio alginolyticus</i> downregulates the expression of specific receptors and transporters in its membrane, which may enable the bacterium to evade infection by lytic bacteriophages. In our current study, our objective was to explore how the development of bacteriophage resistance in <i>Vibrio</i> species disrupts the quorum-sensing cascade, subsequently affecting bacterial physiology and metabolic capacity. Using a real-time quantitative PCR (rt-QPCR) platform, we examined the expression pattern of quorum-sensing genes, auto-inducer biosynthesis genes, and cell density regulatory proteins in phage-resistant strains. Our results revealed that bacteriophage-resistant bacteria downregulate the expression of quorum-sensing regulatory proteins, such as <i>LuxM</i>, <i>LuxN</i>, and <i>LuxP</i>. This downregulation attenuates the normal perception of quorum-sensing peptides and subsequently diminishes the expression of cell density regulatory proteins, including <i>LuxU</i>, <i>aphA</i>, and <i>LuxR</i>. These findings align with the diverse phenotypic traits observed in the phage-resistant strains, such as altered biofilm formation, reduced planktonic growth, and reduced virulence. Moreover, the transcriptional depletion of <i>aphA</i>, the master regulator associated with low cell density, was linked to the downregulation of genes related to virulence. This phenomenon appears to be phage-specific, suggesting a finely tuned metabolic adaptation driven by phage–host interaction. These findings contribute to our understanding of the role of <i>Vibrio</i> species in microbial marine ecology and highlight the complex interplay between phage resistance, quorum sensing, and bacterial physiology. |
| first_indexed | 2024-03-10T22:27:06Z |
| format | Article |
| id | doaj.art-7e540ce864d94683b2763d53a6328dea |
| institution | Directory Open Access Journal |
| issn | 2076-2607 |
| language | English |
| last_indexed | 2024-03-10T22:27:06Z |
| publishDate | 2023-09-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Microorganisms |
| spelling | doaj.art-7e540ce864d94683b2763d53a6328dea2023-11-19T12:03:02ZengMDPI AGMicroorganisms2076-26072023-09-01119227310.3390/microorganisms11092273Perturbation of Quorum Sensing after the Acquisition of Bacteriophage Resistance Could Contribute to Novel Traits in <i>Vibrio alginolyticus</i>Dimitrios Skliros0Stavros Droubogiannis1Chrysanthi Kalloniati2Pantelis Katharios3Emmanouil Flemetakis4Laboratory of Molecular Biology, Department of Biotechnology, School of Applied Biology and Biotechnology, Agricultural University of Athens, 11855 Athens, GreeceInstitute of Marine Biology, Biotechnology and Aquaculture, Hellenic Centre for Marine Research, 71500 Heraklion, GreeceLaboratory of Molecular Biology, Department of Biotechnology, School of Applied Biology and Biotechnology, Agricultural University of Athens, 11855 Athens, GreeceInstitute of Marine Biology, Biotechnology and Aquaculture, Hellenic Centre for Marine Research, 71500 Heraklion, GreeceLaboratory of Molecular Biology, Department of Biotechnology, School of Applied Biology and Biotechnology, Agricultural University of Athens, 11855 Athens, GreeceBacteria employ a wide range of molecular mechanisms to confer resistance to bacteriophages, and these mechanisms are continuously being discovered and characterized. However, there are instances where certain bacterial species, despite lacking these known mechanisms, can still develop bacteriophage resistance through intricate metabolic adaptation strategies, potentially involving mutations in transcriptional regulators or phage receptors. <i>Vibrio</i> species have been particularly useful for studying the orchestrated metabolic responses of Gram-negative marine bacteria in various challenges. In a previous study, we demonstrated that <i>Vibrio alginolyticus</i> downregulates the expression of specific receptors and transporters in its membrane, which may enable the bacterium to evade infection by lytic bacteriophages. In our current study, our objective was to explore how the development of bacteriophage resistance in <i>Vibrio</i> species disrupts the quorum-sensing cascade, subsequently affecting bacterial physiology and metabolic capacity. Using a real-time quantitative PCR (rt-QPCR) platform, we examined the expression pattern of quorum-sensing genes, auto-inducer biosynthesis genes, and cell density regulatory proteins in phage-resistant strains. Our results revealed that bacteriophage-resistant bacteria downregulate the expression of quorum-sensing regulatory proteins, such as <i>LuxM</i>, <i>LuxN</i>, and <i>LuxP</i>. This downregulation attenuates the normal perception of quorum-sensing peptides and subsequently diminishes the expression of cell density regulatory proteins, including <i>LuxU</i>, <i>aphA</i>, and <i>LuxR</i>. These findings align with the diverse phenotypic traits observed in the phage-resistant strains, such as altered biofilm formation, reduced planktonic growth, and reduced virulence. Moreover, the transcriptional depletion of <i>aphA</i>, the master regulator associated with low cell density, was linked to the downregulation of genes related to virulence. This phenomenon appears to be phage-specific, suggesting a finely tuned metabolic adaptation driven by phage–host interaction. These findings contribute to our understanding of the role of <i>Vibrio</i> species in microbial marine ecology and highlight the complex interplay between phage resistance, quorum sensing, and bacterial physiology.https://www.mdpi.com/2076-2607/11/9/2273bacteriophagesquorum sensingphage resistancebiofilmvirulencevibrio |
| spellingShingle | Dimitrios Skliros Stavros Droubogiannis Chrysanthi Kalloniati Pantelis Katharios Emmanouil Flemetakis Perturbation of Quorum Sensing after the Acquisition of Bacteriophage Resistance Could Contribute to Novel Traits in <i>Vibrio alginolyticus</i> Microorganisms bacteriophages quorum sensing phage resistance biofilm virulence vibrio |
| title | Perturbation of Quorum Sensing after the Acquisition of Bacteriophage Resistance Could Contribute to Novel Traits in <i>Vibrio alginolyticus</i> |
| title_full | Perturbation of Quorum Sensing after the Acquisition of Bacteriophage Resistance Could Contribute to Novel Traits in <i>Vibrio alginolyticus</i> |
| title_fullStr | Perturbation of Quorum Sensing after the Acquisition of Bacteriophage Resistance Could Contribute to Novel Traits in <i>Vibrio alginolyticus</i> |
| title_full_unstemmed | Perturbation of Quorum Sensing after the Acquisition of Bacteriophage Resistance Could Contribute to Novel Traits in <i>Vibrio alginolyticus</i> |
| title_short | Perturbation of Quorum Sensing after the Acquisition of Bacteriophage Resistance Could Contribute to Novel Traits in <i>Vibrio alginolyticus</i> |
| title_sort | perturbation of quorum sensing after the acquisition of bacteriophage resistance could contribute to novel traits in i vibrio alginolyticus i |
| topic | bacteriophages quorum sensing phage resistance biofilm virulence vibrio |
| url | https://www.mdpi.com/2076-2607/11/9/2273 |
| work_keys_str_mv | AT dimitriosskliros perturbationofquorumsensingaftertheacquisitionofbacteriophageresistancecouldcontributetonoveltraitsinivibrioalginolyticusi AT stavrosdroubogiannis perturbationofquorumsensingaftertheacquisitionofbacteriophageresistancecouldcontributetonoveltraitsinivibrioalginolyticusi AT chrysanthikalloniati perturbationofquorumsensingaftertheacquisitionofbacteriophageresistancecouldcontributetonoveltraitsinivibrioalginolyticusi AT panteliskatharios perturbationofquorumsensingaftertheacquisitionofbacteriophageresistancecouldcontributetonoveltraitsinivibrioalginolyticusi AT emmanouilflemetakis perturbationofquorumsensingaftertheacquisitionofbacteriophageresistancecouldcontributetonoveltraitsinivibrioalginolyticusi |