Complementary killing activities of Pbunavirus LS1 and Bruynoghevirus LUZ24 phages on planktonic and sessile Pseudomonas aeruginosa PAO1 derivatives
Four P. aeruginosa phages active against a representative panel of strains, and with complementary spectra of action were chosen with the goal of using them for phage therapy. Two of them were myoviruses belonging to the Pbunavirus LS1 species, and two were podoviruses belonging to the Bruynogheviru...
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09.04.2025
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| Abstract | Four P. aeruginosa phages active against a representative panel of strains, and with complementary spectra of action were chosen with the goal of using them for phage therapy. Two of them were myoviruses belonging to the Pbunavirus LS1 species, and two were podoviruses belonging to the Bruynoghevirus LUZ24 species. In order to better apprehend the interactions of these phages with their P. aeruginosa host bacteria, we undertook the characterization of their bacterial receptors, using a PAO1 derivative as a recipient strain. Whereas the receptor of the P. LS1 phage Ab27 had already been characterized as the O-antigen chain of the lipopolysaccharides, no information was available at the onset of this work on the receptor used by the phages of the B. LUZ24 species. We show that the surface polysaccharide Psl is this receptor. Psl stands for polysaccharide synthesis locus, and it is an important component of the biofilm matrix in a large panel of P. aeruginosa strains, including PAO1. Remarkably, the B. LUZ24 phages were more active against PAO1 in minimal medium compared to rich medium. Consistently, this was correlated with larger amounts of Psl bound at the bacterial surface during exponential growth in the minimal medium compared to the rich medium. Biofilms formed on a medical intubation device, as well as in in 96-well plates, were degraded to different extent by the two phage species: biofilms grown for 7 hours on tubing device were degraded more efficiently by the B. LUZ24 than the P. LS1 phage, whereas mature biofilms (16 hours) formed in 96-well plates were degraded more rapidly by P. LS1 than by B. LUZ24 phage. The frequency of genetic mutants resisting to each phage were determined in liquid medium by a fluctuation assay and found in the range of 10-5 to 10-6 per generation. Interestingly, most of the P. LS1 resisting mutants were more sensitive to the B. LUZ24 phage. We conclude that the combination of the four selected phages has very promising properties, which should be relevant in the framework of phage therapy. |
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| AbstractList | Four P. aeruginosa phages active against a representative panel of strains, and with complementary spectra of action were chosen with the goal of using them for phage therapy. Two of them were myoviruses belonging to the Pbunavirus LS1 species, and two were podoviruses belonging to the Bruynoghevirus LUZ24 species. In order to better apprehend the interactions of these phages with their P. aeruginosa host bacteria, we undertook the characterization of their bacterial receptors, using a PAO1 derivative as a recipient strain. Whereas the receptor of the P. LS1 phage Ab27 had already been characterized as the O-antigen chain of the lipopolysaccharides, no information was available at the onset of this work on the receptor used by the phages of the B. LUZ24 species. We show that the surface polysaccharide Psl is this receptor. Psl stands for polysaccharide synthesis locus, and it is an important component of the biofilm matrix in a large panel of P. aeruginosa strains, including PAO1. Remarkably, the B. LUZ24 phages were more active against PAO1 in minimal medium compared to rich medium. Consistently, this was correlated with larger amounts of Psl bound at the bacterial surface during exponential growth in the minimal medium compared to the rich medium. Biofilms formed on a medical intubation device, as well as in in 96-well plates, were degraded to different extent by the two phage species: biofilms grown for 7 hours on tubing device were degraded more efficiently by the B. LUZ24 than the P. LS1 phage, whereas mature biofilms (16 hours) formed in 96-well plates were degraded more rapidly by P. LS1 than by B. LUZ24 phage. The frequency of genetic mutants resisting to each phage were determined in liquid medium by a fluctuation assay and found in the range of 10-5 to 10-6 per generation. Interestingly, most of the P. LS1 resisting mutants were more sensitive to the B. LUZ24 phage. We conclude that the combination of the four selected phages has very promising properties, which should be relevant in the framework of phage therapy. |
| Author | Lossouarn, Julien Ollivier, Emma Moncaut, Elisabeth Petit, Marie-Agnès Cleret, Aurore Lerouge, Benoît Fevre, Cindy Deschamps, Julien Briandet, Romain Demarre, Gaëlle Billaud, Maud Plantady, Clarisse |
| Author_xml | – sequence: 1 givenname: Maud surname: Billaud fullname: Billaud, Maud organization: Phaxiam Therapeutics – sequence: 2 givenname: Clarisse surname: Plantady fullname: Plantady, Clarisse organization: Phaxiam Therapeutics – sequence: 3 givenname: Benoît surname: Lerouge fullname: Lerouge, Benoît organization: Université Paris-Saclay, AgroParisTech, INRAE – sequence: 4 givenname: Emma surname: Ollivier fullname: Ollivier, Emma organization: Université Paris-Saclay, AgroParisTech, INRAE – sequence: 5 givenname: Julien surname: Lossouarn fullname: Lossouarn, Julien organization: Université Paris-Saclay, AgroParisTech, INRAE – sequence: 6 givenname: Elisabeth surname: Moncaut fullname: Moncaut, Elisabeth organization: Université Paris-Saclay, AgroParisTech, INRAE – sequence: 7 givenname: Julien surname: Deschamps fullname: Deschamps, Julien organization: Université Paris-Saclay, AgroParisTech, INRAE – sequence: 8 givenname: Romain surname: Briandet fullname: Briandet, Romain organization: Université Paris-Saclay, AgroParisTech, INRAE – sequence: 9 givenname: Aurore surname: Cleret fullname: Cleret, Aurore organization: Phaxiam Therapeutics – sequence: 10 givenname: Cindy surname: Fevre fullname: Fevre, Cindy organization: Phaxiam Therapeutics – sequence: 11 givenname: Gaëlle surname: Demarre fullname: Demarre, Gaëlle organization: Phaxiam Therapeutics – sequence: 12 givenname: Marie-Agnès surname: Petit fullname: Petit, Marie-Agnès email: marie-agnes.petit@inrae.fr organization: Université Paris-Saclay, AgroParisTech, INRAE |
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| ContentType | Paper |
| Copyright | 2025, Posted by Cold Spring Harbor Laboratory |
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| DBID | FX. |
| DOI | 10.1101/2025.04.09.647956 |
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| Discipline | Biology |
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| Edition | 1.1 |
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| Keywords | bacteriophage biofilm |
| Language | English |
| License | The copyright holder for this pre-print is the author. All rights reserved. The material may not be redistributed, re-used or adapted without the author's permission. |
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| Notes | Competing Interest Statement: The authors have declared no competing interest. |
| OpenAccessLink | https://www.biorxiv.org/content/10.1101/2025.04.09.647956 |
| PageCount | 36 |
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| PublicationTitle | bioRxiv |
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| Publisher | Cold Spring Harbor Laboratory |
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An update from the Infectious Diseases Society of America publication-title: Clin Infect Dis – volume: 11 start-page: 327 year: 2020 ident: 2025.04.09.647956v1.56 article-title: Development of a Bacteriophage Cocktail to Constrain the Emergence of Phage-Resistant Pseudomonas aeruginosa publication-title: Front Microbiol – volume: 5 start-page: 1041 year: 2010 end-page: 1055 ident: 2025.04.09.647956v1.7 article-title: Bacteriophages of Pseudomonas publication-title: Future Microbiol – volume: 73 start-page: 622 year: 2009 end-page: 638 ident: 2025.04.09.647956v1.5 article-title: Genetic and biochemical analyses of the Pseudomonas aeruginosa Psl exopolysaccharide reveal overlapping roles for polysaccharide synthesis enzymes in Psl and LPS production publication-title: Mol Microbiol – volume: 501 start-page: 151 year: 2009 end-page: 155 ident: 2025.04.09.647956v1.28 article-title: Measurement of the rate of attachment of bacteriophage to cells publication-title: Methods Mol Biol – volume: 7 start-page: 16065 year: 2017 ident: 2025.04.09.647956v1.46 article-title: Anti-Psl Targeting of Pseudomonas aeruginosa Biofilms for Neutrophil-Mediated Disruption publication-title: Sci Rep – volume: 2 start-page: 1010 year: 2013 end-page: 1023 ident: 2025.04.09.647956v1.13 article-title: Developing an international Pseudomonas aeruginosa reference panel publication-title: Microbiologyopen – volume: 190 start-page: 3622 year: 2008 end-page: 3631 ident: 2025.04.09.647956v1.45 article-title: Catalytic mechanism of cyclic di-GMP-specific phosphodiesterase: a study of the EAL domain-containing RocR from Pseudomonas aeruginosa publication-title: J Bacteriol – volume: 6 start-page: 26717 year: 2016 ident: 2025.04.09.647956v1.8 article-title: Phage selection restores antibiotic sensitivity in MDR Pseudomonas aeruginosa publication-title: Sci Rep |
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| Title | Complementary killing activities of Pbunavirus LS1 and Bruynoghevirus LUZ24 phages on planktonic and sessile Pseudomonas aeruginosa PAO1 derivatives |
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