Escherichia coli protein synthesis is limited by mRNA availability rather than ribosomal capacity during phosphate starvation
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Escherichia coli protein synthesis is limited by mRNA availability rather than ribosomal capacity during phosphate starvation. / Espinosa, Rocio; Sørensen, Michael Askvad; Svenningsen, Sine Lo.
In: Frontiers in Microbiology, Vol. 13, 989818, 2022.Research output: Contribution to journal › Journal article › Research › peer-review
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TY - JOUR
T1 - Escherichia coli protein synthesis is limited by mRNA availability rather than ribosomal capacity during phosphate starvation
AU - Espinosa, Rocio
AU - Sørensen, Michael Askvad
AU - Svenningsen, Sine Lo
N1 - Publisher Copyright: Copyright © 2022 Espinosa, Sørensen and Svenningsen.
PY - 2022
Y1 - 2022
N2 - 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.
AB - 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.
KW - bacterial stress response
KW - Escherichia coli
KW - macromolecular synthesis
KW - phosphate starvation
KW - protein synthesis regulation
KW - resource allocation
KW - rRNA stability
U2 - 10.3389/fmicb.2022.989818
DO - 10.3389/fmicb.2022.989818
M3 - Journal article
C2 - 36620012
AN - SCOPUS:85145722797
VL - 13
JO - Frontiers in Microbiology
JF - Frontiers in Microbiology
SN - 1664-302X
M1 - 989818
ER -
ID: 332936500