Effectiveness of Pseudomonas aeruginosa type VI secretion system relies on toxin potency and type IV pili-dependent interaction

The type VI secretion system (T6SS) is an antibacterial weapon that is used by numerous Gram-negative bacteria to gain competitive advantage by injecting toxins into adjacent prey cells. Predicting the outcome of a T6SS-dependent competition is not only reliant on presence-absence of the system but...

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Main Authors: Rudzite, Marta, Subramoni, Sujatha, Endres, Robert G., Filloux, Alain
Other Authors: Singapore Centre for Environmental Life Sciences and Engineering
Format: Article
Language:English
Published: 2023
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Online Access:https://hdl.handle.net/10356/171706
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Institution: Nanyang Technological University
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spelling sg-ntu-dr.10356-1717062023-11-09T15:30:20Z Effectiveness of Pseudomonas aeruginosa type VI secretion system relies on toxin potency and type IV pili-dependent interaction Rudzite, Marta Subramoni, Sujatha Endres, Robert G. Filloux, Alain Singapore Centre for Environmental Life Sciences and Engineering Science::Biological sciences Social Evolution Protein The type VI secretion system (T6SS) is an antibacterial weapon that is used by numerous Gram-negative bacteria to gain competitive advantage by injecting toxins into adjacent prey cells. Predicting the outcome of a T6SS-dependent competition is not only reliant on presence-absence of the system but instead involves a multiplicity of factors. Pseudomonas aeruginosa possesses 3 distinct T6SSs and a set of more than 20 toxic effectors with diverse functions including disruption of cell wall integrity, degradation of nucleic acids or metabolic impairment. We generated a comprehensive collection of mutants with various degrees of T6SS activity and/or sensitivity to each individual T6SS toxin. By imaging whole mixed bacterial macrocolonies, we then investigated how these P. aeruginosa strains gain a competitive edge in multiple attacker/prey combinations. We observed that the potency of single T6SS toxin varies significantly from one another as measured by monitoring the community structure, with some toxins acting better in synergy or requiring a higher payload. Remarkably the degree of intermixing between preys and attackers is also key to the competition outcome and is driven by the frequency of contact as well as the ability of the prey to move away from the attacker using type IV pili-dependent twitching motility. Finally, we implemented a computational model to better understand how changes in T6SS firing behaviours or cell-cell contacts lead to population level competitive advantages, thus providing conceptual insight applicable to all types of contact-based competition. Published version This work was supported by a MRC grant n˚ MR/S02316X/1 to AF. MR is supported by a BBSRC DTP studentship (reference 2133361). 2023-11-06T02:11:14Z 2023-11-06T02:11:14Z 2023 Journal Article Rudzite, M., Subramoni, S., Endres, R. G. & Filloux, A. (2023). Effectiveness of Pseudomonas aeruginosa type VI secretion system relies on toxin potency and type IV pili-dependent interaction. PLoS Pathogens, 19(5), e1011428-. https://dx.doi.org/10.1371/journal.ppat.1011428 1553-7366 https://hdl.handle.net/10356/171706 10.1371/journal.ppat.1011428 37253075 2-s2.0-85163922566 5 19 e1011428 en PLoS Pathogens © 2023 The Author(s). This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. application/pdf
institution Nanyang Technological University
building NTU Library
continent Asia
country Singapore
Singapore
content_provider NTU Library
collection DR-NTU
language English
topic Science::Biological sciences
Social Evolution
Protein
spellingShingle Science::Biological sciences
Social Evolution
Protein
Rudzite, Marta
Subramoni, Sujatha
Endres, Robert G.
Filloux, Alain
Effectiveness of Pseudomonas aeruginosa type VI secretion system relies on toxin potency and type IV pili-dependent interaction
description The type VI secretion system (T6SS) is an antibacterial weapon that is used by numerous Gram-negative bacteria to gain competitive advantage by injecting toxins into adjacent prey cells. Predicting the outcome of a T6SS-dependent competition is not only reliant on presence-absence of the system but instead involves a multiplicity of factors. Pseudomonas aeruginosa possesses 3 distinct T6SSs and a set of more than 20 toxic effectors with diverse functions including disruption of cell wall integrity, degradation of nucleic acids or metabolic impairment. We generated a comprehensive collection of mutants with various degrees of T6SS activity and/or sensitivity to each individual T6SS toxin. By imaging whole mixed bacterial macrocolonies, we then investigated how these P. aeruginosa strains gain a competitive edge in multiple attacker/prey combinations. We observed that the potency of single T6SS toxin varies significantly from one another as measured by monitoring the community structure, with some toxins acting better in synergy or requiring a higher payload. Remarkably the degree of intermixing between preys and attackers is also key to the competition outcome and is driven by the frequency of contact as well as the ability of the prey to move away from the attacker using type IV pili-dependent twitching motility. Finally, we implemented a computational model to better understand how changes in T6SS firing behaviours or cell-cell contacts lead to population level competitive advantages, thus providing conceptual insight applicable to all types of contact-based competition.
author2 Singapore Centre for Environmental Life Sciences and Engineering
author_facet Singapore Centre for Environmental Life Sciences and Engineering
Rudzite, Marta
Subramoni, Sujatha
Endres, Robert G.
Filloux, Alain
format Article
author Rudzite, Marta
Subramoni, Sujatha
Endres, Robert G.
Filloux, Alain
author_sort Rudzite, Marta
title Effectiveness of Pseudomonas aeruginosa type VI secretion system relies on toxin potency and type IV pili-dependent interaction
title_short Effectiveness of Pseudomonas aeruginosa type VI secretion system relies on toxin potency and type IV pili-dependent interaction
title_full Effectiveness of Pseudomonas aeruginosa type VI secretion system relies on toxin potency and type IV pili-dependent interaction
title_fullStr Effectiveness of Pseudomonas aeruginosa type VI secretion system relies on toxin potency and type IV pili-dependent interaction
title_full_unstemmed Effectiveness of Pseudomonas aeruginosa type VI secretion system relies on toxin potency and type IV pili-dependent interaction
title_sort effectiveness of pseudomonas aeruginosa type vi secretion system relies on toxin potency and type iv pili-dependent interaction
publishDate 2023
url https://hdl.handle.net/10356/171706
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