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Bacterial cytological profiling reveals interactions between jumbo phage φKZ infection and cell wall active antibiotics in Pseudomonas aeruginosa

The emergence of antibiotic resistance in bacteria has led to the investigation of alternative treatments, such as phage therapy. In this study, we examined the interactions between the nucleus-forming jumbo phage ФKZ and antibiotic treatment against Pseudomonas aeruginosa. Using the fluorescence mi...

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Autores principales: Tsunemoto, Hannah, Sugie, Joseph, Enustun, Eray, Pogliano, Kit, Pogliano, Joe
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10328376/
https://www.ncbi.nlm.nih.gov/pubmed/37418366
http://dx.doi.org/10.1371/journal.pone.0280070
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author Tsunemoto, Hannah
Sugie, Joseph
Enustun, Eray
Pogliano, Kit
Pogliano, Joe
author_facet Tsunemoto, Hannah
Sugie, Joseph
Enustun, Eray
Pogliano, Kit
Pogliano, Joe
author_sort Tsunemoto, Hannah
collection PubMed
description The emergence of antibiotic resistance in bacteria has led to the investigation of alternative treatments, such as phage therapy. In this study, we examined the interactions between the nucleus-forming jumbo phage ФKZ and antibiotic treatment against Pseudomonas aeruginosa. Using the fluorescence microscopy technique of bacterial cytological profiling, we identified mechanism-of-action-specific interactions between antibiotics that target different biosynthetic pathways and ФKZ infection. We found that certain classes of antibiotics strongly inhibited phage replication, while others had no effect or only mildly affected progression through the lytic cycle. Antibiotics that caused an increase in host cell length, such as the cell wall active antibiotic ceftazidime, prevented proper centering of the ФKZ nucleus via the PhuZ spindle at midcell, leading us to hypothesize that the kinetic parameters of the PhuZ spindle evolved to match the average length of the host cell. To test this, we developed a computational model explaining how the dynamic properties of the PhuZ spindle contribute to phage nucleus centering and why some antibiotics affect nucleus positioning while others do not. These findings provide an understanding of the molecular mechanisms underlying the interactions between antibiotics and jumbo phage replication.
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spelling pubmed-103283762023-07-08 Bacterial cytological profiling reveals interactions between jumbo phage φKZ infection and cell wall active antibiotics in Pseudomonas aeruginosa Tsunemoto, Hannah Sugie, Joseph Enustun, Eray Pogliano, Kit Pogliano, Joe PLoS One Research Article The emergence of antibiotic resistance in bacteria has led to the investigation of alternative treatments, such as phage therapy. In this study, we examined the interactions between the nucleus-forming jumbo phage ФKZ and antibiotic treatment against Pseudomonas aeruginosa. Using the fluorescence microscopy technique of bacterial cytological profiling, we identified mechanism-of-action-specific interactions between antibiotics that target different biosynthetic pathways and ФKZ infection. We found that certain classes of antibiotics strongly inhibited phage replication, while others had no effect or only mildly affected progression through the lytic cycle. Antibiotics that caused an increase in host cell length, such as the cell wall active antibiotic ceftazidime, prevented proper centering of the ФKZ nucleus via the PhuZ spindle at midcell, leading us to hypothesize that the kinetic parameters of the PhuZ spindle evolved to match the average length of the host cell. To test this, we developed a computational model explaining how the dynamic properties of the PhuZ spindle contribute to phage nucleus centering and why some antibiotics affect nucleus positioning while others do not. These findings provide an understanding of the molecular mechanisms underlying the interactions between antibiotics and jumbo phage replication. Public Library of Science 2023-07-07 /pmc/articles/PMC10328376/ /pubmed/37418366 http://dx.doi.org/10.1371/journal.pone.0280070 Text en © 2023 Tsunemoto et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Tsunemoto, Hannah
Sugie, Joseph
Enustun, Eray
Pogliano, Kit
Pogliano, Joe
Bacterial cytological profiling reveals interactions between jumbo phage φKZ infection and cell wall active antibiotics in Pseudomonas aeruginosa
title Bacterial cytological profiling reveals interactions between jumbo phage φKZ infection and cell wall active antibiotics in Pseudomonas aeruginosa
title_full Bacterial cytological profiling reveals interactions between jumbo phage φKZ infection and cell wall active antibiotics in Pseudomonas aeruginosa
title_fullStr Bacterial cytological profiling reveals interactions between jumbo phage φKZ infection and cell wall active antibiotics in Pseudomonas aeruginosa
title_full_unstemmed Bacterial cytological profiling reveals interactions between jumbo phage φKZ infection and cell wall active antibiotics in Pseudomonas aeruginosa
title_short Bacterial cytological profiling reveals interactions between jumbo phage φKZ infection and cell wall active antibiotics in Pseudomonas aeruginosa
title_sort bacterial cytological profiling reveals interactions between jumbo phage φkz infection and cell wall active antibiotics in pseudomonas aeruginosa
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10328376/
https://www.ncbi.nlm.nih.gov/pubmed/37418366
http://dx.doi.org/10.1371/journal.pone.0280070
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