pH-dependent activation of cytokinesis modulates Escherichia coli cell size

Autoři: Elizabeth A. Mueller aff001;  Corey S. Westfall aff001;  Petra Anne Levin aff001
Působiště autorů: Department of Biology, Washington University in St. Louis, St. Louis, Missouri, United States of America aff001
Vyšlo v časopise: pH-dependent activation of cytokinesis modulates Escherichia coli cell size. PLoS Genet 16(3): e32767. doi:10.1371/journal.pgen.1008685
Kategorie: Research Article


Cell size is a complex trait, derived from both genetic and environmental factors. Environmental determinants of bacterial cell size identified to date primarily target assembly of cytosolic components of the cell division machinery. Whether certain environmental cues also impact cell size through changes in the assembly or activity of extracytoplasmic division proteins remains an open question. Here, we identify extracellular pH as a modulator of cell division and a significant determinant of cell size across evolutionarily distant bacterial species. In the Gram-negative model organism Escherichia coli, our data indicate environmental pH impacts the length at which cells divide by altering the ability of the terminal cell division protein FtsN to localize to the cytokinetic ring where it activates division. Acidic environments lead to enrichment of FtsN at the septum and activation of division at a reduced cell length. Alkaline pH inhibits FtsN localization and suppresses division activation. Altogether, our work reveals a previously unappreciated role for pH in bacterial cell size control.

Klíčová slova:

Bacterial evolution – Cell cycle and cell division – Cell walls – Cytokinesis – Glucose – Hyperexpression techniques – Periplasm – Phase contrast microscopy


1. Campos M, Surovtsev IV, Kato S, Paintdakhi A, Beltran B, Ebmeier SE, et al. A constant size extension drives bacterial cell size homeostasis. Cell. 2014;159: 1433–1446. doi: 10.1016/j.cell.2014.11.022 25480302

2. Taheri-Araghi S, Bradde S, Sauls JT, Hill NS, Levin PA, Paulsson J, et al. Cell-Size Control and Homeostasis in Bacteria. Curr Biol. 2017;27: 1392. doi: 10.1016/j.cub.2017.04.028 28486111

3. Si F, Le Treut G, Sauls JT, Vadia S, Levin PA, Jun S. Mechanistic Origin of Cell-Size Control and Homeostasis in Bacteria. Curr Biol. 2019;29: 1760–1770.e7. doi: 10.1016/j.cub.2019.04.062 31104932

4. Weart RB, Lee AH, Chien A-C, Haeusser DP, Hill NS, Levin PA. A metabolic sensor governing cell size in bacteria. Cell. 2007;130: 335–347. doi: 10.1016/j.cell.2007.05.043 17662947

5. Hill NS, Buske PJ, Shi Y, Levin PA. A moonlighting enzyme links Escherichia coli cell size with central metabolism. Casadesús J, editor. PLoS Genet. 2013;9: e1003663. doi: 10.1371/journal.pgen.1003663 23935518

6. Fantes P, Nurse P. Control of cell size at division in fission yeast by a growth-modulated size control over nuclear division. Exp Cell Res. 1977;107: 377–386. doi: 10.1016/0014-4827(77)90359-7 872891

7. Bachmann BJ. Pedigrees of some mutant strains of Escherichia coli K-12. Bacteriol Rev. American Society for Microbiology (ASM); 1972;36: 525–557.

8. Casadaban MJ. Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu. J Mol Biol. 1976;104: 541–555. doi: 10.1016/0022-2836(76)90119-4 781293

9. Vadia S, Tse JL, Lucena R, Yang Z, Kellogg DR, Wang JD, et al. Fatty Acid Availability Sets Cell Envelope Capacity and Dictates Microbial Cell Size. Curr Biol. 2017;27: 1757–1767.e5. doi: 10.1016/j.cub.2017.05.076 28602657

10. Billaudeau C, Chastanet A, Yao Z, Cornilleau C, Mirouze N, Fromion V, et al. Contrasting mechanisms of growth in two model rod-shaped bacteria. Nature Communications 2016 7. Nature Publishing Group; 2017;8: 15370. doi: 10.1038/ncomms15370 28589952

11. Monahan LG, Hajduk IV, Blaber SP, Charles IG, Harry EJ. Coordinating bacterial cell division with nutrient availability: a role for glycolysis. Gottesman S, editor. MBio. 3rd ed. 2014;5: e00935–14. doi: 10.1128/mBio.00935-14 24825009

12. Westfall CS, Levin PA. Comprehensive analysis of central carbon metabolism illuminates connections between nutrient availability, growth rate, and cell morphology in Escherichia coli. Søgaard-Andersen L, editor. PLoS Genet. Public Library of Science; 2018;14: e1007205. doi: 10.1371/journal.pgen.1007205 29432413

13. Aarsman MEG, Piette A, Fraipont C, Vinkenvleugel TMF, Nguyen-Distèche M, Blaauwen den T. Maturation of the Escherichia coli divisome occurs in two steps. Mol Microbiol. John Wiley & Sons, Ltd (10.1111); 2005;55: 1631–1645. doi: 10.1111/j.1365-2958.2005.04502.x 15752189

14. Haeusser DP, Margolin W. Splitsville: structural and functional insights into the dynamic bacterial Z ring. Nature Reviews Microbiology 2011 10:2. Nature Publishing Group; 2016;14: 305–319. doi: 10.1038/nrmicro.2016.26 27040757

15. Slonczewski JL, Rosen BP, Alger JR, Macnab RM. pH homeostasis in Escherichia coli: measurement by 31P nuclear magnetic resonance of methylphosphonate and phosphate. Proc Natl Acad Sci USA. National Academy of Sciences; 1981;78: 6271–6275.

16. Wilks JC, Slonczewski JL. pH of the cytoplasm and periplasm of Escherichia coli: rapid measurement by green fluorescent protein fluorimetry. J Bacteriol. American Society for Microbiology; 2007;189: 5601–5607. doi: 10.1128/JB.00615-07 17545292

17. Chakraborty S, Winardhi RS, Morgan LK, Yan J, Kenney LJ. Non-canonical activation of OmpR drives acid and osmotic stress responses in single bacterial cells. Nature Communications 2016 7. Nature Publishing Group; 2017;8: 1587. doi: 10.1038/s41467-017-02030-0 29138484

18. Ishino F, Jung HK, Ikeda M, Doi M, Wachi M, Matsuhashi M. New mutations fts-36, lts-33, and ftsW clustered in the mra region of the Escherichia coli chromosome induce thermosensitive cell growth and division. J Bacteriol. American Society for Microbiology Journals; 1989;171: 5523–5530. doi: 10.1128/jb.171.10.5523-5530.1989

19. Modell JW, Kambara TK, Perchuk BS, Laub MT. A DNA damage-induced, SOS-independent checkpoint regulates cell division in Caulobacter crescentus. Michel B, editor. PLoS Biol. 2014;12: e1001977. doi: 10.1371/journal.pbio.1001977 25350732

20. Liu B, Persons L, Lee L, de Boer PAJ. Roles for both FtsA and the FtsBLQ subcomplex in FtsN-stimulated cell constriction in Escherichia coli. Mol Microbiol. Wiley/Blackwell (10.1111); 2015;95: 945–970. doi: 10.1111/mmi.12906 25496160

21. Tsang M-J, Bernhardt TG. A role for the FtsQLB complex in cytokinetic ring activation revealed by an ftsL allele that accelerates division. Mol Microbiol. John Wiley & Sons, Ltd (10.1111); 2015;95: 925–944. doi: 10.1111/mmi.12905 25496050

22. Lambert A, Vanhecke A, Archetti A, Holden S, Schaber F, Pincus Z, et al. Constriction Rate Modulation Can Drive Cell Size Control and Homeostasis in C. crescentus. iScience. 2018;4: 180–189. doi: 10.1016/j.isci.2018.05.020 30240739

23. Bilobrov VM, Chugaj AV, Bessarabov VI. Urine pH variation dynamics in healthy individuals and stone formers. Urol Int. Karger Publishers; 1990;45: 326–331. doi: 10.1159/000281730 2288048

24. Watson BW, Meldrum SJ, Riddle HC, Brown RL, Sladen GE. pH profile of gut as measured by radiotelemetry capsule. Br Med J. BMJ Publishing Group; 1972;2: 104–106.

25. Perez AJ, Cesbron Y, Shaw SL, Bazan Villicana J, Tsui H-CT, Boersma MJ, et al. Movement dynamics of divisome proteins and PBP2x:FtsW in cells of Streptococcus pneumoniae. Proc Natl Acad Sci USA. 2019;116: 3211–3220. doi: 10.1073/pnas.1816018116 30718427

26. Heinrich K, Leslie DJ, Morlock M, Bertilsson S, Jonas K. Molecular Basis and Ecological Relevance of Caulobacter Cell Filamentation in Freshwater Habitats. Justice S, editor. MBio. American Society for Microbiology; 2019;10: 162. doi: 10.1128/mBio.01557-19 31431551

27. Hale CA, de Boer PA. Direct binding of FtsZ to ZipA, an essential component of the septal ring structure that mediates cell division in E. coli. Cell. 1997;88: 175–185. doi: 10.1016/s0092-8674(00)81838-3 9008158

28. Coltharp C, Buss J, Plumer TM, Xiao J. Defining the rate-limiting processes of bacterial cytokinesis. Proc Natl Acad Sci USA. National Academy of Sciences; 2016;113: E1044–53. doi: 10.1073/pnas.1514296113 26831086

29. Yang X, Lyu Z, Miguel A, McQuillen R, Huang KC, Xiao J. GTPase activity-coupled treadmilling of the bacterial tubulin FtsZ organizes septal cell wall synthesis. Science. 2017;355: 744–747. doi: 10.1126/science.aak9995 28209899

30. Liu G, Draper GC, Donachie WD. FtsK is a bifunctional protein involved in cell division and chromosome localization in Escherichia coli. Mol Microbiol. John Wiley & Sons, Ltd (10.1111); 1998;29: 893–903. doi: 10.1046/j.1365-2958.1998.00986.x 9723927

31. Chen JC, Beckwith J. FtsQ, FtsL and FtsI require FtsK, but not FtsN, for co-localization with FtsZ during Escherichia coli cell division. Mol Microbiol. John Wiley & Sons, Ltd (10.1111); 2001;42: 395–413. doi: 10.1046/j.1365-2958.2001.02640.x 11703663

32. Guzman LM, Weiss DS, Beckwith J. Domain-swapping analysis of FtsI, FtsL, and FtsQ, bitopic membrane proteins essential for cell division in Escherichia coli. J Bacteriol. American Society for Microbiology Journals; 1997;179: 5094–5103. doi: 10.1128/jb.179.16.5094-5103.1997

33. Taguchi A, Welsh MA, Marmont LS, Lee W, Sjodt M, Kruse AC, et al. FtsW is a peptidoglycan polymerase that is functional only in complex with its cognate penicillin-binding protein. Nat Microbiol. Nature Publishing Group; 2019;2: a000414. doi: 10.1038/s41564-018-0345-x 30692671

34. Addinall SG, Cao C, Lutkenhaus J. FtsN, a late recruit to the septum in Escherichia coli. Mol Microbiol. John Wiley & Sons, Ltd (10.1111); 1997;25: 303–309. doi: 10.1046/j.1365-2958.1997.4641833.x 9282742

35. Gerding MA, Liu B, Bendezú FO, Hale CA, Bernhardt TG, de Boer PAJ. Self-enhanced accumulation of FtsN at Division Sites and Roles for Other Proteins with a SPOR domain (DamX, DedD, and RlpA) in Escherichia coli cell constriction. J Bacteriol. American Society for Microbiology Journals; 2009;191: 7383–7401. doi: 10.1128/JB.00811-09 19684127

36. Du S, Pichoff S, Lutkenhaus J. FtsEX acts on FtsA to regulate divisome assembly and activity. Proc Natl Acad Sci USA. 2016;113: E5052–61. doi: 10.1073/pnas.1606656113 27503875

37. Durand-Heredia JM, Yu HH, De Carlo S, Lesser CF, Janakiraman A. Identification and characterization of ZapC, a stabilizer of the FtsZ ring in Escherichia coli. J Bacteriol. American Society for Microbiology Journals; 2011;193: 1405–1413. doi: 10.1128/JB.01258-10 21216995

38. Hale CA, Shiomi D, Liu B, Bernhardt TG, Margolin W, Niki H, et al. Identification of Escherichia coli ZapC (YcbW) as a component of the division apparatus that binds and bundles FtsZ polymers. J Bacteriol. American Society for Microbiology Journals; 2011;193: 1393–1404. doi: 10.1128/JB.01245-10 21216997

39. Durand-Heredia J, Rivkin E, Fan G, Morales J, Janakiraman A. Identification of ZapD as a cell division factor that promotes the assembly of FtsZ in Escherichia coli. J Bacteriol. American Society for Microbiology Journals; 2012;194: 3189–3198. doi: 10.1128/JB.00176-12 22505682

40. Samaluru H, SaiSree L, Reddy M. Role of SufI (FtsP) in cell division of Escherichia coli: evidence for its involvement in stabilizing the assembly of the divisome. J Bacteriol. 2007;189: 8044–8052. doi: 10.1128/JB.00773-07 17766410

41. Bertsche U, Kast T, Wolf B, Fraipont C, Aarsman MEG, Kannenberg K, et al. Interaction between two murein (peptidoglycan) synthases, PBP3 and PBP1B, in Escherichia coli. Mol Microbiol. Wiley/Blackwell (10.1111); 2006;61: 675–690. doi: 10.1111/j.1365-2958.2006.05280.x 16803586

42. Banzhaf M, van den Berg van Saparoea B, Terrak M, Fraipont C, Egan A, Philippe J, et al. Cooperativity of peptidoglycan synthases active in bacterial cell elongation. Mol Microbiol. John Wiley & Sons, Ltd (10.1111); 2012;85: 179–194. doi: 10.1111/j.1365-2958.2012.08103.x 22606933

43. Bernhardt TG, de Boer PAJ. The Escherichia coli amidase AmiC is a periplasmic septal ring component exported via the twin-arginine transport pathway. Mol Microbiol. NIH Public Access; 2003;48: 1171–1182.

44. Schmidt KL, Peterson ND, Kustusch RJ, Wissel MC, Graham B, Phillips GJ, et al. A predicted ABC transporter, FtsEX, is needed for cell division in Escherichia coli. J Bacteriol. 2004;186: 785–793. doi: 10.1128/JB.186.3.785-793.2004 14729705

45. Du S, Pichoff S, Lutkenhaus J. FtsEX acts on FtsA to regulate divisome assembly and activity. Proc Natl Acad Sci USA. National Academy of Sciences; 2016;113: E5052–61. doi: 10.1073/pnas.1606656113 27503875

46. Mueller EA, Egan AJ, Breukink E, Vollmer W, Levin PA. Plasticity of Escherichia coli cell wall metabolism promotes fitness and antibiotic resistance across environmental conditions. eLife. eLife Sciences Publications Limited; 2019;8: 492. doi: 10.7554/eLife.40754 30963998

47. Ricard M, Hirota Y. Process of cellular division in Escherichia coli: physiological study on thermosensitive mutants defective in cell division. J Bacteriol. American Society for Microbiology (ASM); 1973;116: 314–322.

48. Dai K, Xu Y, Lutkenhaus J. Cloning and characterization of ftsN, an essential cell division gene in Escherichia coli isolated as a multicopy suppressor of ftsA12(Ts). J Bacteriol. 1993;175: 3790–3797. doi: 10.1128/jb.175.12.3790-3797.1993 8509333

49. Broome-Smith JK, Hedge PJ, Spratt BG. Production of thiol-penicillin-binding protein 3 of Escherichia coli using a two primer method of site-directed mutagenesis. EMBO J. European Molecular Biology Organization; 1985;4: 231–235.

50. Vischer NOE, Verheul J, Postma M, van den Berg van Saparoea B, Galli E, Natale P, et al. Cell age dependent concentration of Escherichia coli divisome proteins analyzed with ImageJ and ObjectJ. Front Microbiol. Frontiers; 2015;6: 586. doi: 10.3389/fmicb.2015.00586 26124755

51. Pichoff S, Du S, Lutkenhaus J. The bypass of ZipA by overexpression of FtsN requires a previously unknown conserved FtsN motif essential for FtsA-FtsN interaction supporting a model in which FtsA monomers recruit late cell division proteins to the Z ring. Mol Microbiol. Wiley/Blackwell (10.1111); 2015;95: 971–987. doi: 10.1111/mmi.12907 25496259

52. Busiek KK, Eraso JM, Wang Y, Margolin W. The early divisome protein FtsA interacts directly through its 1c subdomain with the cytoplasmic domain of the late divisome protein FtsN. J Bacteriol. 2012;194: 1989–2000. doi: 10.1128/JB.06683-11 22328664

53. Yahashiri A, Jorgenson MA, Weiss DS. Bacterial SPOR domains are recruited to septal peptidoglycan by binding to glycan strands that lack stem peptides. Proc Natl Acad Sci USA. 2015;112: 11347–11352. doi: 10.1073/pnas.1508536112 26305949

54. Pichoff S, Du S, Lutkenhaus J. Disruption of divisome assembly rescued by FtsN-FtsA interaction in Escherichia coli. Proc Natl Acad Sci USA. National Academy of Sciences; 2018;180: 201806450. doi: 10.1073/pnas.1806450115 29967164

55. Stoddard A, Rolland V. I see the light! Fluorescent proteins suitable for cell wall/apoplast targeting in Nicotiana benthamiana leaves. Plant Direct. 2019;3: e00112. doi: 10.1002/pld3.112 31245754

56. Baranova N, Radler P, Hernández-Rocamora VM, Alfonso C, López-Pelegrín M, Rivas G, et al. Diffusion and capture permits dynamic coupling between treadmilling FtsZ filaments and cell division proteins. Nat Microbiol. Nature Publishing Group; 2020;16: 38–11. doi: 10.1038/s41564-019-0657-5 31959972

57. Sekar K, Rusconi R, Sauls JT, Fuhrer T, Noor E, Nguyen J, et al. Synthesis and degradation of FtsZ quantitatively predict the first cell division in starved bacteria. Molecular Systems Biology. John Wiley & Sons, Ltd; 2018;14: e8623. doi: 10.15252/msb.20188623 30397005

58. Geissler B, Shiomi D, Margolin W. The ftsA* gain-of-function allele of Escherichia coli and its effects on the stability and dynamics of the Z ring. Microbiology (Reading, Engl). Microbiology Society; 2007;153: 814–825. doi: 10.1099/mic.0.2006/001834-0 17322202

59. Krupka M, Rowlett VW, Morado D, Vitrac H, Schoenemann K, Liu J, et al. Escherichia coli FtsA forms lipid-bound minirings that antagonize lateral interactions between FtsZ protofilaments. Nature Communications 2016 7. Nature Publishing Group; 2017;8: 305–12. doi: 10.1038/ncomms15957 28695917

60. Bernard CS, Sadasivam M, Shiomi D, Margolin W. An altered FtsA can compensate for the loss of essential cell division protein FtsN in Escherichia coli. Mol Microbiol. John Wiley & Sons, Ltd (10.1111); 2007;64: 1289–1305. doi: 10.1111/j.1365-2958.2007.05738.x 17542921

61. SCHAECHTER M, MAALOE O, KJELDGAARD NO. Dependency on medium and temperature of cell size and chemical composition during balanced grown of Salmonella typhimurium. J Gen Microbiol. Microbiology Society; 1958;19: 592–606. doi: 10.1099/00221287-19-3-592 13611202

62. Ursell T, Lee TK, Shiomi D, Shi H, Tropini C, Monds RD, et al. Rapid, precise quantification of bacterial cellular dimensions across a genomic-scale knockout library. BMC Biol. BioMed Central; 2017;15: 17–15. doi: 10.1186/s12915-017-0348-8 28222723

63. Campos M, Govers SK, Irnov I, Dobihal GS, Cornet F, Jacobs-Wagner C. Genomewide phenotypic analysis of growth, cell morphogenesis, and cell cycle events in Escherichia coli. Molecular Systems Biology. John Wiley & Sons, Ltd; 2018;14: e7573. doi: 10.15252/msb.20177573 29941428

64. Boes A, Olatunji S, Breukink E, Terrak M. Regulation of the Peptidoglycan Polymerase Activity of PBP1b by Antagonist Actions of the Core Divisome Proteins FtsBLQ and FtsN. den Blaauwen T, Salama NR, editors. MBio. 2019;10: 220. doi: 10.1128/mBio.01912-18 30622193

65. Draper GC, McLennan N, Begg K, Masters M, Donachie WD. Only the N-terminal domain of FtsK functions in cell division. J Bacteriol. American Society for Microbiology (ASM); 1998;180: 4621–4627.

66. Goehring NW, Robichon C, Beckwith J. Role for the nonessential N terminus of FtsN in divisome assembly. J Bacteriol. American Society for Microbiology Journals; 2007;189: 646–649. doi: 10.1128/JB.00992-06 17071748

67. Peters NT, Dinh T, Bernhardt TG. A Fail-Safe Mechanism in the Septal Ring Assembly Pathway Generated by the Sequential Recruitment of Cell Separation Amidases and Their Activators. J Bacteriol. American Society for Microbiology Journals; 2011;193: 4973–4983. doi: 10.1128/JB.00316-11 21764913

68. Goehring NW, Gueiros-Filho F, Beckwith J. Premature targeting of a cell division protein to midcell allows dissection of divisome assembly in Escherichia coli. Genes Dev. 2005;19: 127–137. doi: 10.1101/gad.1253805 15630023

69. Corbin BD, Geissler B, Sadasivam M, Margolin W. Z-ring-independent interaction between a subdomain of FtsA and late septation proteins as revealed by a polar recruitment assay. J Bacteriol. 2004;186: 7736–7744. doi: 10.1128/JB.186.22.7736-7744.2004 15516588

70. Daley DO, Skoglund U, Söderström B. FtsZ does not initiate membrane constriction at the onset of division. Sci Rep. Nature Publishing Group; 2016;6: 33138. doi: 10.1038/srep33138 27609565

71. Wissel MC, Weiss DS. Genetic analysis of the cell division protein FtsI (PBP3): amino acid substitutions that impair septal localization of FtsI and recruitment of FtsN. J Bacteriol. American Society for Microbiology Journals; 2004;186: 490–502. doi: 10.1128/jb.186.2.490-502.2004

72. Busiek KK, Margolin W. A role for FtsA in SPOR-independent localization of the essential Escherichia coli cell division protein FtsN. Mol Microbiol. John Wiley & Sons, Ltd (10.1111); 2014;92: 1212–1226. doi: 10.1111/mmi.12623 24750258

73. Yang X, McQuillen R, Lyu Z, Phillips-Mason P, La Cruz De A, McCausland JW, et al. FtsW exhibits distinct processive movements driven by either septal cell wall synthesis or FtsZ treadmilling in E. coli. bioRxiv. Cold Spring Harbor Laboratory; 2019;1: 850073. doi: 10.1101/850073

74. Müller P, Ewers C, Bertsche U, Anstett M, Kallis T, Breukink E, et al. The essential cell division protein FtsN interacts with the murein (peptidoglycan) synthase PBP1B in Escherichia coli. J Biol Chem. 2007;282: 36394–36402. doi: 10.1074/jbc.M706390200 17938168

75. Pazos M, Peters K, Casanova M, Palacios P, VanNieuwenhze M, Breukink E, et al. Z-ring membrane anchors associate with cell wall synthases to initiate bacterial cell division. Nature Communications 2016 7. Nature Publishing Group; 2018;9: 5090–12. doi: 10.1038/s41467-018-07559-2 30504892

76. Cho H, Wivagg CN, Kapoor M, Barry Z, Rohs PDA, Suh H, et al. Bacterial cell wall biogenesis is mediated by SEDS and PBP polymerase families functioning semi-autonomously. Nat Microbiol. 2016;1: 16172–33. doi: 10.1038/nmicrobiol.2016.172 27643381

77. Morè N, Martorana AM, Biboy J, Otten C, Winkle M, Serrano CKG, et al. Peptidoglycan Remodeling Enables Escherichia coli To Survive Severe Outer Membrane Assembly Defect. Kline KA, editor. MBio. 2019;10: a000414. doi: 10.1128/mBio.02729-18 30723128

78. Vigouroux A, Cordier B, Aristov A, Oldewurtel E, Özbaykal G, Chaze T, et al. Cell-wall synthases contribute to bacterial cell-envelope integrity by actively repairing defects. bioRxiv. Cold Spring Harbor Laboratory; 2019;98: 763508. doi: 10.1101/763508

79. van Straaten KE, Dijkstra BW, Vollmer W, Thunnissen A-MWH. Crystal structure of MltA from Escherichia coli reveals a unique lytic transglycosylase fold. J Mol Biol. 2005;352: 1068–1080. doi: 10.1016/j.jmb.2005.07.067 16139297

80. Peters K, Kannan S, Rao VA, Biboy J, Vollmer D, Erickson SW, et al. The Redundancy of Peptidoglycan Carboxypeptidases Ensures Robust Cell Shape Maintenance in Escherichia coli. MBio. 2016;7: e00819–16. doi: 10.1128/mBio.00819-16 27329754

81. Castanheira S, Cestero JJ, Rico-Pérez G, García P, Cava F, Ayala JA, et al. A Specialized Peptidoglycan Synthase PromotesSalmonellaCell Division inside Host Cells. Sansonetti PJ, editor. MBio. American Society for Microbiology; 2017;8: e01685–17. doi: 10.1128/mBio.01685-17 29259085

82. Meiresonne NY, Consoli E, Mertens LMY, Chertkova AO, Goedhart J, Blaauwen den T. Superfolder mTurquoise2ox optimized for the bacterial periplasm allows high efficiency in vivo FRET of cell division antibiotic targets. Mol Microbiol. 2019;111: 1025–1038. doi: 10.1111/mmi.14206 30648295

83. Weart RB, Levin PA. Growth rate-dependent regulation of medial FtsZ ring formation. J Bacteriol. 2003;185: 2826–2834. doi: 10.1128/JB.185.9.2826-2834.2003 12700262

84. Modell JW, Hopkins AC, Laub MT. A DNA damage checkpoint in Caulobacter crescentus inhibits cell division through a direct interaction with FtsW. Genes Dev. Cold Spring Harbor Lab; 2011;25: 1328–1343. doi: 10.1101/gad.2038911 21685367

85. Geissler B, Elraheb D, Margolin W. A gain-of-function mutation in ftsA bypasses the requirement for the essential cell division gene zipA in Escherichia coli. Proceedings of the National Academy of Sciences. 2003;100: 4197–4202. doi: 10.1073/pnas.0635003100 12634424

86. Pazos M, Peters K, Vollmer W. Robust peptidoglycan growth by dynamic and variable multi-protein complexes. Curr Opin Microbiol. 2017;36: 55–61. doi: 10.1016/j.mib.2017.01.006 28214390

87. Reddy M. Role of FtsEX in cell division of Escherichia coli: viability of ftsEX mutants is dependent on functional SufI or high osmotic strength. J Bacteriol. American Society for Microbiology Journals; 2007;189: 98–108. doi: 10.1128/JB.01347-06 17071757

88. Dai X, Zhu M. High Osmolarity Modulates Bacterial Cell Size through Reducing Initiation Volume in Escherichia coli. Bowman GR, editor. mSphere. American Society for Microbiology Journals; 2018;3: R340. doi: 10.1128/mSphere.00430-18 30355666

89. Peters K, Pazos M, Edoo Z, Hugonnet J-E, Martorana AM, Polissi A, et al. Copper inhibits peptidoglycan LD-transpeptidases suppressing β-lactam resistance due to bypass of penicillin-binding proteins. Proc Natl Acad Sci USA. 2018;115: 10786–10791. doi: 10.1073/pnas.1809285115 30275297

90. Murphy SG, Alvarez L, Adams MC, Liu S, Chappie JS, Cava F, et al. Endopeptidase Regulation as a Novel Function of the Zur-Dependent Zinc Starvation Response. Salama NR, editor. MBio. 2019;10: 161. doi: 10.1128/mBio.02620-18 30782657

91. Lonergan ZR, Nairn BL, Wang J, Hsu Y-P, Hesse LE, Beavers WN, et al. An Acinetobacter baumannii, Zinc-Regulated Peptidase Maintains Cell Wall Integrity during Immune-Mediated Nutrient Sequestration. Cell Rep. 2019;26: 2009–2018.e6. doi: 10.1016/j.celrep.2019.01.089 30784584

92. Stylianidou S, Brennan C, Nissen SB, Kuwada NJ, Wiggins PA. SuperSegger: robust image segmentation, analysis and lineage tracking of bacterial cells. Mol Microbiol. Wiley/Blackwell (10.1111); 2016;102: 690–700. doi: 10.1111/mmi.13486 27569113

93. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. Nature Publishing Group; 2012;9: 676–682. doi: 10.1038/nmeth.2019 22743772

Článek vyšel v časopise

PLOS Genetics

2020 Číslo 3
Nejčtenější tento týden
Nejčtenější v tomto čísle

Zvyšte si kvalifikaci online z pohodlí domova

Hypertenze a hypercholesterolémie – synergický efekt léčby
nový kurz
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Multidisciplinární zkušenosti u pacientů s diabetem
Autoři: Prof. MUDr. Martin Haluzík, DrSc., prof. MUDr. Vojtěch Melenovský, CSc., prof. MUDr. Vladimír Tesař, DrSc.

Úloha kombinovaných preparátů v léčbě arteriální hypertenze
Autoři: prof. MUDr. Martin Haluzík, DrSc.

Autoři: MUDr. Ladislav Korábek, CSc., MBA

Terapie roztroušené sklerózy v kostce
Autoři: MUDr. Dominika Šťastná, Ph.D.

Všechny kurzy
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.


Nemáte účet?  Registrujte se