Bacterial morphogenesis and the enigmatic mreb helix

Bacterial morphogenesis and the enigmatic mreb helix


Play all audios:


ABSTRACT Work over the past decade has highlighted the pivotal role of the actin-like MreB family of proteins in the determination and maintenance of rod cell shape in bacteria. Early images


of MreB localization revealed long helical filaments, which were suggestive of a direct role in governing cell wall architecture. However, several more recent, higher-resolution studies


have questioned the existence or importance of the helical structures. In this Opinion article, I navigate a path through these conflicting reports, revive the helix model and summarize the


key questions that remain to be answered. Access through your institution Buy or subscribe This is a preview of subscription content, access via your institution ACCESS OPTIONS Access


through your institution Subscribe to this journal Receive 12 print issues and online access $209.00 per year only $17.42 per issue Learn more Buy this article * Purchase on SpringerLink *


Instant access to full article PDF Buy now Prices may be subject to local taxes which are calculated during checkout ADDITIONAL ACCESS OPTIONS: * Log in * Learn about institutional


subscriptions * Read our FAQs * Contact customer support SIMILAR CONTENT BEING VIEWED BY OTHERS CYTOSKELETAL COMPONENTS CAN TURN WALL-LESS SPHERICAL BACTERIA INTO KINKING HELICES Article


Open access 14 November 2022 SELF-ASSOCIATION OF MREC AS A REGULATORY SIGNAL IN BACTERIAL CELL WALL ELONGATION Article Open access 20 May 2021 CELL WALL SYNTHESIS AND REMODELLING DYNAMICS


DETERMINE DIVISION SITE ARCHITECTURE AND CELL SHAPE IN _ESCHERICHIA COLI_ Article Open access 12 September 2022 REFERENCES * Siefert, J. L. & Fox, G. E. Phylogenetic mapping of bacterial


morphology. _Microbiology_ 144, 2803–2808 (1998). Article  CAS  Google Scholar  * Koch, A. L. Were Gram-positive rods the first bacteria? _Trends Microbiol._ 11, 166–170 (2003). Article 


CAS  PubMed  Google Scholar  * Errington, J. L-form bacteria, cell walls and the origins of life. _Open Biol._ 3, 120143 (2013). Article  PubMed  PubMed Central  CAS  Google Scholar  *


Abhayawardhane, Y. & Stewart, G. C. _Bacillus subtilis_ possesses a second determinant with extensive sequence similarity to the _Escherichia coli mreB_ morphogene. _J. Bacteriol._ 177,


765–773 (1995). Article  CAS  PubMed  PubMed Central  Google Scholar  * Doi, M. et al. Determinations of the DNA sequence of the _mreB_ gene and of the gene products of the _mre_ region that


function in formation of the rod shape of _Escherichia coli_ cells. _J. Bacteriol._ 170, 4619–4624 (1988). Article  CAS  PubMed  PubMed Central  Google Scholar  * Levin, P. A., Margolis, P.


S., Setlow, P., Losick, R. & Sun, D. Identification of _Bacillus subtilis_ genes for septum placement and shape determination. _J. Bacteriol._ 174, 6717–6728 (1992). Article  CAS 


PubMed  PubMed Central  Google Scholar  * Normark, S. Mutation in _Escherichia coli_ K-12 mediating spherelike envelopes and changes tolerance to ultraviolet irradiation and some


antibiotics. _J. Bacteriol._ 98, 1274–1277 (1969). Article  CAS  PubMed  PubMed Central  Google Scholar  * Varley, A. W. & Stewart, G. C. The _divIVB_ region of the _Bacillus subtilis_


chromosome encodes homologs of _Escherichia coli_ septum placement (MinCD) and cell shape (MreBCD) determinants. _J. Bacteriol._ 174, 6729–6742 (1992). Article  CAS  PubMed  PubMed Central 


Google Scholar  * Wachi, M. et al. Mutant isolation and molecular cloning of _mre_ genes, which determine cell shape, sensitivity to mecillinam, and amount of penicillin-binding proteins in


_Escherichia coli_. _J. Bacteriol._ 169, 4935–4940 (1987). Article  CAS  PubMed  PubMed Central  Google Scholar  * Jones, L. J. F., Carballido-López, R. & Errington, J. Control of cell


shape in bacteria: helical, actin-like filaments in _Bacillus subtilis_. _Cell_ 104, 913–922 (2001). Article  CAS  PubMed  Google Scholar  * Daniel, R. A. & Errington, J. Control of cell


morphogenesis in bacteria: two distinct ways to make a rod-shaped cell. _Cell_ 113, 767–776 (2003). Article  CAS  PubMed  Google Scholar  * Brown, P. J. et al. Polar growth in the


Alphaproteobacterial order Rhizobiales. _Proc. Natl Acad. Sci. USA_ 109, 1697–1701 (2012). Article  CAS  PubMed  PubMed Central  Google Scholar  * de Pedro, M. A., Young, K. D., Holtje, J.


V. & Schwarz, H. Branching of _Escherichia coli_ cells arises from multiple sites of inert peptidoglycan. _J. Bacteriol._ 185, 1147–1152 (2003). Article  CAS  PubMed  PubMed Central 


Google Scholar  * Mobley, H. L., Koch, A. L., Doyle, R. J. & Streips, U. N. Insertion and fate of the cell wall in _Bacillus subtilis_. _J. Bacteriol._ 158, 169–179 (1984). Article  CAS


  PubMed  PubMed Central  Google Scholar  * Pooley, H. M. Turnover and spreading of old wall during surface growth of _Bacillus subtilis_. _J. Bacteriol._ 125, 1127–1138 (1976). Article  CAS


  PubMed  PubMed Central  Google Scholar  * Divakaruni, A. V., Loo, R. R., Xie, Y., Loo, J. A. & Gober, J. W. The cell-shape protein MreC interacts with extracytoplasmic proteins


including cell wall assembly complexes in _Caulobacter crescentus_. _Proc. Natl Acad. Sci. USA_ 102, 18602–18607 (2005). Article  CAS  PubMed  PubMed Central  Google Scholar  * Divakaruni,


A. V., Baida, C., White, C. L. & Gober, J. W. The cell shape proteins MreB and MreC control cell morphogenesis by positioning cell wall synthetic complexes. _Mol. Microbiol._ 66, 174–188


(2007). Article  CAS  PubMed  Google Scholar  * Kawai, Y., Daniel, R. A. & Errington, J. Regulation of cell wall morphogenesis in _Bacillus subtilis_ by recruitment of PBP1 to the MreB


helix. _Mol. Microbiol._ 71, 1131–1144 (2009). Article  CAS  PubMed  Google Scholar  * Lee, T. K. et al. A dynamically assembled cell wall synthesis machinery buffers cell growth. _Proc.


Natl Acad. Sci. USA_ 111, 4554–4559 (2014). Article  CAS  PubMed  PubMed Central  Google Scholar  * Mohammadi, T. et al. The essential peptidoglycan glycosyltransferase MurG forms a complex


with proteins involved in lateral envelope growth as well as with proteins involved in cell division in _Escherichia coli_. _Mol. Microbiol._ 65, 1106–1121 (2007). Article  CAS  PubMed 


PubMed Central  Google Scholar  * White, C. L., Kitich, A. & Gober, J. W. Positioning cell wall synthetic complexes by the bacterial morphogenetic proteins MreB and MreD. _Mol.


Microbiol._ 76, 616–633 (2010). Article  CAS  PubMed  Google Scholar  * Favini-Stabile, S., Contreras-Martel, C., Thielens, N. & Dessen, A. MreB and MurG as scaffolds for the cytoplasmic


steps of peptidoglycan biosynthesis. _Environ. Microbiol._ 15, 3218–3228 (2013). Article  CAS  PubMed  Google Scholar  * Rueff, A. S. et al. An early cytoplasmic step of peptidoglycan


synthesis is associated to MreB in _Bacillus subtilis_. _Mol. Microbiol._ 91, 348–362 (2014). Article  CAS  PubMed  Google Scholar  * Formstone, A., Carballido-López, R., Noirot, P.,


Errington, J. & Scheffers, D. J. Localization and interactions of teichoic acid synthetic enzymes in _Bacillus subtilis_. _J. Bacteriol._ 190, 1812–1821 (2008). Article  CAS  PubMed 


Google Scholar  * Kawai, Y. et al. A widespread family of bacterial cell wall assembly proteins. _EMBO J._ 30, 4931–4941 (2011). Article  CAS  PubMed  PubMed Central  Google Scholar  *


Carballido-López, R. et al. Actin homolog MreBH governs cell morphogenesis by localization of the cell wall hydrolase LytE. _Dev. Cell_ 11, 399–409 (2006). Article  PubMed  CAS  Google


Scholar  * Domínguez-Cuevas, P., Porcelli, I., Daniel, R. A. & Errington, J. Differentiated roles for MreB-actin isologues and autolytic enzymes in _Bacillus subtilis_ morphogenesis.


_Mol. Microbiol._ 89, 1084–1098 (2013). Article  PubMed  PubMed Central  CAS  Google Scholar  * Höltje, J. V. Growth of the stress-bearing and shape-maintaining murein sacculus of


_Escherichia coli_. _Microbiol. Mol. Biol. Rev._ 62, 181–203 (1998). Article  PubMed  PubMed Central  Google Scholar  * Vollmer, W. & Bertsche, U. Murein (peptidoglycan) structure,


architecture and biosynthesis in _Escherichia coli_. _Biochim. Biophys. Acta_ 1778, 1714–1734 (2008). Article  CAS  PubMed  Google Scholar  * Kruse, T., Bork-Jensen, J. & Gerdes, K. The


morphogenetic MreBCD proteins of _Escherichia coli_ form an essential membrane-bound complex. _Mol. Microbiol._ 55, 78–89 (2005). Article  CAS  PubMed  Google Scholar  * Leaver, M. &


Errington, J. Roles for MreC and MreD proteins in helical growth of the cylindrical cell wall in _Bacillus subtilis_. _Mol. Microbiol._ 57, 1196–1209 (2005). Article  CAS  PubMed  Google


Scholar  * Defeu Soufo, H. J. & Graumann, P. L. _Bacillus subtilis_ actin-like protein MreB influences the positioning of the replication machinery and requires membrane proteins MreC/D


and other actin-like proteins for proper localization. _BMC Cell Biol._ 6, 10 (2005). Article  PubMed  PubMed Central  CAS  Google Scholar  * Shiomi, D., Sakai, M. & Niki, H.


Determination of bacterial rod shape by a novel cytoskeletal membrane protein. _EMBO J._ 27, 3081–3091 (2008). Article  CAS  PubMed  PubMed Central  Google Scholar  * Bendezu, F. O., Hale,


C. A., Bernhardt, T. G. & de Boer, P. A. RodZ (YfgA) is required for proper assembly of the MreB actin cytoskeleton and cell shape in _E. coli_. _EMBO J._ 28, 193–204 (2009). Article 


CAS  PubMed  Google Scholar  * Alyahya, S. A. et al. RodZ, a component of the bacterial core morphogenic apparatus. _Proc. Natl Acad. Sci. USA_ 106, 1239–1244 (2009). Article  CAS  PubMed 


PubMed Central  Google Scholar  * van den Ent, F., Johnson, C. M., Persons, L., de Boer, P. & Löwe, J. Bacterial actin MreB assembles in complex with cell shape protein RodZ. _EMBO J._


29, 1081–1090 (2010). Article  CAS  PubMed  PubMed Central  Google Scholar  * Muchova, K., Chromikova, Z. & Barak, I. Control of _Bacillus subtilis_ cell shape by RodZ. _Environ.


Microbiol._ 15, 3259–3271 (2013). Article  CAS  PubMed  Google Scholar  * Strahl, H., Burmann, F. & Hamoen, L. W. The actin homologue MreB organizes the bacterial cell membrane. _Nature


Commun._ 5, 3442 (2014). Article  CAS  Google Scholar  * Fenton, A. K. & Gerdes, K. Direct interaction of FtsZ and MreB is required for septum synthesis and cell division in _Escherichia


coli_. _EMBO J._ 32, 1953–1965 (2013). Article  CAS  PubMed  PubMed Central  Google Scholar  * Figge, R. M., Divakaruni, A. V. & Gober, J. W. MreB, the cell shape-determining bacterial


actin homologue, co-ordinates cell wall morphogenesis in _Caulobacter crescentus_. _Mol. Microbiol._ 51, 1321–1332 (2004). Article  CAS  PubMed  Google Scholar  * Slovak, P. M., Wadhams, G.


H. & Armitage, J. P. Localization of MreB in _Rhodobacter sphaeroides_ under conditions causing changes in cell shape and membrane structure. _J. Bacteriol._ 187, 54–64 (2005). Article 


CAS  PubMed  PubMed Central  Google Scholar  * Lee, S. & Price, C. W. The _minCD_ locus of _Bacillus subtilis_ lacks the _minE_ determinant that provides topological specificity to cell


division. _Mol. Microbiol._ 7, 601–610 (1993). Article  CAS  PubMed  Google Scholar  * Defeu Soufo, H. J. & Graumann, P. L. Dynamic localization and interaction with other _Bacillus


subtilis_ actin-like proteins are important for the function of MreB. _Mol. Microbiol._ 62, 1340–1356 (2006). Article  CAS  PubMed  Google Scholar  * Kawai, Y., Asai, K. & Errington, J.


Partial functional redundancy of MreB isoforms, MreB, Mbl and MreBH, in cell morphogenesis of _Bacillus subtilis_. _Mol. Microbiol._ 73, 719–731 (2009). Article  CAS  PubMed  Google Scholar


  * Bork, P., Sander, C. & Valencia, A. An ATPase domain common to prokaryotic cell cycle proteins, sugar kinases, actin, and hsp70 heat shock proteins. _Proc. Natl Acad. Sci. USA_ 89,


7290–7294 (1992). Article  CAS  PubMed  PubMed Central  Google Scholar  * van den Ent, F., Amos, L. A. & Löwe, J. Prokaryotic origin of the actin cytoskeleton. _Nature_ 413, 39–44


(2001). Article  CAS  PubMed  Google Scholar  * Esue, O., Cordero, M., Wirtz, D. & Tseng, Y. The assembly of MreB, a prokaryotic homolog of actin. _J. Biol. Chem._ 280, 2628–2635 (2005).


Article  CAS  PubMed  Google Scholar  * Salje, J., van den Ent, F., de Boer, P. & Löwe, J. Direct membrane binding by bacterial actin MreB. _Mol. Cell_ 43, 478–487 (2011). Article  CAS


  PubMed  PubMed Central  Google Scholar  * Van den Ent, F., Izore, T., Bharat, T. A., Johnson, C. M. & Löwe, J. Bacterial actin MreB forms antiparallel double filaments. _eLife_ 3,


e02634 (2014). Article  PubMed  PubMed Central  CAS  Google Scholar  * Carballido-López, R. & Errington, J. The bacterial cytoskeleton: _in vivo_ dynamics of the actin-like protein Mbl


of _Bacillus subtilis_. _Dev. Cell_ 4, 19–28 (2003). Article  PubMed  Google Scholar  * Defeu Soufo, H. J. & Graumann, P. L. Dynamic movement of actin-like proteins within bacterial


cells. _EMBO Rep._ 5, 789–794 (2004). Article  CAS  PubMed  PubMed Central  Google Scholar  * Kruse, T., Møller-Jensen, J., Løbner-Olesen, A. & Gerdes, K. Dysfunctional MreB inhibits


chromosome segregation in _Escherichia coli_. _EMBO J._ 22, 5283–5292 (2003). Article  CAS  PubMed  PubMed Central  Google Scholar  * Gitai, Z., Dye, N. & Shapiro, L. An actin-like gene


can determine cell polarity in bacteria. _Proc. Natl Acad. Sci. USA_ 101, 8643–8648 (2004). Article  CAS  PubMed  PubMed Central  Google Scholar  * Vats, P. & Rothfield, L. Duplication


and segregation of the actin (MreB) cytoskeleton during the prokaryotic cell cycle. _Proc. Natl Acad. Sci. USA_ 104, 17795–17800 (2007). Article  CAS  PubMed  PubMed Central  Google Scholar


  * Shih, Y. L., Le, T. & Rothfield, L. Division site selection in _Escherichia coli_ involves dynamic redistribution of Min proteins within coiled structures that extend between the two


cell poles. _Proc. Natl Acad. Sci. USA_ 100, 7865–7870 (2003). Article  CAS  PubMed  PubMed Central  Google Scholar  * Espeli, O., Nurse, P., Levine, C., Lee, C. & Marians, K. J. SetB:


an integral membrane protein that affects chromosome segregation in _Escherichia coli_. _Mol. Microbiol._ 50, 495–509 (2003). Article  CAS  PubMed  Google Scholar  * Campo, N. et al.


Subcellular sites for bacterial protein export. _Mol. Microbiol._ 53, 1583–1599 (2004). Article  CAS  PubMed  Google Scholar  * Foulquier, E., Pompeo, F., Bernadac, A., Espinosa, L. &


Galinier, A. The YvcK protein is required for morphogenesis via localization of PBP1 under gluconeogenic growth conditions in _Bacillus subtilis_. _Mol. Microbiol._ 80, 309–318 (2011).


Article  CAS  PubMed  Google Scholar  * Tiyanont, K. et al. Imaging peptidoglycan biosynthesis in _Bacillus subtilis_ with fluorescent antibiotics. _Proc. Natl Acad. Sci. USA_ 103,


11033–11038 (2006). Article  CAS  PubMed  PubMed Central  Google Scholar  * Swulius, M. T. et al. Long helical filaments are not seen encircling cells in electron cryotomograms of rod-shaped


bacteria. _Biochem. Biophys. Res. Commun._ 407, 650–655 (2011). Article  CAS  PubMed  PubMed Central  Google Scholar  * Swulius, M. T. & Jensen, G. J. The helical MreB cytoskeleton in


_Escherichia coli_ MC1000/pLE7 is an artifact of the N-terminal yellow fluorescent protein tag. _J. Bacteriol._ 194, 6382–6386 (2012). Article  CAS  PubMed  PubMed Central  Google Scholar  *


Garner, E. C. et al. Coupled, circumferential motions of the cell wall synthesis machinery and MreB filaments in _B. subtilis_. _Science_ 333, 222–225 (2011). Article  CAS  PubMed  PubMed


Central  Google Scholar  * Domínguez-Escobar, J. et al. Processive movement of MreB-associated cell wall biosynthetic complexes in bacteria. _Science_ 333, 225–228 (2011). Article  PubMed 


CAS  Google Scholar  * van Teeffelen, S. et al. The bacterial actin MreB rotates, and rotation depends on cell-wall assembly. _Proc. Natl Acad. Sci. USA_ 108, 15822–15827 (2011). Article 


CAS  PubMed  PubMed Central  Google Scholar  * Strahl, H. & Hamoen, L. W. Membrane potential is important for bacterial cell division. _Proc. Natl Acad. Sci. USA_ 107, 12281–12286


(2010). Article  CAS  PubMed  PubMed Central  Google Scholar  * Reimold, C., Defeu Soufo, H. J., Dempwolff, F. & Graumann, P. L. Motion of variable-length MreB filaments at the bacterial


cell membrane influences cell morphology. _Mol. Biol. Cell_ 24, 2340–2349 (2013). Article  CAS  PubMed  PubMed Central  Google Scholar  * Kawai, Y., Mercier, R. & Errington, J.


Bacterial cell morphogenesis does not require a preexisting template structure. _Curr. Biol._ 24, 863–867 (2014). Article  CAS  PubMed  PubMed Central  Google Scholar  * Schaechter, M.,


Maaloe, O. & Kjelgaard, N. O. Dependency on medium and temperature on cell size and chemical coposition during balanced growth of _Salmonella typhimurium_. _J. Gen. Microbiol._ 19,


592–606 (1958). Article  CAS  PubMed  Google Scholar  * Olshausen, P. V. et al. Superresolution imaging of dynamic MreB filaments in _B. subtilis_—a multiple-motor-driven transport?


_Biophys. J._ 105, 1171–1181 (2013). Article  PubMed  PubMed Central  CAS  Google Scholar  * Ursell, T. S. et al. Rod-like bacterial shape is maintained by feedback between cell curvature


and cytoskeletal localization. _Proc. Natl Acad. Sci. USA_ 111, E1025–E1034 (2014). Article  CAS  PubMed  PubMed Central  Google Scholar  * Wang, S. & Wingreen, N. S. Cell shape can


mediate the spatial organization of the bacterial cytoskeleton. _Biophys. J._ 104, 541–552 (2013). Article  CAS  PubMed  PubMed Central  Google Scholar  * Huang, K. C., Mukhopadhyay, R.,


Wen, B., Gitai, Z. & Wingreen, N. S. Cell shape and cell-wall organization in Gram-negative bacteria. _Proc. Natl Acad. Sci. USA_ 105, 19282–19287 (2008). Article  CAS  PubMed  PubMed


Central  Google Scholar  * Kuru, E. et al. _In situ_ probing of newly synthesized peptidoglycan in live bacteria with fluorescent D-amino acids. _Angew. Chem. Int. Ed. Engl._ 51, 12519–12523


(2012). Article  CAS  PubMed  PubMed Central  Google Scholar  * Lebar, M. D. et al. Reconstitution of peptidoglycan cross-linking leads to improved fluorescent probes of cell wall


synthesis. _J. Am. Chem. Soc._ 136, 10874–10877 (2014). Article  CAS  PubMed  PubMed Central  Google Scholar  * Typas, A., Banzhaf, M., Gross, C. A. & Vollmer, W. From the regulation of


peptidoglycan synthesis to bacterial growth and morphology. _Nature Rev. Microbiol._ 10, 123–136 (2012). Article  CAS  Google Scholar  * Lovering, A. L., Safadi, S. S. & Strynadka, N. C.


Structural perspective of peptidoglycan biosynthesis and assembly. _Annu. Rev. Biochem._ 81, 451–478 (2012). Article  CAS  PubMed  Google Scholar  * Cava, F. & de Pedro, M. A.


Peptidoglycan plasticity in bacteria: emerging variability of the murein sacculus and their associated biological functions. _Curr. Opin. Microbiol._ 18, 46–53 (2014). Article  CAS  PubMed 


Google Scholar  * Kandler, O. Cell wall biochemistry in Archaea and its phylogenetic implications. _J. Biol. Phys._ 20, 165–169 (1994). Article  CAS  Google Scholar  * Barreteau, H. et al.


Cytoplasmic steps of peptidoglycan biosynthesis. _FEMS Microbiol. Rev._ 32, 168–207 (2008). Article  CAS  PubMed  Google Scholar  * Vollmer, W., Joris, B., Charlier, P. & Foster, S.


Bacterial peptidoglycan (murein) hydrolases. _FEMS Microbiol. Rev._ 32, 259–286 (2008). Article  CAS  PubMed  Google Scholar  Download references ACKNOWLEDGEMENTS Work on cell wall synthesis


in the Errington laboratory is supported by grant BB/G015902/1 from the UK Biotechnology and Biological Sciences Research Council. The author thanks W. Vollmer, L. J. Wu and K. Gerdes for


helpful discussions and comments on the manuscript. AUTHOR INFORMATION AUTHORS AND AFFILIATIONS * Jeff Errington is at the Centre for Bacterial Cell Biology, Medical Faculty, Newcastle


University, Richardson Road, Newcastle-upon-Tyne NE2 4AX, UK., Jeff Errington Authors * Jeff Errington View author publications You can also search for this author inPubMed Google Scholar


CORRESPONDING AUTHOR Correspondence to Jeff Errington. ETHICS DECLARATIONS COMPETING INTERESTS The author declares no competing financial interests. POWERPOINT SLIDES POWERPOINT SLIDE FOR


FIG. 1 POWERPOINT SLIDE FOR FIG. 2 POWERPOINT SLIDE FOR FIG. 3 POWERPOINT SLIDE FOR TABLE 1 RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Errington, J.


Bacterial morphogenesis and the enigmatic MreB helix. _Nat Rev Microbiol_ 13, 241–248 (2015). https://doi.org/10.1038/nrmicro3398 Download citation * Published: 12 January 2015 * Issue


Date: April 2015 * DOI: https://doi.org/10.1038/nrmicro3398 SHARE THIS ARTICLE Anyone you share the following link with will be able to read this content: Get shareable link Sorry, a


shareable link is not currently available for this article. Copy to clipboard Provided by the Springer Nature SharedIt content-sharing initiative