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Chromosome and plasmid-borne PLacO3O1 promoters differ in sensitivity to critically low temperatures

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Chromosome and plasmid-borne PLacO3O1 promoters differ in sensitivity to critically low temperatures. / Oliveira, Samuel M.D.; Goncalves, Nadia S.M.; Kandavalli, Vinodh K.; Martins, Leonardo; Neeli-Venkata, Ramakanth; Reyelt, Jan; Fonseca, Jose M; Lloyd-Price, Jason; Kranz, Harald; Ribeiro, Andre S.

In: Scientific Reports, Vol. 9, 4486, 14.03.2019.

Research output: Contribution to journalArticleScientificpeer-review

Harvard

Oliveira, SMD, Goncalves, NSM, Kandavalli, VK, Martins, L, Neeli-Venkata, R, Reyelt, J, Fonseca, JM, Lloyd-Price, J, Kranz, H & Ribeiro, AS 2019, 'Chromosome and plasmid-borne PLacO3O1 promoters differ in sensitivity to critically low temperatures', Scientific Reports, vol. 9, 4486. https://doi.org/10.1038/s41598-019-39618-z

APA

Oliveira, S. M. D., Goncalves, N. S. M., Kandavalli, V. K., Martins, L., Neeli-Venkata, R., Reyelt, J., ... Ribeiro, A. S. (2019). Chromosome and plasmid-borne PLacO3O1 promoters differ in sensitivity to critically low temperatures. Scientific Reports, 9, [4486]. https://doi.org/10.1038/s41598-019-39618-z

Vancouver

Oliveira SMD, Goncalves NSM, Kandavalli VK, Martins L, Neeli-Venkata R, Reyelt J et al. Chromosome and plasmid-borne PLacO3O1 promoters differ in sensitivity to critically low temperatures. Scientific Reports. 2019 Mar 14;9. 4486. https://doi.org/10.1038/s41598-019-39618-z

Author

Oliveira, Samuel M.D. ; Goncalves, Nadia S.M. ; Kandavalli, Vinodh K. ; Martins, Leonardo ; Neeli-Venkata, Ramakanth ; Reyelt, Jan ; Fonseca, Jose M ; Lloyd-Price, Jason ; Kranz, Harald ; Ribeiro, Andre S. / Chromosome and plasmid-borne PLacO3O1 promoters differ in sensitivity to critically low temperatures. In: Scientific Reports. 2019 ; Vol. 9.

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@article{1a9d870a8ece4a7ca5aa0e90e7ec0424,
title = "Chromosome and plasmid-borne PLacO3O1 promoters differ in sensitivity to critically low temperatures",
abstract = "Temperature shifts trigger genome-wide changes in Escherichia coli's gene expression. We studied if chromosome integration impacts on a gene's sensitivity to these shifts, by comparing the single-RNA production kinetics of a PLacO3O1 promoter, when chromosomally-integrated and when single-copy plasmid-borne. At suboptimal temperatures their induction range, fold change, and response to decreasing temperatures are similar. At critically low temperatures, the chromosome-integrated promoter becomes weaker and noisier. Dissection of its initiation kinetics reveals longer lasting states preceding open complex formation, suggesting enhanced supercoiling buildup. Measurements with Gyrase and Topoisomerase I inhibitors suggest hindrance to escape supercoiling buildup at low temperatures. Consistently, similar phenomena occur in energy-depleted cells by DNP at 30 °C. Transient, critically-low temperatures have no long-term consequences, as raising temperature quickly restores transcription rates. We conclude that the chromosomally-integrated PLacO3O1 has higher sensitivity to low temperatures, due to longer-lasting super-coiled states. A lesser active, chromosome-integrated native lac is shown to be insensitive to Gyrase overexpression, even at critically low temperatures, indicating that the rate of escaping positive supercoiling buildup is temperature and transcription rate dependent. A genome-wide analysis supports this, since cold-shock genes exhibit atypical supercoiling-sensitivities. This phenomenon might partially explain the temperature-sensitivity of some transcriptional programs of E. coli.",
author = "Oliveira, {Samuel M.D.} and Goncalves, {Nadia S.M.} and Kandavalli, {Vinodh K.} and Leonardo Martins and Ramakanth Neeli-Venkata and Jan Reyelt and Fonseca, {Jose M} and Jason Lloyd-Price and Harald Kranz and Ribeiro, {Andre S}",
year = "2019",
month = "3",
day = "14",
doi = "10.1038/s41598-019-39618-z",
language = "English",
volume = "9",
journal = "Scientific Reports",
issn = "2045-2322",
publisher = "Nature Publishing Group",

}

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TY - JOUR

T1 - Chromosome and plasmid-borne PLacO3O1 promoters differ in sensitivity to critically low temperatures

AU - Oliveira, Samuel M.D.

AU - Goncalves, Nadia S.M.

AU - Kandavalli, Vinodh K.

AU - Martins, Leonardo

AU - Neeli-Venkata, Ramakanth

AU - Reyelt, Jan

AU - Fonseca, Jose M

AU - Lloyd-Price, Jason

AU - Kranz, Harald

AU - Ribeiro, Andre S

PY - 2019/3/14

Y1 - 2019/3/14

N2 - Temperature shifts trigger genome-wide changes in Escherichia coli's gene expression. We studied if chromosome integration impacts on a gene's sensitivity to these shifts, by comparing the single-RNA production kinetics of a PLacO3O1 promoter, when chromosomally-integrated and when single-copy plasmid-borne. At suboptimal temperatures their induction range, fold change, and response to decreasing temperatures are similar. At critically low temperatures, the chromosome-integrated promoter becomes weaker and noisier. Dissection of its initiation kinetics reveals longer lasting states preceding open complex formation, suggesting enhanced supercoiling buildup. Measurements with Gyrase and Topoisomerase I inhibitors suggest hindrance to escape supercoiling buildup at low temperatures. Consistently, similar phenomena occur in energy-depleted cells by DNP at 30 °C. Transient, critically-low temperatures have no long-term consequences, as raising temperature quickly restores transcription rates. We conclude that the chromosomally-integrated PLacO3O1 has higher sensitivity to low temperatures, due to longer-lasting super-coiled states. A lesser active, chromosome-integrated native lac is shown to be insensitive to Gyrase overexpression, even at critically low temperatures, indicating that the rate of escaping positive supercoiling buildup is temperature and transcription rate dependent. A genome-wide analysis supports this, since cold-shock genes exhibit atypical supercoiling-sensitivities. This phenomenon might partially explain the temperature-sensitivity of some transcriptional programs of E. coli.

AB - Temperature shifts trigger genome-wide changes in Escherichia coli's gene expression. We studied if chromosome integration impacts on a gene's sensitivity to these shifts, by comparing the single-RNA production kinetics of a PLacO3O1 promoter, when chromosomally-integrated and when single-copy plasmid-borne. At suboptimal temperatures their induction range, fold change, and response to decreasing temperatures are similar. At critically low temperatures, the chromosome-integrated promoter becomes weaker and noisier. Dissection of its initiation kinetics reveals longer lasting states preceding open complex formation, suggesting enhanced supercoiling buildup. Measurements with Gyrase and Topoisomerase I inhibitors suggest hindrance to escape supercoiling buildup at low temperatures. Consistently, similar phenomena occur in energy-depleted cells by DNP at 30 °C. Transient, critically-low temperatures have no long-term consequences, as raising temperature quickly restores transcription rates. We conclude that the chromosomally-integrated PLacO3O1 has higher sensitivity to low temperatures, due to longer-lasting super-coiled states. A lesser active, chromosome-integrated native lac is shown to be insensitive to Gyrase overexpression, even at critically low temperatures, indicating that the rate of escaping positive supercoiling buildup is temperature and transcription rate dependent. A genome-wide analysis supports this, since cold-shock genes exhibit atypical supercoiling-sensitivities. This phenomenon might partially explain the temperature-sensitivity of some transcriptional programs of E. coli.

U2 - 10.1038/s41598-019-39618-z

DO - 10.1038/s41598-019-39618-z

M3 - Article

VL - 9

JO - Scientific Reports

JF - Scientific Reports

SN - 2045-2322

M1 - 4486

ER -