Escherichia coli protein synthesis is limited by mRNA availability rather than ribosomal capacity during phosphate starvation
Protein synthesis is the most energetically costly process in the cell. Consequently, it is a tightly regulated process, and regulation of the resources allocated to the protein synthesis machinery is at the heart of bacterial growth optimization theory. However, the molecular mechanisms that result...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-12-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2022.989818/full |
| _version_ | 1797979323535196160 |
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| author | Rocio Espinosa Michael Askvad Sørensen Sine Lo Svenningsen |
| author_facet | Rocio Espinosa Michael Askvad Sørensen Sine Lo Svenningsen |
| author_sort | Rocio Espinosa |
| collection | DOAJ |
| description | Protein synthesis is the most energetically costly process in the cell. Consequently, it is a tightly regulated process, and regulation of the resources allocated to the protein synthesis machinery is at the heart of bacterial growth optimization theory. However, the molecular mechanisms that result in dynamic downregulation of protein synthesis in response to nutrient starvation are not well described. Here, we first quantify the Escherichia coli response to phosphate starvation at the level of accumulation rates for protein, RNA and DNA. Escherichia coli maintains a low level of protein synthesis for hours after the removal of phosphate while the RNA contents decrease, primarily as a consequence of ribosomal RNA degradation combined with a reduced RNA synthesis rate. To understand the molecular basis for the low protein synthesis rate of phosphate-starved cells, template mRNA for translation was overproduced in the form of a highly induced long-lived mRNA. Remarkably, starved cells increased the rate of protein synthesis and reduced the rate of ribosomal RNA degradation upon mRNA induction. These observations suggest that protein synthesis in phosphate-starved cells is primarily limited by the availability of template, and does not operate at the maximum capacity of the ribosomes. We suggest that mRNA limitation is an adaptive response to phosphate starvation that prevents the deleterious consequences of overcommitting resources to protein synthesis. Moreover, our results support the model that degradation of ribosomal RNA occurs as a consequence of the availability of idle ribosomal subunits. |
| first_indexed | 2024-04-11T05:37:12Z |
| format | Article |
| id | doaj.art-a5f9c669cbb04a8ba650a40882b6eb8a |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-04-11T05:37:12Z |
| publishDate | 2022-12-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-a5f9c669cbb04a8ba650a40882b6eb8a2022-12-22T10:31:46ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-12-011310.3389/fmicb.2022.989818989818Escherichia coli protein synthesis is limited by mRNA availability rather than ribosomal capacity during phosphate starvationRocio EspinosaMichael Askvad SørensenSine Lo SvenningsenProtein synthesis is the most energetically costly process in the cell. Consequently, it is a tightly regulated process, and regulation of the resources allocated to the protein synthesis machinery is at the heart of bacterial growth optimization theory. However, the molecular mechanisms that result in dynamic downregulation of protein synthesis in response to nutrient starvation are not well described. Here, we first quantify the Escherichia coli response to phosphate starvation at the level of accumulation rates for protein, RNA and DNA. Escherichia coli maintains a low level of protein synthesis for hours after the removal of phosphate while the RNA contents decrease, primarily as a consequence of ribosomal RNA degradation combined with a reduced RNA synthesis rate. To understand the molecular basis for the low protein synthesis rate of phosphate-starved cells, template mRNA for translation was overproduced in the form of a highly induced long-lived mRNA. Remarkably, starved cells increased the rate of protein synthesis and reduced the rate of ribosomal RNA degradation upon mRNA induction. These observations suggest that protein synthesis in phosphate-starved cells is primarily limited by the availability of template, and does not operate at the maximum capacity of the ribosomes. We suggest that mRNA limitation is an adaptive response to phosphate starvation that prevents the deleterious consequences of overcommitting resources to protein synthesis. Moreover, our results support the model that degradation of ribosomal RNA occurs as a consequence of the availability of idle ribosomal subunits.https://www.frontiersin.org/articles/10.3389/fmicb.2022.989818/fullphosphate starvationprotein synthesis regulationmacromolecular synthesisresource allocationrRNA stabilitybacterial stress response |
| spellingShingle | Rocio Espinosa Michael Askvad Sørensen Sine Lo Svenningsen Escherichia coli protein synthesis is limited by mRNA availability rather than ribosomal capacity during phosphate starvation Frontiers in Microbiology phosphate starvation protein synthesis regulation macromolecular synthesis resource allocation rRNA stability bacterial stress response |
| title | Escherichia coli protein synthesis is limited by mRNA availability rather than ribosomal capacity during phosphate starvation |
| title_full | Escherichia coli protein synthesis is limited by mRNA availability rather than ribosomal capacity during phosphate starvation |
| title_fullStr | Escherichia coli protein synthesis is limited by mRNA availability rather than ribosomal capacity during phosphate starvation |
| title_full_unstemmed | Escherichia coli protein synthesis is limited by mRNA availability rather than ribosomal capacity during phosphate starvation |
| title_short | Escherichia coli protein synthesis is limited by mRNA availability rather than ribosomal capacity during phosphate starvation |
| title_sort | escherichia coli protein synthesis is limited by mrna availability rather than ribosomal capacity during phosphate starvation |
| topic | phosphate starvation protein synthesis regulation macromolecular synthesis resource allocation rRNA stability bacterial stress response |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2022.989818/full |
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