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A fitness trade-off between growth and survival governed by Spo0A-mediated proteome allocation constraints in Bacillus subtilis

Growth and survival are key determinants of bacterial fitness. However, how resource allocation of bacteria could reconcile these two traits to maximize fitness remains poorly understood. Here, we find that the resource allocation strategy of Bacillus subtilis does not lead to growth maximization on...

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Autores principales: Zhu, Manlu, Wang, Qian, Mu, Haoyan, Han, Fei, Wang, Yanling, Dai, Xiongfeng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Association for the Advancement of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10530083/
https://www.ncbi.nlm.nih.gov/pubmed/37756393
http://dx.doi.org/10.1126/sciadv.adg9733
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author Zhu, Manlu
Wang, Qian
Mu, Haoyan
Han, Fei
Wang, Yanling
Dai, Xiongfeng
author_facet Zhu, Manlu
Wang, Qian
Mu, Haoyan
Han, Fei
Wang, Yanling
Dai, Xiongfeng
author_sort Zhu, Manlu
collection PubMed
description Growth and survival are key determinants of bacterial fitness. However, how resource allocation of bacteria could reconcile these two traits to maximize fitness remains poorly understood. Here, we find that the resource allocation strategy of Bacillus subtilis does not lead to growth maximization on various carbon sources. Survival-related pathways impose strong proteome constraints on B. subtilis. Knockout of a master regulator gene, spo0A, triggers a global resource reallocation from survival-related pathways to biosynthesis pathways, further strongly stimulating the growth of B. subtilis. However, the fitness of spo0A-null strain is severely compromised because of various disadvantageous phenotypes (e.g., abolished sporulation and enhanced cell lysis). In particular, it also exhibits a strong defect in peptide utilization, being unable to efficiently recycle nutrients from the lysed cell debris to maintain long-term viability. Our work uncovers a fitness trade-off between growth and survival that governed by Spo0A-mediated proteome allocation constraints in B. subtilis, further shedding light on the fundamental design principle of bacteria.
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spelling pubmed-105300832023-09-28 A fitness trade-off between growth and survival governed by Spo0A-mediated proteome allocation constraints in Bacillus subtilis Zhu, Manlu Wang, Qian Mu, Haoyan Han, Fei Wang, Yanling Dai, Xiongfeng Sci Adv Biomedicine and Life Sciences Growth and survival are key determinants of bacterial fitness. However, how resource allocation of bacteria could reconcile these two traits to maximize fitness remains poorly understood. Here, we find that the resource allocation strategy of Bacillus subtilis does not lead to growth maximization on various carbon sources. Survival-related pathways impose strong proteome constraints on B. subtilis. Knockout of a master regulator gene, spo0A, triggers a global resource reallocation from survival-related pathways to biosynthesis pathways, further strongly stimulating the growth of B. subtilis. However, the fitness of spo0A-null strain is severely compromised because of various disadvantageous phenotypes (e.g., abolished sporulation and enhanced cell lysis). In particular, it also exhibits a strong defect in peptide utilization, being unable to efficiently recycle nutrients from the lysed cell debris to maintain long-term viability. Our work uncovers a fitness trade-off between growth and survival that governed by Spo0A-mediated proteome allocation constraints in B. subtilis, further shedding light on the fundamental design principle of bacteria. American Association for the Advancement of Science 2023-09-27 /pmc/articles/PMC10530083/ /pubmed/37756393 http://dx.doi.org/10.1126/sciadv.adg9733 Text en Copyright © 2023 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC). https://creativecommons.org/licenses/by-nc/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license (https://creativecommons.org/licenses/by-nc/4.0/) , which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.
spellingShingle Biomedicine and Life Sciences
Zhu, Manlu
Wang, Qian
Mu, Haoyan
Han, Fei
Wang, Yanling
Dai, Xiongfeng
A fitness trade-off between growth and survival governed by Spo0A-mediated proteome allocation constraints in Bacillus subtilis
title A fitness trade-off between growth and survival governed by Spo0A-mediated proteome allocation constraints in Bacillus subtilis
title_full A fitness trade-off between growth and survival governed by Spo0A-mediated proteome allocation constraints in Bacillus subtilis
title_fullStr A fitness trade-off between growth and survival governed by Spo0A-mediated proteome allocation constraints in Bacillus subtilis
title_full_unstemmed A fitness trade-off between growth and survival governed by Spo0A-mediated proteome allocation constraints in Bacillus subtilis
title_short A fitness trade-off between growth and survival governed by Spo0A-mediated proteome allocation constraints in Bacillus subtilis
title_sort fitness trade-off between growth and survival governed by spo0a-mediated proteome allocation constraints in bacillus subtilis
topic Biomedicine and Life Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10530083/
https://www.ncbi.nlm.nih.gov/pubmed/37756393
http://dx.doi.org/10.1126/sciadv.adg9733
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