ECF02 ECF proteins

General description: Members of ECF02 have homology against proteins of original ECF02 (99.29%) and appear in Proteobacteria (100%).

Anti-σ factor: Members of ECF02 are regulated by RseA-like AS factors with one transmembrane helix encoded in position +1. Even though TopCons failed to predict the transmembrane helix in most of the cases, an MSA revealed the presence of one transmembrane helix in most of the proteins encoded in +1 of members of ECF02. RseA-like AS factors take their name from RseA, the AS factor of RpoE in E. coli (ECF02s1) (Missiakas, Mayer, Lemaire, Georgopoulos, & Raina, 1997).

Genomic context conservation: Other conserved domains in the context of ECF02 are associated with translation and protein secretion. We found a 50S ribosome-binding GTPase fused to a KH domain, an elongation factor Tu involved in the translation elongation, a ribonuclease-III-like protein involved in rDNA transcription and rRNA processing, a signal peptidase S24 (Pfam: Peptidase_S24), a signal peptidase S26 and a fumarate reductase (only ECF02s2).

Studied members: Among the characterized members of ECF02 we found RpoE, from E. coli, which plays a key role during stationary phase, metal resistance (Egler, Grosse, Grass, & Nies, 2005), folding and degradation of periplasmic proteins, lipopolysaccharide biogenesis, heat shock response (Rowley, Spector, Kormanec, & Roberts, 2006) and virulence (Smith et al., 2017). Unlike other ECFs, RpoE is essential in E. coli (Hiratsu, Amemura, Nashimoto, Shinagawa, & Makino, 1995), potentially due to the lack of a complete lipopolysaccharide in respect to the closely related Salmonella enterica, where RpoE is not essential (Amar, Pezzoni, Pizarro, & Costa, 2018). RpoE is regulated by its AS factor, RseA, which is inactivated by Regulated Intramembrane Proteolysis (RIP) sequentially carried out by the proteases DegS, RseP and cytoplasmic proteases (Akiyama, Kanehara, & Ito, 2004; Walsh, Alba, Bose, Gross, & Sauer, 2003). DegS is a membrane-bound periplasmic protein able to sense stress signal originated from different unfolded OMP via its PDZ domain (Hasselblatt et al., 2007). RseP contains a pair of permutated PDZ domains in its periplasmic region that controls its activity as site-2 protease (Inaba et al., 2008). Indeed, proteins with PDZ domain appear in the genetic context of ECF02 (1.17 per ECF). The other two proteins in the operon of RpoE - RseB (+2) and RseC (+3), are an extracytoplasmic stabilizer of RseA and an inner membrane positive regulator of RpoE, respectively (Cezairliyan & Sauer, 2007; Missiakas et al., 1997). While RseB-like proteins are conserved in positions +2 of all the subgroups, RseC-like proteins are not conserved in ECF02s3.

RpoE from S. enterica (ECF02s1) is activated by UVA radiation, envelope stress generated by phage infection or hypo-osmotic shock in the absence of periplasmic glycans (OPG) (Amar et al., 2018; Spöring et al., 2018; E. C. Woods & McBride, 2017). RpoE from Burkholderia pseudomallei is induced under high salt concentrations and is required for heat and oxidative stress since it turns on the expression of speG, stabilizing the levels of spermidine (Duangurai, Indrawattana, & Pumirat, 2018). RpoE from Xylella fastidiosa participates in heat shock response due to 21-gene sigmulon (da Silva Neto, Koide, Gomes, & Marques, 2007). Similarly, RpoE from Shewanella oneidensis is essential for growth under suboptimal conditions caused by temperature, salinity, oxidative stress, minimal medium, metals, absence of oxygen, among others, and it typically targets the synthesis of extracytoplasmic and outer membrane components (Barchinger et al., 2016; Dai et al., 2015). Vibrio parahaemolyticus contains an ECF02 (VP2578) involved in cell envelope stress required for intestinal colonization (!!!Haines-Menges et al., 2014!!!).

Interestingly, RpoE1 from Xanthomonas campestris (ECF02s1) is induced under cultivation in minimal medium or plant extract, and it is required by plant pathogenesis since it induces the expression of T3SS (Yang et al., 2018). This function is typical from group ECF32, which is in close evolutionary proximity to ECF02. Therefore, RpoE1 from X. campestris could be the mixture of both systems where the ECF kept the sequence of members of ECF02 but the function of ECF32.

Other members of ECF02 are the AlgU-like proteins — AlgU from Pseudomonas aeruginosa in involved in alginate production leading to transition the mucoid and biofilm phenotypes. AlgU helps to relieve oxidative stress, and it is involved in virulence, β-lactamase production, and repression of flagella biosynthesis. AlgU is induced by antibiotics that block peptidoglycan synthesis as in the case of RpoE from E. coli (Llamas et al., 2014; E. C. Woods & McBride, 2017) (Chevalier et al., 2018; Delgado et al., 2018; Tart, Wolfgang, & Wozniak, 2005). Homologs of AlgU appear in other Pseudomonas species such as P. putida and P. syringae, but also in Azotobacter vinelandii.

Promoter motif conservation: Promoter motifs are well conserved and contain GAACTTT in -35 and GTCT in -10 in agreement with the binding motif of RpoE in E. coli (Rhodius & Mutalik, 2010), Shewanella oneidensis (Barchinger et al., 2016) and original ECF02 (Staroń et al., 2009). Nevertheless, some members of ECF02, such as RpoE from Xylella fastidiosa are not autoregulated (da Silva Neto et al., 2007).

Summary: ECF02 keeps the characteristics of the original group ECF02 (Staroń et al., 2009). ECF02 is one of the key factors contributing to cell envelope homeostasis in Proteobacteria. These ECFs are also involved in biofilm formation since they induce the production of alginate in bacteria from the genus Pseudomonas. Members of ECF02 are negatively regulated by a RseA-like AS factor encoded in position +1, a RseB-like extracytoplasmic negative regulator that protects RseA from degradation and a RseC-like inner membrane positive regulator.


 


Basic information

Number of representative ECFs: 3344

Number of non-redundant ECFs: 2262

Sequences with C-terminal extension: 0.00%

Sequences with N-terminal extension: 3.36%

Overrepresented phylum: Proteobacteria [99.85%]



Sample Neighborhood

Protein WP_038686981.1 of Assembly GCF_000661955.1 (Stenotrophomonas rhizophila)


Promoter Motif



Figures

Protein sequence length distribution

Gene neighbourhood conservation analysis


Overall Pfam domain distribution: Cumulative frequency of Pfam domains across the genetic neighborhoods. Frequency is expressed as number of Pfam domains per ECF sigma factor. Only domains present in more than 75% of the neighborhoods are shown. Genetic neighborhoods contain the proteins encoded in ±10 from the ECF coding sequence. Only the non-overlapping, highest scoring domains are considered positive. If a protein contains several copies of a domain, only one instance is further considered. In order to avoid sequence bias, only proteins from assemblies defined as "representative" or "reference" by NCBI are included (see https://www.ncbi.nlm.nih.gov/assembly/help/).
Pfam domain distribution per position: Frequency of Pfam domain architectures in the proteins encoded in ±10 (x-axis) from the ECF coding sequences. Frequency is expressed as number of times a certain domain architecture appears per ECF sigma factor. Only the highest scoring domains with no position overlap are considered in the domain architectures. Note that the order of the Pfam domains in domain architectures may differ from their name. When a protein contains several copies of a domain, only one instance is further considered. Only domain architectures present in more than 20% of the proteins encoded in any position are shown. In order to avoid sequence bias, only proteins from assemblies defined as "representative" or "reference" by NCBI are included (see https://www.ncbi.nlm.nih.gov/assembly/help/).

Related publications

Title Journal Year Authors PubMed ECF groups
The rpoE gene of Escherichia coli, which encodes sigma E, is essential for bacterial growth at high temperature. Journal of bacteriology 1995 K. Hiratsu, M. Amemura, H. Nashimoto, H. Shinagawa, K. Makino PubMed: 7751307 ECF02, ECF227
Modulation of the Escherichia coli sigmaE (RpoE) heat-shock transcription-factor activity by the RseA, RseB and RseC proteins. Molecular microbiology 1997 D. Missiakas, M. Mayer, M. Lemaire, C. Georgopoulos, S. Raina PubMed: 9159522 ECF02
OMP peptide signals initiate the envelope-stress response by activating DegS protease via relief of inhibition mediated by its PDZ domain. Cell 2003 N. Walsh, B. Alba, B. Bose, C. Gross, R. Sauer PubMed: 12679035 ECF02
A new staphylococcal sigma factor in the conserved gene cassette: functional significance and implication for the evolutionary processes. Genes to cells : devoted to molecular & cellular mechanisms 2003 K. Morikawa, Y. Inose, H. Okamura, A. Maruyama, H. Hayashi, K. Takeyasu, T. Ohta PubMed: 12875655 ECF02
Control of the alternative sigma factor sigmaE in Escherichia coli. Current opinion in microbiology 2004 S. Ades PubMed: 15063853 ECF02
Regulation of the Escherichia coli sigma-dependent envelope stress response. Molecular microbiology 2004 B. Alba, C. Gross PubMed: 15101969 ECF02
RseP (YaeL), an Escherichia coli RIP protease, cleaves transmembrane sequences. The EMBO journal 2004 Y. Akiyama, K. Kanehara, K. Ito PubMed: 15496982 ECF02
Role of the extracytoplasmic function protein family sigma factor RpoE in metal resistance of Escherichia coli. Journal of bacteriology 2005 M. Egler, C. Grosse, G. Grass, D. Nies PubMed: 15774872 ECF02
The alternative sigma factor AlgT represses Pseudomonas aeruginosa flagellum biosynthesis by inhibiting expression of fleQ. Journal of bacteriology 2005 A. Tart, M. Wolfgang, D. Wozniak PubMed: 16291668 ECF02
Pushing the envelope: extracytoplasmic stress responses in bacterial pathogens. Nature reviews. Microbiology 2006 G. Rowley, M. Spector, J. Kormanec, M. Roberts PubMed: 16715050 ECF02
The single extracytoplasmic-function sigma factor of Xylella fastidiosa is involved in the heat shock response and presents an unusual regulatory mechanism. Journal of bacteriology 2007 J. da Silva Neto, T. Koide, S. Gomes, M. Marques PubMed: 17098905 ECF02
Inhibition of regulated proteolysis by RseB. Proceedings of the National Academy of Sciences of the United States of America 2007 B. Cezairliyan, R. Sauer PubMed: 17360428 ECF02
Regulation of the sigmaE stress response by DegS: how the PDZ domain keeps the protease inactive in the resting state and allows integration of different OMP-derived stress signals upon folding stress. Genes & development 2007 H. Hasselblatt, R. Kurzbauer, C. Wilken, T. Krojer, J. Sawa, J. Kurt, R. Kirk, S. Hasenbein, M. Ehrmann, T. Clausen PubMed: 17938245 ECF02, ECF214, ECF273
A pair of circularly permutated PDZ domains control RseP, the S2P family intramembrane protease of Escherichia coli. The Journal of biological chemistry 2008 K. Inaba, M. Suzuki, K. Maegawa, S. Akiyama, K. Ito, Y. Akiyama PubMed: 18945679 ECF02, ECF273
Use of cell wall stress to characterize sigma 22 (AlgT/U) activation by regulated proteolysis and its regulon in Pseudomonas aeruginosa. Molecular microbiology 2009 L. Wood, D. Ohman PubMed: 19226327 ECF02
The third pillar of bacterial signal transduction: classification of the extracytoplasmic function (ECF) sigma factor protein family. Molecular microbiology 2009 A. Staroń, H. Sofia, S. Dietrich, L. Ulrich, H. Liesegang, T. Mascher PubMed: 19737356 ECF103, ECF21, ECF123, ECF51, ECF39, ECF281, ECF102, ECF130, ECF122, ECF291, ECF15, ECF242, ECF22, ECF285, ECF106, ECF27, ECF31, ECF240, ECF114, ECF16, ECF38, ECF41, ECF105, ECF116, ECF111, ECF03, ECF239, ECF42, ECF294, ECF17, ECF11, ECF29, ECF235, ECF293, ECF118, ECF265, ECF30, ECF23, ECF14, ECF249, ECF18, ECF115, ECF290, ECF25, ECF121, ECF02, ECF120, ECF289, ECF28, ECF243, ECF19, ECF43, ECF107, ECF12, ECF32, ECF36, ECF292, ECF286, ECF271, ECF26, ECF40, ECF56, ECF33
Predicting strength and function for promoters of the Escherichia coli alternative sigma factor, sigmaE. Proceedings of the National Academy of Sciences of the United States of America 2010 V. Rhodius, V. Mutalik PubMed: 20133665 ECF02
Cell-surface signaling in Pseudomonas: stress responses, iron transport, and pathogenicity. FEMS microbiology reviews 2014 M. Llamas, F. Imperi, P. Visca, I. Lamont PubMed: 24923658 ECF02, ECF243
An extracytoplasmic function sigma factor-dependent periplasmic glutathione peroxidase is involved in oxidative stress response of Shewanella oneidensis. BMC microbiology 2015 J. Dai, H. Wei, C. Tian, F. Damron, J. Zhou, D. Qiu PubMed: 25887418 ECF02
The lysis cassette of DLP12 defective prophage is regulated by RpoE. Microbiology (Reading, England) 2015 K. Rueggeberg, F. Toba, J. Bird, N. Franck, M. Thompson, A. Hay PubMed: 25998262 ECF02
ChIP-Seq Analysis of the σE Regulon of Salmonella enterica Serovar Typhimurium Reveals New Genes Implicated in Heat Shock and Oxidative Stress Response. PloS one 2015 J. Li, C. Overall, R. Johnson, M. Jones, J. McDermott, F. Heffron, J. Adkins, E. Cambronne PubMed: 26389830 ECF02
Regulation of Gene Expression in Shewanella oneidensis MR-1 during Electron Acceptor Limitation and Bacterial Nanowire Formation. Applied and environmental microbiology 2016 S. Barchinger, S. Pirbadian, C. Sambles, C. Baker, K. Leung, N. Burroughs, M. El-Naggar, J. Golbeck PubMed: 27342561 ECF02
The Production of Curli Amyloid Fibers Is Deeply Integrated into the Biology of Escherichia coli. Biomolecules 2017 D. Smith, J. Price, P. Burby, L. Blanco, J. Chamberlain, M. Chapman PubMed: 29088115 ECF02
<i>Burkholderia pseudomallei</i> Adaptation for Survival in Stressful Conditions. BioMed research international 2018 T. Duangurai, N. Indrawattana, P. Pumirat PubMed: 29992136 ECF02
Systematic Functional Analysis of Sigma (σ) Factors in the Phytopathogen <i>Xanthomonas campestris</i> Reveals Novel Roles in the Regulation of Virulence and Viability. Frontiers in microbiology 2018 L. Yang, L. Yang, Y. Gan, L. Wang, W. Zhao, Y. He, W. Jiang, B. Jiang, J. Tang PubMed: 30123197 ECF02
Regulation of Flagellum Biosynthesis in Response to Cell Envelope Stress in <i>Salmonella enterica</i> Serovar Typhimurium. mBio 2018 I. Spöring, S. Felgner, M. Preuße, D. Eckweiler, M. Rohde, S. Häussler, S. Weiss, M. Erhardt PubMed: 29717015 ECF02
Extracytoplasmic function sigma factors in Pseudomonas aeruginosa. Biochimica et biophysica acta. Gene regulatory mechanisms 2018 S. Chevalier, E. Bouffartigues, A. Bazire, A. Tahrioui, R. Duchesne, D. Tortuel, O. Maillot, T. Clamens, N. Orange, M. Feuilloley, O. Lesouhaitier, A. Dufour, P. Cornelis PubMed: 29729420 ECF02, ECF102, ECF243, ECF293, ECF35
Pseudomonas aeruginosa Regulated Intramembrane Proteolysis: Protease MucP Can Overcome Mutations in the AlgO Periplasmic Protease To Restore Alginate Production in Nonmucoid Revertants. Journal of bacteriology 2018 C. Delgado, L. Florez, I. Lollett, C. Lopez, S. Kangeyan, H. Kumari, M. Stylianou, R. Smiddy, L. Schneper, R. Sautter, D. Smith, G. Szatmari, K. Mathee PubMed: 29784885 ECF02
New envelope stress factors involved in σ<sup>E</sup> activation and conditional lethality of rpoE mutations in Salmonella enterica. Microbiology (Reading, England) 2018 A. Amar, M. Pezzoni, R. Pizarro, C. Costa PubMed: 30084765 ECF02
Regulation of antimicrobial resistance by extracytoplasmic function (ECF) sigma factors. Microbes and infection 2019 E. Woods, S. McBride PubMed: 28153747 ECF02, ECF30
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