User menu

Accès à distance ? S'identifier sur le proxy UCLouvain

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

Primary tabs

download
  • Open access
  • PDF
  • 4.02 M
Asmar, Abir [UCL] Ferreira, Josie L Cohen, Eli J Cho, Seung Hyun [UCL] Beeby, Morgan Collet, Jean-François [UCL]

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.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès libre
Publication date 2017
Language Anglais
Journal information "PLoS Biology" - Vol. 15, no. 12, p. e2004303 [1-16] (2017)
Peer reviewed yes
Publisher Public Library of Science ((United States) San Francisco, CA)
issn 1544-9173
e-issn 1545-7885
Publication status Publié
Affiliations UCL - SSS/DDUV
UCL - SSS/DDUV/BCHM - Biochimie-Recherche métabolique
Links
  1. Silhavy T. J., Kahne D., Walker S., The Bacterial Cell Envelope, 10.1101/cshperspect.a000414
  2. Simpson Brent W., May Janine M., Sherman David J., Kahne Daniel, Ruiz Natividad, Lipopolysaccharide transport to the cell surface: biosynthesis and extraction from the inner membrane, 10.1098/rstb.2015.0029
  3. A Typas, Nature reviews Microbiology, 10, 123 (2011)
  4. Okuda Suguru, Tokuda Hajime, Lipoprotein Sorting in Bacteria, 10.1146/annurev-micro-090110-102859
  5. Noinaj Nicholas, Gumbart James C., Buchanan Susan K., The β-barrel assembly machinery in motion, 10.1038/nrmicro.2016.191
  6. Braun V., Rehn K., Chemical Characterization, Spatial Distribution and Function of a Lipoprotein (Murein-Lipoprotein) of the E. coli Cell Wall. The Specific Effect of Trypsin on the Membrane Structure, 10.1111/j.1432-1033.1969.tb00707.x
  7. Li Gene-Wei, Burkhardt David, Gross Carol, Weissman Jonathan S., Quantifying Absolute Protein Synthesis Rates Reveals Principles Underlying Allocation of Cellular Resources, 10.1016/j.cell.2014.02.033
  8. Magnet S., Dubost L., Marie A., Arthur M., Gutmann L., Identification of the L,D-Transpeptidases for Peptidoglycan Cross-Linking in Escherichia coli, 10.1128/jb.00025-08
  9. Braun Volkmar, Bosch Valerie, Sequence of the Murein . Lipoprotein and the Attachment Site of the Lipid, 10.1111/j.1432-1033.1972.tb01883.x
  10. Hirota Y., Suzuki H., Nishimura Y., Yasuda S., On the process of cellular division in Escherichia coli: a mutant of E. coli lacking a murein-lipoprotein., 10.1073/pnas.74.4.1417
  11. Cho Seung-Hyun, Szewczyk Joanna, Pesavento Christina, Zietek Matylda, Banzhaf Manuel, Roszczenko Paula, Asmar Abir, Laloux Géraldine, Hov Ann-Kristin, Leverrier Pauline, Van der Henst Charles, Vertommen Didier, Typas Athanasios, Collet Jean-François, Detecting Envelope Stress by Monitoring β-Barrel Assembly, 10.1016/j.cell.2014.11.045
  12. Majdalani Nadim, Gottesman Susan, THE RCS PHOSPHORELAY: A Complex Signal Transduction System, 10.1146/annurev.micro.59.050405.101230
  13. G Laloux, Journal of bacteriology (2017)
  14. Huang Ya-Hui, Ferrières Lionel, Clarke David J., The role of the Rcs phosphorelay in Enterobacteriaceae, 10.1016/j.resmic.2005.11.005
  15. Farris C., Sanowar S., Bader M. W., Pfuetzner R., Miller S. I., Antimicrobial Peptides Activate the Rcs Regulon through the Outer Membrane Lipoprotein RcsF, 10.1128/jb.00505-10
  16. Laubacher M. E., Ades S. E., The Rcs Phosphorelay Is a Cell Envelope Stress Response Activated by Peptidoglycan Stress and Contributes to Intrinsic Antibiotic Resistance, 10.1128/jb.01740-07
  17. Evans K. L., Kannan S., Li G., de Pedro M. A., Young K. D., Eliminating a Set of Four Penicillin Binding Proteins Triggers the Rcs Phosphorelay and Cpx Stress Responses in Escherichia coli, 10.1128/jb.00596-13
  18. Spratt B. G., The mechanism of action of mecillinam, 10.1093/jac/3.suppl_b.13
  19. Bean G. J., Flickinger S. T., Westler W. M., McCully M. E., Sept D., Weibel D. B., Amann K. J., A22 Disrupts the Bacterial Actin Cytoskeleton by Directly Binding and Inducing a Low-Affinity State in MreB, 10.1021/bi900014d
  20. IWAI Noritaka, NAGAI Kazuo, WACHI Masaaki, NovelS-Benzylisothiourea Compound That Induces Spherical Cells inEscherichia coliProbably by Acting on a Rod-shape-determining Protein(s) Other Than Penicillin-binding Protein 2, 10.1271/bbb.66.2658
  21. Den Blaauwen Tanneke, Aarsman Mirjam E. G., Vischer Norbert O. E., Nanninga Nanne, Penicillin-binding protein PBP2 of Escherichia coli localizes preferentially in the lateral wall and at mid-cell in comparison with the old cell pole : Localization of PBP2, 10.1046/j.1365-2958.2003.03316.x
  22. Castanie-Cornet M.-P., Cam K., Jacq A., RcsF Is an Outer Membrane Lipoprotein Involved in the RcsCDB Phosphorelay Signaling Pathway in Escherichia coli, 10.1128/jb.00004-06
  23. Wu Tao, Malinverni Juliana, Ruiz Natividad, Kim Seokhee, Silhavy Thomas J., Kahne Daniel, Identification of a Multicomponent Complex Required for Outer Membrane Biogenesis in Escherichia coli, 10.1016/j.cell.2005.02.015
  24. Konovalova A., Perlman D. H., Cowles C. E., Silhavy T. J., Transmembrane domain of surface-exposed outer membrane lipoprotein RcsF is threaded through the lumen of  -barrel proteins, 10.1073/pnas.1417138111
  25. Cohen Eli J., Ferreira Josie L., Ladinsky Mark S., Beeby Morgan, Hughes Kelly T., Nanoscale-length control of the flagellar driveshaft requires hitting the tethered outer membrane, 10.1126/science.aam6512
  26. I Sonntag, Journal of bacteriology, 136, 280 (1978)
  27. Nichols Robert J., Sen Saunak, Choo Yoe Jin, Beltrao Pedro, Zietek Matylda, Chaba Rachna, Lee Sueyoung, Kazmierczak Krystyna M., Lee Karis J., Wong Angela, Shales Michael, Lovett Susan, Winkler Malcolm E., Krogan Nevan J., Typas Athanasios, Gross Carol A., Phenotypic Landscape of a Bacterial Cell, 10.1016/j.cell.2010.11.052
  28. Guo M. S., Updegrove T. B., Gogol E. B., Shabalina S. A., Gross C. A., Storz G., MicL, a new  E-dependent sRNA, combats envelope stress by repressing synthesis of Lpp, the major outer membrane lipoprotein, 10.1101/gad.243485.114
  29. Chen Zhao-Yuan, Cao Jie, Xie Li, Li Xiao-Fei, Yu Zhen-Hai, Tong Wang-Yu, Construction of leaky strains and extracellular production of exogenous proteins in recombinantEscherichia coli : Extracellular production of exogenous proteins, 10.1111/1751-7915.12127
  30. Leverrier Pauline, Declercq Jean-Paul, Denoncin Katleen, Vertommen Didier, Hiniker Annie, Cho Seung-Hyun, Collet Jean-François, Crystal Structure of the Outer Membrane Protein RcsF, a New Substrate for the Periplasmic Protein-disulfide Isomerase DsbC, 10.1074/jbc.m111.224865
  31. Rogov Vladimir V., Rogova Natalia Yu., Bernhard Frank, Löhr Frank, Dötsch Volker, A Disulfide Bridge Network within the Soluble Periplasmic Domain Determines Structure and Function of the Outer Membrane Protein RCSF, 10.1074/jbc.m111.230185
  32. Samsudin Firdaus, Ortiz-Suarez Maite L., Piggot Thomas J., Bond Peter J., Khalid Syma, OmpA: A Flexible Clamp for Bacterial Cell Wall Attachment, 10.1016/j.str.2016.10.009
  33. Cascales E., Bernadac A., Gavioli M., Lazzaroni J.-C., Lloubes R., Pal Lipoprotein of Escherichia coli Plays a Major Role in Outer Membrane Integrity, 10.1128/jb.184.3.754-759.2002
  34. Baba Tomoya, Ara Takeshi, Hasegawa Miki, Takai Yuki, Okumura Yoshiko, Baba Miki, Datsenko Kirill A, Tomita Masaru, Wanner Barry L, Mori Hirotada, Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection, 10.1038/msb4100050
  35. Majdalani Nadim, Hernandez David, Gottesman Susan, Regulation and mode of action of the second small RNA activator of RpoS translation, RprA : RprA regulation and mode of action, 10.1046/j.1365-2958.2002.03203.x
  36. Datsenko K. A., Wanner B. L., One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products, 10.1073/pnas.120163297
  37. Gennaris Alexandra, Ezraty Benjamin, Henry Camille, Agrebi Rym, Vergnes Alexandra, Oheix Emmanuel, Bos Julia, Leverrier Pauline, Espinosa Leon, Szewczyk Joanna, Vertommen Didier, Iranzo Olga, Collet Jean-François, Barras Frédéric, Repairing oxidized proteins in the bacterial envelope using respiratory chain electrons, 10.1038/nature15764
  38. Cowles Charles E., Li Yongfeng, Semmelhack Martin F., Cristea Ileana M., Silhavy Thomas J., The free and bound forms of Lpp occupy distinct subcellular locations in Escherichia coli : Free-form Lpp is surface-exposed in E. coli, 10.1111/j.1365-2958.2011.07539.x
  39. J.H. M. Experiments in molecular genetics N.Y.: Cold Spring Harbor; 1972.
  40. Sliusarenko Oleksii, Heinritz Jennifer, Emonet Thierry, Jacobs-Wagner Christine, High-throughput, subpixel precision analysis of bacterial morphogenesis and intracellular spatio-temporal dynamics : Quantitative analysis of spatio-temporal dynamics, 10.1111/j.1365-2958.2011.07579.x
  41. Suloway Christian, Shi Jian, Cheng Anchi, Pulokas James, Carragher Bridget, Potter Clinton S., Zheng Shawn Q., Agard David A., Jensen Grant J., Fully automated, sequential tilt-series acquisition with Leginon, 10.1016/j.jsb.2009.03.019
  42. Kremer James R., Mastronarde David N., McIntosh J.Richard, Computer Visualization of Three-Dimensional Image Data Using IMOD, 10.1006/jsbi.1996.0013
  43. Pettersen Eric F., Goddard Thomas D., Huang Conrad C., Couch Gregory S., Greenblatt Daniel M., Meng Elaine C., Ferrin Thomas E., UCSF Chimera?A visualization system for exploratory research and analysis, 10.1002/jcc.20084
  44. Delano WL. The PyMOL Molecular Graphics System. 2002. citeulike-article-id:2816763
  45. Ishida T., Kinoshita K., PrDOS: prediction of disordered protein regions from amino acid sequence, 10.1093/nar/gkm363
  46. Liu Jie, Cao Wei, Lu Min, Core Side-chain Packing and Backbone Conformation in Lpp-56 Coiled-coil Mutants, 10.1016/s0022-2836(02)00138-9
Bibliographic reference Asmar, Abir ; Ferreira, Josie L ; Cohen, Eli J ; Cho, Seung Hyun ; Beeby, Morgan ; et. al. Communication across the bacterial cell envelope depends on the size of the periplasm.. In: PLoS Biology, Vol. 15, no. 12, p. e2004303 [1-16] (2017)
Permanent URL http://hdl.handle.net/2078.1/194542