Toward a Mechanistic Understanding of Bacterial Rod Shape Formation and Regulation

Literature Cited

1. Auer GK, Weibel DB. 2017. Bacterial cell mechanics. Biochemistry 56:293710–24
   [Google Scholar]
2. Badrinarayanan A, Le TBK, Laub MT. 2015. Bacterial chromosome organization and segregation. Annu. Rev. Cell Dev. Biol. 31:171–99
   [Google Scholar]
3. Banzhaf M, van den Berg van Saparoea B, Terrak M, Fraipont C, Egan A et al. 2012. Cooperativity of peptidoglycan synthases active in bacterial cell elongation. Mol. Microbiol. 85:1179–94
   [Google Scholar]
4. Baskin TI. 2005. Anisotropic expansion of the plant cell wall. Annu. Rev. Cell Dev. Biol. 21:203–22
   [Google Scholar]
5. Bean GJ, Amann KJ. 2008. Polymerization properties of the Thermotoga maritima actin MreB: roles of temperature, nucleotides, and ions. Biochemistry 47:2826–35
   [Google Scholar]
6. Billaudeau C, Chastanet A, Yao Z, Cornilleau C, Mirouze N et al. 2017. Contrasting mechanisms of growth in two model rod-shaped bacteria. Nat. Commun. 8:115370
   [Google Scholar]
7. Billaudeau C, Yao Z, Cornilleau C, Carballido-López R, Chastanet A. 2019. MreB forms subdiffraction nanofilaments during active growth in Bacillus subtilis. mBio 10:1e01879-18
   [Google Scholar]
8. Billings G, Ouzounov N, Ursell T, Desmarais SM, Shaevitz J et al. 2014. De novo morphogenesis in L-forms via geometric control of cell growth. Mol. Microbiol. 93:5883–96
   [Google Scholar]
9. Bork P, Sander C, Valencia A 1992. An ATPase domain common to prokaryotic cell cycle proteins, sugar kinases, actin, and hsp70 heat shock proteins. PNAS 89:167290–94
   [Google Scholar]
10. Bratton BP, Shaevitz JW, Gitai Z, Morgenstein RM. 2018. MreB polymers and curvature localization are enhanced by RodZ and predict E. coli’s cylindrical uniformity. Nat. Commun. 9:2797
    [Google Scholar]
11. Carballido-López R, Formstone A, Li Y, Ehrlich SD, Noirot P, Errington J. 2006. Actin homolog MreBH governs cell morphogenesis by localization of the cell wall hydrolase LytE. Dev. Cell. 11:3399–409
    [Google Scholar]
12. Cho H, Wivagg CN, Kapoor M, Barry Z, Rohs PDA et al. 2016. Bacterial cell wall biogenesis is mediated by SEDS and PBP polymerase families functioning semi-autonomously. Nat. Microbiol. 1:1016172
    [Google Scholar]
13. Colavin A, Hsin J, Huang KC 2014. Effects of polymerization and nucleotide identity on the conformational dynamics of the bacterial actin homolog MreB. PNAS 111:93585–90
    [Google Scholar]
14. Colavin A, Shi H, Huang KC. 2018. RodZ modulates geometric localization of the bacterial actin MreB to regulate cell shape. Nat. Commun. 9:1280
    [Google Scholar]
15. Contreras-Martel C, Martins A, Ecobichon C, Trindade DM, Matteï P-J et al. 2017. Molecular architecture of the PBP2-MreC core bacterial cell wall synthesis complex. Nat. Commun. 8:776
    [Google Scholar]
16. Cooper S, Denny MW. 1997. A conjecture on the relationship of bacterial shape to motility in rod-shaped bacteria. FEMS Microbiol. Lett. 148:2227–31
    [Google Scholar]
17. Daniel RA, Errington J. 2003. Control of cell morphogenesis in bacteria two distinct ways to make a rod-shaped cell. Cell 113:6767–76
    [Google Scholar]
18. D'Elia MA, Millar KE, Beveridge TJ, Brown ED. 2006. Wall teichoic acid polymers are dispensable for cell viability in Bacillus subtilis. J. Bacteriol. 188:238313–16
    [Google Scholar]
19. Dempwolff F, Reimold C, Reth M, Graumann PL. 2011. Bacillus subtilis MreB orthologs self-organize into filamentous structures underneath the cell membrane in a heterologous cell system. PLOS ONE 6:11e27035
    [Google Scholar]
20. Dhar S, Kumari H, Balasubramanian D, Mathee K. 2017. Cell-wall recycling and synthesis in Escherichia coli and Pseudomonas aeruginosa – their role in the development of resistance. J. Med. Microbiol. 67:11–21
    [Google Scholar]
21. Dion MF, Kapoor M, Sun Y, Wilson S, Ryan J et al. 2019. Bacillus subtilis cell diameter is determined by the opposing actions of two distinct cell wall synthetic systems. Nat. Microbiol. 4:81294–305
    [Google Scholar]
22. Divakaruni AV, Baida C, White CL, Gober JW. 2007. The cell shape proteins MreB and MreC control cell morphogenesis by positioning cell wall synthetic complexes. Mol. Microbiol. 66:1174–88
    [Google Scholar]
23. Domínguez-Escobar J, Chastanet A, Crevenna AH, Fromion V, Wedlich-Söldner R, Carballido-López R. 2011. Processive movement of MreB-associated cell wall biosynthetic complexes in bacteria. Science 333:6039225–28
    [Google Scholar]
24. Duhart JC, Parsons TT, Raftery LA. 2017. The repertoire of epithelial morphogenesis on display: progressive elaboration of Drosophila egg structure. Mech. Dev. 148:18–39
    [Google Scholar]
25. Emami K, Guyet A, Kawai Y, Devi J, Wu LJ et al. 2017. RodA as the missing glycosyltransferase in Bacillus subtilis and antibiotic discovery for the peptidoglycan polymerase pathway. Nat. Microbiol. 2:16253
    [Google Scholar]
26. Esue O, Cordero M, Wirtz D, Tseng Y. 2005. The assembly of MreB, a prokaryotic homolog of actin. J. Biol. Chem. 280:42628–35
    [Google Scholar]
27. Figge RM, Divakaruni AV, Gober JW. 2004. MreB, the cell shape-determining bacterial actin homologue, co-ordinates cell wall morphogenesis in Caulobacter crescentus. Mol. Microbiol. 51:51321–32
    [Google Scholar]
28. Formstone A, Errington J. 2005. A magnesium-dependent mreB null mutant: implications for the role of mreB in Bacillus subtilis. Mol. Microbiol. 55:61646–57
    [Google Scholar]
29. Gallet R, Violle C, Fromin N, Jabbour-Zahab R, Enquist BJ, Lenormand T. 2017. The evolution of bacterial cell size: the internal diffusion-constraint hypothesis. ISME J 11:71559–68
    [Google Scholar]
30. Garner EC, Bernard R, Wang W, Zhuang X, Rudner DZ, Mitchison T. 2011. Coupled, circumferential motions of the cell wall synthesis machinery and MreB filaments in B. subtilis. Science 333:6039222–25
    [Google Scholar]
31. Gitai Z, Dye NA, Reisenauer A, Wachi M, Shapiro L. 2005. MreB actin-mediated segregation of a specific region of a bacterial chromosome. Cell 120:3329–41
    [Google Scholar]
32. Herrmann M, Schneck E, Gutsmann T, Brandenburg K, Tanaka M. 2015. Bacterial lipopolysaccharides form physically cross-linked, two-dimensional gels in the presence of divalent cations. Soft Matter 11:306037–44
    [Google Scholar]
33. Höltje J-V. 1998. Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol. . Mol. Biol. R 62:1181–203
    [Google Scholar]
34. Hussain S, Wivagg CN, Szwedziak P, Wong F, Schaefer K et al. 2018. MreB filaments align along greatest principal membrane curvature to orient cell wall synthesis. eLife 7:1239
    [Google Scholar]
35. Ikebe R, Kuwabara Y, Chikada T, Niki H, Shiomi D 2018. The periplasmic disordered domain of RodZ promotes its self-interaction in Escherichia coli. Genes Cells 23:4307–17
    [Google Scholar]
36. Jones LJF, Carballido-López R, Errington J. 2001. Control of cell shape in bacteria helical, actin-like filaments in Bacillus subtilis. Cell 104:6913–22
    [Google Scholar]
37. Karsenti E. 2008. Self-organization in cell biology: a brief history. Nat. Rev. Mol. Cell Biol. 9:3255–62
    [Google Scholar]
38. Kawai Y, Asai K, Errington J. 2009. Partial functional redundancy of MreB isoforms, MreB, Mbl and MreBH, in cell morphogenesis of Bacillus subtilis. Mol. Microbiol. 73:4719–31
    [Google Scholar]
39. Kawai Y, Marles-Wright J, Cleverley RM, Emmins R, Ishikawa S et al. 2011. A widespread family of bacterial cell wall assembly proteins. EMBO J 30:244931–41
    [Google Scholar]
40. Kern T, Giffard M, Hediger S, Amoroso A, Giustini C et al. 2010. Dynamics characterization of fully hydrated bacterial cell walls by solid-state NMR: evidence for cooperative binding of metal ions. J. Am. Chem. Soc. 132:3110911–19
    [Google Scholar]
41. Koch AL. 1988. Biophysics of bacterial walls viewed as stress-bearing fabric. Microbiol. Rev. 52:3337–53
    [Google Scholar]
42. Lai GC, Cho H, Bernhardt TG. 2017. The mecillinam resistome reveals a role for peptidoglycan endopeptidases in stimulating cell wall synthesis in Escherichia coli. PLOS Genet 13:7e1006934
    [Google Scholar]
43. Landgraf D, Okumus B, Chien P, Baker TA, Paulsson J. 2012. Segregation of molecules at cell division reveals native protein localization. Nat. Methods 9:5480
    [Google Scholar]
44. Lee TK, Meng K, Shi H, Huang KC. 2016. Single-molecule imaging reveals modulation of cell wall synthesis dynamics in live bacterial cells. Nat. Commun. 7:13170
    [Google Scholar]
45. Mathelié-Guinlet M, Asmar AT, Collet J-F, Dufrêne YF. 2020. Lipoprotein Lpp regulates the mechanical properties of the E. coli cell envelope. Nat. Commun. 11:1789
    [Google Scholar]
46. Matias VRF, Beveridge TJ. 2005. Cryo-electron microscopy reveals native polymeric cell wall structure in Bacillus subtilis 168 and the existence of a periplasmic space. Mol. Microbiol. 56:1240–51
    [Google Scholar]
47. Mayer JA, Amann KJ. 2009. Assembly properties of the Bacillus subtilis actin, MreB. Cell Motil. Cytoskelet 66:2109–18
    [Google Scholar]
48. Meeske AJ, Riley EP, Robins WP, Uehara T, Mekalanos JJ et al. 2016. SEDS proteins are a widespread family of bacterial cell wall polymerases. Nature 537:7622634
    [Google Scholar]
49. Meisner J, Llopis PM, Sham L, Garner E, Bernhardt TG, Rudner DZ. 2013. FtsEX is required for CwlO peptidoglycan hydrolase activity during cell wall elongation in Bacillus subtilis. Mol. Microbiol. 89:61069–83
    [Google Scholar]
50. Neugebauer J, Wallner-Novak M, Lehner T, Wrulich C, Baumgartner M 2018. Movable thin glass elements in façades. Challenging Glass Conference Proceedings, Vol. 6, eds. C Louter, F Bos, J Belis, F Veer, R Nijsse 195–202 Delft, Neth: TU Delft Open
51. Nurse P, Marians KJ. 2013. Purification and characterization of Escherichia coli MreB protein. J. Biol. Chem. 288:53469–75
    [Google Scholar]
52. Olshausen PV, Defeu Soufo HJ, Wicker K, Heintzmann R, Graumann PL, Rohrbach A 2013. Superresolution imaging of dynamic MreB filaments in B. subtilis—a multiple-motor-driven transport?. Biophys. J. 105:51171–81
    [Google Scholar]
53. Ouzounov N, Nguyen JP, Bratton BP, Jacobowitz D, Gitai Z, Shaevitz JW. 2016. MreB orientation correlates with cell diameter in Escherichia coli. Biophys. J. 111:51035–43
    [Google Scholar]
54. Özbaykal G, Wollrab E, Simon F, Vigouroux A, Cordier B et al. 2020. The transpeptidase PBP2 governs initial localization and activity of the major cell-wall synthesis machinery in E. coli. eLife 9:e50629
    [Google Scholar]
55. Paradis-Bleau C, Markovski M, Uehara T, Lupoli TJ, Walker S et al. 2010. Lipoprotein cofactors located in the outer membrane activate bacterial cell wall polymerases. Cell 143:71110–20
    [Google Scholar]
56. Paredez AR, Somerville CR, Ehrhardt DW. 2006. Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312:57791491–95
    [Google Scholar]
57. Pazos M, Peters K, Vollmer W. 2017. Robust peptidoglycan growth by dynamic and variable multi-protein complexes. Curr. Opin. Microbiol. 36:55–61
    [Google Scholar]
58. Pooley HM. 1976. Layered distribution, according to age, within the cell wall of bacillus subtilis. J. Bacteriol. 125:31139–47
    [Google Scholar]
59. Popp D, Narita A, Maeda K, Fujisawa T, Ghoshdastider U et al. 2010. Filament structure, organization, and dynamics in MreB sheets. J. Biol. Chem. 285:2115858–65
    [Google Scholar]
60. Renner LD, Eswaramoorthy P, Ramamurthi KS, Weibel DB. 2013. Studying biomolecule localization by engineering bacterial cell wall curvature. PLOS ONE 8:12e84143
    [Google Scholar]
61. Rohs PDA, Buss J, Sim SI, Squyres GR, Srisuknimit V et al. 2018. A central role for PBP2 in the activation of peptidoglycan polymerization by the bacterial cell elongation machinery. PLOS Genet 14:10e1007726
    [Google Scholar]
62. Rojas ER, Billings G, Odermatt PD, Auer GK, Zhu L et al. 2018. The outer membrane is an essential load-bearing element in Gram-negative bacteria. Nature 559:7715617–21
    [Google Scholar]
63. Rothfield L, Taghbalout A, Shih YL. 2005. Spatial control of bacterial division-site placement. Nat. Rev. Microbiol. 3:12959–68
    [Google Scholar]
64. Rueff A, Chastanet A, Domínguez-Escobar J, Yao Z, Yates J et al. 2014. An early cytoplasmic step of peptidoglycan synthesis is associated to MreB in Bacillus subtilis. Mol. Microbiol. 91:2348–62
    [Google Scholar]
65. Salje J, van den Ent F, de Boer P, Löwe J. 2011. Direct membrane binding by bacterial actin MreB. Mol. Cell 43:3478–87
    [Google Scholar]
66. Savage DF, Afonso B, Chen AH, Silver PA. 2010. Spatially ordered dynamics of the bacterial carbon fixation machinery. Science 327:59701258–61
    [Google Scholar]
67. Schirner K, Eun Y-J, Dion M, Luo Y, Helmann JD et al. 2015. Lipid-linked cell wall precursors regulate membrane association of bacterial actin MreB. Nat. Chem. Biol. 11:138–45
    [Google Scholar]
68. Sham L-T, Butler EK, Lebar MD, Kahne D, Bernhardt TG, Ruiz N. 2014. MurJ is the flippase of lipid-linked precursors for peptidoglycan biogenesis. Science 345:6193220–22
    [Google Scholar]
69. Shi H, Colavin A, Bigos M, Tropini C, Monds RD, Huang KC. 2017. Deep phenotypic mapping of bacterial cytoskeletal mutants reveals physiological robustness to cell size. Curr. Biol. 27:223419–29.e4
    [Google Scholar]
70. Shi H, Quint DA, Grason GM, Gopinathan A, Huang KC. 2020. Chiral twisting in a bacterial cytoskeletal polymer affects filament size and orientation. Nat. Commun. 11:1408
    [Google Scholar]
71. Shih Y-L, Le T, Rothfield L 2003. Division site selection in Escherichia coli involves dynamic redistribution of Min proteins within coiled structures that extend between the two cell poles. PNAS 100:137865–70
    [Google Scholar]
72. Silhavy TJ, Kahne D, Walker S 2010. The bacterial cell envelope. Cold Spring Harb. Perspect. Biol. 2:5a000414
    [Google Scholar]
73. Sjodt M, Rohs PDA, Gilman MSA, Erlandson SC, Zheng S et al. 2020. Structural coordination of polymerization and crosslinking by a SEDS–bPBP peptidoglycan synthase complex. Nat. Microbiol. 5:813–20
    [Google Scholar]
74. Smith WPJ, Davit Y, Osborne JM, Kim W, Foster KR, Pitt-Francis JM 2017. Cell morphology drives spatial patterning in microbial communities. PNAS 114:3E280–86
    [Google Scholar]
75. Stoddard PR, Williams TA, Garner E, Baum B. 2017. Evolution of polymer formation within the actin superfamily. Mol. Biol. Cell 28:192461–69
    [Google Scholar]
76. Sun Y, Garner EC. 2020. PrkC modulates MreB filament density and cellular growth rate by monitoring cell wall precursors. bioRxiv 272336 https://doi.org/10.1101/2020.08.28.272336
    [Crossref] [Google Scholar]
77. Swulius MT, Chen S, Ding HJ, Pilhofer M, Tocheva EI et al. 2011. Long helical filaments are not seen encircling cells in electron cryotomograms of rod-shaped bacteria. Biochem. Biophys. Res. Commun. 407:4650–55
    [Google Scholar]
78. Swulius MT, Jensen GJ. 2012. The helical MreB cytoskeleton in Escherichia coli MC1000/pLE7 is an artifact of the N-terminal yellow fluorescent protein tag. J. Bacteriol. 194:236382–86
    [Google Scholar]
79. Taguchi A, Welsh MA, Marmont LS, Lee W, Sjodt M et al. 2019. FtsW is a peptidoglycan polymerase that is functional only in complex with its cognate penicillin-binding protein. Nat. Microbiol. 4:4587–94
    [Google Scholar]
80. Thomas KJ, Rice CV. 2014. Revised model of calcium and magnesium binding to the bacterial cell wall. Biometals 27:61361–70
    [Google Scholar]
81. Toyoda A, Aizu T, Ejima F, Fujiyama A, Shini T et al. 2013. Mutations in cell elongation genes mreB, mrdA and mrdB suppress the shape defect of RodZ-deficient cells. Mol. Microbiol. 87:51029–44
    [Google Scholar]
82. Tropini C, Lee TK, Hsin J, Desmarais SM, Ursell T et al. 2014. Principles of bacterial cell-size determination revealed by cell-wall synthesis perturbations. Cell Rep 9:41520–27
    [Google Scholar]
83. Ursell T, Lee TK, Shiomi D, Shi H, Tropini C et al. 2017. Rapid, precise quantification of bacterial cellular dimensions across a genomic-scale knockout library. BMC Biol 15:17
    [Google Scholar]
84. Vadillo-Rodriguez V, Schooling SR, Dutcher JR. 2009. In situ characterization of differences in the viscoelastic response of individual Gram-negative and Gram-positive bacterial cells. J. Bacteriol. 191:175518–25
    [Google Scholar]
85. van den Ent F, Amos LA, Löwe J 2001. Prokaryotic origin of the actin cytoskeleton. Nature 413:685139–44
    [Google Scholar]
86. van den Ent F, Izoré T, Bharat TA, Johnson CM, Lowe J 2014. Bacterial actin MreB forms antiparallel double filaments. eLife 3:e02634
    [Google Scholar]
87. van den Ent F, Johnson CM, Persons L, de Boer P, Lowe J. 2010. Bacterial actin MreB assembles in complex with cell shape protein RodZ. EMBO J 29:61081–90
    [Google Scholar]
88. van den Ent F, Leaver M, Bendezu F, Errington J, de Boer P, Lowe J. 2006. Dimeric structure of the cell shape protein MreC and its functional implications. Mol. Microbiol. 62:61631–42
    [Google Scholar]
89. van Teeffelen S, Wang S, Furchtgott L, Huang KC, Wingreen NS et al. 2011. The bacterial actin MreB rotates, and rotation depends on cell-wall assembly. PNAS 108:3815822–27
    [Google Scholar]
90. Vigouroux A, Cordier B, Aristov A, Alvarez L, Özbaykal G et al. 2020. Class-A penicillin binding proteins do not contribute to cell shape but repair cell-wall defects. eLife 9:e51998
    [Google Scholar]
91. Wang S, Wingreen NS. 2013. Cell shape can mediate the spatial organization of the bacterial cytoskeleton. Biophys. J. 104:3541–52
    [Google Scholar]
92. Whatmore AM, Chudek JA, Reed RH. 1990. The effects of osmotic upshock on the intracellular solute pools of Bacillus subtilis. Microbiology 136:122527–35
    [Google Scholar]
93. Wong F, Garner EC, Amir A 2019. Mechanics and dynamics of translocating MreB filaments on curved membranes. eLife 8:e40472
    [Google Scholar]
94. Wong F, Renner LD, Özbaykal G, Paulose J, Weibel DB et al. 2017. Mechanical strain sensing implicated in cell shape recovery in Escherichia coli. Nat. Microbiol. 2:917115
    [Google Scholar]
95. Wu LJ, Lee S, Park S, Eland LE, Wipat A et al. 2020. Geometric principles underlying the proliferation of a model cell system. Nat. Commun. 11:4149
    [Google Scholar]
96. Wu Y, Kaiser AD, Jiang Y, Alber MS 2009. Periodic reversal of direction allows Myxobacteria to swarm. PNAS 106:41222–27
    [Google Scholar]
97. Yao X, Jericho M, Pink D, Beveridge T. 1999. Thickness and elasticity of Gram-negative murein sacculi measured by atomic force microscopy. J. Bacteriol. 181:226865–75
    [Google Scholar]
98. Young KD. 2006. The selective value of bacterial shape. Microbiol. Mol. Biol. Rev. 70:3660–703
    [Google Scholar]
99. Yu Z, Qin W, Lin J, Fang S, Qiu J. 2015. Antibacterial mechanisms of polymyxin and bacterial resistance. Biomed. Res. Int. 2015:679109
    [Google Scholar]