Transcriptome and proteome dynamics of a light-dark synchronized bacterial cell cycle.

BACKGROUND: Growth of the ocean's most abundant primary producer, the cyanobacterium Prochlorococcus, is tightly synchronized to the natural 24-hour light-dark cycle. We sought to quantify the relationship between transcriptome and proteome dynamics that underlie this obligate photoautotroph�...

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Main Authors: Jacob R Waldbauer, Sébastien Rodrigue, Maureen L Coleman, Sallie W Chisholm
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2012-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC3430701?pdf=render
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spelling doaj-26d6a2db8f754989999ccc5c424e5e802020-11-25T01:18:26ZengPublic Library of Science (PLoS)PLoS ONE1932-62032012-01-0178e4343210.1371/journal.pone.0043432Transcriptome and proteome dynamics of a light-dark synchronized bacterial cell cycle.Jacob R WaldbauerSébastien RodrigueMaureen L ColemanSallie W ChisholmBACKGROUND: Growth of the ocean's most abundant primary producer, the cyanobacterium Prochlorococcus, is tightly synchronized to the natural 24-hour light-dark cycle. We sought to quantify the relationship between transcriptome and proteome dynamics that underlie this obligate photoautotroph's highly choreographed response to the daily oscillation in energy supply. METHODOLOGY/PRINCIPAL FINDINGS: Using RNA-sequencing transcriptomics and mass spectrometry-based quantitative proteomics, we measured timecourses of paired mRNA-protein abundances for 312 genes every 2 hours over a light-dark cycle. These temporal expression patterns reveal strong oscillations in transcript abundance that are broadly damped at the protein level, with mRNA levels varying on average 2.3 times more than the corresponding protein. The single strongest observed protein-level oscillation is in a ribonucleotide reductase, which may reflect a defense strategy against phage infection. The peak in abundance of most proteins also lags that of their transcript by 2-8 hours, and the two are completely antiphase for some genes. While abundant antisense RNA was detected, it apparently does not account for the observed divergences between expression levels. The redirection of flux through central carbon metabolism from daytime carbon fixation to nighttime respiration is associated with quite small changes in relative enzyme abundances. CONCLUSIONS/SIGNIFICANCE: Our results indicate that expression responses to periodic stimuli that are common in natural ecosystems (such as the diel cycle) can diverge significantly between the mRNA and protein levels. Protein expression patterns that are distinct from those of cognate mRNA have implications for the interpretation of transcriptome and metatranscriptome data in terms of cellular metabolism and its biogeochemical impact.http://europepmc.org/articles/PMC3430701?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Jacob R Waldbauer
Sébastien Rodrigue
Maureen L Coleman
Sallie W Chisholm
spellingShingle Jacob R Waldbauer
Sébastien Rodrigue
Maureen L Coleman
Sallie W Chisholm
Transcriptome and proteome dynamics of a light-dark synchronized bacterial cell cycle.
PLoS ONE
author_facet Jacob R Waldbauer
Sébastien Rodrigue
Maureen L Coleman
Sallie W Chisholm
author_sort Jacob R Waldbauer
title Transcriptome and proteome dynamics of a light-dark synchronized bacterial cell cycle.
title_short Transcriptome and proteome dynamics of a light-dark synchronized bacterial cell cycle.
title_full Transcriptome and proteome dynamics of a light-dark synchronized bacterial cell cycle.
title_fullStr Transcriptome and proteome dynamics of a light-dark synchronized bacterial cell cycle.
title_full_unstemmed Transcriptome and proteome dynamics of a light-dark synchronized bacterial cell cycle.
title_sort transcriptome and proteome dynamics of a light-dark synchronized bacterial cell cycle.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2012-01-01
description BACKGROUND: Growth of the ocean's most abundant primary producer, the cyanobacterium Prochlorococcus, is tightly synchronized to the natural 24-hour light-dark cycle. We sought to quantify the relationship between transcriptome and proteome dynamics that underlie this obligate photoautotroph's highly choreographed response to the daily oscillation in energy supply. METHODOLOGY/PRINCIPAL FINDINGS: Using RNA-sequencing transcriptomics and mass spectrometry-based quantitative proteomics, we measured timecourses of paired mRNA-protein abundances for 312 genes every 2 hours over a light-dark cycle. These temporal expression patterns reveal strong oscillations in transcript abundance that are broadly damped at the protein level, with mRNA levels varying on average 2.3 times more than the corresponding protein. The single strongest observed protein-level oscillation is in a ribonucleotide reductase, which may reflect a defense strategy against phage infection. The peak in abundance of most proteins also lags that of their transcript by 2-8 hours, and the two are completely antiphase for some genes. While abundant antisense RNA was detected, it apparently does not account for the observed divergences between expression levels. The redirection of flux through central carbon metabolism from daytime carbon fixation to nighttime respiration is associated with quite small changes in relative enzyme abundances. CONCLUSIONS/SIGNIFICANCE: Our results indicate that expression responses to periodic stimuli that are common in natural ecosystems (such as the diel cycle) can diverge significantly between the mRNA and protein levels. Protein expression patterns that are distinct from those of cognate mRNA have implications for the interpretation of transcriptome and metatranscriptome data in terms of cellular metabolism and its biogeochemical impact.
url http://europepmc.org/articles/PMC3430701?pdf=render
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