Mini review Special Issues

RodZ: a key-player in cell elongation and cell division in Escherichia coli

  • Received: 28 August 2019 Accepted: 06 November 2019 Published: 07 November 2019
  • RodZ is required for determination of cell shape in rod-shaped bacterium, such as Escherichia coli. RodZ is a transmembrane protein and forms a supramolecular complex called the Rod complex with other proteins, such as MreB-actin and peptidoglycan synthesis enzymes (for e.g., PBP2). Deletion of the rodZ gene changes the cell shape from rod to round or ovoid. Another supramolecular complex called divisome that controls cell division mainly consists of FtsZ-tubulin. MreB directly interacts with FtsZ and this interaction is critical to trigger a transition from cell elongation to cell division. Recently, we found that RodZ also directly interacts with FtsZ, and RodZ recruits MreB to the divisome. Formation of the division ring, called Z ring, is delayed if RodZ does not interact with FtsZ, indicating that RodZ might facilitate the formation of the Z ring during the cell division process. In this mini-review, we have summarized the roles of RodZ in cell elongation and cell division, especially based on our recent study.

    Citation: Risa Ago, Daisuke Shiomi. RodZ: a key-player in cell elongation and cell division in Escherichia coli[J]. AIMS Microbiology, 2019, 5(4): 358-367. doi: 10.3934/microbiol.2019.4.358

    Related Papers:

  • RodZ is required for determination of cell shape in rod-shaped bacterium, such as Escherichia coli. RodZ is a transmembrane protein and forms a supramolecular complex called the Rod complex with other proteins, such as MreB-actin and peptidoglycan synthesis enzymes (for e.g., PBP2). Deletion of the rodZ gene changes the cell shape from rod to round or ovoid. Another supramolecular complex called divisome that controls cell division mainly consists of FtsZ-tubulin. MreB directly interacts with FtsZ and this interaction is critical to trigger a transition from cell elongation to cell division. Recently, we found that RodZ also directly interacts with FtsZ, and RodZ recruits MreB to the divisome. Formation of the division ring, called Z ring, is delayed if RodZ does not interact with FtsZ, indicating that RodZ might facilitate the formation of the Z ring during the cell division process. In this mini-review, we have summarized the roles of RodZ in cell elongation and cell division, especially based on our recent study.


    加载中

    Acknowledgments



    The work on RodZ was partly carried out in Dr. Hironori Niki's lab (National Institute of Genetics, Japan). The work in our lab was supported by the JSPS KAKENHI (Grant Numbers 24770191, 25117528, 15H01333, and 15H04731) and by the NIG-JOINT (2016-A1[40], 61A2017, 57A2018, and 60A2019).

    Conflict of interest



    The authors declare no conflict of interest in this review.

    [1] Szwedziak P, Löwe J (2013) Do the divisome and elongasome share a common evolutionary past? Curr Opin Microbiol 16: 745–751. doi: 10.1016/j.mib.2013.09.003
    [2] Blaauwen den T, de Pedro MA, Nguyen-Distèche M, et al. (2008) Morphogenesis of rod-shaped sacculi. FEMS Microbiol Rev 32: 321–344. doi: 10.1111/j.1574-6976.2007.00090.x
    [3] 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: 1321–1332. doi: 10.1111/j.1365-2958.2003.03936.x
    [4] Vats P, Rothfield L (2007) Duplication and segregation of the actin (MreB) cytoskeleton during the prokaryotic cell cycle. Proc Natl Acad Sci USA 104: 17795–17800. doi: 10.1073/pnas.0708739104
    [5] Vats P, Shih YL, Rothfield L (2009) Assembly of the MreB-associated cytoskeletal ring of Escherichia coli. Mol Microbiol 72: 170–182. doi: 10.1111/j.1365-2958.2009.06632.x
    [6] van der Ploeg R, Verheul J, Vischer NOE, et al. (2013) Colocalization and interaction between elongasome and divisome during a preparative cell division phase in Escherichia coli. Mol Microbiol 87: 1074–1087. doi: 10.1111/mmi.12150
    [7] Fenton AK, Gerdes K (2013) Direct interaction of FtsZ and MreB is required for septum synthesis and cell division in Escherichia coli. EMBO J 32: 1953–1965. doi: 10.1038/emboj.2013.129
    [8] Yoshii Y, Niki H, Shiomi D (2019) Division-site localization of RodZ is required for efficient Z ring formation in Escherichia coli. Mol Microbiol 111: 1229–1244. doi: 10.1111/mmi.14217
    [9] Shiomi D, Sakai M, Niki H (2008) Determination of bacterial rod shape by a novel cytoskeletal membrane protein. EMBO J 27: 3081–3091. doi: 10.1038/emboj.2008.234
    [10] Bendezú FO, Hale CA, Bernhardt TG, et al. (2009) RodZ (YfgA) is required for proper assembly of the MreB actin cytoskeleton and cell shape in E. coli. EMBO J 28: 193–204. doi: 10.1038/emboj.2008.264
    [11] Alyahya SA, Alexander R, Costa T, et al. (2009) RodZ, a component of the bacterial core morphogenic apparatus. Proc Natl Acad Sci USa 106: 1239–1244. doi: 10.1073/pnas.0810794106
    [12] Bendezú FO, de Boer PAJ (2008) Conditional lethality, division defects, membrane involution, and endocytosis in mre and mrd shape mutants of Escherichia coli. J Bacteriol 190: 1792–811. doi: 10.1128/JB.01322-07
    [13] Muchová K, Chromiková Z, Barák I (2013) Control of Bacillus subtilis cell shape by RodZ. Environ Microbiol 15: 3259–3271. doi: 10.1111/1462-2920.12200
    [14] Okumura M, Narumi I, Nishida H (2019) Sensitivity of Deinococcus grandis rodZ deletion mutant to calcium ions results in enhanced spheroplast size. AIMS Microbiology 5: 176–185. doi: 10.3934/microbiol.2019.2.176
    [15] van den Ent F, Johnson CM, Persons L, et al. (2010) Bacterial actin MreB assembles in complex with cell shape protein RodZ. EMBO J 29: 1081–1090. doi: 10.1038/emboj.2010.9
    [16] Mitobe J, Yanagihara I, Ohnishi K, et al. (2011) RodZ regulates the post-transcriptional processing of the Shigella sonnei type III secretion system. EMBO Rep 12: 911–916. doi: 10.1038/embor.2011.132
    [17] Pereira AC, Paiva A, Saraiva IH, et al. (2015) Chemical shift assignments and secondary structure determination of the ectodomain of Bacillus subtilis morphogenic protein RodZ. Biomol NMR Assign 9: 285–288. doi: 10.1007/s12104-014-9593-8
    [18] Ikebe R, Kuwabara Y, Chikada T, et al. (2018) The periplasmic disordered domain of RodZ promotes its self-interaction in Escherichia coli. Genes Cells 23: 307–317. doi: 10.1111/gtc.12572
    [19] Daniel RA, Errington J (2003) Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell. Cell 113: 767–776. doi: 10.1016/S0092-8674(03)00421-5
    [20] Philippe J, Vernet T, Zapun A (2014) The elongation of ovococci. Microb Drug Resist 20: 215–221. doi: 10.1089/mdr.2014.0032
    [21] Jones LJ, Carballido-López R, Errington J (2001) Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis. Cell 104: 913–922. doi: 10.1016/S0092-8674(01)00287-2
    [22] Shih YL, 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. Proc Natl Acad Sci USA 100: 7865–7870. doi: 10.1073/pnas.1232225100
    [23] Bean GJ, Flickinger ST, Westler WM, et al. (2009) A22 disrupts the bacterial actin cytoskeleton by directly binding and inducing a low-affinity state in MreB. Biochemistry 48: 4852–4857. doi: 10.1021/bi900014d
    [24] Iwai N, Nagai K, 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. doi: 10.1271/bbb.66.2658
    [25] 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: 6382–6386. doi: 10.1128/JB.00505-12
    [26] Bratton BP, Shaevitz JW, Gitai Z, et al. (2018) MreB polymers and curvature localization are enhanced by RodZ and predict E. coli's cylindrical uniformity. Nat Commun 9: 2797.
    [27] Morgenstein RM, Bratton BP, Nguyen JP, et al. (2015) RodZ links MreB to cell wall synthesis to mediate MreB rotation and robust morphogenesis. Proc Natl Acad Sci USA 112: 12510–12515. doi: 10.1073/pnas.1509610112
    [28] van der Ploeg R, Goudelis ST, Blaauwen den T (2015) Validation of FRET assay for the screening of growth inhibitors of Escherichia coli reveals elongasome assembly dynamics. Int J Mol Sci 16: 17637–17654. doi: 10.3390/ijms160817637
    [29] Ursell TS, Nguyen J, Monds RD, et al. (2014) Rod-like bacterial shape is maintained by feedback between cell curvature and cytoskeletal localization. Proc Natl Acad Sci USA 111: E1025–E1034. doi: 10.1073/pnas.1317174111
    [30] Kawazura T, Matsumoto K, Kojima K, et al. (2017) Exclusion of assembled MreB by anionic phospholipids at cell poles confers cell polarity for bidirectional growth. Mol Microbiol 104: 472–486. doi: 10.1111/mmi.13639
    [31] Colavin A, Shi H, Huang KC (2018) RodZ modulates geometric localization of the bacterial actin MreB to regulate cell shape. Nat Commun 9: 1280. doi: 10.1038/s41467-018-03633-x
    [32] Dion MF, Kapoor M, Sun Y, et al. (2019) Bacillus subtilis cell diameter is determined by the opposing actions of two distinct cell wall synthetic systems. Nat Microbiol 24: 96.
    [33] Garner EC, Bernard R, Wang W, et al. (2011) Coupled, circumferential motions of the cell wall synthesis machinery and MreB filaments in B. subtilis. Science 333: 222–225.
    [34] Domínguez-Escobar J, Chastanet A, Crevenna AH, et al. (2011) Processive movement of MreB-associated cell wall biosynthetic complexes in bacteria. Science 333: 225–228. doi: 10.1126/science.1203466
    [35] van Teeffelen S, Wang S, Furchtgott L, et al. (2011) The bacterial actin MreB rotates, and rotation depends on cell-wall assembly. Proc Natl Acad Sci USA 108: 15822–15827. doi: 10.1073/pnas.1108999108
    [36] Shiomi D, Toyoda A, Aizu T, et al. (2013) Mutations in cell elongation genes mreB, mrdA and mrdB suppress the shape defect of RodZ-deficient cells. Mol Microbiol 87: 1029–1044. doi: 10.1111/mmi.12148
    [37] van den Ent F, Izoré T, Bharat TA, et al. (2014) Bacterial actin MreB forms antiparallel double filaments. Elife 2014: e02634.
    [38] Pinho MG, Kjos M, Veening JW (2013) How to get (a)round: mechanisms controlling growth and division of coccoid bacteria. Nat Rev Microbiol 11: 601–614. doi: 10.1038/nrmicro3088
    [39] Land AD, Winkler ME (2011) The requirement for pneumococcal MreC and MreD is relieved by inactivation of the gene encoding PBP1a. J Bacteriol 193: 4166–4179. doi: 10.1128/JB.05245-11
    [40] Tavares AC, Fernandes PB, Carballido-Lopez R, et al. (2015) MreC and MreD Proteins are not required for growth of Staphylococcus aureus. PLoS One 10: e0140523. doi: 10.1371/journal.pone.0140523
    [41] Ouellette SP, Karimova G, Subtil A, et al. (2012) Chlamydia co-opts the rod shape-determining proteins MreB and Pbp2 for cell division. Mol Microbiol 85: 164–178. doi: 10.1111/j.1365-2958.2012.08100.x
    [42] Ouellette SP, Rueden KJ, Gauliard E, et al. (2014) Analysis of MreB interactors in Chlamydia reveals a RodZ homolog but fails to detect an interaction with MraY. Front Microbiol 5: 279.
    [43] Kemege KE, Hickey JM, Barta ML, et al. (2015) Chlamydia trachomatis protein CT009 is a structural and functional homolog to the key morphogenesis component RodZ and interacts with division septal plane localized MreB. Mol Microbiol 95: 365–382. doi: 10.1111/mmi.12855
    [44] Niba ETE, Li G, Aoki K, et al. (2010) Characterization of rodZ mutants: RodZ is not absolutely required for the cell shape and motility. FEMS Microbiol Lett 309: 35–42.
    [45] Niba ETE, Naka Y, Nagase M, et al. (2007) A genome-wide approach to identify the genes involved in biofilm formation in E. coli. DNA Res 14: 237–246.
    [46] Jovanovic G, Mehta P, Ying L, et al. (2014) Anionic lipids and the cytoskeletal proteins MreB and RodZ define the spatio-temporal distribution and function of membrane stress controller PspA in Escherichia coli. Microbiology 160: 2374–2386. doi: 10.1099/mic.0.078527-0
    [47] van Beilen J, Blohmke CJ, Folkerts H, et al. (2016) RodZ and PgsA play intertwined roles in membrane homeostasis of Bacillus subtilis and resistance to weak organic acid stress. Front Microbiol 7: 1015–1012.
  • Reader Comments
  • © 2019 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)
通讯作者: 陈斌, bchen63@163.com
  • 1. 

    沈阳化工大学材料科学与工程学院 沈阳 110142

  1. 本站搜索
  2. 百度学术搜索
  3. 万方数据库搜索
  4. CNKI搜索

Metrics

Article views(4435) PDF downloads(653) Cited by(4)

Article outline

Figures and Tables

Figures(1)

Other Articles By Authors

/

DownLoad:  Full-Size Img  PowerPoint
Return
Return

Catalog