Homeostatic Cell Growth Is Accomplished Mechanically through Membrane Tension Inhibition of Cell-Wall Synthesis

Cell Systems

Volumn 5, Issue 6, 2017, Pages 578-590.e6

  Rojas, Enrique R ^a,b   Huang, Kerwyn Casey ^a,b,c   Theriot, Julie A ^b  

^a Stanford University   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CHAN ZUCKERBERG BIOHUB   (United States)

Author keywords

homeostasis; mathematical modeling; membrane potential; osmotic stress; peptidoglycan; turgor pressure

Indexed keywords

ARTICLE; BACILLUS SUBTILIS; BACTERIAL CELL WALL; CELL GROWTH; CELL MEMBRANE DEPOLARIZATION; CELL SIZE; CONTROLLED STUDY; HOMEOSTASIS; HYPEROSMOTIC STRESS; HYPOOSMOTIC STRESS; MATHEMATICAL MODEL; MECHANICAL STRESS; NEGATIVE FEEDBACK; NONHUMAN; PRIORITY JOURNAL; TURGOR PRESSURE; CELL MEMBRANE; CELL PROLIFERATION; CELL WALL; ESCHERICHIA COLI; GRAM POSITIVE BACTERIUM; MECHANICS; MECHANOTRANSDUCTION; METABOLISM; OSMOTIC PRESSURE; PHYSIOLOGY; PRESSURE; SURFACE TENSION;

CELL MEMBRANE; CELL PROLIFERATION; CELL WALL; ESCHERICHIA COLI; GRAM-POSITIVE BACTERIA; HOMEOSTASIS; MECHANICAL PHENOMENA; MECHANOTRANSDUCTION, CELLULAR; OSMOTIC PRESSURE; PRESSURE; STRESS, MECHANICAL; SURFACE TENSION;

EID: 85035339373     PISSN: 24054712     EISSN: 24054720     Source Type: Journal    
DOI: 10.1016/j.cels.2017.11.005     Document Type: Article

References (37)

1. Albersheim, P., Darvill, A., Roberts, K., Sederoff, R., Staehelin, A., Plant Cell Walls. 2010, Garland Science.
2. Amir, A., Babaeipour, F., McIntosh, D.B., Nelson, D.R., Jun, S., Bending forces plastically deform growing bacterial cell walls. Proc. Natl. Acad. Sci. USA 111 (2014), 5778–5783.
3. Amir, A., Nelson, D.R., Dislocation-mediated growth of bacterial cell walls. Proc. Natl. Acad. Sci. USA 109 (2012), 9833–9838.
4. Berrier, C., Coulombe, A., Szabo, I., Zoratti, M., Ghazi, A., Gadolinium ion inhibits loss of metabolites induced by osmotic shock and large stretch-activated channels in bacteria. Eur. J. Biochem. 206 (1992), 559–565.
5. Boucher, P.A., Morris, C.E., Joos, B., Mechanosensitive closed-closed transitions in large membrane proteins: osmoprotection and tension damping. Biophys. J. 97 (2009), 2761–2770.
6. Brehm, S.P., Staal, S.P., Hoch, J.A., Phenotypes of pleiotropic-negative sporulation mutants of Bacillus subtilis. J. Bacteriol. 115 (1973), 1063–1070.
7. Cao, M., Kobel, P.A., Morshedi, M.M., Wu, M.F.W., Paddon, C., Helmann, J.D., Defining the Bacillus subtilis σ W regulon: a comparative analysis of promoter consensus search, run-off transcription/macroarray analysis (ROMA), and transcriptional profiling approaches. J. Mol. Biol. 316 (2002), 443–457.
8. Cayley, D.S., Guttman, H.J., Record, M.T. Jr., Biophysical characterization of changes in amounts and activity of Escherichia coli cell and compartment water and turgor pressure in response to osmotic stress. Biophys. J. 78 (2000), 1748–1764.
9. de Winter, J.C., Using the Student's t-test with extremely small sample sizes. Practical Assess. Res. Eval. 18 (2013), 1–12.
10. Deng, Y., Sun, M., Shaevitz, J.W., Direct measurement of cell wall stress stiffening and turgor pressure in live bacterial cells. Phys. Rev. Lett., 107, 2011, 158101.
11. Domínguez-Escobar, J., Chastanet, A., Crevenna, A.H., Fromion, V., Wedlich-Söldner, R., Carballido-López, R., Processive movement of MreB-associated cell wall biosynthetic complexes in bacteria. Science 333 (2011), 225–228.
12. Gan, L., Chen, S., Jensen, G.J., Molecular organization of Gram-negative peptidoglycan. Proc. Natl. Acad. Sci. USA 105 (2008), 18953–18957.
13. Garner, E.C., Bernard, R., Wang, W., Zhuang, X., Rudner, D.Z., Mitchison, T., Coupled, circumferential motions of the cell wall synthesis machinery and MreB filaments in B. subtilis. Science 333 (2011), 222–225.
14. Green, P.B., Growth physics in Nitella: a method for continuous in vivo analysis of extensibility based on a micro-manometer technique for turgor pressure. Plant Physiol. 43 (1968), 1169–1184.
15. Hashimoto, M., Ooiwa, S., Sekiguchi, J., Synthetic lethality of the lytE cwlO genotype in Bacillus subtilis is caused by lack of D,L-endopeptidase activity at the lateral cell wall. J. Bacteriol. 194 (2012), 796–803.
16. Hoffmann, T., Boiangiu, C., Moses, S., Bremer, E., Responses of Bacillus subtilis to hypotonic challenges: physiological contributions of mechanosensitive channels to cellular survival. Appl. Environ. Microbiol. 74 (2008), 2454–2460.
17. Inman, D.J., Engineering Vibration. 2014, Prentice Hall.
18. Jaqaman, K., Loerke, D., Mettlen, M., Kuwata, H., Grinstein, S., Schmid, S.L., Danuser, G., Robust single-particle tracking in live-cell time-lapse sequences. Nat. Methods 5 (2008), 695–702.
19. Kempf, B., Bremer, E., Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments. Arch. Microbiol. 170 (1998), 319–330.
20. Koch, A.L., Higgins, M.L., Doyle, R.J., The role of surface stress in the morphology of microbes. Microbiology 128 (1982), 927–945.
21. Labbe, R., Huang, T., Generation times and modeling of enterotoxin-positive and enterotoxin-negative strains of Clostridium perfringens in laboratory media and ground beef. J. Food Prot. 58 (1995), 1303–1306.
22. Lee, T.K., Tropini, C., Hsin, J., Desmarais, S.M., Ursell, T.S., Gong, E., Gitai, Z., Monds, R.D., Huang, K.C., A dynamically assembled cell wall synthesis machinery buffers cell growth. Proc. Natl. Acad. Sci. USA 111 (2014), 4554–4559.
23. Levina, N., Tötemeyer, S., Stokes, N.R., Louis, P., Jones, M.A., Booth, I.R., Protection of Escherichia coli cells against extreme turgor by activation of MscS and MscL mechanosensitive channels: identification of genes required for MscS activity. EMBO J. 18 (1999), 1730–1737.
24. Li, Y., Moe, P.C., Chandrasekaran, S., Booth, I.R., Blount, P., Ionic regulation of MscK, a mechanosensitive channel from Escherichia coli. EMBO J. 21 (2002), 5323–5330.
25. Meeske, A.J., Sham, L.-T., Kimsey, H., Koo, B.-M., Gross, C.A., Bernhardt, T.G., Rudner, D.Z., MurJ and a novel lipid II flippase are required for cell wall biogenesis in Bacillus subtilis. Proc. Natl. Acad. Sci. USA 112 (2015), 6437–6442.
26. Mercier, R., Kawai, Y., Errington, J., Excess membrane synthesis drives a primitive mode of cell proliferation. Cell 152 (2013), 997–1007.
27. Misra, G., Rojas, E.R., Gopinathan, A., Huang, K.C., Mechanical consequences of cell-wall turnover in the elongation of a Gram-positive bacterium. Biophys. J. 104 (2013), 2342–2352.
28. Prindle, A., Liu, J., Asally, M., Ly, S., Garcia-Ojalvo, J., Süel, G.M., Ion channels enable electrical communication in bacterial communities. Nature 527 (2015), 59–63.
29. Proseus, T.E., Zhu, G.L., Boyer, J.S., Turgor, temperature and the growth of plant cells: using Chara corallina as a model system. J. Exp. Bot. 51 (2000), 1481–1494.
30. Rojas, E., Theriot, J.A., Huang, K.C., Response of Escherichia coli growth rate to osmotic shock. Proc. Natl. Acad. Sci. USA 111 (2014), 7807–7812.
31. Singh, S.K., SaiSree, L., Amrutha, R.N., Reddy, M., Three redundant murein endopeptidases catalyse an essential cleavage step in peptidoglycan synthesis of Escherichia coli K12. Mol. Microbiol. 86 (2012), 1036–1051.
32. Strahl, H., Burman, F., Hamoen, L.W., The actin homologue MreB organizes the bacterial cell membrane. Nat. Commun., 5, 2014, 3442.
33. Tsapis, A., Kepes, A., Transient breakdown of the permeability barrier of the membrane of Escherichia coli upon hypoosmotic shock. Biochim. Biophys. Acta 469 (1977), 1–12.
34. Wahome, P.G., Setlow, P., Growth, osmotic downshock resistance and differentiation of Bacillus subtilis strains lacking mechanosensitive channels. Arch. Microbiol. 189 (2008), 49–58.
35. Walter, H., Plasmaquellung und wachstum. Z. Bot., 16, 1924, 1931.
36. Wang, P., Robert, L., Pelletier, J., Dang, W.L., Taddei, F., Wright, A., Jun, S., Robust growth of Escherichia coli. Curr. Biol. 20 (2010), 1099–1103.
37. + in turgor regulation. Microbiology 136 (1990), 2521–2526.