Short RNA half-lives in the slow-growing marine cyanobacterium Prochlorococcus

Background RNA turnover plays an important role in the gene regulation of microorganisms and influences their speed of acclimation to environmental changes. We investigated whole-genome RNA stability of Prochlorococcus, a relatively slow-growing marine cyanobacterium doubling approximately once a da...

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Main Authors: Steglich, Claudia, Lindell, Debbie, Futschik, Matthias, Rector, Trent, Steen, Robert, Chisholm, Sallie (Penny)
Other Authors: Massachusetts Institute of Technology. Department of Civil and Environmental Engineering
Format: Article
Language:English
Published: BioMed Central Ltd 2012
Online Access:http://hdl.handle.net/1721.1/69653
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author Steglich, Claudia
Lindell, Debbie
Futschik, Matthias
Rector, Trent
Steen, Robert
Chisholm, Sallie (Penny)
author2 Massachusetts Institute of Technology. Department of Civil and Environmental Engineering
author_facet Massachusetts Institute of Technology. Department of Civil and Environmental Engineering
Steglich, Claudia
Lindell, Debbie
Futschik, Matthias
Rector, Trent
Steen, Robert
Chisholm, Sallie (Penny)
author_sort Steglich, Claudia
collection MIT
description Background RNA turnover plays an important role in the gene regulation of microorganisms and influences their speed of acclimation to environmental changes. We investigated whole-genome RNA stability of Prochlorococcus, a relatively slow-growing marine cyanobacterium doubling approximately once a day, which is extremely abundant in the oceans. Results Using a combination of microarrays, quantitative RT-PCR and a new fitting method for determining RNA decay rates, we found a median half-life of 2.4 minutes and a median decay rate of 2.6 minutes for expressed genes - twofold faster than that reported for any organism. The shortest transcript half-life (33 seconds) was for a gene of unknown function, while some of the longest (approximately 18 minutes) were for genes with high transcript levels. Genes organized in operons displayed intriguing mRNA decay patterns, such as increased stability, and delayed onset of decay with greater distance from the transcriptional start site. The same phenomenon was observed on a single probe resolution for genes greater than 2 kb. Conclusions We hypothesize that the fast turnover relative to the slow generation time in Prochlorococcus may enable a swift response to environmental changes through rapid recycling of nucleotides, which could be advantageous in nutrient poor oceans. Our growing understanding of RNA half-lives will help us interpret the growing bank of metatranscriptomic studies of wild populations of Prochlorococcus. The surprisingly complex decay patterns of large transcripts reported here, and the method developed to describe them, will open new avenues for the investigation and understanding of RNA decay for all organisms.
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spelling mit-1721.1/696532022-09-26T15:45:43Z Short RNA half-lives in the slow-growing marine cyanobacterium Prochlorococcus Steglich, Claudia Lindell, Debbie Futschik, Matthias Rector, Trent Steen, Robert Chisholm, Sallie (Penny) Massachusetts Institute of Technology. Department of Civil and Environmental Engineering Lindell, Debbie Chisholm, Sallie (Penny) Steglich, Claudia Background RNA turnover plays an important role in the gene regulation of microorganisms and influences their speed of acclimation to environmental changes. We investigated whole-genome RNA stability of Prochlorococcus, a relatively slow-growing marine cyanobacterium doubling approximately once a day, which is extremely abundant in the oceans. Results Using a combination of microarrays, quantitative RT-PCR and a new fitting method for determining RNA decay rates, we found a median half-life of 2.4 minutes and a median decay rate of 2.6 minutes for expressed genes - twofold faster than that reported for any organism. The shortest transcript half-life (33 seconds) was for a gene of unknown function, while some of the longest (approximately 18 minutes) were for genes with high transcript levels. Genes organized in operons displayed intriguing mRNA decay patterns, such as increased stability, and delayed onset of decay with greater distance from the transcriptional start site. The same phenomenon was observed on a single probe resolution for genes greater than 2 kb. Conclusions We hypothesize that the fast turnover relative to the slow generation time in Prochlorococcus may enable a swift response to environmental changes through rapid recycling of nucleotides, which could be advantageous in nutrient poor oceans. Our growing understanding of RNA half-lives will help us interpret the growing bank of metatranscriptomic studies of wild populations of Prochlorococcus. The surprisingly complex decay patterns of large transcripts reported here, and the method developed to describe them, will open new avenues for the investigation and understanding of RNA decay for all organisms. Deutsche Forschungsgemeinschaft (DFG (SPP 1258)) German-Israeli Foundation for Scientific Research and Development (GIF (young investigator grant 2167-1743.9/2007)) National Science Foundation (U.S.) United States. Dept. of Energy (DOE-GTL grant) Gordon and Betty Moore Foundation (Investigatorship) Israel Science Foundation (Morasha grant 1504/06) Fundação para a Ciência e a Tecnologia (FCT grant (IBB/CBME, LA, FEDER/POCI 2010)) 2012-03-14T16:37:09Z 2012-03-14T16:37:09Z 2010-05 2010-03 2012-02-23T16:07:11Z Article http://purl.org/eprint/type/JournalArticle http://hdl.handle.net/1721.1/69653 Steglich, Claudia et al. “Short RNA Half-lives in the Slow-growing Marine Cyanobacterium Prochlorococcus.” Genome Biology 11.5 (2010): R54. en http://dx.doi.org/10.1186/gb-2010-11-5-r54 Genome Biology Creative Commons Attribution http://creativecommons.org/licenses/by/2.0 Steglich et al.; licensee BioMed Central Ltd. application/pdf BioMed Central Ltd BioMed Central Ltd
spellingShingle Steglich, Claudia
Lindell, Debbie
Futschik, Matthias
Rector, Trent
Steen, Robert
Chisholm, Sallie (Penny)
Short RNA half-lives in the slow-growing marine cyanobacterium Prochlorococcus
title Short RNA half-lives in the slow-growing marine cyanobacterium Prochlorococcus
title_full Short RNA half-lives in the slow-growing marine cyanobacterium Prochlorococcus
title_fullStr Short RNA half-lives in the slow-growing marine cyanobacterium Prochlorococcus
title_full_unstemmed Short RNA half-lives in the slow-growing marine cyanobacterium Prochlorococcus
title_short Short RNA half-lives in the slow-growing marine cyanobacterium Prochlorococcus
title_sort short rna half lives in the slow growing marine cyanobacterium prochlorococcus
url http://hdl.handle.net/1721.1/69653
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