Absolute Measurements of mRNA Translation in <named-content content-type="genus-species">Caulobacter crescentus</named-content> Reveal Important Fitness Costs of Vitamin B<sub>12</sub> Scavenging

ABSTRACT Caulobacter crescentus is a model for the bacterial cell cycle which culminates in asymmetric cell division, yet little is known about the absolute levels of protein synthesis of the cellular parts needed to complete the cell cycle. Here we utilize ribosome profiling to provide absolute mea...

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Autores principales:	James R. Aretakis, Alisa Gega, Jared M. Schrader
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	absolute quantitation Caulobacter crescentus ribosome profiling vitamin B12 cell cycle Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/72a8efd141df4b4dba189498d8abf481
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spelling	oai:doaj.org-article:72a8efd141df4b4dba189498d8abf4812021-12-02T19:46:18ZAbsolute Measurements of mRNA Translation in <named-content content-type="genus-species">Caulobacter crescentus</named-content> Reveal Important Fitness Costs of Vitamin B<sub>12</sub> Scavenging10.1128/mSystems.00170-192379-5077https://doaj.org/article/72a8efd141df4b4dba189498d8abf4812019-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00170-19https://doaj.org/toc/2379-5077ABSTRACT Caulobacter crescentus is a model for the bacterial cell cycle which culminates in asymmetric cell division, yet little is known about the absolute levels of protein synthesis of the cellular parts needed to complete the cell cycle. Here we utilize ribosome profiling to provide absolute measurements of mRNA translation in C. crescentus, providing an important resource with quantitative genome-wide measurements of protein output across individual genes. Analysis of protein synthesis rates revealed ∼4.5% of cellular protein synthesis is for genes related to vitamin B12 import (btuB) and B12-independent methionine biosynthesis (metE) when grown in common growth media lacking B12. While its facultative B12 lifestyle provides a fitness advantage in the absence of B12, we find that it provides a fitness disadvantage of the cells in the presence of B12, potentially explaining why many Caulobacter species have lost the metE gene and become obligates for B12. IMPORTANCE Caulobacter crescentus is a model system of the bacterial cell cycle culminating in asymmetric cell division, with each daughter cell inheriting a distinct set of proteins. While a genetic network of master transcription factors coordinates the cell cycle timing of transcription for nearly 20% of Caulobacter genes, we lack knowledge of how many of each protein “part” encoded in the genome are synthesized. Therefore, to determine the absolute production rates across the genome, we performed ribosome profiling, providing, for the first time, a quantitative resource with measurements of each protein “part” needed to generate daughter cells. This resource furthers the goal of a systems-level understanding of the genetic network controlling asymmetric cell division. To highlight the utility of this data set, we probe the protein synthesis cost of a B12 utilization pathway and provide new insights into Caulobacter’s adaptation to its natural environments. Author Video: An author video summary of this article is available.James R. AretakisAlisa GegaJared M. SchraderAmerican Society for Microbiologyarticleabsolute quantitationCaulobacter crescentusribosome profilingvitamin B12cell cycleMicrobiologyQR1-502ENmSystems, Vol 4, Iss 4 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	absolute quantitation Caulobacter crescentus ribosome profiling vitamin B12 cell cycle Microbiology QR1-502
spellingShingle	absolute quantitation Caulobacter crescentus ribosome profiling vitamin B12 cell cycle Microbiology QR1-502 James R. Aretakis Alisa Gega Jared M. Schrader Absolute Measurements of mRNA Translation in <named-content content-type="genus-species">Caulobacter crescentus</named-content> Reveal Important Fitness Costs of Vitamin B<sub>12</sub> Scavenging
description	ABSTRACT Caulobacter crescentus is a model for the bacterial cell cycle which culminates in asymmetric cell division, yet little is known about the absolute levels of protein synthesis of the cellular parts needed to complete the cell cycle. Here we utilize ribosome profiling to provide absolute measurements of mRNA translation in C. crescentus, providing an important resource with quantitative genome-wide measurements of protein output across individual genes. Analysis of protein synthesis rates revealed ∼4.5% of cellular protein synthesis is for genes related to vitamin B12 import (btuB) and B12-independent methionine biosynthesis (metE) when grown in common growth media lacking B12. While its facultative B12 lifestyle provides a fitness advantage in the absence of B12, we find that it provides a fitness disadvantage of the cells in the presence of B12, potentially explaining why many Caulobacter species have lost the metE gene and become obligates for B12. IMPORTANCE Caulobacter crescentus is a model system of the bacterial cell cycle culminating in asymmetric cell division, with each daughter cell inheriting a distinct set of proteins. While a genetic network of master transcription factors coordinates the cell cycle timing of transcription for nearly 20% of Caulobacter genes, we lack knowledge of how many of each protein “part” encoded in the genome are synthesized. Therefore, to determine the absolute production rates across the genome, we performed ribosome profiling, providing, for the first time, a quantitative resource with measurements of each protein “part” needed to generate daughter cells. This resource furthers the goal of a systems-level understanding of the genetic network controlling asymmetric cell division. To highlight the utility of this data set, we probe the protein synthesis cost of a B12 utilization pathway and provide new insights into Caulobacter’s adaptation to its natural environments. Author Video: An author video summary of this article is available.
format	article
author	James R. Aretakis Alisa Gega Jared M. Schrader
author_facet	James R. Aretakis Alisa Gega Jared M. Schrader
author_sort	James R. Aretakis
title	Absolute Measurements of mRNA Translation in <named-content content-type="genus-species">Caulobacter crescentus</named-content> Reveal Important Fitness Costs of Vitamin B<sub>12</sub> Scavenging
title_short	Absolute Measurements of mRNA Translation in <named-content content-type="genus-species">Caulobacter crescentus</named-content> Reveal Important Fitness Costs of Vitamin B<sub>12</sub> Scavenging
title_full	Absolute Measurements of mRNA Translation in <named-content content-type="genus-species">Caulobacter crescentus</named-content> Reveal Important Fitness Costs of Vitamin B<sub>12</sub> Scavenging
title_fullStr	Absolute Measurements of mRNA Translation in <named-content content-type="genus-species">Caulobacter crescentus</named-content> Reveal Important Fitness Costs of Vitamin B<sub>12</sub> Scavenging
title_full_unstemmed	Absolute Measurements of mRNA Translation in <named-content content-type="genus-species">Caulobacter crescentus</named-content> Reveal Important Fitness Costs of Vitamin B<sub>12</sub> Scavenging
title_sort	absolute measurements of mrna translation in <named-content content-type="genus-species">caulobacter crescentus</named-content> reveal important fitness costs of vitamin b<sub>12</sub> scavenging
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/72a8efd141df4b4dba189498d8abf481
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_version_	1718376031833817088

Absolute Measurements of mRNA Translation in <named-content content-type="genus-species">Caulobacter crescentus</named-content> Reveal Important Fitness Costs of Vitamin B<sub>12</sub> Scavenging

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