1932

Abstract

Responding to environmental cues is a prerequisite for survival in the microbial world. Extracytoplasmic function σ factors (ECFs) represent the third most abundant and by far the most diverse type of bacterial signal transduction. While archetypal ECFs are controlled by cognate anti-σ factors, comprehensive comparative genomics efforts have revealed a much higher abundance and regulatory diversity of ECF regulation than previously appreciated. They have also uncovered a diverse range of anti-σ factor–independent modes of controlling ECF activity, including fused regulatory domains and phosphorylation-dependent mechanisms. While our understanding of ECF diversity is comprehensive for well-represented and heavily studied bacterial phyla—such as , , and Actinobacteria (phylum )—our current knowledge about ECF-dependent signaling in the vast majority of underrepresented phyla is still far from complete. In particular, the dramatic extension of bacterial diversity in the course of metagenomic studies represents both a new challenge and an opportunity in expanding the world of ECF-dependent signal transduction.

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2023-09-15
2024-04-21
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Literature Cited

  1. 1.
    Ades SE. 2008. Regulation by destruction: design of the σE envelope stress response. Curr. Opin. Microbiol. 11:535–40
    [Google Scholar]
  2. 2.
    Barchinger SE, Ades SE. 2013. Regulated proteolysis: control of the Escherichia coli σE-dependent cell envelope stress response. Subcell. Biochem. 66:129–60
    [Google Scholar]
  3. 3.
    Bibb MJ, Buttner MJ. 2003. The Streptomyces coelicolor developmental transcription factor σBldN is synthesized as a proprotein. J. Bacteriol. 185:2338–45
    [Google Scholar]
  4. 4.
    Bordi C, Butcher BG, Shi Q, Hachmann AB, Peters JE, Helmann JD. 2008. In vitro mutagenesis of Bacillus subtilis by using a modified Tn7 transposon with an outward-facing inducible promoter. Appl. Environ. Microbiol. 74:3419–25
    [Google Scholar]
  5. 5.
    Braun V, Mahren S, Sauter A. 2006. Gene regulation by transmembrane signaling. Biometals 19:103–13
    [Google Scholar]
  6. 6.
    Brooks BE, Buchanan SK. 2008. Signaling mechanisms for activation of extracytoplasmic function (ECF) sigma factors. Biochim. Biophys. Acta Biomembr. 1778:1930–45
    [Google Scholar]
  7. 7.
    Browning DF, Busby SJ. 2016. Local and global regulation of transcription initiation in bacteria. Nat. Rev. Microbiol. 14:638–50
    [Google Scholar]
  8. 8.
    Buchner S, Schlundt A, Lassak J, Sattler M, Jung K. 2015. Structural and functional analysis of the signal-transducing linker in the pH-responsive one-component system CadC of Escherichia coli. J. Mol. Biol. 427:2548–61
    [Google Scholar]
  9. 9.
    Butcher BG, Mascher T, Helmann JD. 2008. Environmental sensing and the role of extracytoplasmic function (ECF) sigma factors. Bacterial Physiology: A Molecular Approach WM El-Sharoud 233–61. Berlin/Heidelberg: Springer
    [Google Scholar]
  10. 10.
    Campbell EA, Greenwell R, Anthony JR, Wang S, Lim L et al. 2007. A conserved structural module regulates transcriptional responses to diverse stress signals in bacteria. Mol. Cell 27:793–805
    [Google Scholar]
  11. 11.
    Casas-Pastor D, Müller RR, Jaenicke S, Brinkrolf K, Becker A et al. 2021. Expansion and re-classification of the extracytoplasmic function (ECF) sigma factor family. Nucleic Acids Res. 49:986–1005
    [Google Scholar]
  12. 12.
    Chevalier S, Bouffartigues E, Bazire A, Tahrioui A, Duchesne R et al. 2019. Extracytoplasmic function sigma factors in Pseudomonas aeruginosa. Biochim. Biophys. Acta Gene Regul. Mech. 1862:706–21
    [Google Scholar]
  13. 13.
    Darnell RL, Nakatani Y, Knottenbelt MK, Gebhard S, Cook GM. 2019. Functional characterization of BcrR: a one-component transmembrane signal transduction system for bacitracin resistance. Microbiology 165:475–87
    [Google Scholar]
  14. 14.
    Donohue TJ. 2019. Shedding light on a group IV (ECF11) alternative σ factor. Mol. Microbiol. 112:374–84
    [Google Scholar]
  15. 15.
    Dubey AP, Pandey P, Singh VS, Mishra MN, Singh S et al. 2020. An ECF41 family σ factor controls motility and biogenesis of lateral flagella in Azospirillum brasilense Sp245. J. Bacteriol. 202:e00231
    [Google Scholar]
  16. 16.
    Fiebig A, Herrou J, Willett J, Crosson S. 2015. General stress signaling in the Alphaproteobacteria. Annu. Rev. Genet. 49:603–25
    [Google Scholar]
  17. 17.
    Fleischmann RD, Adams MD, White O, Clayton RA, Kirkness EF et al. 1995. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269:496–512
    [Google Scholar]
  18. 18.
    Francez-Charlot A, Kaczmarczyk A, Fischer HM, Vorholt JA. 2015. The general stress response in Alphaproteobacteria. Trends Microbiol. 23:164–71
    [Google Scholar]
  19. 19.
    Fraser CM, Gocayne JD, White O, Adams MD, Clayton RA et al. 1995. The minimal gene complement of Mycoplasma genitalium. Science 270:397–403
    [Google Scholar]
  20. 20.
    Gao R, Stock AM. 2009. Biological insights from structures of two-component proteins. Annu. Rev. Microbiol. 63:133–54
    [Google Scholar]
  21. 21.
    Gómez-Santos N, Pérez J, Sánchez-Sutil MC, Moraleda-Muñoz A, Muñoz-Dorado J. 2011. CorE from Myxococcus xanthus is a copper-dependent RNA polymerase sigma factor. PLOS Genet. 7:e1002106
    [Google Scholar]
  22. 22.
    Goutam K, Gupta AK, Gopal B. 2017. The fused SnoaL_2 domain in the Mycobacterium tuberculosis sigma factor σJ modulates promoter recognition. Nucleic Acids Res. 45:9760–72
    [Google Scholar]
  23. 23.
    Gruber TM, Gross CA. 2003. Multiple sigma subunits and the partitioning of bacterial transcription space. Annu. Rev. Microbiol. 57:441–66
    [Google Scholar]
  24. 24.
    Hecker M, Pane-Farre J, Völker U. 2007. σB-dependent general stress response in Bacillus subtilis and related gram-positive bacteria. Annu. Rev. Microbiol. 61:215–36
    [Google Scholar]
  25. 25.
    Heinrich J, Wiegert T. 2009. Regulated intramembrane proteolysis in the control of extracytoplasmic function sigma factors. Res. Microbiol. 160:696–703
    [Google Scholar]
  26. 26.
    Helmann JD. 2002. The extracytoplasmic function (ECF) sigma factors. Adv. Microb. Physiol. 46:47–110
    [Google Scholar]
  27. 27.
    Helmann JD. 2006. Deciphering a complex genetic regulatory network: the Bacillus subtilis σW protein and intrinsic resistance to antimicrobial compounds. Sci. Prog. 89:243–66
    [Google Scholar]
  28. 28.
    Helmann JD. 2016. Bacillus subtilis extracytoplasmic function (ECF) sigma factors and defense of the cell envelope. Curr. Opin. Microbiol. 30:122–32
    [Google Scholar]
  29. 29.
    Helmann JD. 2019. Where to begin? Sigma factors and the selectivity of transcription initiation in bacteria. Mol. Microbiol. 112:335–47
    [Google Scholar]
  30. 30.
    Helmann JD, Chamberlin MJ. 1988. Structure and function of bacterial sigma factors. Annu. Rev. Biochem. 57:839–72
    [Google Scholar]
  31. 31.
    Hengge R. 2008. The two-component network and the general stress sigma factor RpoS (σS) in Escherichia coli. Adv. Exp. Med. Biol. 631:40–53
    [Google Scholar]
  32. 32.
    Hengge R. 2009. Proteolysis of σS (RpoS) and the general stress response in Escherichia coli. Res. Microbiol. 160:667–76
    [Google Scholar]
  33. 33.
    Hengge R 2011. The general stress response in gram-negative bacteria. Bacterial Stress Responses G Storz, R Hengge 251–90. Washington, DC: ASM
    [Google Scholar]
  34. 34.
    Ho TD, Ellermeier CD. 2012. Extracytoplasmic function sigma factor activation. Curr. Opin. Microbiol. 15:182–88
    [Google Scholar]
  35. 35.
    Ho TD, Ellermeier CD. 2019. Activation of the extracytoplasmic function sigma factor σV by lysozyme. Mol. Microbiol. 112:410–19
    [Google Scholar]
  36. 36.
    Hu Y, Kendall S, Stoker NG, Coates AR. 2004. The Mycobacterium tuberculosis sigJ gene controls sensitivity of the bacterium to hydrogen peroxide. FEMS Microbiol. Lett. 237:415–23
    [Google Scholar]
  37. 37.
    Huang XL, Pinto D, Fritz G, Mascher T. 2015. Environmental sensing in Actinobacteria: a comprehensive survey on the signaling capacity of this phylum. J. Bacteriol. 197:2517–35
    [Google Scholar]
  38. 38.
    Iyer SC, Casas-Pastor D, Kraus D, Mann P, Schirner K et al. 2020. Transcriptional regulation by σ factor phosphorylation in bacteria. Nat. Microbiol. 5:395–406
    [Google Scholar]
  39. 39.
    Jogler C, Waldmann J, Huang X, Jogler M, Glöckner FO et al. 2012. Identification of proteins likely to be involved in morphogenesis, cell division, and signal transduction in planctomycetes by comparative genomics. J. Bacteriol. 194:6419–30
    [Google Scholar]
  40. 40.
    Kadowaki T, Yukitake H, Naito M, Sato K, Kikuchi Y et al. 2016. A two-component system regulates gene expression of the type IX secretion component proteins via an ECF σ factor. Sci. Rep. 6:23288
    [Google Scholar]
  41. 41.
    Kim MS, Hahn MY, Cho Y, Cho SN, Roe JH. 2009. Positive and negative feedback regulatory loops of thiol-oxidative stress response mediated by an unstable isoform of σR in actinomycetes. Mol. Microbiol. 73:815–25
    [Google Scholar]
  42. 42.
    Li LT, Fang CL, Zhuang NN, Wang TT, Zhang Y. 2019. Structural basis for transcription initiation by bacterial ECF σ factors. Nat. Commun. 10:1153
    [Google Scholar]
  43. 43.
    Lin W, Mandal S, Degen D, Cho MS, Feng Y et al. 2019. Structural basis of ECF-σ-factor-dependent transcription initiation. Nat. Commun. 10:710
    [Google Scholar]
  44. 44.
    Liu Q, Pinto D, Mascher T. 2018. Characterization of the widely distributed novel ECF42 group of extracytoplasmic function σ factors in Streptomyces venezuelae. J. Bacteriol. 200:e00437
    [Google Scholar]
  45. 45.
    Lonetto MA, Brown KL, Rudd KE, Buttner MJ. 1994. Analysis of the Streptomyces coelicolor sigE gene reveals the existence of a subfamily of eubacterial RNA polymerase sigma factors involved in the regulation of extracytoplasmic functions. PNAS 91:7573–77
    [Google Scholar]
  46. 46.
    Lonetto MA, Donohue TJ, Gross CA, Buttner MJ. 2019. Discovery of the extracytoplasmic function σ factors. Mol. Microbiol. 112:348–55
    [Google Scholar]
  47. 47.
    Mahren S, Schnell H, Braun V. 2005. Occurrence and regulation of the ferric citrate transport system in Escherichia coli B, Klebsiella pneumoniae, Enterobacter aerogenes, and Photorhabdus luminescens. Arch. Microbiol. 184:175–86
    [Google Scholar]
  48. 48.
    Mallick Gupta A, Mandal S 2020. The C-terminal domain of M. tuberculosis ECF σ factor I (SigI) interferes in SigI-RNAP interaction. J. Mol. Model. 26:77
    [Google Scholar]
  49. 49.
    Marcos-Torres FJ, Pérez J, Gomez-Santos N, Moraleda-Muñoz A, Muñoz-Dorado J 2016. In depth analysis of the mechanism of action of metal-dependent σ factors: characterization of CorE2 from Myxococcus xanthus. Nucleic Acids Res. 44:5571–84
    [Google Scholar]
  50. 50.
    Mascher T. 2013. Signaling diversity and evolution of extracytoplasmic function (ECF) σ factors. Curr. Opin. Microbiol. 16:148–55
    [Google Scholar]
  51. 51.
    Missiakas D, Raina S 1998. The extracytoplasmic function sigma factors: role and regulation. Mol. Microbiol. 28:1059–66
    [Google Scholar]
  52. 52.
    Moraleda-Muñoz A, Marcos-Torres FJ, Pérez J, Muñoz-Dorado J 2019. Metal-responsive RNA polymerase extracytoplasmic function (ECF) sigma factors. Mol. Microbiol. 112:385–98
    [Google Scholar]
  53. 53.
    Oliveira R, Bush MJ, Pires S, Chandra G, Casas-Pastor D et al. 2020. The novel ECF56 SigG1-RsfG system modulates morphological differentiation and metal-ion homeostasis in Streptomyces tsukubaensis. Sci. Rep. 10:21728
    [Google Scholar]
  54. 54.
    Paget MS, Helmann JD. 2003. The σ70 family of sigma factors. Genome Biol. 4:203
    [Google Scholar]
  55. 55.
    Park JH, Lee JH, Roe JH. 2019. SigR, a hub of multilayered regulation of redox and antibiotic stress responses. Mol. Microbiol. 112:420–31
    [Google Scholar]
  56. 56.
    Pinto D, da Fonseca RR. 2020. Evolution of the extracytoplasmic function σ factor protein family. NAR Genom. Bioinform. 2:lqz026
    [Google Scholar]
  57. 57.
    Pinto D, Liu Q, Mascher T. 2019. ECF σ factors with regulatory extensions: the one-component systems of the σ universe. Mol. Microbiol. 112:399–409
    [Google Scholar]
  58. 58.
    Pinto D, Mascher T. 2016. (Actino)bacterial “intelligence”: using comparative genomics to unravel the information processing capacities of microbes. Curr. Genet. 62:487–98
    [Google Scholar]
  59. 59.
    Pinto D, Mascher T. 2016. The ECF classification: a phylogenetic reflection of the regulatory diversity in the extracytoplasmic function σ factor protein family. Stress and Environmental Regulation of Gene Expression and Adaptation in Bacteria ed. FJ De Bruijn , Vol. 164–96. Hoboken, NJ: Wiley Blackwell
    [Google Scholar]
  60. 60.
    Price CW 2011. The general stress response in Bacillus subtilis and related gram-positive bacteria. Bacterial Stress Responses G Storz, R Hengge 301–18. Washington, DC: ASM
    [Google Scholar]
  61. 61.
    Schneider JS, Glickman MS. 2013. Function of site-2 proteases in bacteria and bacterial pathogens. Biochim. Biophys. Acta Biomembr. 1828:2808–14
    [Google Scholar]
  62. 62.
    Seipke RF, Patrick E, Hutchings MI. 2014. Regulation of antimycin biosynthesis by the orphan ECF RNA polymerase σ factor σAntA. PeerJ 2:e253
    [Google Scholar]
  63. 63.
    Sineva E, Savkina M, Ades SE. 2017. Themes and variations in gene regulation by extracytoplasmic function (ECF) σ factors. Curr. Opin. Microbiol. 36:128–37
    [Google Scholar]
  64. 64.
    Staroń A, Mascher T. 2010. Extracytoplasmic function σ factors come of age. Microbe 5:164–70
    [Google Scholar]
  65. 65.
    Staroń A, Mascher T. 2010. General stress response in α-proteobacteria: PhyR and beyond. Mol. Microbiol. 78:271–77
    [Google Scholar]
  66. 66.
    Staroń A, Sofia HJ, Dietrich S, Ulrich LE, Liesegang H, Mascher T. 2009. The third pillar of bacterial signal transduction: classification of the extracytoplasmic function (ECF) σ factor protein family. Mol. Microbiol. 74:557–81
    [Google Scholar]
  67. 67.
    Stock AM, Robinson VL, Goudreau PN. 2000. Two-component signal transduction. Annu. Rev. Biochem. 69:183–215
    [Google Scholar]
  68. 68.
    Thakur KG, Joshi AM, Gopal B. 2007. Structural and biophysical studies on two promoter recognition domains of the extra-cytoplasmic function σ factor σC from Mycobacterium tuberculosis. J. Biol. Chem. 282:4711–18
    [Google Scholar]
  69. 69.
    Tran NT, Huang X, Hong HJ, Bush MJ, Chandra G et al. 2019. Defining the regulon of genes controlled by σE, a key regulator of the cell envelope stress response in Streptomyces coelicolor. Mol. Microbiol. 112:461–81
    [Google Scholar]
  70. 70.
    Ulrich LE, Koonin EV, Zhulin IB. 2005. One-component systems dominate signal transduction in prokaryotes. Trends Microbiol. 13:52–56
    [Google Scholar]
  71. 71.
    Wecke T, Halang P, Staron A, Dufour YS, Donohue TJ, Mascher T. 2012. Extracytoplasmic function σ factors of the widely distributed group ECF41 contain a fused regulatory domain. MicrobiologyOpen 1:194–213
    [Google Scholar]
  72. 72.
    Wiegand S, Jogler M, Boedeker C, Pinto D, Vollmers J et al. 2020. Cultivation and functional characterization of 79 planctomycetes uncovers their unique biology. Nat. Microbiol. 5:126–40
    [Google Scholar]
  73. 73.
    Wu H, Liu Q, Casas-Pastor D, Durr F, Mascher T, Fritz G. 2019. The role of C-terminal extensions in controlling ECF σ factor activity in the widely conserved groups ECF41 and ECF42. Mol. Microbiol. 112:498–514
    [Google Scholar]
  74. 74.
    Yanamandra SS, Sarrafee SS, Anaya-Bergman C, Jones K, Lewis JP. 2012. Role of the Porphyromonas gingivalis extracytoplasmic function σ factor, SigH. Mol. Oral Microbiol. 27:202–19
    [Google Scholar]
  75. 75.
    Yoshimura M, Asai K, Sadaie Y, Yoshikawa H. 2004. Interaction of Bacillus subtilis extracytoplasmic function (ECF) sigma factors with the N-terminal regions of their potential anti-sigma factors. Microbiology 150:591–99
    [Google Scholar]
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