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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Nature Publishing Group
2018
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| 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 |
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| author | Read, Robert W Neveux, Iva Grzymski, Joseph J Berube, Paul M. Biller, Steven Cubillos, Andres Fernando Chisholm, Sallie (Penny) |
| author2 | Massachusetts Institute of Technology. Department of Biology |
| author_facet | Massachusetts Institute of Technology. Department of Biology Read, Robert W Neveux, Iva Grzymski, Joseph J Berube, Paul M. Biller, Steven Cubillos, Andres Fernando Chisholm, Sallie (Penny) |
| author_sort | Read, Robert W |
| collection | MIT |
| description | 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. |
| first_indexed | 2024-09-23T10:02:36Z |
| format | Article |
| id | mit-1721.1/117202 |
| institution | Massachusetts Institute of Technology |
| last_indexed | 2024-09-23T10:02:36Z |
| publishDate | 2018 |
| publisher | Nature Publishing Group |
| record_format | dspace |
| spelling | mit-1721.1/1172022022-09-30T18:32:28Z Nitrogen cost minimization is promoted by structural changes in the transcriptome of N-deprived Prochlorococcus cells Read, Robert W Neveux, Iva Grzymski, Joseph J Berube, Paul M. Biller, Steven Cubillos, Andres Fernando Chisholm, Sallie (Penny) Massachusetts Institute of Technology. Department of Biology Massachusetts Institute of Technology. Department of Civil and Environmental Engineering Massachusetts Institute of Technology. Microbiology Graduate Program Berube, Paul M. Biller, Steven Cubillos, Andres Fernando Chisholm, Sallie W 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. Gordon and Betty Moore Foundation (Grant GBMF495) Simons Foundation (Award 329108) National Science Foundation (U.S.) (Grant DBI-0424599) 2018-07-30T18:25:07Z 2018-07-30T18:25:07Z 2017-06 2017-04 2018-07-30T17:45:23Z Article http://purl.org/eprint/type/JournalArticle 1751-7362 1751-7370 http://hdl.handle.net/1721.1/117202 Read, Robert W et al. “Nitrogen Cost Minimization Is Promoted by Structural Changes in the Transcriptome of N-Deprived Prochlorococcus Cells.” The ISME Journal 11, 10 (June 2017): 2267–2278 © 2017 International Society for Microbial Ecology 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 http://dx.doi.org/10.1038/ISMEJ.2017.88 ISME Journal Creative Commons Attribution 4.0 International License http://creativecommons.org/licenses/by/4.0/ application/pdf Nature Publishing Group Nature |
| spellingShingle | Read, Robert W Neveux, Iva Grzymski, Joseph J Berube, Paul M. Biller, Steven Cubillos, Andres Fernando Chisholm, Sallie (Penny) Nitrogen cost minimization is promoted by structural changes in the transcriptome of N-deprived Prochlorococcus cells |
| title | Nitrogen cost minimization is promoted by structural changes in the transcriptome of N-deprived Prochlorococcus cells |
| title_full | Nitrogen cost minimization is promoted by structural changes in the transcriptome of N-deprived Prochlorococcus cells |
| title_fullStr | Nitrogen cost minimization is promoted by structural changes in the transcriptome of N-deprived Prochlorococcus cells |
| title_full_unstemmed | Nitrogen cost minimization is promoted by structural changes in the transcriptome of N-deprived Prochlorococcus cells |
| title_short | Nitrogen cost minimization is promoted by structural changes in the transcriptome of N-deprived Prochlorococcus cells |
| title_sort | nitrogen cost minimization is promoted by structural changes in the transcriptome of n deprived prochlorococcus cells |
| url | 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 |
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