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The Vibrio fischeri type VI secretion system incurs a fitness cost under host-like conditions

The type VI secretion system (T6SS) is an interbacterial weapon composed of thousands of protein subunits and predicted to require significant cellular energy to deploy, yet a fitness cost from T6SS use is rarely observed. Here, we identify host-like conditions where the T6SS incurs a fitness cost u...

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Autores principales: Septer, Alecia N., Sharpe, Garrett, Shook, Erika A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10028907/
https://www.ncbi.nlm.nih.gov/pubmed/36945377
http://dx.doi.org/10.1101/2023.03.07.529561
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author Septer, Alecia N.
Sharpe, Garrett
Shook, Erika A.
author_facet Septer, Alecia N.
Sharpe, Garrett
Shook, Erika A.
author_sort Septer, Alecia N.
collection PubMed
description The type VI secretion system (T6SS) is an interbacterial weapon composed of thousands of protein subunits and predicted to require significant cellular energy to deploy, yet a fitness cost from T6SS use is rarely observed. Here, we identify host-like conditions where the T6SS incurs a fitness cost using the beneficial symbiont, Vibrio fischeri, which uses its T6SS to eliminate competitors in the natural squid host. We hypothesized that a fitness cost for the T6SS could be dependent on the cellular energetic state and used theoretical ATP cost estimates to predict when a T6SS-dependent fitness cost may be apparent. Theoretical energetic cost estimates predicted a minor relative cost for T6SS use in fast-growing populations (0.4–0.45% of total ATP used cell(−1)), and a higher relative cost (3.1–13.6%) for stationary phase cells. Consistent with these predictions, we observed no significant T6SS-dependent fitness cost for fast-growing populations typically used for competition assays. However, the stationary phase cell density was significantly lower in the wild-type strain, compared to a regulator mutant that does not express the T6SS, and this T6SS-dependent fitness cost was between 11 and 23%. Such a fitness cost could influence the prevalence and biogeography of T6SSs in animal-associated bacteria. While the T6SS may be required in kill or be killed scenarios, once the competitor is eliminated there is no longer selective pressure to maintain the weapon. Our findings indicate an evolved genotype lacking the T6SS would have a growth advantage over its parent, resulting in the eventual dominance of the unarmed population.
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spelling pubmed-100289072023-03-22 The Vibrio fischeri type VI secretion system incurs a fitness cost under host-like conditions Septer, Alecia N. Sharpe, Garrett Shook, Erika A. bioRxiv Article The type VI secretion system (T6SS) is an interbacterial weapon composed of thousands of protein subunits and predicted to require significant cellular energy to deploy, yet a fitness cost from T6SS use is rarely observed. Here, we identify host-like conditions where the T6SS incurs a fitness cost using the beneficial symbiont, Vibrio fischeri, which uses its T6SS to eliminate competitors in the natural squid host. We hypothesized that a fitness cost for the T6SS could be dependent on the cellular energetic state and used theoretical ATP cost estimates to predict when a T6SS-dependent fitness cost may be apparent. Theoretical energetic cost estimates predicted a minor relative cost for T6SS use in fast-growing populations (0.4–0.45% of total ATP used cell(−1)), and a higher relative cost (3.1–13.6%) for stationary phase cells. Consistent with these predictions, we observed no significant T6SS-dependent fitness cost for fast-growing populations typically used for competition assays. However, the stationary phase cell density was significantly lower in the wild-type strain, compared to a regulator mutant that does not express the T6SS, and this T6SS-dependent fitness cost was between 11 and 23%. Such a fitness cost could influence the prevalence and biogeography of T6SSs in animal-associated bacteria. While the T6SS may be required in kill or be killed scenarios, once the competitor is eliminated there is no longer selective pressure to maintain the weapon. Our findings indicate an evolved genotype lacking the T6SS would have a growth advantage over its parent, resulting in the eventual dominance of the unarmed population. Cold Spring Harbor Laboratory 2023-03-07 /pmc/articles/PMC10028907/ /pubmed/36945377 http://dx.doi.org/10.1101/2023.03.07.529561 Text en https://creativecommons.org/licenses/by/4.0/This work is licensed under a Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/) , which allows reusers to distribute, remix, adapt, and build upon the material in any medium or format, so long as attribution is given to the creator. The license allows for commercial use.
spellingShingle Article
Septer, Alecia N.
Sharpe, Garrett
Shook, Erika A.
The Vibrio fischeri type VI secretion system incurs a fitness cost under host-like conditions
title The Vibrio fischeri type VI secretion system incurs a fitness cost under host-like conditions
title_full The Vibrio fischeri type VI secretion system incurs a fitness cost under host-like conditions
title_fullStr The Vibrio fischeri type VI secretion system incurs a fitness cost under host-like conditions
title_full_unstemmed The Vibrio fischeri type VI secretion system incurs a fitness cost under host-like conditions
title_short The Vibrio fischeri type VI secretion system incurs a fitness cost under host-like conditions
title_sort vibrio fischeri type vi secretion system incurs a fitness cost under host-like conditions
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10028907/
https://www.ncbi.nlm.nih.gov/pubmed/36945377
http://dx.doi.org/10.1101/2023.03.07.529561
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