Nitrogen cost minimization is promoted by structural changes in the transcriptome of N-deprived Prochlorococcus cells

Prochlorococcus is a globally abundant marine cyanobacterium with many adaptations that reduce cellular nutrient requirements, facilitating growth in its nutrient-poor environment. One such genomic adaptation is the preferential utilization of amino acids containing fewer N-atoms, which minimizes ce...

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Bibliographic Details
Main Authors: Read, Robert W, Neveux, Iva, Grzymski, Joseph J, Berube, Paul M., Biller, Steven, Cubillos, Andres Fernando, Chisholm, Sallie (Penny)
Other Authors: Massachusetts Institute of Technology. Department of Biology
Format: Article
Published: Nature Publishing Group 2018
Online Access:http://hdl.handle.net/1721.1/117202
https://orcid.org/0000-0001-5598-6602
https://orcid.org/0000-0002-2638-823X
https://orcid.org/0000-0002-8566-5567
https://orcid.org/0000-0003-1480-2445
Description
Summary:Prochlorococcus is a globally abundant marine cyanobacterium with many adaptations that reduce cellular nutrient requirements, facilitating growth in its nutrient-poor environment. One such genomic adaptation is the preferential utilization of amino acids containing fewer N-atoms, which minimizes cellular nitrogen requirements. We predicted that transcriptional regulation might further reduce cellular N budgets during transient N limitation. To explore this, we compared transcription start sites (TSSs) in Prochlorococcus MED4 under N-deprived and N-replete conditions. Of 64 genes with primary and internal TSSs in both conditions, N-deprived cells initiated transcription downstream of primary TSSs more frequently than N-replete cells. Additionally, 117 genes with only an internal TSS demonstrated increased internal transcription under N-deprivation. These shortened transcripts encode predicted proteins with an average of 21% less N content compared to full-length transcripts. We hypothesized that low translation rates, which afford greater control over protein abundances, would be beneficial to relatively slow-growing organisms like Prochlorococcus. Consistent with this idea, we found that Prochlorococcus exhibits greater usage of glycine-glycine motifs, which causes translational pausing, when compared to faster growing microbes. Our findings indicate that structural changes occur within the Prochlorococcus MED4 transcriptome during N-deprivation, potentially altering the size and structure of proteins expressed under nutrient limitation.