Communication across the bacterial cell envelope depends on the size of the periplasm.

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  • Additional Information
    • Source:
      Publisher: Public Library of Science Country of Publication: United States NLM ID: 101183755 Publication Model: eCollection Cited Medium: Internet ISSN: 1545-7885 (Electronic) Linking ISSN: 15449173 NLM ISO Abbreviation: PLoS Biol Subsets: MEDLINE
    • Publication Information:
      Original Publication: San Francisco, CA : Public Library of Science, [2003]-
    • Subject Terms:
      Bacterial Outer Membrane Proteins/*metabolism ; Bacterial Outer Membrane Proteins/*physiology ; Periplasm/*physiology; Cell Membrane/metabolism ; Cell Wall ; Cytoplasm/metabolism ; Escherichia coli/metabolism ; Escherichia coli Proteins/metabolism ; Gram-Negative Bacteria/metabolism ; Lipoproteins/metabolism ; Membrane Proteins/metabolism ; Membrane Proteins/physiology ; Peptidoglycan ; Periplasm/metabolism
    • Abstract:
      The cell envelope of gram-negative bacteria, a structure comprising an outer (OM) and an inner (IM) membrane, is essential for life. The OM and the IM are separated by the periplasm, a compartment that contains the peptidoglycan. The OM is tethered to the peptidoglycan via the lipoprotein, Lpp. However, the importance of the envelope's multilayered architecture remains unknown. Here, when we removed physical coupling between the OM and the peptidoglycan, cells lost the ability to sense defects in envelope integrity. Further experiments revealed that the critical parameter for the transmission of stress signals from the envelope to the cytoplasm, where cellular behaviour is controlled, is the IM-to-OM distance. Augmenting this distance by increasing the length of the lipoprotein Lpp destroyed signalling, whereas simultaneously increasing the length of the stress-sensing lipoprotein RcsF restored signalling. Our results demonstrate the physiological importance of the size of the periplasm. They also reveal that strict control over the IM-to-OM distance is required for effective envelope surveillance and protection, suggesting that cellular architecture and the structure of transenvelope protein complexes have been evolutionarily co-optimised for correct function. Similar strategies are likely at play in cellular compartments surrounded by 2 concentric membranes, such as chloroplasts and mitochondria.
    • References:
      Proc Natl Acad Sci U S A. 2014 Oct 14;111(41):E4350-8. (PMID: 25267629)
      J Biol Chem. 2011 May 13;286(19):16734-42. (PMID: 21454485)
      Cell. 2011 Jan 7;144(1):143-56. (PMID: 21185072)
      Microb Biotechnol. 2014 Jul;7(4):360-70. (PMID: 24779863)
      Annu Rev Microbiol. 2011;65:239-59. (PMID: 21663440)
      Eur J Biochem. 1969 Oct;10(3):426-38. (PMID: 4899922)
      Biochemistry. 2009 Jun 9;48(22):4852-7. (PMID: 19382805)
      Biosci Biotechnol Biochem. 2002 Dec;66(12):2658-62. (PMID: 12596863)
      Nucleic Acids Res. 2007 Jul;35(Web Server issue):W460-4. (PMID: 17567614)
      J Bacteriol. 1978 Oct;136(1):280-5. (PMID: 361695)
      J Bacteriol. 2008 Jul;190(13):4782-5. (PMID: 18456808)
      Mol Microbiol. 2003 Jan;47(2):539-47. (PMID: 12519203)
      J Comput Chem. 2004 Oct;25(13):1605-12. (PMID: 15264254)
      J Bacteriol. 2013 Oct;195(19):4415-24. (PMID: 23893115)
      Mol Microbiol. 2002 Nov;46(3):813-26. (PMID: 12410838)
      Structure. 2016 Dec 6;24(12 ):2227-2235. (PMID: 27866852)
      J Bacteriol. 2017 Oct 3;199(21):. (PMID: 28674071)
      Eur J Biochem. 1972 Jun 23;28(1):51-69. (PMID: 4261992)
      Mol Syst Biol. 2006;2:2006.0008. (PMID: 16738554)
      Mol Microbiol. 2011 May;80(3):612-27. (PMID: 21414037)
      Philos Trans R Soc Lond B Biol Sci. 2015 Oct 5;370(1679):. (PMID: 26370941)
      Cell. 2005 Apr 22;121(2):235-45. (PMID: 15851030)
      J Bacteriol. 2002 Feb;184(3):754-9. (PMID: 11790745)
      Annu Rev Microbiol. 2005;59:379-405. (PMID: 16153174)
      J Mol Biol. 2002 May 3;318(3):877-88. (PMID: 12054830)
      J Antimicrob Chemother. 1977 Jul;3 Suppl B:13-9. (PMID: 330482)
      J Biol Chem. 2011 May 27;286(21):18775-83. (PMID: 21471196)
      Cell. 2014 Dec 18;159(7):1652-64. (PMID: 25525882)
      Res Microbiol. 2006 Apr;157(3):206-12. (PMID: 16427772)
      J Struct Biol. 2009 Jul;167(1):11-8. (PMID: 19361558)
      Mol Microbiol. 2011 Mar;79(5):1168-81. (PMID: 21219470)
      Science. 2017 Apr 14;356(6334):197-200. (PMID: 28408605)
      Nat Rev Microbiol. 2011 Dec 28;10(2):123-36. (PMID: 22203377)
      Nature. 2015 Dec 17;528(7582):409-412. (PMID: 26641313)
      J Bacteriol. 2008 Mar;190(6):2065-74. (PMID: 18192383)
      Cold Spring Harb Perspect Biol. 2010 May;2(5):a000414. (PMID: 20452953)
      Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6640-5. (PMID: 10829079)
      Proc Natl Acad Sci U S A. 1977 Apr;74(4):1417-20. (PMID: 323852)
      Genes Dev. 2014 Jul 15;28(14):1620-34. (PMID: 25030700)
      J Struct Biol. 1996 Jan-Feb;116(1):71-6. (PMID: 8742726)
      J Bacteriol. 2006 Jun;188(12):4264-70. (PMID: 16740933)
      J Bacteriol. 2010 Oct;192(19):4894-903. (PMID: 20675476)
      Cell. 2014 Apr 24;157(3):624-35. (PMID: 24766808)
      Nat Rev Microbiol. 2017 Apr;15(4):197-204. (PMID: 28216659)
    • Grant Information:
      R01 GM056141 United States GM NIGMS NIH HHS
    • Accession Number:
      0 (Bacterial Outer Membrane Proteins)
      0 (Escherichia coli Proteins)
      0 (Lipoproteins)
      0 (Membrane Proteins)
      0 (Peptidoglycan)
    • Publication Date:
      Date Created: 20171220 Date Completed: 20171227 Latest Revision: 20190213
    • Publication Date:
      20240104
    • Accession Number:
      PMC5736177
    • Accession Number:
      10.1371/journal.pbio.2004303
    • Accession Number:
      29257832