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Volume 168, Issue 10

A bacterial secretosome for regulated envelope biogenesis and quality control? Open Access

Abstract

The Gram-negative bacterial envelope is the first line of defence against environmental stress and antibiotics. Therefore, its biogenesis is of considerable fundamental interest, as well as a challenge to address the growing problem of antimicrobial resistance. All bacterial proteins are synthesised in the cytosol, so inner- and outer-membrane proteins, and periplasmic residents have to be transported to their final destinations via specialised protein machinery. The Sec translocon, a ubiquitous integral inner-membrane (IM) complex, is key to this process as the major gateway for protein transit from the cytosol to the cell envelope; this can be achieved during their translation, or afterwards. Proteins need to be directed into the inner-membrane (usually co-translational), otherwise SecA utilises ATP and the proton-motive-force (PMF) to drive proteins across the membrane post-translationally. These proteins are then picked up by chaperones for folding in the periplasm, or delivered to the β-barrel assembly machinery (BAM) for incorporation into the outer-membrane. The core hetero-trimeric SecYEG-complex forms the hub for an extensive network of interactions that regulate protein delivery and quality control. Here, we conduct a biochemical exploration of this ‘secretosome’ –a very large, versatile and inter-changeable assembly with the Sec-translocon at its core; featuring interactions that facilitate secretion (SecDF), inner- and outer-membrane protein insertion (respectively, YidC and BAM), protein folding and quality control (e.g. PpiD, YfgM and FtsH). We propose the dynamic interplay amongst these, and other factors, act to ensure efficient envelope biogenesis, regulated to accommodate the requirements of cell elongation and division. We believe this organisation is critical for cell wall biogenesis and remodelling and thus its perturbation could be a means for the development of anti-microbials.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): bacterial secretion , cell division , envelope biogenesis , quality control , Sec-BAM complex and secretosome
Funding
This study was supported by the:
  • Biotechnology and Biological Sciences Research Council (Award BB/T008741/1)
    • Principle Award Recipient: SophieL Williams
  • Biotechnology and Biological Sciences Research Council (Award BB/S008349/1)
    • Principle Award Recipient: IanCollinson
© 2022 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2022-10-19
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References

  1. Pogliano JA, Beckwith J. SecD and SecF facilitate protein export in Escherichia coli. EMBO J 1994; 13:554–561 [View Article]
     [Google Scholar]
  2. Collinson I. The dynamic ATP-driven mechanism of bacterial protein translocation and the critical role of phospholipids. Front Microbiol 2019; 10:1217 [View Article]
     [Google Scholar]
  3. Brundage L, Hendrick JP, Schiebel E, Driessen AJ, Wickner W. The purified E. coli integral membrane protein SecY/E is sufficient for reconstitution of SecA-dependent precursor protein translocation. Cell 1990; 62:649–657 [View Article]
     [Google Scholar]
  4. Allen WJ, Corey RA, Watkins DW, Oliveira ASF, Hards K et al. Rate-limiting transport of positively charged arginine residues through the Sec-machinery is integral to the mechanism of protein secretion. Elife 2022; 11:e77586 [View Article]
     [Google Scholar]
  5. Samuelson JC, Chen M, Jiang F, Möller I, Wiedmann M et al. YidC mediates membrane protein insertion in bacteria. Nature 2000; 406:637–641 [View Article] [PubMed]
     [Google Scholar]
  6. Scotti PA, Urbanus ML, Brunner J, de Gier JW, von Heijne G et al. YidC, the Escherichia coli homologue of mitochondrial Oxa1p, is a component of the Sec translocase. EMBO J 2000; 19:542–549 [View Article]
     [Google Scholar]
  7. Schulze RJ, Komar J, Botte M, Allen WJ, Whitehouse S. Membrane protein insertion and proton-motive-force-dependent secretion through the bacterial holo-translocon SecYEG–SecDF–YajC–YidC. Proc Natl Acad Sci USA 2014; 111:4844–4849 [View Article]
     [Google Scholar]
  8. Komar J, Alvira S, Schulze RJ, Martin R, Lycklama A Nijeholt JA et al. Membrane protein insertion and assembly by the bacterial holo-translocon SecYEG-SecDF-YajC-YidC. Biochem J 2016; 473:3341–3354 [View Article] [PubMed]
     [Google Scholar]
  9. Martin R, Larsen AH, Corey RA, Midtgaard SR, Frielinghaus H et al. Structure and dynamics of the central lipid pool and proteins of the bacterial holo-translocon. Biophys J 2019; 116:1931–1940 [View Article]
     [Google Scholar]
  10. Sklar JG, Wu T, Kahne D, Silhavy TJ. Defining the roles of the periplasmic chaperones SurA, Skp, and DegP in Escherichia coli. Genes Dev 2007; 21:2473–2484 [View Article]
     [Google Scholar]
  11. Rizzitello AE, Harper JR, Silhavy TJ. Genetic evidence for parallel pathways of chaperone activity in the periplasm of Escherichia coli. J Bacteriol 2001; 183:6794–6800 [View Article]
     [Google Scholar]
  12. Spiess C, Beil A, Ehrmann M. A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein. Cell 1999; 97:339–347 [View Article]
     [Google Scholar]
  13. Wu T, Malinverni J, Ruiz N, Kim S, Silhavy TJ et al. Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli. Cell 2005; 121:235–245 [View Article]
     [Google Scholar]
  14. Ricci DP, Silhavy TJ. Outer membrane protein insertion by the β-barrel assembly machine. EcoSal Plus 2019; 8: [View Article]
     [Google Scholar]
  15. Wang Y, Wang R, Jin F, Liu Y, Yu J et al. A supercomplex spanning the inner and outer membranes mediates the biogenesis of β-barrel outer membrane proteins in bacteria. J Biol Chem 2016; 291:16720–16729 [View Article]
     [Google Scholar]
  16. Alvira S, Watkins DW, Troman L, Allen WJ, Lorriman JS et al. Inter-membrane association of the Sec and BAM translocons for bacterial outer-membrane biogenesis. Elife 2020; 9:e60669 [View Article]
     [Google Scholar]
  17. Carlson ML, Stacey RG, Young JW, Wason IS, Zhao Z et al. Profiling the Escherichia coli membrane protein interactome captured in peptidisc libraries. Elife 2019; 8:e46615 [View Article]
     [Google Scholar]
  18. Corey RA, Pyle E, Allen WJ, Watkins DW, Casiraghi M et al. Specific cardiolipin-SecY interactions are required for proton-motive force stimulation of protein secretion. Proc Natl Acad Sci U S A 2018; 115:7967–7972 [View Article]
     [Google Scholar]
  19. Collinson I, Breyton C, Duong F, Tziatzios C, Schubert D et al. Projection structure and oligomeric properties of a bacterial core protein translocase. EMBO J 2001; 20:2462–2471 [View Article]
     [Google Scholar]
  20. Miroux B, Walker JE. Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J Mol Biol 1996; 260:289–298 [View Article]
     [Google Scholar]
  21. Carranza G, Angius F, Ilioaia O, Solgadi A, Miroux B et al. Cardiolipin plays an essential role in the formation of intracellular membranes in Escherichia coli. Biochim Biophys Acta Biomembr 2017; 1859:1124–1132 [View Article]
     [Google Scholar]
  22. Gold VAM, Robson A, Bao H, Romantsov T, Duong F et al. The action of cardiolipin on the bacterial translocon. Proc Natl Acad Sci U S A 2010; 107:10044–10049 [View Article]
     [Google Scholar]
  23. Corey RA, Pyle E, Allen WJ, Casiraghi M, Miroux B et al. Specific cardiolipin-SecY interactions are required for proton-motive-force stimulation of protein secretion. Biophysics 2018; 202184: [View Article]
     [Google Scholar]
  24. Alvira S, Corey RA, Collinson I, Römisch K. Membrane protein biogenesis by the EMC. EMBO J 2021; 40:e107407 [View Article]
     [Google Scholar]
  25. Bieniossek C, Nie Y, Frey D, Olieric N, Schaffitzel C et al. Automated unrestricted multigene recombineering for multiprotein complex production. Nat Methods 2009; 6:447–450 [View Article] [PubMed]
     [Google Scholar]
  26. Jauss B, Petriman N-A, Drepper F, Franz L, Sachelaru I et al. Noncompetitive binding of PpiD and YidC to the SecYEG translocon expands the global view on the SecYEG interactome in Escherichia coli. J Biol Chem 2019; 294:19167–19183 [View Article] [PubMed]
     [Google Scholar]
  27. Götzke H, Palombo I, Muheim C, Perrody E, Genevaux P et al. YfgM is an ancillary subunit of the SecYEG translocon in Escherichia coli. J Biol Chem 2014; 289:19089–19097 [View Article] [PubMed]
     [Google Scholar]
  28. Bittner L-M, Arends J, Narberhaus F. When, how and why? regulated proteolysis by the essential FtsH protease in Escherichia coli. Biol Chem 2017; 398:625–635 [View Article]
     [Google Scholar]
  29. Akiyama Y, Yoshihisa T, Ito K. FtsH, a membrane-bound ATPase, forms a complex in the cytoplasmic membrane of Escherichia coli. J Biol Chem 1995; 270:23485–23490 [View Article] [PubMed]
     [Google Scholar]
  30. Akiyama Y, Ehrmann M, Kihara A, Ito K. Polypeptide binding of Escherichia coli FtsH (HflB). Mol Microbiol 1998; 28:803–812 [View Article]
     [Google Scholar]
  31. Kihara A, Akiyama Y, Ito K. FtsH is required for proteolytic elimination of uncomplexed forms of SecY, an essential protein translocase subunit. Proc Natl Acad Sci U S A 1995; 92:4532–4536 [View Article]
     [Google Scholar]
  32. van Stelten J, Silva F, Belin D, Silhavy TJ. Effects of antibiotics and a proto-oncogene homolog on destruction of protein translocator SecY. Science 2009; 325:753–756 [View Article] [PubMed]
     [Google Scholar]
  33. van Bloois E, Dekker HL, Fröderberg L, Houben ENG, Urbanus ML et al. Detection of cross-links between FtsH, YidC, HflK/C suggests a linked role for these proteins in quality control upon insertion of bacterial inner membrane proteins. FEBS Lett 2008; 582:1419–1424 [View Article] [PubMed]
     [Google Scholar]
  34. Nishiyama K, Hanada M, Tokuda H. Disruption of the gene encoding p12 (SecG) reveals the direct involvement and important function of SecG in the protein translocation of Escherichia coli at low temperature. EMBO J 1994; 13:3272–3277 [View Article]
     [Google Scholar]
  35. Lee J, Xue M, Wzorek JS, Wu T, Grabowicz M et al. Characterization of a stalled complex on the β-barrel assembly machine. Proc Natl Acad Sci U S A 2016; 113:8717–8722 [View Article]
     [Google Scholar]
  36. Irazoki O, Hernandez SB, Cava F. Peptidoglycan muropeptides: release, perception, and functions as signaling molecules. Front Microbiol 2019; 10:500 [View Article]
     [Google Scholar]
  37. Chahboune A, Decaffmeyer M, Brasseur R, Joris B. Membrane topology of the Escherichia coli AmpG permease required for recycling of cell wall anhydromuropeptides and AmpC beta-lactamase induction. Antimicrob Agents Chemother 2005; 49:1145–1149 [View Article]
     [Google Scholar]
  38. Mallik D, Pal S, Ghosh AS. Involvement of AmpG in mediating a dynamic relationship between serine beta-lactamase induction and biofilm-forming ability of Escherichia coli. FEMS Microbiol Lett 2018; 365: [View Article]
     [Google Scholar]
  39. Chorev DS, Baker LA, Wu D, Beilsten-Edmands V, Rouse SL et al. Protein assemblies ejected directly from native membranes yield complexes for mass spectrometry. Science 2018; 362:829–834 [View Article]
     [Google Scholar]
  40. Gardel C, Benson S, Hunt J, Michaelis S, Beckwith J. secD, a new gene involved in protein export in Escherichia coli. J Bacteriol 1987; 169:1286–1290 [View Article] [PubMed]
     [Google Scholar]
  41. Duong F, Wickner W. Distinct catalytic roles of the SecYE, SecG and SecDFyajC subunits of preprotein translocase holoenzyme. EMBO J 1997; 16:2756–2768 [View Article] [PubMed]
     [Google Scholar]
  42. Allen WJ, Watkins DW, Dillingham MS, Collinson I. Refined measurement of SecA-driven protein secretion reveals that translocation is indirectly coupled to ATP turnover. Proc Natl Acad Sci U S A 2020; 117:31808–31816 [View Article]
     [Google Scholar]
  43. Renner LD, Weibel DB. Cardiolipin microdomains localize to negatively curved regions of Escherichia coli membranes. Proc Natl Acad Sci U S A 2011; 108:6264–6269 [View Article]
     [Google Scholar]
  44. Kawai F, Shoda M, Harashima R, Sadaie Y, Hara H et al. Cardiolipin domains in Bacillus subtilis marburg membranes. J Bacteriol 2004; 186:1475–1483 [View Article] [PubMed]
     [Google Scholar]
  45. Mileykovskaya E, Dowhan W. Visualization of phospholipid domains in Escherichia coli by using the cardiolipin-specific fluorescent dye 10-N-nonyl acridine orange. J Bacteriol 2000; 182:1172–1175 [View Article]
     [Google Scholar]
  46. Barák I, Muchová K, Wilkinson AJ, O’Toole PJ, Pavlendová N. Lipid spirals in Bacillus subtilis and their role in cell division. Mol Microbiol 2008; 68:1315–1327 [View Article] [PubMed]
     [Google Scholar]
  47. Rassam P, Long KR, Kaminska R, Williams DJ, Papadakos G et al. Intermembrane crosstalk drives inner-membrane protein organization in Escherichia coli. Nat Commun 2018; 9:1082 [View Article]
     [Google Scholar]
  48. Rassam P, Copeland NA, Birkholz O, Tóth C, Chavent M et al. Supramolecular assemblies underpin turnover of outer membrane proteins in bacteria. Nature 2015; 523:333–336 [View Article] [PubMed]
     [Google Scholar]
  49. Oliver PM, Crooks JA, Leidl M, Yoon EJ, Saghatelian A et al. Localization of anionic phospholipids in Escherichia coli cells. J Bacteriol 2014; 196:3386–3398 [View Article]
     [Google Scholar]
  50. Seinen A-B, Spakman D, van Oijen AM, Driessen AJM. Cellular dynamics of the SecA ATPase at the single molecule level. Sci Rep 2021; 11:1433 [View Article]
     [Google Scholar]
  51. Tan BK, Bogdanov M, Zhao J, Dowhan W, Raetz CRH et al. Discovery of a cardiolipin synthase utilizing phosphatidylethanolamine and phosphatidylglycerol as substrates. Proc Natl Acad Sci U S A 2012; 109:16504–16509 [View Article]
     [Google Scholar]
  52. Mamou G, Inns PG, Sun D, Kaminska R, Housden NG et al. Spatiotemporal organization of BamA governs the pattern of outer membrane protein distribution in growing Escherichia coli cells. Microbiology 2012; 2021 [View Article]
     [Google Scholar]
  53. Mamou G, Corona F, Cohen-Khait R, Housden NG, Yeung V et al. Peptidoglycan maturation controls outer membrane protein assembly. Nature 2022; 606:953–959 [View Article] [PubMed]
     [Google Scholar]
  54. Consoli E, Luirink J, den Blaauwen T. The Escherichia coli outer membrane β-barrel assembly machinery (BAM) crosstalks with the divisome. Int J Mol Sci 2021; 22:12101 [View Article]
     [Google Scholar]
  55. Bayramova F, Jacquier N, Greub G. Interactions screenings unearth potential new divisome components in the Chlamydia-related bacterium, Waddlia chondrophila. Microorganisms 2019; 7:617 [View Article]
     [Google Scholar]
  56. Ranava D, Yang Y, Orenday-Tapia L, Rousset F, Turlan C et al. Lipoprotein DolP supports proper folding of BamA in the bacterial outer membrane promoting fitness upon envelope stress. Elife 2021; 10:e67817 [View Article]
     [Google Scholar]
  57. Tsang M-J, Yakhnina AA, Bernhardt TG, Søgaard-Andersen L. NlpD links cell wall remodeling and outer membrane invagination during cytokinesis in Escherichia coli. PLoS Genet 2017; 13:e1006888 [View Article]
     [Google Scholar]
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A bacterial secretosome for regulated envelope biogenesis and quality control?
Microbiology 168, 001255 (2022); https://doi.org/10.1099/mic.0.001255
/content/journal/micro/10.1099/mic.0.001255
/content/journal/micro/10.1099/mic.0.001255
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