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Escherichia coli translation strategies differ across carbon, nitrogen and phosphorus limitation conditions.

ABSTRACT: For cells to grow faster they must increase their protein production rate. Microorganisms have traditionally been thought to accomplish this increase by producing more ribosomes to enhance protein synthesis capacity, leading to the linear relationship between ribosome level and growth rate observed under most growth conditions previously examined. Past studies have suggested that this linear relationship represents an optimal resource allocation strategy for each growth rate, independent of any specific nutrient state. Here we investigate protein production strategies in continuous cultures limited for carbon, nitrogen and phosphorus, which differentially impact substrate supply for protein versus nucleic acid metabolism. Unexpectedly, we find that at slow growth rates, Escherichia coli achieves the same protein production rate using three different strategies under the three different nutrient limitations. Under phosphorus (P) limitation, translation is slow due to a particularly low abundance of ribosomes, which are RNA-rich and thus particularly costly for phosphorous-limited cells. Under nitrogen (N) limitation, translation elongation is slowed by processes including ribosome stalling at glutamine codons. Under carbon (C) limitation, translation is slowed by accumulation of inactive ribosomes not bound to messenger RNA. These extra ribosomes enable rapid growth acceleration during nutrient upshift. Thus, bacteria tune ribosome usage across different limiting nutrients to enable balanced nutrient-limited growth while also preparing for future nutrient upshifts.

SUBMITTER: Li SH

PROVIDER: S-EPMC6278830 | biostudies-literature | 2018 Aug

REPOSITORIES: biostudies-literature

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Escherichia coli translation strategies differ across carbon, nitrogen and phosphorus limitation conditions.

Li Sophia Hsin-Jung SH Li Zhiyuan Z Park Junyoung O JO King Christopher G CG Rabinowitz Joshua D JD Wingreen Ned S NS Gitai Zemer Z

Nature microbiology 20180723 8

For cells to grow faster they must increase their protein production rate. Microorganisms have traditionally been thought to accomplish this increase by producing more ribosomes to enhance protein synthesis capacity, leading to the linear relationship between ribosome level and growth rate observed under most growth conditions previously examined. Past studies have suggested that this linear relationship represents an optimal resource allocation strategy for each growth rate, independent of any ...[more]

PMID: 30038306

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Project description:Gene expression profiles of Escherichia coli, grown anaerobically, with or without Acacia mearnsii (Black wattle) extract were compared to identify tannin-resistance strategies. The cell envelope stress protein, spy, and the multidrug transporter-encoding mdtABCD, both under the control of the BaeSR two-component regulatory system, were significantly up-regulated in the presence of tannins. BaeSR mutants were more tannin-sensitive than their wild-type counterparts. Experiment Overall Design: E. coli BW13711 cells were grown anaerobically in continuous culture (d = 0.14h-1) in the presence and absence of Acacia mearnsii (Black Wattle) tannin extract (WTE) at 37Â°C. Under both steady state conditions, E. coli reached an OD600 of ~0.2. The pH at steady-state was 5.7 and 5.3 without and with WTE, respectively. These conditions indicated that the presence of tannins in the medium did not inhibit the growth of E. coli. E. coli BW13711 cells were harvested from continuous culture after steady-state conditions were reached. Duplicate samples were collected after an additional four volume turnover of the culture medium and total RNA was isolated from these samples using the RNeasy mini kit (Qiagen Inc., Valencia, CA). The presence of residual DNA was checked by PCR using the primers for amplification of cca. If necessary, the remaining DNA was removed by RQ1 RNase-Free DNase (Promega corp, Madison, WI) according to the manufacturerâs instructions. E. coli whole genome transcriptional profiling was performed by hybridization on the GeneChipÂ® E. coli Antisense Genome Array (Affymetrix Inc., Santa Clara, CA) according to the manufacturerâs instructions. Microarray data were analyzed using MicroArray Suite 5.0 (Affymetrix Inc.) and GeneSpring 5.0 (Silicon Genetics, Redwood City, CA) software. The 95% confidence interval of the WTE array duplicates demonstrated that genes >1.9 times up- or down-regulated could be considered as significantly differentially regulated. After removing significantly up- or down-regulated genes which had large variability in expression on the duplicate arrays, it was found that in total 1,498 genes were up- or down-regulated

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Escherichia coli translation strategies differ across carbon, nitrogen and phosphorus limitation conditions.

Publications

Escherichia coli translation strategies differ across carbon, nitrogen and phosphorus limitation conditions.

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