Measuring the stiffness of bacterial cells from growth rates in hydrogels of tunable elasticity

Molecular Microbiology

Volumn 84, Issue 5, 2012, Pages 874-891

  Tuson, Hannah H ^a   Auer, George K ^a   Renner, Lars D ^a   Hasebe, Mariko ^a   Tropini, Carolina ^b   Salick, Max ^c   Crone, Wendy C ^a,c   Gopinathan, Ajay ^d   Huang, Kerwyn Casey ^b   Weibel, Douglas B ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b Stanford University   (United States)

^c University of Wisconsin Madison   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

(3,4 DICHLOROBENZYL) ISOTHIOUREA; AGAROSE; MREB PROTEIN; THIOUREA DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; ATOMIC FORCE MICROSCOPY; BACILLUS SUBTILIS; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL MEMBRANE; BACTERIAL MEMBRANE STIFFNESS; DEPOLYMERIZATION; ELASTICITY; ENCAPSULATION; ESCHERICHIA COLI; GENOTYPE; GROWTH RATE; HYDROGEL; INTERMETHOD COMPARISON; MECHANICS; MEMBRANE BIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN MODIFICATION; PSEUDOMONAS AERUGINOSA; YOUNG MODULUS;

BACILLUS SUBTILIS; BACTERIOLOGICAL TECHNIQUES; BIOMECHANICS; CULTURE MEDIA; ELASTICITY; ESCHERICHIA COLI; HYDROGELS; MODELS, THEORETICAL; PSEUDOMONAS AERUGINOSA;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; PSEUDOMONAS AERUGINOSA;

EID: 84861347051     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2012.08063.x     Document Type: Article

References (64)

1. Abu-Lail, N.I., and Camesano, T.A. (2006) The effect of solvent polarity on the molecular surface properties and adhesion of Escherichia coli. Colloids Surf B Biointerfaces 51: 62-70.
2. ASTM Standard D638 (2003) Standard Test Method for Tensile Properties of Plastics. West Conshohocken, PA: ASTM International, doi:10.1520/D0638-03 [WWW document]. URL:.
3. Bashan, Y., and Gonzalez, L. (1999) Long-term survival of the plant-growth-promoting bacteria Azospirillum brasilense and Pseudomonas fluorescens in dry alginate inoculant. Appl Microbiol Biotechnol 51: 262-266.
4. Bean, G.J., Flickinger, S.T., Westler, W.M., McCully, M.E., Sept, D., Weibel, D.B., and Amann, K.J. (2009) A22 disrupts the bacterial actin cytoskeleton by directly binding and inducing a low-affinity state in MreB. Biochemistry 48: 4852-4857.
5. Bendezú, F.O., Hale, C.A., Bernhardt, T.G., and de Boer, P.A.J. (2009) RodZ (YfgA) is required for proper assembly of the MreB actin cytoskeleton and cell shape in E. coli. EMBO J 28: 193-204.
6. Ben-Dov, E., Kramarsky-Winter, E., and Kushmaro, A. (2009) An in situ method for cultivating microorganisms using a double encapsulation technique. FEMS Microbiol Ecol 68: 363-371.
7. Boulbitch, A., Quinn, B., and Pink, D. (2000) Elasticity of the rod-shaped Gram-negative Eubacteria. Phys Rev Lett 85: 5246-5249.
8. Carballido-Lopez, R., and Formstone, A. (2007) Shape determination in Bacillus subtilis. Curr Opin Microbiol 10: 611-616.
9. Cerf, A., Cau, J.-C., Vieu, C., and Dague, E. (2009) Nanomechanical properties of dead or alive single-patterned bacteria. Langmuir 25: 5731-5736.
10. Chen, Y.-Y., Wu, C.-C., Hsu, J.-L., Peng, H.-L., Chang, H.-Y., and Yew, T.-R. (2009) Surface rigidity change of Escherichia coli after filamentous bacteriophage infection. Langmuir 25: 4607-4614.
11. van Dam, V., Olrichs, N., and Breukink, E. (2009) Specific labeling of peptidoglycan precursors as a tool for bacterial cell wall studies. Chembiochem 10: 617-624.
12. Defeu Soufo, H.J., Reimold, C., Linne, U., Knust, T., Gescher, J., and Graumann, P.L. (2010) Bacterial translation elongation factor EF-Tu interacts and colocalizes with actin-like MreB protein. Proc Natl Acad Sci USA 107: 3163-3168.
13. Deng, Y., Sun, M., and Shaevitz, J.W. (2011) Direct measurement of cell wall stress stiffening and turgor pressure in live bacterial cells. Phys Rev Lett 107: 158101.
14. Eaton, P., Fernandes, J.C., Pereira, E., Pintado, M.E., and Malcata, F.X. (2008) Atomic force microscopy study of the antibacterial effects of chitosans on Escherichia coli and Staphylococcus aureus. Ultramicroscopy 108: 1128-1134.
15. Eun, Y.-J., Utada, A.S., Copeland, M.F., Takeuchi, S., and Weibel, D.B. (2011) Encapsulating bacteria in agarose microparticles using microfluidics for high-throughput cell analysis and isolation. ACS Chem Biol 6: 260-266.
16. Flemming, C.A., Leung, K.T., Lee, H., Trevors, J.T., and Greer, C.W. (1994) Survival of lux-lac-marked biosurfactant-producing Pseudomonas aeruginosa UG2L in soil monitored by nonselective plating and PCR. Appl Environ Microbiol 60: 1606-1613.
17. Francius, G., Domenech, O., Mingeot-Leclercq, M.P., and Dufrene, Y.F. (2008) Direct observation of Staphylococcus aureus cell wall digestion by lysostaphin. J Bacteriol 190: 7904-7909.
18. Furchtgott, L., Wingreen, N.S., and Huang, K.C. (2011) Mechanisms for maintaining cell shape in rod-shaped Gram-negative bacteria. Mol Microbiol 81: 340-353.
19. Gaboriaud, F., Bailet, S., Dague, E., and Jorand, F. (2005) Surface structure and nanomechanical properties of Shewanella putrefaciens bacteria at two pH values (4 and 10) determined by atomic force microscopy. J Bacteriol 187: 3864-3868.
20. Gaboriaud, F., Parcha, B.S., Gee, M.L., Holden, J.A., and Strugnell, R.A. (2008) Spatially resolved force spectroscopy of bacterial surfaces using force-volume imaging. Colloids Surf B Biointerfaces 62: 206-213.
21. Gan, L., Chen, S., and Jensen, G.J. (2008) Molecular organization of Gram-negative peptidoglycan. Proc Natl Acad Sci USA 105: 18953-18957.
22. Gift, E.A., Park, H.J., Paradis, G.A., Demain, A.L., and Weaver, J.C. (1996) FACS-based isolation of slowly growing cells: double encapsulation of yeast in gel microdrops. Nat Biotechnol 14: 884-887.
23. Gitai, Z., Dye, N., and Shapiro, L. (2004) An actin-like gene can determine cell polarity in bacteria. Proc Natl Acad Sci USA 101: 8643-8648.
24. Gitai, Z., Dye, N.A., Reisenauer, A., Wachi, M., and Shapiro, L. (2005) MreB actin-mediated segregation of a specific region of a bacterial chromosome. Cell 120: 329-341.
25. Gross, B.J., Swoboda, J.G., and Walker, S. (2008) A strategy to discover inhibitors of O-linked glycosylation. J Am Chem Soc 130: 440-441.
26. Ha, S., Gross, B., and Walker, S. (2001) E. coli MurG: a paradigm for a superfamily of glycosyltransferases. Curr Drug Targets Infect Disord 1: 201-213.
27. Hayhurst, E.J., Kailas, L., Hobbs, J.K., and Foster, S.J. (2008) Cell wall peptidoglycan architecture in Bacillus subtilis. Proc Natl Acad Sci USA 105: 14603-14608.
28. Hobot, J.A., Carlemalm, E., Villiger, W., and Kellenberger, E. (1984) Periplasmic gel: new concept resulting from the reinvestigation of bacterial cell envelope ultrastructure by new methods. J Bacteriol 160: 143-152.
29. Holtje, J.V. (1998) Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol Mol Biol Rev 62: 181-203.
30. Huang, K.C., Mukhopadhyay, R., Wen, B., Gitai, Z., and Wingreen, N.S. (2008) Cell shape and cell-wall organization in Gram-negative bacteria. Proc Natl Acad Sci USA 105: 19282-19287.
31. Iwai, N., Nagai, K., and Wachi, M. (2002) Novel S-benzylisothiourea compound that induces spherical cells in Escherichia coli probably by acting on a rod-shape-determining protein(s) other than penicillin-binding protein 2. Biosci Biotechnol Biochem 66: 2658-2662.
32. Iwai, N., Ebata, T., Nagura, H., Kitazume, T., Nagai, K., and Wachi, M. (2004) Structure-activity relationship of S-benzylisothiourea derivatives to induce spherical cells in Escherichia coli. Biosci Biotechnol Biochem 68: 2265-2269.
33. Jain, R., Saxena, J., and Sharma, V. (2010) The evaluation of free and encapsulated Aspergillus awamori for phosphate solubilization in fermentation and soil-plant system. Appl Soil Ecol 46: 90-94.
34. Katsuragi, T., Tanaka, S., Nagahiro, S., and Tani, Y. (2000) Gel microdroplet technique leaving microorganisms alive for sorting by flow cytometry. J Microbiol Methods 42: 81-86.
35. Kruse, T., Bork-Jensen, J., and Gerdes, K. (2005) The morphogenetic MreBCD proteins of Escherichia coli form an essential membrane-bound complex. Mol Microbiol 55: 78-89.
36. 4 nanoparticles. J Phys Chem B 113: 7927-7933.
37. Lange, R.P., Locher, H.H., Wyss, P.C., and Then, R.L. (2007) The targets of currently used antibacterial agents: lessons for drug discovery. Curr Pharm Des 13: 3140-3154.
38. Matias, V.R.F., and Beveridge, T.J. (2005) Cryo-electron microscopy reveals native polymeric cell wall structure in Bacillus subtilis 168 and the existence of a periplasmic space. Mol Microbiol 56: 240-251.
39. Matias, V.R.F., and Beveridge, T.J. (2008) Lipoteichoic acid is a major component of the Bacillus subtilis periplasm. J Bacteriol 190: 7414-7418.
40. Minc, N., Boudaoud, A., and Chang, F. (2009) Mechanical forces of fission yeast growth. Curr Biol 19: 1096-1101.
41. Nilsen, T., Ghosh, A.S., Goldberg, M.B., and Young, K.D. (2004) Branching sites and morphological abnormalities behave as ectopic poles in shape-defective Escherichia coli. Mol Microbiol 52: 1045-1054.
42. Penegar, I., Toque, C., Connell, S.D.A., Smith, J.R., and Campbell, S.A. (1999) Nano-indentation measurements of the marine bacteria Sphingomonas paucimobilis using the atomic force microscope. In 10th International Congress on Marine Corrosion and Fouling. Lewis, J.A. (ed.). Melbourne: DSTO Aeronautical and Maritime Research Laboratory, pp. 5-15.
43. Perry, C.C., Weatherly, M., Beale, T., and Randriamahefa, A. (2009) Atomic force microscopy study of the antimicrobial activity of aqueous garlic versus ampicillin against Escherichia coli and Staphylococcus aureus. J Sci Food Agric 89: 958-964.
44. Popham, D.L., and Young, K.D. (2003) Role of penicillin-binding proteins in bacterial cell morphogenesis. Curr Opin Microbiol 6: 594-599.
45. Sabass, B., Gardel, M.L., Waterman, C.M., and Schwarz, U.S. (2008) High resolution traction force microscopy based on experimental and computational advances. Biophys J 94: 207-220.
46. Silver, L.L. (2003) Novel inhibitors of bacterial cell wall synthesis. Curr Opin Microbiol 6: 431-438.
47. Simmons, G., and Wang, H. (1971) Single Crystal Elastic Constants and Calculated Aggregate Properties: A Handbook. p. xv, 370 pp. Cambridge, MA: MIT Press.
48. Sliusarenko, O., Heinritz, J., Emonet, T., and Jacobs-Wagner, C. (2011) High-throughput, subpixel precision analysis of bacterial morphogenesis and intracellular spatio-temporal dynamics. Mol Microbiol 80: 612-627.
49. van Teeffelen, S., Wang, S., Furchtgott, L., Huang, K.C., Wingreen, N.S., Shaevitz, J.W., and Gitai, Z. (2011) The bacterial actin MreB rotates, and rotation depends on cell-wall assembly. Proc Natl Acad Sci USA 108: 15822-15827.
50. Thwaites, J.J., and Mendelson, N.H. (1989) Mechanical properties of peptidoglycan as determined from bacterial thread. Int J Biol Macromol 11: 201-206.
51. Thwaites, J.J., and Mendelson, N.H. (1991) Mechanical behavior of bacterial cell walls. Adv Microb Physiol 32: 173-222.
52. Thwaites, J.J., and Surana, U.C. (1991) Mechanical properties of Bacillus subtilis cell walls: effects of removing residual culture medium. J Bacteriol 173: 197-203.
53. Vadillo-Rodriguez, V., Beveridge, T.J., and Dutcher, J.R. (2008) Surface viscoelasticity of individual Gram-negative bacterial cells measured using atomic force microscopy. J Bacteriol 190: 4225-4232.
54. Varma, A., and Young, K.D. (2004) FtsZ collaborates with penicillin binding proteins to generate bacterial cell shape in Escherichia coli. J Bacteriol 186: 6768-6774.
55. Vollmer, W. (2006) The prokaryotic cytoskeleton: a putative target for inhibitors and antibiotics? Appl Microbiol Biotechnol 73: 37-47.
56. Vollmer, W., and Bertsche, U. (2008) Murein (peptidoglycan) structure, architecture and biosynthesis in Escherichia coli. Biochim Biophys Acta 1778: 1714-1734.
57. Vollmer, W., Blanot, D., and de Pedro, M.A. (2008) Peptidoglycan structure and architecture. FEMS Microbiol Rev 32: 149-167.
58. Wang, J.H.-C., and Lin, J.-S. (2007) Cell traction force and measurement methods. Biomech Model Mechanobiol 6: 361-371.
59. Wang, S., Arellano-Santoyo, H., Combs, P.A., and Shaevitz, J.W. (2010) Actin-like cytoskeleton filaments contribute to cell mechanics in bacteria. Proc Natl Acad Sci USA 107: 9182-9185.
60. Xu, W., Mulhern, P.J., Blackford, B.L., Jericho, M.H., Firtel, M., and Beveridge, T.J. (1996) Modeling and measuring the elastic properties of an archaeal surface, the sheath of Methanospirillum hungatei, and the implication for methane production. J Bacteriol 178: 3106-3112.
61. Yao, X., Jericho, M., Pink, D., and Beveridge, T. (1999) Thickness and elasticity of gram-negative murein sacculi measured by atomic force microscopy. J Bacteriol 181: 6865-6875.
62. Young, C.-C., Rekha, P.D., Lai, W.-A., and Arun, A.B. (2006) Encapsulation of plant growth-promoting bacteria in alginate beads enriched with humic acid. Biotechnol Bioeng 95: 76-83.
63. Zengler, K., Toledo, G., Rappe, M., Elkins, J., Mathur, E.J., Short, J.M., and Keller, M. (2002) Cultivating the uncultured. Proc Natl Acad Sci USA 99: 15681-15686.
64. Zienkewicz, O.C. (2005) The Finite Element Method for Solid and Structural Mechanics. Oxford: Butterworth-Heinemann.