Coordinating Bacterial Cell Division with Nutrient Availability: a Role for Glycolysis

ABSTRACT Cell division in bacteria is driven by a cytoskeletal ring structure, the Z ring, composed of polymers of the tubulin-like protein FtsZ. Z-ring formation must be tightly regulated to ensure faithful cell division, and several mechanisms that influence the positioning and timing of Z-ring as...

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Autores principales:	Leigh G. Monahan, Isabella V. Hajduk, Sinead P. Blaber, Ian G. Charles, Elizabeth J. Harry
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2014
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/bc7740a829ed4f15a6811fe9d7cba683
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spelling	oai:doaj.org-article:bc7740a829ed4f15a6811fe9d7cba6832021-11-15T15:47:38ZCoordinating Bacterial Cell Division with Nutrient Availability: a Role for Glycolysis10.1128/mBio.00935-142150-7511https://doaj.org/article/bc7740a829ed4f15a6811fe9d7cba6832014-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00935-14https://doaj.org/toc/2150-7511ABSTRACT Cell division in bacteria is driven by a cytoskeletal ring structure, the Z ring, composed of polymers of the tubulin-like protein FtsZ. Z-ring formation must be tightly regulated to ensure faithful cell division, and several mechanisms that influence the positioning and timing of Z-ring assembly have been described. Another important but as yet poorly understood aspect of cell division regulation is the need to coordinate division with cell growth and nutrient availability. In this study, we demonstrated for the first time that cell division is intimately linked to central carbon metabolism in the model Gram-positive bacterium Bacillus subtilis. We showed that a deletion of the gene encoding pyruvate kinase (pyk), which produces pyruvate in the final reaction of glycolysis, rescues the assembly defect of a temperature-sensitive ftsZ mutant and has significant effects on Z-ring formation in wild-type B. subtilis cells. Addition of exogenous pyruvate restores normal division in the absence of the pyruvate kinase enzyme, implicating pyruvate as a key metabolite in the coordination of bacterial growth and division. Our results support a model in which pyruvate levels are coupled to Z-ring assembly via an enzyme that actually metabolizes pyruvate, the E1α subunit of pyruvate dehydrogenase. We have shown that this protein localizes over the nucleoid in a pyruvate-dependent manner and may stimulate more efficient Z-ring formation at the cell center under nutrient-rich conditions, when cells must divide more frequently.IMPORTANCE How bacteria coordinate cell cycle processes with nutrient availability and growth is a fundamental yet unresolved question in microbiology. Recent breakthroughs have revealed that nutritional information can be transmitted directly from metabolic pathways to the cell cycle machinery and that this can serve as a mechanism for fine-tuning cell cycle processes in response to changes in environmental conditions. Here we identified a novel link between glycolysis and cell division in Bacillus subtilis. We showed that pyruvate, the final product of glycolysis, plays an important role in maintaining normal division. Nutrient-dependent changes in pyruvate levels affect the function of the cell division protein FtsZ, most likely by modifying the activity of an enzyme that metabolizes pyruvate, namely, pyruvate dehydrogenase E1α. Ultimately this system may help to coordinate bacterial division with nutritional conditions to ensure the survival of newborn cells.Leigh G. MonahanIsabella V. HajdukSinead P. BlaberIan G. CharlesElizabeth J. HarryAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 3 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Leigh G. Monahan Isabella V. Hajduk Sinead P. Blaber Ian G. Charles Elizabeth J. Harry Coordinating Bacterial Cell Division with Nutrient Availability: a Role for Glycolysis
description	ABSTRACT Cell division in bacteria is driven by a cytoskeletal ring structure, the Z ring, composed of polymers of the tubulin-like protein FtsZ. Z-ring formation must be tightly regulated to ensure faithful cell division, and several mechanisms that influence the positioning and timing of Z-ring assembly have been described. Another important but as yet poorly understood aspect of cell division regulation is the need to coordinate division with cell growth and nutrient availability. In this study, we demonstrated for the first time that cell division is intimately linked to central carbon metabolism in the model Gram-positive bacterium Bacillus subtilis. We showed that a deletion of the gene encoding pyruvate kinase (pyk), which produces pyruvate in the final reaction of glycolysis, rescues the assembly defect of a temperature-sensitive ftsZ mutant and has significant effects on Z-ring formation in wild-type B. subtilis cells. Addition of exogenous pyruvate restores normal division in the absence of the pyruvate kinase enzyme, implicating pyruvate as a key metabolite in the coordination of bacterial growth and division. Our results support a model in which pyruvate levels are coupled to Z-ring assembly via an enzyme that actually metabolizes pyruvate, the E1α subunit of pyruvate dehydrogenase. We have shown that this protein localizes over the nucleoid in a pyruvate-dependent manner and may stimulate more efficient Z-ring formation at the cell center under nutrient-rich conditions, when cells must divide more frequently.IMPORTANCE How bacteria coordinate cell cycle processes with nutrient availability and growth is a fundamental yet unresolved question in microbiology. Recent breakthroughs have revealed that nutritional information can be transmitted directly from metabolic pathways to the cell cycle machinery and that this can serve as a mechanism for fine-tuning cell cycle processes in response to changes in environmental conditions. Here we identified a novel link between glycolysis and cell division in Bacillus subtilis. We showed that pyruvate, the final product of glycolysis, plays an important role in maintaining normal division. Nutrient-dependent changes in pyruvate levels affect the function of the cell division protein FtsZ, most likely by modifying the activity of an enzyme that metabolizes pyruvate, namely, pyruvate dehydrogenase E1α. Ultimately this system may help to coordinate bacterial division with nutritional conditions to ensure the survival of newborn cells.
format	article
author	Leigh G. Monahan Isabella V. Hajduk Sinead P. Blaber Ian G. Charles Elizabeth J. Harry
author_facet	Leigh G. Monahan Isabella V. Hajduk Sinead P. Blaber Ian G. Charles Elizabeth J. Harry
author_sort	Leigh G. Monahan
title	Coordinating Bacterial Cell Division with Nutrient Availability: a Role for Glycolysis
title_short	Coordinating Bacterial Cell Division with Nutrient Availability: a Role for Glycolysis
title_full	Coordinating Bacterial Cell Division with Nutrient Availability: a Role for Glycolysis
title_fullStr	Coordinating Bacterial Cell Division with Nutrient Availability: a Role for Glycolysis
title_full_unstemmed	Coordinating Bacterial Cell Division with Nutrient Availability: a Role for Glycolysis
title_sort	coordinating bacterial cell division with nutrient availability: a role for glycolysis
publisher	American Society for Microbiology
publishDate	2014
url	https://doaj.org/article/bc7740a829ed4f15a6811fe9d7cba683
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Coordinating Bacterial Cell Division with Nutrient Availability: a Role for Glycolysis

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