RNase I regulates Escherichia coli 2 0 ,3 0 -cyclic nucleotide monophosphate levels and biofilm formation

Benjamin M. Fontaine, Kevin S. Martin, Jennifer M. Garcia-Rodriguez, Claire Jung, Laura Briggs, Jessica E. Southwell, Xin Jia, Emily E. Weinert

Research output: Contribution to journalArticle

5 Citations (Scopus)

Abstract

Regulation of nucleotide and nucleoside concentrations is critical for faithful DNA replication, transcription, and translation in all organisms, and has been linked to bacterial biofilm formation. Unusual 2 0 ,3 0 -cyclic nucleotide monophosphates (2 0 ,3 0 -cNMPs) recently were quantified in mammalian systems, and previous reports have linked these nucleotides to cellular stress and damage in eukaryotes, suggesting an intriguing connection with nucleotide/nucleoside pools and/or cyclic nucleotide signaling. This work reports the first quantification of 2 0 ,3 0 -cNMPs in Escherichia coli and demonstrates that 2 0 ,3 0 -cNMP levels in E. coli are generated specifically from RNase I-catalyzed RNA degradation, presumably as part of a previously unidentified nucleotide salvage pathway. Furthermore, RNase I and 2 0 ,3 0 -cNMP levels are demonstrated to play an important role in controlling biofilm formation. This work identifies a physiological role for cytoplasmic RNase I and constitutes the first progress toward elucidating the biological functions of bacterial 2 0 ,3 0 -cNMPs.

Original languageEnglish (US)
Pages (from-to)1491-1506
Number of pages16
JournalBiochemical Journal
Volume475
Issue number8
DOIs
StatePublished - Apr 30 2018

Fingerprint

Pancreatic Ribonuclease
Cyclic Nucleotides
Biofilms
Escherichia coli
Nucleotides
Nucleosides
Salvaging
RNA Stability
Transcription
Eukaryota
DNA Replication
Degradation
DNA

All Science Journal Classification (ASJC) codes

  • Biochemistry
  • Molecular Biology
  • Cell Biology

Cite this

Fontaine, B. M., Martin, K. S., Garcia-Rodriguez, J. M., Jung, C., Briggs, L., Southwell, J. E., ... Weinert, E. E. (2018). RNase I regulates Escherichia coli 2 0 ,3 0 -cyclic nucleotide monophosphate levels and biofilm formation Biochemical Journal, 475(8), 1491-1506. https://doi.org/10.1042/BCJ20170906
Fontaine, Benjamin M. ; Martin, Kevin S. ; Garcia-Rodriguez, Jennifer M. ; Jung, Claire ; Briggs, Laura ; Southwell, Jessica E. ; Jia, Xin ; Weinert, Emily E. / RNase I regulates Escherichia coli 2 0 ,3 0 -cyclic nucleotide monophosphate levels and biofilm formation In: Biochemical Journal. 2018 ; Vol. 475, No. 8. pp. 1491-1506.
@article{45636f60ad164fefaf314372ee3c131f,
title = "RNase I regulates Escherichia coli 2 0 ,3 0 -cyclic nucleotide monophosphate levels and biofilm formation",
abstract = "Regulation of nucleotide and nucleoside concentrations is critical for faithful DNA replication, transcription, and translation in all organisms, and has been linked to bacterial biofilm formation. Unusual 2 0 ,3 0 -cyclic nucleotide monophosphates (2 0 ,3 0 -cNMPs) recently were quantified in mammalian systems, and previous reports have linked these nucleotides to cellular stress and damage in eukaryotes, suggesting an intriguing connection with nucleotide/nucleoside pools and/or cyclic nucleotide signaling. This work reports the first quantification of 2 0 ,3 0 -cNMPs in Escherichia coli and demonstrates that 2 0 ,3 0 -cNMP levels in E. coli are generated specifically from RNase I-catalyzed RNA degradation, presumably as part of a previously unidentified nucleotide salvage pathway. Furthermore, RNase I and 2 0 ,3 0 -cNMP levels are demonstrated to play an important role in controlling biofilm formation. This work identifies a physiological role for cytoplasmic RNase I and constitutes the first progress toward elucidating the biological functions of bacterial 2 0 ,3 0 -cNMPs.",
author = "Fontaine, {Benjamin M.} and Martin, {Kevin S.} and Garcia-Rodriguez, {Jennifer M.} and Claire Jung and Laura Briggs and Southwell, {Jessica E.} and Xin Jia and Weinert, {Emily E.}",
year = "2018",
month = "4",
day = "30",
doi = "10.1042/BCJ20170906",
language = "English (US)",
volume = "475",
pages = "1491--1506",
journal = "Biochemical Journal",
issn = "0264-6021",
publisher = "Portland Press Ltd.",
number = "8",

}

Fontaine, BM, Martin, KS, Garcia-Rodriguez, JM, Jung, C, Briggs, L, Southwell, JE, Jia, X & Weinert, EE 2018, ' RNase I regulates Escherichia coli 2 0 ,3 0 -cyclic nucleotide monophosphate levels and biofilm formation ', Biochemical Journal, vol. 475, no. 8, pp. 1491-1506. https://doi.org/10.1042/BCJ20170906

RNase I regulates Escherichia coli 2 0 ,3 0 -cyclic nucleotide monophosphate levels and biofilm formation . / Fontaine, Benjamin M.; Martin, Kevin S.; Garcia-Rodriguez, Jennifer M.; Jung, Claire; Briggs, Laura; Southwell, Jessica E.; Jia, Xin; Weinert, Emily E.

In: Biochemical Journal, Vol. 475, No. 8, 30.04.2018, p. 1491-1506.

Research output: Contribution to journalArticle

TY - JOUR

T1 - RNase I regulates Escherichia coli 2 0 ,3 0 -cyclic nucleotide monophosphate levels and biofilm formation

AU - Fontaine, Benjamin M.

AU - Martin, Kevin S.

AU - Garcia-Rodriguez, Jennifer M.

AU - Jung, Claire

AU - Briggs, Laura

AU - Southwell, Jessica E.

AU - Jia, Xin

AU - Weinert, Emily E.

PY - 2018/4/30

Y1 - 2018/4/30

N2 - Regulation of nucleotide and nucleoside concentrations is critical for faithful DNA replication, transcription, and translation in all organisms, and has been linked to bacterial biofilm formation. Unusual 2 0 ,3 0 -cyclic nucleotide monophosphates (2 0 ,3 0 -cNMPs) recently were quantified in mammalian systems, and previous reports have linked these nucleotides to cellular stress and damage in eukaryotes, suggesting an intriguing connection with nucleotide/nucleoside pools and/or cyclic nucleotide signaling. This work reports the first quantification of 2 0 ,3 0 -cNMPs in Escherichia coli and demonstrates that 2 0 ,3 0 -cNMP levels in E. coli are generated specifically from RNase I-catalyzed RNA degradation, presumably as part of a previously unidentified nucleotide salvage pathway. Furthermore, RNase I and 2 0 ,3 0 -cNMP levels are demonstrated to play an important role in controlling biofilm formation. This work identifies a physiological role for cytoplasmic RNase I and constitutes the first progress toward elucidating the biological functions of bacterial 2 0 ,3 0 -cNMPs.

AB - Regulation of nucleotide and nucleoside concentrations is critical for faithful DNA replication, transcription, and translation in all organisms, and has been linked to bacterial biofilm formation. Unusual 2 0 ,3 0 -cyclic nucleotide monophosphates (2 0 ,3 0 -cNMPs) recently were quantified in mammalian systems, and previous reports have linked these nucleotides to cellular stress and damage in eukaryotes, suggesting an intriguing connection with nucleotide/nucleoside pools and/or cyclic nucleotide signaling. This work reports the first quantification of 2 0 ,3 0 -cNMPs in Escherichia coli and demonstrates that 2 0 ,3 0 -cNMP levels in E. coli are generated specifically from RNase I-catalyzed RNA degradation, presumably as part of a previously unidentified nucleotide salvage pathway. Furthermore, RNase I and 2 0 ,3 0 -cNMP levels are demonstrated to play an important role in controlling biofilm formation. This work identifies a physiological role for cytoplasmic RNase I and constitutes the first progress toward elucidating the biological functions of bacterial 2 0 ,3 0 -cNMPs.

UR - http://www.scopus.com/inward/record.url?scp=85046889001&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85046889001&partnerID=8YFLogxK

U2 - 10.1042/BCJ20170906

DO - 10.1042/BCJ20170906

M3 - Article

C2 - 29555843

AN - SCOPUS:85046889001

VL - 475

SP - 1491

EP - 1506

JO - Biochemical Journal

JF - Biochemical Journal

SN - 0264-6021

IS - 8

ER -

Fontaine BM, Martin KS, Garcia-Rodriguez JM, Jung C, Briggs L, Southwell JE et al. RNase I regulates Escherichia coli 2 0 ,3 0 -cyclic nucleotide monophosphate levels and biofilm formation Biochemical Journal. 2018 Apr 30;475(8):1491-1506. https://doi.org/10.1042/BCJ20170906