Aging of a Bacterial Colony Enforces the Evolvement of Nondifferentiating Mutants

ABSTRACT Bacteria in nature are known to survive for long periods under restricting conditions, mainly by reducing their growth rate and metabolic activity. Here, we uncover a novel strategy utilized by bacterial cells to resist aging by propagating rather than halting division. Bacterial aging was...

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Autores principales: Rachel Hashuel, Sigal Ben-Yehuda
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Lenguaje:EN
Publicado: American Society for Microbiology 2019
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spelling oai:doaj.org-article:9de18242ce864594aef92dbbff223fb62021-11-15T15:59:41ZAging of a Bacterial Colony Enforces the Evolvement of Nondifferentiating Mutants10.1128/mBio.01414-192150-7511https://doaj.org/article/9de18242ce864594aef92dbbff223fb62019-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01414-19https://doaj.org/toc/2150-7511ABSTRACT Bacteria in nature are known to survive for long periods under restricting conditions, mainly by reducing their growth rate and metabolic activity. Here, we uncover a novel strategy utilized by bacterial cells to resist aging by propagating rather than halting division. Bacterial aging was monitored by inspecting colonies of the Gram-positive soil bacterium Bacillus subtilis, which is capable of differentiating into various cell types under nutrient exhaustion. We revealed that after days of incubation, rejuvenating subpopulations, arrayed over the mother colony, emerged. These subpopulations were found to harbor mutations in a variety of genes, restricting the ability of the cells to differentiate. Surprisingly, even mutations that are not classically designated to developmental pathways, concluded in differentiation deficiency, indicating that multiple paths can reach this same outcome. We provide evidence that the evolved mutants continue to divide under conditions that favor entry into quiescence, hence becoming abundant within the aging population. The occurrence of such nondifferentiating mutants could impact bacterial population dynamics in natural niches. IMPORTANCE Until now, bacterial cells facing nutrient deprivation were shown to enter dormancy as a strategy to survive prolonged stress, with the most established examples being sporulation, stationary phase, and persistence. Here, we uncovered an opposing strategy for long-term bacterial survival, in which mutant subpopulations cope with a challenging niche by proliferating rather than by stalling division. We show that this feature stems from mutations in genes disturbing the capability of the cells to differentiate into a quiescent state, enabling them to divide under restrictive conditions. Our study challenges the dogma of bacterial aging by highlighting an additional survival strategy resembling that of cancerous cells in animal organs.Rachel HashuelSigal Ben-YehudaAmerican Society for MicrobiologyarticleBacillus subtiliscolonylong-term stationary phasesporulationspo0AMicrobiologyQR1-502ENmBio, Vol 10, Iss 5 (2019)
institution DOAJ
collection DOAJ
language EN
topic Bacillus subtilis
colony
long-term stationary phase
sporulation
spo0A
Microbiology
QR1-502
spellingShingle Bacillus subtilis
colony
long-term stationary phase
sporulation
spo0A
Microbiology
QR1-502
Rachel Hashuel
Sigal Ben-Yehuda
Aging of a Bacterial Colony Enforces the Evolvement of Nondifferentiating Mutants
description ABSTRACT Bacteria in nature are known to survive for long periods under restricting conditions, mainly by reducing their growth rate and metabolic activity. Here, we uncover a novel strategy utilized by bacterial cells to resist aging by propagating rather than halting division. Bacterial aging was monitored by inspecting colonies of the Gram-positive soil bacterium Bacillus subtilis, which is capable of differentiating into various cell types under nutrient exhaustion. We revealed that after days of incubation, rejuvenating subpopulations, arrayed over the mother colony, emerged. These subpopulations were found to harbor mutations in a variety of genes, restricting the ability of the cells to differentiate. Surprisingly, even mutations that are not classically designated to developmental pathways, concluded in differentiation deficiency, indicating that multiple paths can reach this same outcome. We provide evidence that the evolved mutants continue to divide under conditions that favor entry into quiescence, hence becoming abundant within the aging population. The occurrence of such nondifferentiating mutants could impact bacterial population dynamics in natural niches. IMPORTANCE Until now, bacterial cells facing nutrient deprivation were shown to enter dormancy as a strategy to survive prolonged stress, with the most established examples being sporulation, stationary phase, and persistence. Here, we uncovered an opposing strategy for long-term bacterial survival, in which mutant subpopulations cope with a challenging niche by proliferating rather than by stalling division. We show that this feature stems from mutations in genes disturbing the capability of the cells to differentiate into a quiescent state, enabling them to divide under restrictive conditions. Our study challenges the dogma of bacterial aging by highlighting an additional survival strategy resembling that of cancerous cells in animal organs.
format article
author Rachel Hashuel
Sigal Ben-Yehuda
author_facet Rachel Hashuel
Sigal Ben-Yehuda
author_sort Rachel Hashuel
title Aging of a Bacterial Colony Enforces the Evolvement of Nondifferentiating Mutants
title_short Aging of a Bacterial Colony Enforces the Evolvement of Nondifferentiating Mutants
title_full Aging of a Bacterial Colony Enforces the Evolvement of Nondifferentiating Mutants
title_fullStr Aging of a Bacterial Colony Enforces the Evolvement of Nondifferentiating Mutants
title_full_unstemmed Aging of a Bacterial Colony Enforces the Evolvement of Nondifferentiating Mutants
title_sort aging of a bacterial colony enforces the evolvement of nondifferentiating mutants
publisher American Society for Microbiology
publishDate 2019
url https://doaj.org/article/9de18242ce864594aef92dbbff223fb6
work_keys_str_mv AT rachelhashuel agingofabacterialcolonyenforcestheevolvementofnondifferentiatingmutants
AT sigalbenyehuda agingofabacterialcolonyenforcestheevolvementofnondifferentiatingmutants
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