How and why cells grow as rods

BMC Biology

Volumn 12, Issue 1, 2014, Pages

  Chang, Fred ^a   Huang, Kerwyn C ^b,c  

^a NewYork Presbyterian Hospital   (United States)

^b Stanford University   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cell wall; Cytoskeleton; Morphogenesis

Indexed keywords

BACTERIUM; BIOLOGICAL MODEL; CELL GROWTH; CELL WALL; CYTOLOGY; ESCHERICHIA COLI; FUNGUS; METABOLISM; MORPHOGENESIS; SCHIZOSACCHAROMYCES;

BACTERIA; CELL GROWTH PROCESSES; CELL WALL; ESCHERICHIA COLI; FUNGI; MODELS, BIOLOGICAL; MORPHOGENESIS; SCHIZOSACCHAROMYCES;

EID: 84905902696     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/s12915-014-0054-8     Document Type: Review

References (107)

1. Campas O, Mahadevan L. Shape and dynamics of tip-growing cells. Curr Biol 2009, 19:2102-2107. 10.1016/j.cub.2009.10.075, 20022245.
2. Furchtgott L, Wingreen NS, Huang KC. Mechanisms for maintaining cell shape in rod-shaped Gram-negative bacteria. Mol Microbiol 2011, 81:340-353. 10.1111/j.1365-2958.2011.07616.x, 21501250.
3. Bernal R, Rojas ER, Dumais J. The mechanics of tip growth morphogenesis: what we have learned from rubber balloons. J Mech Mater Struct 2007, 2:1157-1168. 10.2140/jomms.2007.2.1157.
4. De Pedro MA, Schwarz H, Koch AL: Patchiness of murein insertion into the sidewall of Escherichia coli.Microbiology 2003, 149:1753-1761..
5. Daniel RA, Errington J. Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell. Cell 2003, 113:767-776. 10.1016/S0092-8674(03)00421-5, 12809607.
6. Mitchison JM, Nurse P: Growth in cell length in the fission yeastSchizosaccharomyces pombe.J Cell Sci 1985, 75:357-376.
7. Rojas ER, Hotton S, Dumais J. Chemically mediated mechanical expansion of the pollen tube cell wall. Biophys J 2011, 101:1844-1853. 10.1016/j.bpj.2011.08.016, 22004737.
8. Brown PJ, de Pedro MA, Kysela DT, Van der Henst C, Kim J, De Bolle X, Fuqua C, Brun YV. Polar growth in the Alphaproteobacterial order Rhizobiales. Proc Natl Acad Sci U S A 2012, 109:1697-1701. 10.1073/pnas.1114476109, 22307633.
9. Letek M, Fiuza M, Ordonez E, Villadangos AF, Ramos A, Mateos LM, Gil JA: Cell growth and cell division in the rod-shaped actinomyceteCorynebacterium glutamicum.Antonie Van Leeuwenhoek 2008, 94:99-109..
10. Rojas E, Theriot JA, Huang KC: Response ofEscherichia coli growth rate to osmotic shock.Proc Natl Acad Sci U S A 2014, 111:7807-7812..
11. Yao X, Jericho M, Pink D, Beveridge T. Thickness and elasticity of Gram-negative murein sacculi measured by atomic force microscopy. J Bacteriol 1999, 181:6865-6875. 10559150.
12. Gan L, Chen S, Jensen GJ. Molecular organization of Gram-negative peptidoglycan. Proc Natl Acad Sci U S A 2008, 105:18953-18957. 10.1073/pnas.0808035105, 19033194.
13. Deng Y, Sun M, Shaevitz JW. Direct measurement of cell wall stress stiffening and turgor pressure in live bacterial cells. Phys Rev Lett 2011, 107:158101. 10.1103/PhysRevLett.107.158101, 22107320.
14. Zhou X, Cegelski L: Nutrient-dependent structural changes inS. aureus peptidoglycan revealed by solid-state NMR spectroscopy.Biochemistry 2012, 51:8143-8153..
15. Amir A, Nelson DR. Dislocation-mediated growth of bacterial cell walls. Proc Natl Acad Sci U S A 2012, 109:9833-9838. 10.1073/pnas.1207105109, 22660931.
16. Dumais J. Modes of deformation of walled cells. J Exp Bot 2013, 64:4681-4695. 10.1093/jxb/ert268, 24014868.
17. Holtje JV: Growth of the stress-bearing and shape-maintaining murein sacculus ofEscherichia coli.Microbiol Mol Biol Rev 1998, 62:181-203..
18. Scheffers DJ, Pinho MG. Bacterial cell wall synthesis: new insights from localization studies. Microbiol Mol Biol Rev 2005, 69:585-607. 10.1128/MMBR.69.4.585-607.2005, 16339737.
19. Young KD. The selective value of bacterial shape. Microbiol Mol Biol Rev 2006, 70:660-703. 10.1128/MMBR.00001-06, 16959965.
20. Young KD. Bacterial shape: two-dimensional questions and possibilities. Annu Rev Microbiol 2010, 64:223-240. 10.1146/annurev.micro.112408.134102, 20825347.
21. Sun SX, Jiang H. Physics of bacterial morphogenesis. Microbiol Mol Biol Rev 2011, 75:543-565. 10.1128/MMBR.00006-11, 22126993.
22. Firtel M, Henderson G, Sokolov I: Nanosurgery: observation of peptidoglycan strands inLactobacillus helveticus cell walls.Ultramicroscopy 2004, 101:105-109..
23. Gitai Z, Dye N, Shapiro L. An actin-like gene can determine cell polarity in bacteria. Proc Natl Acad Sci U S A 2004, 101:8643-8648. 10.1073/pnas.0402638101, 15159537.
24. Sv T, Wang S, Furchtgott L, Huang KC, Wingreen NS, Shaevitz JW, Gitai Z: The bacterial actin MreB rotates and rotation depends on cell-wall assembly.Proc Natl Acad Sci U S A 2011, 108:15822-15827..
25. Ursell TS, Nguyen J, Monds RD, Colavin A, Billings G, Ouzounov N, Gitai Z, Shaevitz JW, Huang KC. Rod-like bacterial shape is maintained by feedback between cell curvature and cytoskeletal localization. Proc Natl Acad Sci U S A 2014, 111:E1025-E1034. 10.1073/pnas.1317174111, 24550515.
26. Wang S, Furchtgott L, Huang KC, Shaevitz JW. Helical insertion of peptidoglycan produces chiral ordering of the bacterial cell wall. Proc Natl Acad Sci U S A 2012, 109:E595-E604. 10.1073/pnas.1117132109, 22343529.
27. Dominguez-Escobar J, Chastanet A, Crevenna AH, Fromion V, Wedlich-Soldner R, Carballido-Lopez R. Processive movement of MreB-associated cell wall biosynthetic complexes in bacteria. Science 2011, 333:225-228. 10.1126/science.1203466, 21636744.
28. Garner EC, Bernard R, Wang W, Zhuang X, Rudner DZ, Mitchison T: Coupled, circumferential motions of the cell wall synthesis machinery and MreB filaments inB. subtilis.Science 2011, 333:222-225..
29. Kruse T, Bork-Jensen J, Gerdes K: The morphogenetic MreBCD proteins ofEscherichia coli form an essential membrane-bound complex.Mol Microbiol 2005, 55:78-89..
30. Wang P, Robert L, Pelletier J, Dang WL, Taddei F, Wright A, Jun S: Robust growth ofEscherichia coli.Curr Biol 2010, 20:1099-1103..
31. Belgrave AM, Wolgemuth CW. Elasticity and biochemistry of growth relate replication rate to cell length and cross-link density in rod-shaped bacteria. Biophys J 2013, 104:2607-2611. 10.1016/j.bpj.2013.04.028, 23790368.
32. Misra G, Rojas ER, Gopinathan A, Huang KC. Mechanical consequences of cell-wall turnover in the elongation of a Gram-positive bacterium. Biophys J 2013, 104:2342-2352. 10.1016/j.bpj.2013.04.047, 23746506.
33. Jiang H, Si F, Margolin W, Sun SX. Mechanical control of bacterial cell shape. Biophys J 2011, 101:327-335. 10.1016/j.bpj.2011.06.005, 21767484.
34. Jiang H, Sun SX. Morphology, growth, and size limit of bacterial cells. Phys Rev Lett 2010, 105:028101. 10.1103/PhysRevLett.105.028101, 20867742.
35. Kim JS, Sun SX: Morphology ofCaulobacter crescentus and the mechanical role of Crescentin.Biophys J 2009, 96:L47-L49..
36. Jiang H, Sun SX. Growth of curved and helical bacterial cells. Soft Matter 2012, 8:7446-7451. 10.1039/c2sm25452b.
37. Koch AL. The surface stress theory of microbial morphogenesis. Adv Microbial Physiol 1983, 24:301-366. 10.1016/S0065-2911(08)60388-4.
38. Drake T, Vavylonis D. Model of fission yeast cell shape driven by membrane-bound growth factors and the cytoskeleton. PLoS Comput Biol 2013, 9:e1003287. 10.1371/journal.pcbi.1003287, 24146607.
39. Goriely A, Tabor M. Biomechanical models of hyphal growth in actinomycetes. J Theoret Biol 2003, 222:211-218. 10.1016/S0022-5193(03)00029-8.
40. Goriely A, Tabor M. Self-similar tip growth in filamentary organisms. Phys Rev Lett 2003, 90:108101. 10.1103/PhysRevLett.90.108101, 12689036.
41. Campas O, Rojas E, Dumais J, Mahadevan L. Strategies for cell shape control in tip-growing cells. Am J Bot 2012, 99:1577-1582. 10.3732/ajb.1200087, 22935361.
42. Cortes JC, Konomi M, Martins IM, Munoz J, Moreno MB, Osumi M, Duran A, Ribas JC. The (1,3)beta-D-glucan synthase subunit Bgs1p is responsible for the fission yeast primary septum formation. Mol Microbiol 2007, 65:201-217. 10.1111/j.1365-2958.2007.05784.x, 17581129.
43. Ursell TS, Trepagnier EH, Huang KC, Theriot JA. Analysis of surface protein expression reveals the growth pattern of the Gram-negative outer membrane. PLoS Comput Biol 2012, 8:e1002680. 10.1371/journal.pcbi.1002680, 23028278.
44. Chang F, Martin SG. Shaping fission yeast with microtubules. Cold Spring Harb Perspect Biol 2009, 1:a001347. 10.1101/cshperspect.a001347, 20066076.
45. Perez P, Rincon SA. Rho GTPases: regulation of cell polarity and growth in yeasts. Biochem J 2010, 426:243-253. 10.1042/BJ20091823, 20175747.
46. Minc N, Boudaoud A, Chang F. Mechanical forces of fission yeast growth. Curr Biol 2009, 19:1096-1101. 10.1016/j.cub.2009.05.031, 19500986.
47. Schuster M, Treitschke S, Kilaru S, Molloy J, Harmer NJ, Steinberg G. Myosin-5, kinesin-1 and myosin-17 cooperate in secretion of fungal chitin synthase. EMBO J 2012, 31:214-227. 10.1038/emboj.2011.361, 22027862.
48. Taheri-Talesh N, Horio T, Araujo-Bazan L, Dou X, Espeso EA, Penalva MA, Osmani SA, Oakley BR: The tip growth apparatus ofAspergillus nidulans.Mol Biol Cell 2008, 19:1439-1449..
49. Minc N, Bratman SV, Basu R, Chang F. Establishing new sites of polarization by microtubules. Curr Biol 2009, 19:83-94. 10.1016/j.cub.2008.12.008, 19147354.
50. Terenna CR, Makushok T, Velve-Casquillas G, Baigl D, Chen Y, Bornens M, Paoletti A, Piel M, Tran PT. Physical mechanisms redirecting cell polarity and cell shape in fission yeast. Curr Biol 2008, 18:1748-1753. 10.1016/j.cub.2008.09.047, 19026544.
51. Bicho CC, Kelly DA, Snaith HA, Goryachev AB, Sawin KE. A catalytic role for Mod5 in the formation of the Tea1 cell polarity landmark. Curr Biol 2010, 20:1752-1757. 10.1016/j.cub.2010.08.035, 20850323.
52. Das M, Drake T, Wiley DJ, Buchwald P, Vavylonis D, Verde F. Oscillatory dynamics of Cdc42 GTPase in the control of polarized growth. Science 2012, 337:239-243. 10.1126/science.1218377, 22604726.
53. Kelly FD, Nurse P. Spatial control of Cdc42 activation determines cell width in fission yeast. Mol Biol Cell 2011, 22:3801-3811. 10.1091/mbc.E11-01-0057, 21849474.
54. Koch AL. What size should a bacterium be? A question of scale. Annu Rev Microbiol 1996, 50:317-348. 10.1146/annurev.micro.50.1.317, 8905083.
55. Sliusarenko O, Heinritz J, Emonet T, Jacobs-Wagner C. High-throughput, subpixel precision analysis of bacterial morphogenesis and intracellular spatio-temporal dynamics. Mol Microbiol 2011, 80:612-627. 10.1111/j.1365-2958.2011.07579.x, 21414037.
56. Guberman JM, Fay A, Dworkin J, Wingreen NS, Gitai Z. PSICIC: noise and asymmetry in bacterial division revealed by computational image analysis at sub-pixel resolution. PLoS Comput Biol 2008, 4:e1000233. 10.1371/journal.pcbi.1000233, 19043544.
57. Green PB: Growth physics inNitella: a method for continuous in vivo analysis of extensibility based on a micro-manometer technique for turgor pressure.Plant Physiol 1968, 43:1169-1184..
58. Milani P, Braybrook SA, Boudaoud A. Shrinking the hammer: micromechanical approaches to morphogenesis. J Exp Bot 2013, 64:4651-4662. 10.1093/jxb/ert169, 23873995.
59. Tuson HH, Auer GK, Renner LD, Hasebe M, Tropini C, Salick M, Crone WC, Gopinathan A, Huang KC, Weibel DB. Measuring the stiffness of bacterial cells from growth rates in hydrogels of tunable elasticity. Mol Microbiol 2012, 84:874-891. 10.1111/j.1365-2958.2012.08063.x, 22548341.
60. Whatmore AM, Reed RH: Determination of turgor pressure inBacillus subtilis: a possible role for K+ in turgor regulation.J Gen Microbiol 1990, 136:2521-2526..
61. Cayley DS, Guttman HJ, Record MT Jr: Biophysical characterization of changes in amounts and activity ofEscherichia coli cell and compartment water and turgor pressure in response to osmotic stress. Biophys J 2000, 78:1748-1764..
62. Tuson HH, Renner LD, Weibel DB. Polyacrylamide hydrogels as substrates for studying bacteria. Chem Commun 2012, 48:1595-1597. 10.1039/c1cc14705f.
63. Turner JJ, Ewald JC, Skotheim JM. Cell size control in yeast. Curr Biol 2012, 22:R350-R359. 10.1016/j.cub.2012.02.041, 22575477.
64. Chien AC, Hill NS, Levin PA. Cell size control in bacteria. Curr Biol 2012, 22:R340-R349. 10.1016/j.cub.2012.02.032, 22575476.
65. Pan KZ, Saunders TE, Flor-Parra I, Howard M, Chang F. Cortical regulation of cell size by a sizer cdr2p. eLife 2014, 2014:e02040. 10.7554/eLife.02040.
66. Bonazzi D, Julien JD, Romao M, Seddiki R, Piel M, Boudaoud A, Minc N. Symmetry breaking in spore germination relies on an interplay between polar cap stability and spore wall mechanics. Dev Cell 2014, 28:534-546. 10.1016/j.devcel.2014.01.023, 24636258.
67. Kelly FD, Nurse P: De novo growth zone formation from fission yeast spheroplasts.PLoS One 2011, 6:e27977..
68. Lederberg J. Bacterial protoplasts induced by penicillin. Proc Natl Acad Sci U S A 1956, 42:574-577. 10.1073/pnas.42.9.574, 16589908.
69. Ranjit DK, Young KD: The Rcs stress response and accessory envelope proteins are required forde novo generation of cell shape inEscherichia coli.J Bacteriol 2013, 195:2452-2462..
70. Kawai Y, Mercier R, Errington J. Bacterial cell morphogenesis does not require a preexisting template structure. Curr Biol 2014, 24:863-867. 10.1016/j.cub.2014.02.053, 24704074.
71. Mitchison JM: The growth of single cells, I.Schizosaccharomyces pombe.Exp Cell Res 1957, 13:244-262..
72. Kubitschek HE, Clay KB: A second growth state forSchizosaccharomyces pombe.Exp Cell Res 1986, 165:243-254..
73. Johnson BF, Miyata M, Miyata H. Morphogenesis of fission yeasts. Molecular Biology of the Fission Yeast 1989, 469331-469366. Academic Press, New York, Nasim A, Young P, Johnson BF.
74. Lan G, Wolgemuth CW, Sun SX. Z-ring force and cell shape during division in rod-like bacteria. Proc Natl Acad Sci U S A 2007, 104:16110-16115. 10.1073/pnas.0702925104, 17913889.
75. Mata J, Nurse P. Tea1 and the microtubular cytoskeleton are important for generating global spatial order within the fission yeast cell. Cell 1997, 89:939-949. 10.1016/S0092-8674(00)80279-2, 9200612.
76. Toda T, Umesono K, Hirata A, Yanagida M: Cold-sensitive nuclear division arrest mutants of the fission yeastSchizosaccharomyces pombe.J Mol Biol 1983, 168:251-270..
77. Piel M, Tran PT. Cell shape and cell division in fission yeast. Curr Biol 2009, 19:R823-R827. 10.1016/j.cub.2009.08.012, 19906584.
78. Theriot JA. Why are bacteria different from eukaryotes?. BMC Biol 2013, 11:119. 10.1186/1741-7007-11-119, 24330667.
79. Sipiczki M. Splitting of the fission yeast septum. FEMS Yeast Res 2007, 7:761-770. 10.1111/j.1567-1364.2007.00266.x, 17596184.
80. Matias VR, Beveridge TJ: Cryo-electron microscopy reveals native polymeric cell wall structure inBacillus subtilis 168 and the existence of a periplasmic space.Mol Microbiol 2005, 56:240-251..
81. Reshes G, Vanounou S, Fishov I, Feingold M: Timing the start of division inE. coli: a single-cell study. Phys Biol 2008, 5:046001..
82. Hsin J, Gopinathan A, Huang KC. Nucleotide-dependent conformations of FtsZ dimers and force generation observed through molecular dynamics simulations. Proc Natl Acad Sci U S A 2012, 109:9432-9437. 10.1073/pnas.1120761109, 22647609.
83. Li Y, Hsin J, Zhao L, Cheng Y, Shang W, Huang KC, Wang HW, Ye S: FtsZ protofilaments use a hinge-opening mechanism for constrictive force generation.Science 2013, 341:392-395..
84. Huang KC, Mukhopadhyay R, Wingreen NS. A curvature-mediated mechanism for localization of lipids to bacterial poles. PLoS Comput Biol 2006, 2:e151. 10.1371/journal.pcbi.0020151, 17096591.
85. Huang KC, Meir Y, Wingreen NS: Dynamic structures inEscherichia coli: spontaneous formation of MinE rings and MinD polar zones.Proc Natl Acad Sci U S A 2003, 100:12724-12728..
86. Shebelut CW, Guberman JM, van Teeffelen S, Yakhnina AA, Gitai Z: Caulobacter chromosome segregation is an ordered multistep process.Proc Natl Acad Sci U S A 2010, 107:14194-14198..
87. Chen YE, Tropini C, Jonas K, Tsokos CG, Huang KC, Laub MT. Spatial gradient of protein phosphorylation underlies replicative asymmetry in a bacterium. Proc Natl Acad Sci U S A 2011, 108:1052-1057. 10.1073/pnas.1015397108, 21191097.
88. Lam H, Matroule JY, Jacobs-Wagner C. The asymmetric spatial distribution of bacterial signal transduction proteins coordinates cell cycle events. Dev Cell 2003, 5:149-159. 10.1016/S1534-5807(03)00191-6, 12852859.
89. Davis BM, Waldor MK. Establishing polar identity in Gram-negative rods. Curr Opin Microbiol 2013, 16:752-759. 10.1016/j.mib.2013.08.006, 24029491.
90. Thiem S, Kentner D, Sourjik V: Positioning of chemosensory clusters inE. coli and its relation to cell division.EMBO J 2007, 26:1615-1623..
91. Mishra M, Huang Y, Srivastava P, Srinivasan R, Sevugan M, Shlomovitz R, Gov N, Rao M, Balasubramanian M. Cylindrical cellular geometry ensures fidelity of division site placement in fission yeast. J Cell Sci 2012, 125:3850-3857. 10.1242/jcs.103788, 22505610.
92. Margolin W. FtsZ and the division of prokaryotic cells and organelles. Nat Rev Mol Cell Biol 2005, 6:862-871. 10.1038/nrm1745, 16227976.
93. Corbin BD, Yu XC, Margolin W: Exploring intracellular space: function of the Min system in round-shapedEscherichia coli.EMBO J 2002, 21:1998-2008..
94. Lundgren K, Walworth N, Booher R, Dembski M, Kirschner M, Beach D. mik1 and wee1 cooperate in the inhibitory tyrosine phosphorylation of cdc2. Cell 1991, 64:1111-1122. 10.1016/0092-8674(91)90266-2, 1706223.
95. Ptacin JL, Lee SF, Garner EC, Toro E, Eckart M, Comolli LR, Moerner WE, Shapiro L. A spindle-like apparatus guides bacterial chromosome segregation. Nat Cell Biol 2010, 12:791-798. 10.1038/ncb2083, 20657594.
96. Wu Y, Kaiser AD, Jiang Y, Alber MS. Periodic reversal of direction allows Myxobacteria to swarm. Proc Natl Acad Sci U S A 2009, 106:1222-1227. 10.1073/pnas.0811662106, 19164578.
97. Cooper S, Denny MW. A conjecture on the relationship of bacterial shape to motility in rod-shaped bacteria. FEMS Microbiol Lett 1997, 148:227-231. 10.1111/j.1574-6968.1997.tb10293.x.
98. Kearns DB. A field guide to bacterial swarming motility. Nat Rev Microbiol 2010, 8:634-644. 10.1038/nrmicro2405, 20694026.
99. Shapiro JA, Hsu C: Escherichia coliK-12 cell-cell interactions seen by time-lapse video.J Bacteriol 1989, 171:5963-5974..
100. Rudge TJ, Steiner PJ, Phillips A, Haseloff J. Computational modeling of synthetic microbial biofilms. ACS Synthetic Biol 2012, 1:345-352. 10.1021/sb300031n.
101. Lenski RE, Travisano M. Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations. Proc Natl Acad Sci U S A 1994, 91:6808-6814. 10.1073/pnas.91.15.6808, 8041701.
102. Schaechter M, Maaloe O, Kjeldgaard NO: Dependency on medium and temperature of cell size and chemical composition during balanced grown ofSalmonella typhimurium.J Gen Microbiol 1958, 19:592-606..
103. Takeuchi S, DiLuzio WR, Weibel DB, Whitesides GM: Controlling the shape of filamentous cells ofEscherichia coli.Nano Lett 2005, 5:1819-1823..
104. Tenaillon O, Rodriguez-Verdugo A, Gaut RL, McDonald P, Bennett AF, Long AD, Gaut BS. The molecular diversity of adaptive convergence. Science 2012, 335:457-461. 10.1126/science.1212986, 22282810.
105. Domingue G, Costerton JW, Brown MR: Bacterial doubling time modulates the effects of opsonisation and available iron upon interactions betweenStaphylococcus aureus and human neutrophils.FEMS Immunol Med Microbiol 1996, 16:223-228..
106. Bochner BR. Global phenotypic characterization of bacteria. FEMS Microbiol Rev 2009, 33:191-205. 10.1111/j.1574-6976.2008.00149.x, 19054113.
107. Ingolia NT, Ghaemmaghami S, Newman JR, Weissman JS. Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 2009, 324:218-223. 10.1126/science.1168978, 19213877.