Differential Expression of Secretion Machinery During Bacterial Growth: SecY and SecF Decrease While SecA Increases During Transition from Exponential Phase to Stationary Phase

Overview

Journal Curr Microbiol

Specialty Microbiology

Date 2013 Jul 16

PMID 23852076

Citations 5

Authors

Chun-Kai Yang

Chung-Dar Lu

Phang C Tai

Affiliations

Soon will be listed here.

Abstract

Transcription of many house-keeping genes, including secY and some other sec genes, decreases in the transition from the exponential phase to the stationary phase (feast to famine) in Bacillus subtilis. Unexpectedly and in contradiction to earlier reports, enhanced transcription was observed for another group of sec genes, including secA which codes for an essential ATPase for protein secretion. Consistent with the transcription data, the SecA protein of B. subtilis increases significantly in the stationary phase. Immunoblot analyses of Sec proteins during the transition in Escherichia coli also revealed the pronounced decreases of SecY and SecF and the increase of SecA, resulting in drastic increases of SecA/SecY and SecA/SecF ratios from exponential to stationary phases. The differential expression of Sec proteins in the stationary phase suggests the possibility of specific physiological functions.

Citing Articles

The Dynamic SecYEG Translocon.

Oswald J, Njenga R, Natriashvili A, Sarmah P, Koch H Front Mol Biosci. 2021; 8:664241.

PMID: 33937339 PMC: 8082313. DOI: 10.3389/fmolb.2021.664241.

SecA inhibitors as potential antimicrobial agents: differential actions on SecA-only and SecA-SecYEG protein-conducting channels.

Jin J, Hsieh Y, Chaudhary A, Cui J, Houghton J, Sui S FEMS Microbiol Lett. 2018; 365(15).

PMID: 30007321 PMC: 7190897. DOI: 10.1093/femsle/fny145.

The Sec System: Protein Export in .

Crane J, Randall L EcoSal Plus. 2017; 7(2).

PMID: 29165233 PMC: 5807066. DOI: 10.1128/ecosalplus.ESP-0002-2017.

Dissecting structures and functions of SecA-only protein-conducting channels: ATPase, pore structure, ion channel activity, protein translocation, and interaction with SecYEG/SecDF•YajC.

Hsieh Y, Huang Y, Zhang H, Liu Q, Lu Y, Yang H PLoS One. 2017; 12(6):e0178307.

PMID: 28575061 PMC: 5456053. DOI: 10.1371/journal.pone.0178307.

Specificity of SecYEG for PhoA precursors and SecA homologs on SecA protein-conducting channels.

Zhang H, Hsieh Y, Lin B, Yu L, Yang H, Jiang C Biochem Biophys Res Commun. 2013; 437(2):212-216.

PMID: 23791875 PMC: 3740335. DOI: 10.1016/j.bbrc.2013.06.039.

References

Blom E, Ridder A, Lulko A, Roerdink J, Kuipers O . Time-resolved transcriptomics and bioinformatic analyses reveal intrinsic stress responses during batch culture of Bacillus subtilis. PLoS One. 2011; 6(11):e27160. PMC: 3210768. DOI: 10.1371/journal.pone.0027160. View

Sjostrom M, Wold S, Wieslander A, Rilfors L . Signal peptide amino acid sequences in Escherichia coli contain information related to final protein localization. A multivariate data analysis. EMBO J. 1987; 6(3):823-31. PMC: 553468. DOI: 10.1002/j.1460-2075.1987.tb04825.x. View

Leloup L, Driessen A, Freudl R, Chambert R, Petit-Glatron M . Differential dependence of levansucrase and alpha-amylase secretion on SecA (Div) during the exponential phase of growth of Bacillus subtilis. J Bacteriol. 1999; 181(6):1820-6. PMC: 93580. DOI: 10.1128/JB.181.6.1820-1826.1999. View

Kwon D, Lu C . Polyamines induce resistance to cationic peptide, aminoglycoside, and quinolone antibiotics in Pseudomonas aeruginosa PAO1. Antimicrob Agents Chemother. 2006; 50(5):1615-22. PMC: 1472189. DOI: 10.1128/AAC.50.5.1615-1622.2006. View

Haldenwang W . The sigma factors of Bacillus subtilis. Microbiol Rev. 1995; 59(1):1-30. PMC: 239352. DOI: 10.1128/mr.59.1.1-30.1995. View

Lin B, Hsieh Y, Jiang C, Tai P . Escherichia coli membranes depleted of SecYEG elicit SecA-dependent ion-channel activity but lose signal peptide specificity. J Membr Biol. 2012; 245(11):747-57. DOI: 10.1007/s00232-012-9477-8. View

Vitikainen M, Lappalainen I, Seppala R, Antelmann H, Boer H, Taira S . Structure-function analysis of PrsA reveals roles for the parvulin-like and flanking N- and C-terminal domains in protein folding and secretion in Bacillus subtilis. J Biol Chem. 2004; 279(18):19302-14. DOI: 10.1074/jbc.M400861200. View

Hsieh Y, Zhang H, Lin B, Cui N, Na B, Yang H . SecA alone can promote protein translocation and ion channel activity: SecYEG increases efficiency and signal peptide specificity. J Biol Chem. 2011; 286(52):44702-9. PMC: 3247964. DOI: 10.1074/jbc.M111.300111. View

Selinger D, Cheung K, Mei R, Johansson E, Richmond C, Blattner F . RNA expression analysis using a 30 base pair resolution Escherichia coli genome array. Nat Biotechnol. 2000; 18(12):1262-8. DOI: 10.1038/82367. View

10.

Yang C, Ewis H, Zhang X, Lu C, Hu H, Pan Y . Nonclassical protein secretion by Bacillus subtilis in the stationary phase is not due to cell lysis. J Bacteriol. 2011; 193(20):5607-15. PMC: 3187209. DOI: 10.1128/JB.05897-11. View

11.

Derman A, Puziss J, Bassford Jr P, Beckwith J . A signal sequence is not required for protein export in prlA mutants of Escherichia coli. EMBO J. 1993; 12(3):879-88. PMC: 413286. DOI: 10.1002/j.1460-2075.1993.tb05728.x. View

12.

Tjalsma H, Antelmann H, Jongbloed J, Braun P, Darmon E, Dorenbos R . Proteomics of protein secretion by Bacillus subtilis: separating the "secrets" of the secretome. Microbiol Mol Biol Rev. 2004; 68(2):207-33. PMC: 419921. DOI: 10.1128/MMBR.68.2.207-233.2004. View

13.

Herbort M, Klein M, Manting E, Driessen A, Freudl R . Temporal expression of the Bacillus subtilis secA gene, encoding a central component of the preprotein translocase. J Bacteriol. 1999; 181(2):493-500. PMC: 93403. DOI: 10.1128/JB.181.2.493-500.1999. View

14.

Brockmeier U, Caspers M, Freudl R, Jockwer A, Noll T, Eggert T . Systematic screening of all signal peptides from Bacillus subtilis: a powerful strategy in optimizing heterologous protein secretion in Gram-positive bacteria. J Mol Biol. 2006; 362(3):393-402. DOI: 10.1016/j.jmb.2006.07.034. View

15.

Tanji Y, Gennity J, Pollitt S, Inouye M . Effect of OmpA signal peptide mutations on OmpA secretion, synthesis, and assembly. J Bacteriol. 1991; 173(6):1997-2005. PMC: 207733. DOI: 10.1128/jb.173.6.1997-2005.1991. View

16.

Lu C, Yang Z, Li W . Transcriptome analysis of the ArgR regulon in Pseudomonas aeruginosa. J Bacteriol. 2004; 186(12):3855-61. PMC: 419968. DOI: 10.1128/JB.186.12.3855-3861.2004. View