Abstract
BackgroundRNA 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.ResultsUsing 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.ConclusionsWe 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.
Highlights
RNA turnover plays an important role in the gene regulation of microorganisms and influences their speed of acclimation to environmental changes
A genome-wide analysis showed that the half-lives of the vast majority of Escherichia coli transcripts do not differ with growth rate [5], suggesting an inherent median global half-life for a certain organism
We applied two different approaches: the so-called 'twofold' decay step method as proposed previously by Selinger et al [7] in order to determine the RNA half-life; and a new method developed here based on fitting the decay profile to two distinct phases to derive the decay rate
Summary
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. The investigation of global RNA half-lives of archaea, which have intermediate growth rates, led to conflicting conclusions, with one study showing global half-lives similar to bacteria [11] and another showing considerably longer half-lives [12]. To help resolve this issue we examined the global RNA half-live in the slow growing marine cyanobacterium Prochlorococcus MED4
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