Skip to main content
SpringerLink
Log in

Getting into shape: How do rod-like bacteria control their geometry?

  • Research Article
  • Published:
Systems and Synthetic Biology

Abstract

Rod-like bacteria maintain their cylindrical shapes with remarkable precision during growth. However, they are also capable to adapt their shapes to external forces and constraints, for example by growing into narrow or curved confinements. Despite being one of the simplest morphologies, we are still far from a full understanding of how shape is robustly regulated, and how bacteria obtain their near-perfect cylindrical shapes with excellent precision. However, recent experimental and theoretical findings suggest that cell-wall geometry and mechanical stress play important roles in regulating cell shape in rod-like bacteria. We review our current understanding of the cell wall architecture and the growth dynamics, and discuss possible candidates for regulatory cues of shape regulation in the absence or presence of external constraints. Finally, we suggest further future experimental and theoretical directions which may help to shed light on this fundamental problem.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Amir A (2014) Cell size regulation in microorganisms. arXiv:1312.6562

  • Amir A, Nelson DR (2012) Dislocation-mediated growth of bacterial cell walls. Proc Natl Acad Sci 109(25):9833

    Google Scholar 

  • Amir A, Paulose J, Nelson DR (2013) Theory of interacting dislocations on cylinders. Phys Rev E 87:042314

    Article  Google Scholar 

  • Amir A, Babaeipour F, McIntosh D, Nelson DR, Jun S (2014) Bending forces plastically deform growing bacterial cell walls. Proc Natl Acad Sci. 10.1073/pnas.1317497111

  • Andre G, Kulakauskas S, Chapot-Chartier MP, Navet B, Deghorain M, Bernard E, Hols P, Dufrêne YF (2010) Imaging the nanoscale organization of peptidoglycan in living Lactococcus lactis cells. Nat Commun 1:27

    Article  PubMed  Google Scholar 

  • Andrews SS, Arkin AP (2007) A mechanical explanation for cytoskeletal rings and helices in bacteria. Biophys J 93(6):1872–1884

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Armon S, Yanai O, Ori N, Eran S (2014) Quantitative phenotyping of leaf margins in three dimensions, demonstrated on KNOTTED and TCP trangenics in Arabidopsis. J Exp Bot. doi:10.1093/jxb/eru062

  • Beeby M, Gumbart JC, Roux B, Jensen GJ (2013) Architecture and assembly of the Gram-positive cell wall. Mol Microbiol 88(4):664–672

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Boulbitch A, Quinn B, Pink D (2000) Elasticity of the rod-shaped Gram-negative eubacteria. Phys Rev Lett 85:5246–5249

    Article  CAS  PubMed  Google Scholar 

  • Burman LG, Park JT (1984) Molecular model for elongation of the murein sacculus of Escherichia coli. Proc Natl Acad Sci 81(6):1844–1848

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cabeen MT, Charbon G, Vollmer W, Born P, Ausmees N, Weibel DB, Jacobs-Wagner C (2009) Bacterial cell curvature through mechanical control of cell growth. EMBO J 28(9):1208–1219

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chastanet A, Carballido-Lopez R (2012) The actin-like mreb proteins in Bacillus subtilis: a new turn. Front Biosci (Schol Ed) 4:1582

    Article  Google Scholar 

  • de Boer PA, Crossley RE, Rothfield LI (1990) Central role for the Escherichia coli minC gene product in two different cell division-inhibition systems. Proc Natl Acad Sci 87(3):1129–1133

    Article  PubMed Central  PubMed  Google Scholar 

  • Deng Y, Sun M, Shaevitz JW (2011) Direct measurement of cell wall stress stiffening and turgor pressure in live bacterial cells. Phys Rev Lett 107(15):158101

    Article  PubMed  Google Scholar 

  • Deng Y, Sun M, Shaevitz JW (2011) Direct measurement of cell wall stress stiffening and turgor pressure in live bacterial cells. Phys Rev Lett 107(15):158101

    Article  PubMed  Google Scholar 

  • Domínguez-Escobar J, Chastanet A, Crevenna AH, Fromion V, Wedlich-Sldner R, Carballido-Lpez R (2011) Processive movement of mreb-associated cell wall biosynthetic complexes in bacteria. Science 333(6039):225–228

    Article  PubMed  Google Scholar 

  • Dumais J (2013) Modes of deformation of walled cells. J Exp Bot. doi:10.1093/jxb/ert268

  • Efrati ESE, Kupferman R (2013) The metric description of elasticity in residually stressed soft materials. Soft Matter 9:8187

    Article  CAS  Google Scholar 

  • Egan AJ, Vollmer W (2013) The physiology of bacterial cell division. Ann N Y Acad Sci 1277(1):8–28

    Article  CAS  PubMed  Google Scholar 

  • Flärdh K, Richards DM, Hempel AM, Howard M and Buttner MJ (2012) Regulation of apical growth and hyphal branching in Streptomyces. Current opinion Microbiol 15(6):737–743

    Google Scholar 

  • Furchtgott L, Wingreen NS, Huang KC (2011) Mechanisms for maintaining cell shape in rod-shaped Gram-negative bacteria. Mol Microbiol 81(2):340–353

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gan L, Chen S, Jensen GJ (2008) Molecular organization of Gram-negative peptidoglycan. Proc Natl Acad Sci 105(48):18953–18957

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Garner E private communications

  • 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(6039):222–225

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Geitmann A, Cresti M, Heath IB (2001) Cell biology of plant and fungal tip growth, vol 328. IOS Press, Amsterdam

    Google Scholar 

  • Goriely A, Robertson-Tessi M, Tabor M, Vandiver R (2008) Elastic growth models. In: Mondaini RP, Pardalos PM (eds) Mathematical modelling of biosystems. Springer, Berlin pp 1–44

  • Guillot C, Lecuit T (2013) Mechanics of epithelial tissue homeostasis and morphogenesis. Science 340(6137):1185–1189

    Article  CAS  PubMed  Google Scholar 

  • Harz H, Burgdorf K, Hltje JV (1990) Isolation and separation of the glycan strands from murein of Escherichia coli by reversed-phase high-performance liquid chromatography. Anal Biochem 190(1):120–128

    Article  CAS  PubMed  Google Scholar 

  • Hayhurst EJ, Kailas L, Hobbs JK, Foster SJ (2008) Cell wall peptidoglycan architecture in Bacillus subtilis. Proc Natl Acad Sci 105(38):14603–14608

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jiang H, Sun SX (2010) Morphology, growth, and size limit of bacterial cells. Phys Rev Lett 105:028101

    Article  PubMed Central  PubMed  Google Scholar 

  • Jiang H, Si F, Margolin W, Sun SX (2011) Mechanical control of bacterial cell shape. Biophys J 101(2):327–335

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jones LJ, Carballido-Lopez R, Errington J (2001) Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis. Cell 104(6):913–922

    Article  CAS  PubMed  Google Scholar 

  • Keijzer M, Emons A, Mulder B (2009) Modeling tip growth: pushing ahead. In: Emons A, Ketelaar T (eds) Root hairs, plant cell monographs, vol 12. Springer, Berlin, pp 103–122

    Google Scholar 

  • Kim J, Hanna JA, Byun M, Santangelo CD, Hayward RC (2012) Designing responsive buckled surfaces by halftone gel lithography. Science 335(6073):1201

    Article  CAS  PubMed  Google Scholar 

  • Klein Y, Efrati E, Sharon E (2007) Shaping of elastic sheets by prescription of non-euclidean metrics. Science 315(5815):1116–1120

    Article  CAS  PubMed  Google Scholar 

  • Koch AL (2001) Bacterial growth and form. Springer, Berlin

    Book  Google Scholar 

  • Kruse T, Møller-Jensen J, Løbner-Olesen A, Gerdes K (2003) Dysfunctional MreB inhibits chromosome segregation in Escherichia coli. EMBO J 22(19):5283–5292

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kruse T, Bork-Jensen J, Gerdes K (2004) The morphogenetic MreBCD proteins of Escherichia coli form an essential membrane-bound complex. Mol Microbiol 55(1):78–89

    Article  Google Scholar 

  • Lee TK, Tropini C, Hsin J, Desmarais SM, Ursell TS, Gong E, Gitai Z, Monds RD, Huang KC (2014) A dynamically assembled cell wall synthesis machinery buffers cell growth. Proc Natl Acad Sci 111(12):4554–4559

    Google Scholar 

  • Li Y, Hsin J, Zhao L, Cheng Y, Shang W, Huang KC, Wang HW, Ye S (2013) Ftsz protofilaments use a hinge-opening mechanism for constrictive force generation. Science 341(6144):392–395

    Article  CAS  PubMed  Google Scholar 

  • Misra G, Rojas ER, Gopinathan A, Huang KC (2013) Mechanical consequences of cell-wall turnover in the elongation of a Gram-positive bacterium. Biophys J 104(11):2342–2352

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Männik J, Driessen R, Galajda P, Keymer JE, Dekker C (2009) Bacterial growth and motility in sub-micron constrictions. Proc Natl Acad Sci 106(35):14861–14866

    Google Scholar 

  • Mukhopadhyay R, Wingreen NS (2009) Curvature and shape determination of growing bacteria. Phys Rev E 80(6):062901

    Article  Google Scholar 

  • Nelson DR (2012) Biophysical dynamics in disorderly environments. Annu Rev Biophys 41(1):371

    Article  CAS  PubMed  Google Scholar 

  • 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(5):1171–1181

    Article  PubMed  Google Scholar 

  • Osella M, Nugent E, Lagomarsino MC (2014) Concerted control of Escherichia coli cell division. Proc Natl Acad Sci 111(9):3431–3435

    Article  CAS  PubMed  Google Scholar 

  • Paulose J, Amir A To be published

  • Piro O, Carmon G, Feingold M, Fishov I (2013) 3D structure of the z-ring as a random network of ftsz filaments. Environ Microbiol 15(12):3252–3258

    Google Scholar 

  • Reimold C, Defeu Soufo HJ, Dempwolff F, Graumann PL (2013) Motion of variable-length MreB filaments at the bacterial cell membrane influences cell morphology. Mol Biol Cell 24(15):2340–2349

    Google Scholar 

  • Robert L, Hoffmann M, Krell N, Aymerich S, Robert J, Doumic M (2014) Division in Escherichia coli is triggered by a size-sensing rather than a timing mechanism. BMC Biol 12(1):17

    Article  PubMed Central  PubMed  Google Scholar 

  • Shaevitz JW, Gitai Z (2010) The structure and function of bacterial actin homologs. Cold Spring Harb Perspect Biol 2(9):a000364

    Google Scholar 

  • Sliusarenko O, Cabeen MT, Wolgemuth CW, Jacobs-Wagner C, Emonet T (2010) Processivity of peptidoglycan synthesis provides a built-in mechanism for the robustness of straight-rod cell morphology. Proc Natl Acad Sci 107:10086

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sun SX, Jiang H (2011) Physics of bacterial morphogenesis. Microbiol Mol Biol Rev 75(4):543–565

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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(23):6382–6386

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sycuro LK, Pincus Z, Gutierrez KD, Biboy J, Stern CA, Vollmer W, Salama NR (2010) Peptidoglycan crosslinking relaxation promotes helicobacter pylori’s helical shape and stomach colonization. Cell 141(5):822–833

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Takeuchi S, DiLuzio WR, Weibel DB, Whitesides GM (2005) Controlling the shape of filamentous cells of Escherichia coli. Nano Lett 5(9):1819–1823

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tuson HH, Auer GK, Renner LD, Hasebe M, Tropini C, Salick M, Crone WC, Gopinathan A, Huang KC, Weibel DB (2012) Measuring the stiffness of bacterial cells from growth rates in hydrogels of tunable elasticity. Mol Microbiol 84(5):874–891

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Typas A, Banzhaf M, Gross CA, Vollmer W (2011) From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nat Rev Microbiol 10(2):123–136

    PubMed  Google Scholar 

  • Ursell TS, Nguyen J, Monds RD, Colavin A, Billings G, Ouzounov N, Gitai Z, Shaevitz JW, Huang KC (2014) Rod-like bacterial shape is maintained by feedback between cell curvature and cytoskeletal localization. Proc Natl Acad Sci 111(11):E1025–E1034

    Google Scholar 

  • van Teeffelen S, Wang S, Furchtgott L, Huang KC, Wingreen NS, Shaevitz JW, Gitai Z (2011) The bacterial actin mreb rotates, and rotation depends on cell-wall assembly. Proc Natl Acad Sci 108:15822

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang S, Arellano-Santoyo H, Combs PA, Shaevitz JW (2010) Actin-like cytoskeleton filaments contribute to cell mechanics in bacteria. Proc Natl Acad Sci 107:9182–9185

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang S, Furchtgott L, Huang KC, Shaevitz JW (2012) Helical insertion of peptidoglycan produces chiral ordering of the bacterial cell wall. Proc Natl Acad Sci 109(10):E595–E604

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang S, Wingreen NS (2013) Cell shape can mediate the spatial organization of the bacterial cytoskeleton. Biophys J 104(3):541–552

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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(22):6865

    CAS  PubMed Central  PubMed  Google Scholar 

  • Young KD (2006) The selective value of bacterial shape. Microbiol Mol Biol Rev 70(3):660–703

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

AA was supported by the Harvard Society of Fellows and the Milton Fund. SvT was supported by a Human Frontier Science Program Postdoctoral Fellowship. The authors acknowledge useful discussions and feedback regarding the manuscript from E. Efrati, O. Amster-Choder, Y. Eun, K. C. Huang, D. R. Nelson, J. Paulose and T. Ursell.

Author information

Authors and Affiliations

  1. Department of Physics, Harvard University, Cambridge, MA, 02138, USA

    Ariel Amir

  2. Groupe Croissance et Morphogénése Microbienne, Institut Pasteur, 28 rue du Docteur Roux, 75724, Paris Cedex 15, France

    Sven van Teeffelen

Authors
  1. Ariel Amir
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sven van Teeffelen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ariel Amir.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Amir, A., van Teeffelen, S. Getting into shape: How do rod-like bacteria control their geometry?. Syst Synth Biol 8, 227–235 (2014). https://doi.org/10.1007/s11693-014-9143-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11693-014-9143-9

Keywords

Search

Navigation