DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Shedding light on a Group IV (ECF11) alternative σ factor

Abstract

This year marks the 50th anniversary of the discovery of σ70 as a protein factor that was needed for bacterial RNA polymerase to accurately transcribe a promoter in vitro. It was 25 years later that the Group IV alternative σs were described as a distinct family of proteins related to σ70. In the intervening time, there has been an ever-growing list of Group IV σs, numbers of genes they transcribe, insight into the diverse suite of processes they control, and appreciation for their impact on bacterial lifestyles. This work summarizes knowledge of the Rhodobacter sphaeroides σE-ChrR pair, a member of the ECF11 subfamily of Group IV alternative σs, in protecting cells from the reactive oxygen species, singlet oxygen. It describes lessons learned from analyzing ChrR, a zinc-dependent anti-σ factor, that are generally applicable to Group IV σs and relevant to the response to single oxygen. This MicroReview also illustrates insights into stress responses in this and other bacteria that have been acquired by analyzing or modeling the activity of the σE-ChrR across the bacterial phylogeny.

Authors:
ORCiD logo [1]
  1. Univ. of Wisconsin, Madison, WI (United States). Bacteriology Dept., Great Lakes Bioenergy Research Center Wisconsin Energy Inst.
Publication Date:
Research Org.:
Univ. of Wisconsin, Madison, WI (United States). Great Lakes Bioenergy Research Center
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1546720
Grant/Contract Number:  
SC0018409
Resource Type:
Accepted Manuscript
Journal Name:
Molecular Microbiology
Additional Journal Information:
Journal Volume: 112; Journal Issue: 2; Journal ID: ISSN 0950-382X
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Donohue, Timothy J. Shedding light on a Group IV (ECF11) alternative σ factor. United States: N. p., 2019. Web. doi:10.1111/mmi.14280.
Donohue, Timothy J. Shedding light on a Group IV (ECF11) alternative σ factor. United States. https://doi.org/10.1111/mmi.14280
Donohue, Timothy J. Mon . "Shedding light on a Group IV (ECF11) alternative σ factor". United States. https://doi.org/10.1111/mmi.14280. https://www.osti.gov/servlets/purl/1546720.
@article{osti_1546720,
title = {Shedding light on a Group IV (ECF11) alternative σ factor},
author = {Donohue, Timothy J.},
abstractNote = {This year marks the 50th anniversary of the discovery of σ70 as a protein factor that was needed for bacterial RNA polymerase to accurately transcribe a promoter in vitro. It was 25 years later that the Group IV alternative σs were described as a distinct family of proteins related to σ70. In the intervening time, there has been an ever-growing list of Group IV σs, numbers of genes they transcribe, insight into the diverse suite of processes they control, and appreciation for their impact on bacterial lifestyles. This work summarizes knowledge of the Rhodobacter sphaeroides σE-ChrR pair, a member of the ECF11 subfamily of Group IV alternative σs, in protecting cells from the reactive oxygen species, singlet oxygen. It describes lessons learned from analyzing ChrR, a zinc-dependent anti-σ factor, that are generally applicable to Group IV σs and relevant to the response to single oxygen. This MicroReview also illustrates insights into stress responses in this and other bacteria that have been acquired by analyzing or modeling the activity of the σE-ChrR across the bacterial phylogeny.},
doi = {10.1111/mmi.14280},
journal = {Molecular Microbiology},
number = 2,
volume = 112,
place = {United States},
year = {2019},
month = {5}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 7 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

The importance of zinc-binding to the function of Rhodobacter sphaeroides ChrR as an anti-sigma factor
journal, October 2001

  • Newman, Jack D.; Anthony, Jennifer R.; Donohue, Timothy J.
  • Journal of Molecular Biology, Vol. 313, Issue 3
  • DOI: 10.1006/jmbi.2001.5069

Defining the disulphide stress response in Streptomyces coelicolor A3(2): identification of the sigmaR regulon
journal, November 2001


Thiol-Based Regulatory Switches
journal, December 2003


Bacterial responses to photo-oxidative stress
journal, November 2009

  • Ziegelhoffer, Eva C.; Donohue, Timothy J.
  • Nature Reviews Microbiology, Vol. 7, Issue 12
  • DOI: 10.1038/nrmicro2237

Reactive species formed on proteins exposed to singlet oxygen
journal, January 2004

  • Davies, Michael J.
  • Photochemical & Photobiological Sciences, Vol. 3, Issue 1
  • DOI: 10.1039/b307576c

Singlet Oxygen in Antimicrobial Photodynamic Therapy: Photosensitizer-Dependent Production and Decay in E. coli
journal, February 2013


The anti-sigma factor RsrA responds to oxidative stress by reburying its hydrophobic core
journal, July 2016

  • Rajasekar, Karthik V.; Zdanowski, Konrad; Yan, Jun
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms12194

How carotenoids protect bacterial photosynthesis
journal, October 2000

  • Cogdell, Richard J.; Howard, Tina D.; Bittl, Robert
  • Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Vol. 355, Issue 1402
  • DOI: 10.1098/rstb.2000.0696

Redox Homeostasis and Antioxidant Signaling: A Metabolic Interface between Stress Perception and Physiological Responses
journal, June 2005


Convergence of the Transcriptional Responses to Heat Shock and Singlet Oxygen Stresses
journal, September 2012


Synthesis and scavenging role of furan fatty acids
journal, August 2014

  • Lemke, R. A. S.; Peterson, A. C.; Ziegelhoffer, E. C.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 33
  • DOI: 10.1073/pnas.1405520111

Development of the bacterial photosynthetic apparatus
journal, December 2006


Protein Synthesis Patterns Reveal a Complex Regulatory Response to Singlet Oxygen in Rhodobacter
journal, July 2007

  • Glaeser, Jens; Zobawa, Monica; Lottspeich, Friedrich
  • Journal of Proteome Research, Vol. 6, Issue 7
  • DOI: 10.1021/pr060624p

The Rhodobacter sphaeroides ECF sigma factor, σE, and the target promoters cycA P3 and rpoE P1
journal, November 1999

  • Newman, Jack D.; Falkowski, Mat J.; Schilke, Brenda A.
  • Journal of Molecular Biology, Vol. 294, Issue 2
  • DOI: 10.1006/jmbi.1999.3263

Oxidation Decomposition of Unsaturated Fatty Acids by Singlet Oxygen in Phospholipid Bilayer Membranes
journal, January 2007

  • Watabe, Naoki; Ishida, Yu; Ochiai, Akira
  • Journal of Oleo Science, Vol. 56, Issue 2
  • DOI: 10.5650/jos.56.73

Themes and variations in gene regulation by extracytoplasmic function (ECF) sigma factors
journal, April 2017


Thiol-Based Redox Switches and Gene Regulation
journal, March 2011

  • Antelmann, Haike; Helmann, John D.
  • Antioxidants & Redox Signaling, Vol. 14, Issue 6
  • DOI: 10.1089/ars.2010.3400

Singlet oxygen generation in the reaction centers of Rhodobacter sphaeroides
journal, February 2008

  • Uchoa, Adjaci F.; Knox, Peter P.; Turchielle, Rozane
  • European Biophysics Journal, Vol. 37, Issue 6
  • DOI: 10.1007/s00249-008-0287-y

Cytochrome c oxidase: exciting progress and remaining mysteries
journal, October 2008

  • Brzezinski, Peter; Gennis, Robert B.
  • Journal of Bioenergetics and Biomembranes, Vol. 40, Issue 5
  • DOI: 10.1007/s10863-008-9181-7

DegS and RseP Homologous Proteases Are Involved in Singlet Oxygen Dependent Activation of RpoE in Rhodobacter sphaeroides
journal, November 2013


The cytochrome bd respiratory oxygen reductases
journal, November 2011

  • Borisov, Vitaliy B.; Gennis, Robert B.; Hemp, James
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1807, Issue 11
  • DOI: 10.1016/j.bbabio.2011.06.016

The physiology and pharmacology of singlet oxygen
journal, April 2003


Singlet Oxygen Signaling: From Intimate to Global
journal, February 2004


Exploiting Thiol Modifications
journal, November 2004


Evolution of photosynthesis and aerobic respiration in the cyanobacteria
journal, August 2019


Changes in the Spin State and Reactivity of Cytochrome c Induced by Photochemically Generated Singlet Oxygen and Free Radicals
journal, July 2004

  • Estevam, Mauren L.; Nascimento, Otaciro R.; Baptista, Mauricio S.
  • Journal of Biological Chemistry, Vol. 279, Issue 38
  • DOI: 10.1074/jbc.M402093200

Redox-dependent Changes in RsrA, an Anti-sigma Factor in Streptomyces coelicolor: Zinc Release and Disulfide Bond Formation
journal, January 2004

  • Bae, Jae-Bum; Park, Joo-Hong; Hahn, Mi-Young
  • Journal of Molecular Biology, Vol. 335, Issue 2
  • DOI: 10.1016/j.jmb.2003.10.065

Reconstruction of the Core and Extended Regulons of Global Transcription Factors
journal, July 2010


Mutational analysis of RsrA, a zinc-binding anti-sigma factor with a thiol-disulphide redox switch: Mutational analysis of RsrA
journal, February 2001


Singlet oxygen in plants: production, detoxification and signaling
journal, April 2009


A transcriptional response to singlet oxygen, a toxic byproduct of photosynthesis
journal, April 2005

  • Anthony, J. R.; Warczak, K. L.; Donohue, T. J.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 18
  • DOI: 10.1073/pnas.0502225102

Evolution of photosynthetic prokaryotes: a maximum-likelihood mapping approach
journal, January 2003

  • Raymond, Jason; Zhaxybayeva, Olga; Gogarten, J. Peter
  • Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Vol. 358, Issue 1429
  • DOI: 10.1098/rstb.2002.1181

Glutathione, oxidative stress and neurodegeneration: Glutathione and neurodegeneration
journal, August 2000


Light and oxygenic photosynthesis: energy dissipation as a protection mechanism against photo-oxidation
journal, July 2005

  • Szabó, Ildikó; Bergantino, Elisabetta; Giacometti, Giorgio Mario
  • EMBO reports, Vol. 6, Issue 7
  • DOI: 10.1038/sj.embor.7400460

Role of Lipid Hydroperoxides in Photo-Oxidative Stress Signaling
journal, April 2004


Formation of radicals from singlet oxygen produced during photoinhibition of isolated light-harvesting proteins of photosystem II
journal, January 2004

  • Rinalducci, Sara; Pedersen, Jens Z.; Zolla, Lello
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1608, Issue 1
  • DOI: 10.1016/j.bbabio.2003.10.009

Optogenetic regulation of engineered cellular metabolism for microbial chemical production
journal, March 2018

  • Zhao, Evan M.; Zhang, Yanfei; Mehl, Justin
  • Nature, Vol. 555, Issue 7698
  • DOI: 10.1038/nature26141

Imaging of photo-oxidative stress responses in leaves
journal, May 2002


Bacterial Sigma Factors: A Historical, Structural, and Genomic Perspective
journal, September 2014


Overlapping Alternative Sigma Factor Regulons in the Response to Singlet Oxygen in Rhodobacter sphaeroides
journal, March 2010

  • Nuss, A. M.; Glaeser, J.; Berghoff, B. A.
  • Journal of Bacteriology, Vol. 192, Issue 10
  • DOI: 10.1128/JB.01605-09

Extracytoplasmic Function σ Factors Can Be Implemented as Robust Heterologous Genetic Switches in Bacillus subtilis
journal, March 2019


Reactive Oxygen Species Production by Escherichia coli Respiratory Complex I
journal, April 2015


Singlet oxygen-triggered chloroplast-to-nucleus retrograde signalling pathways: An emerging perspective: Recent trends in singlet oxygen signaling
journal, June 2018

  • Dogra, Vivek; Rochaix, Jean-David; Kim, Chanhong
  • Plant, Cell & Environment, Vol. 41, Issue 8
  • DOI: 10.1111/pce.13332

Features of Rhodobacter sphaeroides ChrR Required for Stimuli to Promote the Dissociation of σE/ChrR Complexes
journal, April 2011

  • Greenwell, Roger; Nam, Tae-Wook; Donohue, Timothy J.
  • Journal of Molecular Biology, Vol. 407, Issue 4
  • DOI: 10.1016/j.jmb.2011.01.055

Photooxidative stress-induced and abundant small RNAs in Rhodobacter sphaeroides: Small RNAs in Rhodobacter
journal, December 2009


Interactions Between the Rhodobacter sphaeroides ECF Sigma Factor, σ E , and its Anti-sigma Factor, ChrR
journal, August 2004

  • Anthony, Jennifer R.; Newman, Jack D.; Donohue, Timothy J.
  • Journal of Molecular Biology, Vol. 341, Issue 2
  • DOI: 10.1016/j.jmb.2004.06.018

A Conserved Structural Module Regulates Transcriptional Responses to Diverse Stress Signals in Bacteria
journal, September 2007


Carotenoid oxidation products are stress signals that mediate gene responses to singlet oxygen in plants
journal, March 2012

  • Ramel, F.; Birtic, S.; Ginies, C.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 14
  • DOI: 10.1073/pnas.1115982109

Bacterial Adaptation of Respiration from Oxic to Microoxic and Anoxic Conditions: Redox Control
journal, April 2012

  • Bueno, Emilio; Mesa, Socorro; Bedmar, Eulogio J.
  • Antioxidants & Redox Signaling, Vol. 16, Issue 8
  • DOI: 10.1089/ars.2011.4051

Research advances in the use of tetrapyrrolic photosensitizers for photodynamic therapy
journal, January 2004


Reactive oxygen gene network of plants
journal, October 2004


Design of orthogonal genetic switches based on a crosstalk map of σs, anti‐σs, and promoters
journal, January 2013

  • Rhodius, Virgil A.; Segall‐Shapiro, Thomas H.; Sharon, Brian D.
  • Molecular Systems Biology, Vol. 9, Issue 1
  • DOI: 10.1038/msb.2013.58

EARTH SCIENCE: The Story of O2
journal, June 2005


Redox Functions of Carotenoids in Photosynthesis
journal, July 2004

  • Frank, Harry A.; Brudvig, Gary W.
  • Biochemistry, Vol. 43, Issue 27
  • DOI: 10.1021/bi0492096

Phylogeny, Function, and Evolution of the Cupins, a Structurally Conserved, Functionally Diverse Superfamily of Proteins
journal, April 2001


Singlet Oxygen Inhibits the Repair of Photosystem II by Suppressing the Translation Elongation of the D1 Protein in Synechocystis sp. PCC 6803
journal, September 2004

  • Nishiyama, Yoshitaka; Allakhverdiev, Suleyman I.; Yamamoto, Hiroshi
  • Biochemistry, Vol. 43, Issue 35
  • DOI: 10.1021/bi036178q

Assignment of the Zinc Ligands in RsrA, a Redox-Sensing ZAS Protein from Streptomyces coelicolor
journal, July 2006

  • Zdanowski, Konrad; Doughty, Phillip; Jakimowicz, Piotr
  • Biochemistry, Vol. 45, Issue 27
  • DOI: 10.1021/bi060711v

Organization and Evolution of the Biological Response to Singlet Oxygen Stress
journal, November 2008

  • Dufour, Yann S.; Landick, Robert; Donohue, Timothy J.
  • Journal of Molecular Biology, Vol. 383, Issue 3
  • DOI: 10.1016/j.jmb.2008.08.017

Model peptide for anti-sigma factor domain HHCC zinc fingers: high reactivity toward 1 O 2 leads to domain unfolding
journal, January 2019

  • Chabert, Valentin; Lebrun, Vincent; Lebrun, Colette
  • Chemical Science, Vol. 10, Issue 12
  • DOI: 10.1039/C9SC00341J

Singlet oxygen generation in the reaction centers of Rhodobacter sphaeroides
journal, February 2008

  • Uchoa, Adjaci F.; Knox, Peter P.; Turchielle, Rozane
  • European Biophysics Journal, Vol. 37, Issue 6
  • DOI: 10.1007/s00249-008-0287-y

Cytochrome c oxidase: exciting progress and remaining mysteries
journal, October 2008

  • Brzezinski, Peter; Gennis, Robert B.
  • Journal of Bioenergetics and Biomembranes, Vol. 40, Issue 5
  • DOI: 10.1007/s10863-008-9181-7

The cytochrome bd respiratory oxygen reductases
journal, November 2011

  • Borisov, Vitaliy B.; Gennis, Robert B.; Hemp, James
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1807, Issue 11
  • DOI: 10.1016/j.bbabio.2011.06.016

Evolution of photosynthesis and aerobic respiration in the cyanobacteria
journal, August 2019


Extracytoplasmic Function σ Factors Can Be Implemented as Robust Heterologous Genetic Switches in Bacillus subtilis
journal, March 2019


Interactions Between the Rhodobacter sphaeroides ECF Sigma Factor, σ E , and its Anti-sigma Factor, ChrR
journal, August 2004

  • Anthony, Jennifer R.; Newman, Jack D.; Donohue, Timothy J.
  • Journal of Molecular Biology, Vol. 341, Issue 2
  • DOI: 10.1016/j.jmb.2004.06.018

Organization and Evolution of the Biological Response to Singlet Oxygen Stress
journal, November 2008

  • Dufour, Yann S.; Landick, Robert; Donohue, Timothy J.
  • Journal of Molecular Biology, Vol. 383, Issue 3
  • DOI: 10.1016/j.jmb.2008.08.017

Themes and variations in gene regulation by extracytoplasmic function (ECF) sigma factors
journal, April 2017


A Conserved Structural Module Regulates Transcriptional Responses to Diverse Stress Signals in Bacteria
journal, September 2007


Reactive oxygen gene network of plants
journal, October 2004


Redox sensing by prokaryotic transcription factors
journal, January 2000


Redox-regulated chaperone function and conformational changes of Escherichia coli Hsp33
journal, January 2001


Structure of the Bacterial RNA Polymerase Promoter Specificity σ Subunit
journal, March 2002


Reactive Oxygen Species Production by Escherichia coli Respiratory Complex I
journal, April 2015


Singlet Oxygen Inhibits the Repair of Photosystem II by Suppressing the Translation Elongation of the D1 Protein in Synechocystis sp. PCC 6803
journal, September 2004

  • Nishiyama, Yoshitaka; Allakhverdiev, Suleyman I.; Yamamoto, Hiroshi
  • Biochemistry, Vol. 43, Issue 35
  • DOI: 10.1021/bi036178q

Assignment of the Zinc Ligands in RsrA, a Redox-Sensing ZAS Protein from Streptomyces coelicolor
journal, July 2006

  • Zdanowski, Konrad; Doughty, Phillip; Jakimowicz, Piotr
  • Biochemistry, Vol. 45, Issue 27
  • DOI: 10.1021/bi060711v

Protein Synthesis Patterns Reveal a Complex Regulatory Response to Singlet Oxygen in Rhodobacter
journal, July 2007

  • Glaeser, Jens; Zobawa, Monica; Lottspeich, Friedrich
  • Journal of Proteome Research, Vol. 6, Issue 7
  • DOI: 10.1021/pr060624p

Design of orthogonal genetic switches based on a crosstalk map of σs, anti‐σs, and promoters
journal, January 2013

  • Rhodius, Virgil A.; Segall‐Shapiro, Thomas H.; Sharon, Brian D.
  • Molecular Systems Biology, Vol. 9, Issue 1
  • DOI: 10.1038/msb.2013.58

Bacterial responses to photo-oxidative stress
journal, November 2009

  • Ziegelhoffer, Eva C.; Donohue, Timothy J.
  • Nature Reviews Microbiology, Vol. 7, Issue 12
  • DOI: 10.1038/nrmicro2237

Fueled by light
journal, April 2018


Light and oxygenic photosynthesis: energy dissipation as a protection mechanism against photo-oxidation
journal, July 2005

  • Szabó, Ildikó; Bergantino, Elisabetta; Giacometti, Giorgio Mario
  • EMBO reports, Vol. 6, Issue 7
  • DOI: 10.1038/sj.embor.7400460

Redox Switch of Hsp33 Has a Novel Zinc-binding Motif
journal, September 2000

  • Jakob, Ursula; Eser, Markus; Bardwell, James C. A.
  • Journal of Biological Chemistry, Vol. 275, Issue 49
  • DOI: 10.1074/jbc.m005957200

Blue Light Induces Mitochondrial DNA Damage and Free Radical Production in Epithelial Cells
journal, March 2005

  • Godley, Bernard F.; Shamsi, Farrukh A.; Liang, Fong-Qi
  • Journal of Biological Chemistry, Vol. 280, Issue 22
  • DOI: 10.1074/jbc.m502194200

Bacterial Adaptation of Respiration from Oxic to Microoxic and Anoxic Conditions: Redox Control
journal, April 2012

  • Bueno, Emilio; Mesa, Socorro; Bedmar, Eulogio J.
  • Antioxidants & Redox Signaling, Vol. 16, Issue 8
  • DOI: 10.1089/ars.2011.4051

How carotenoids protect bacterial photosynthesis
journal, October 2000

  • Cogdell, Richard J.; Howard, Tina D.; Bittl, Robert
  • Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Vol. 355, Issue 1402
  • DOI: 10.1098/rstb.2000.0696

Redox Homeostasis and Antioxidant Signaling: A Metabolic Interface between Stress Perception and Physiological Responses
journal, June 2005


Activity of Rhodobacter sphaeroides RpoHII, a Second Member of the Heat Shock Sigma Factor Family
journal, August 2006

  • Green, H. A.; Donohue, T. J.
  • Journal of Bacteriology, Vol. 188, Issue 16
  • DOI: 10.1128/jb.00405-06

RpoHII Activates Oxidative-Stress Defense Systems and Is Controlled by RpoE in the Singlet Oxygen-Dependent Response in Rhodobacter sphaeroides
journal, October 2008

  • Nuss, A. M.; Glaeser, J.; Klug, G.
  • Journal of Bacteriology, Vol. 191, Issue 1
  • DOI: 10.1128/jb.00925-08

Metabolic Roles of a Rhodobacter sphaeroides Member of the ς 32 Family
journal, January 1998


Proteins Needed to Activate a Transcriptional Response to the Reactive Oxygen Species Singlet Oxygen
journal, January 2013

  • Nam, Tae-Wook; Ziegelhoffer, Eva C.; Lemke, Rachelle A. S.
  • mBio, Vol. 4, Issue 1
  • DOI: 10.1128/mbio.00541-12

Convergence of Molecular, Modeling, and Systems Approaches for an Understanding of the Escherichia coli Heat Shock Response
journal, September 2008

  • Guisbert, E.; Yura, T.; Rhodius, V. A.
  • Microbiology and Molecular Biology Reviews, Vol. 72, Issue 3
  • DOI: 10.1128/mmbr.00007-08

Reconstruction of the Core and Extended Regulons of Global Transcription Factors
journal, July 2010


Convergence of the Transcriptional Responses to Heat Shock and Singlet Oxygen Stresses
journal, September 2012


DegS and RseP Homologous Proteases Are Involved in Singlet Oxygen Dependent Activation of RpoE in Rhodobacter sphaeroides
journal, November 2013


Oxidation Decomposition of Unsaturated Fatty Acids by Singlet Oxygen in Phospholipid Bilayer Membranes
journal, January 2007

  • Watabe, Naoki; Ishida, Yu; Ochiai, Akira
  • Journal of Oleo Science, Vol. 56, Issue 2
  • DOI: 10.5650/jos.56.73

Works referencing / citing this record:

ECF σ factors with regulatory extensions: the one‐component systems of the σ universe
journal, June 2019

  • Pinto, Daniela; Liu, Qiang; Mascher, Thorsten
  • Molecular Microbiology, Vol. 112, Issue 2
  • DOI: 10.1111/mmi.14323

Discovery of the extracytoplasmic function σ factors
journal, June 2019

  • Lonetto, Michael A.; Donohue, Timothy J.; Gross, Carol A.
  • Molecular Microbiology, Vol. 112, Issue 2
  • DOI: 10.1111/mmi.14307