Advertisement

Antonie van Leeuwenhoek

, Volume 112, Issue 2, pp 145–157 | Cite as

Prokaryotic cytoskeletons: in situ and ex situ structures and cellular locations

  • Ki Woo KimEmail author
Review Paper

Abstract

Cytoskeletons have long been perceived to be present only in eukaryotes. However, this notion changed drastically in the 1990s, with observations of cytoskeleton-like structures in several prokaryotes. Homologs of the main components of eukaryotic cytoskeletons, such as microtubules, microfilaments, and intermediate filaments, have been identified in bacteria and archaea. Tubulin homologs include filamenting temperature-sensitive mutant Z (FtsZ), bacterial tubulin A/B (BtubA/B), and tubulin/FtsZ-like protein (TubZ), whereas actin homologs comprise murein region B (MreB) and crenactin. Unlike other proteins, crescentin (CreS) is a homolog of intermediate filaments. Recent findings elucidated their localization, structural organization, and helical properties in prokaryotes, thus revising traditional models. FtsZ is involved in cell division, forming a bundle of overlapping filaments that cover the entire division plane. Cryogenic transmission electron microscopy identified tubular structures of BtubA/B that were not previously identified using conventional ultrathin plastic sections. TubZ generates two joint filaments to form a quadruplex structure. After a long debate, MreB, a cell shape determinant, was shown to form filament stretches that move circumferentially around rod-shaped bacteria. Initially characterized as single-stranded, crenactin was eventually identified as right-handed double-stranded helical filaments. CreS, another cell shape determinant, forms filament bundles located inside the inner membrane of the concave side of cells. These observations suggest that the use of in situ or ex situ microscopy in combination with structural analysis techniques will enable the elucidation and further understanding of the current models of prokaryotic cytoskeletons.

Keywords

Cytoskeleton Prokaryotes Microscopy 

Notes

Conflict of interest

The author declares that there is no conflict of interest.

References

  1. Amo T, Paje MLF, Inagaki A, Ezaki S, Atomi H, Imanaka T (2002) Pyrobaculum calidifontis sp. nov., a novel hyperthermophilic archaeon that grows in atmospheric air. Archaea 1:113–121CrossRefGoogle Scholar
  2. Ausmees N, Kuhn JR, Jacobs-Wagner C (2003) The bacterial cytoskeleton: an intermediate filament-like function in cell shape. Cell 115:705–713CrossRefGoogle Scholar
  3. Aylett CHS, Wang Q, Michie KA, Amos LA, Löwe J (2010) Filament structure of bacterial tubulin homologue TubZ. Proc Natl Acad Sci USA 107:19766–19771CrossRefGoogle Scholar
  4. Bagchi S, Tomenius H, Belova LM, Ausmees N (2008) Intermediate filament-like proteins in bacteria and a cytoskeletal function in Streptomyces. Mol Micobiol 70:1037–1050Google Scholar
  5. Bi E, Lutkenhaus J (1991) FtsZ ring structure associated with division in Escherichia coli. Nature 354:161–164CrossRefGoogle Scholar
  6. Braun T, Orlova A, Valegård K, Lindås A-C, Schröder GF, Egelman EH (2015) Archaeal actin from a hyperthermophile forms a single-stranded filament. Proc Natl Acad Sci USA 112:9340–9345CrossRefGoogle Scholar
  7. Briegel A, Dias DP, Li Z, Jensen RB, Frangakis AS, Jensen GJ (2006) Multiple large filament bundles observed in Caulobacter crescentus by electron cryotomography. Mol Microbiol 62:5–14CrossRefGoogle Scholar
  8. Briegel A, Oikonomou CM, Chang Y-W, Kjær A, Huang AN, Kim KW, Ghosal D, Nguyen HH, Kenney D, Loo RRO, Gunsalus RP, Jensen GJ (2017) Morphology of the archaellar motor and associated cytoplasmic cone in Thermococcus kodakaraensis. EMBO Rep 18:1660–1670CrossRefGoogle Scholar
  9. Cabeen MT, Jacobs-Wagner C (2010) The bacterial cytoskeleton. Annu Rev Genet 44:365–392CrossRefGoogle Scholar
  10. Carballido-López R, Errington J (2003) A dynamic bacterial cytoskeleton. Trends Cell Biol 13:577–583CrossRefGoogle Scholar
  11. Celler K, Koning RI, Koster AJ, van Wezel GP (2013) Multidimensional view of the bacterial cytoskeleton. J Bacteriol 195:1627–1636CrossRefGoogle Scholar
  12. Charbon G, Cabeen MT, Jacobs-Wagner C (2009) Bacterial intermediate filaments: in vivo assembly, organization, and dynamics of crescentin. Genes Dev 23:1131–1144CrossRefGoogle Scholar
  13. de Boer P, Crossley R, Rothfield L (1992) The essential bacterial cell division protein FtsZ is a GTPase. Nature 359:254–256CrossRefGoogle Scholar
  14. Doi M, Wachi M, Ishino F, Tomioka S, Ito M, Sakagami Y, Suzuki A, Matsuhashi M (1988) 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 170:4619–4624CrossRefGoogle Scholar
  15. Erickson HP (2017) The discovery of the prokaryotic cytoskeleton: 25th anniversary. Mol Biol Cell 28:357–358CrossRefGoogle Scholar
  16. Errington J (2015) Bacterial morphogenesis and the enigmatic MreB helix. Nat Rev Microbiol 13:241–248CrossRefGoogle Scholar
  17. Eun Y-J, Kapoor M, Hussain S, Garner EC (2015) Bacterial filament systems: toward understanding their emergent behavior and cellular functions. J Biol Chem 290:17181–17189CrossRefGoogle Scholar
  18. Fink G, Szewczak-Harris A, Löwe J (2016) The bacterial cytoskeleton. Cell 166:522CrossRefGoogle Scholar
  19. Fletcher DA, Mullins RD (2010) Cell mechanics and the cytoskeleton. Nature 463:485–492CrossRefGoogle Scholar
  20. Fuentes-Pérez ME, Núñez-Ramírez R, Martín-González A, Juan-Rodríguez D, Llorca O, Moreno-Herrero F, Oliva M (2017) TubZ filament assembly dynamics requires the flexible C-terminal tail. Sci Rep 7:43342CrossRefGoogle Scholar
  21. Fujita J, Maeda Y, Mizohata E, Inoue T, Kaul M, Parhi AK, LaVoie EJ, Pilch DS, Matsumura H (2017) Structural flexibility of an inhibitor overcomes drug resistance mutations in Staphylococcus aureus FtsZ. ACS Chem Biol 12:1947–1955CrossRefGoogle Scholar
  22. Furutani M, Iida T, Yoshida T, Maruyama T (1998) Group II chaperonin in a thermophilic methanogen, Methanococcus thermolithotrophicus. Chaperone activity and filament-forming ability. J Biol Chem 273:28399–28407CrossRefGoogle Scholar
  23. Gitai Z (2007) Diversification and specialization of the bacterial cytoskeleton. Curr Opin Cell Biol 19:5–12CrossRefGoogle Scholar
  24. Haydon DJ, Stokes NR, Ure R, Galbraith G, Bennett JM, Brown DR, Baker PJ, Barynin VV, Rice DW, Sedelnikova SE, Heal JR, Sheridan JM, Aiwale ST, Chauhan PK, Srivastava A, Taneja A, Collins I, Errington J, Czaplewski LG (2008) An inhibitor of FtsZ with potent and selective anti-staphylococcal activity. Science 321:1673–1675CrossRefGoogle Scholar
  25. Hussain S, Wivagg CN, Szwedziak P, Wong F, Schaefer K, Izore T, Renner LD, Holmes MJ, Sun Y, Bisson-Filho AW, Walker S, Amir A, Löwe J, Garner EC (2018) MreB filaments align along greatest principal membrane curvature to orient cell wall synthesis. eLife 7:e32471CrossRefGoogle Scholar
  26. Izoré T, Duman R, Kureisaite-Ciziene D, Löwe J (2014) Crenactin from Pyrobaculum calidifontis is closely related to actin in structure and forms steep helical filaments. FEBS Lett 588:776–782CrossRefGoogle Scholar
  27. Izoré T, Kureisaite-Ciziene D, McLaughlin SH, Löwe J (2016) Crenactin forms actin-like double helical filaments regulated by arcadin-2. eLife 5:e21600CrossRefGoogle Scholar
  28. Larsen RA, Cusumano C, Fujioka A, Lim-Fong G, Patterson P, Pogliano J (2007) Treadmilling of a prokaryotic tubulin-like protein, TubZ, required for plasmid stability in Bacillus thuringiensis. Genes Dev 21:1340–1352CrossRefGoogle Scholar
  29. Li Z, Trimble MJ, Brun YV, Jensen GJ (2007) The structure of FtsZ filaments in vivo suggests a force-generating role in cell division. EMBO J 26:4694–4708CrossRefGoogle Scholar
  30. Lin Y, Zhang H, Zhu N, Wang X, Han Y, Chen M, Jiang J, Si S (2018) Identification of TB-E12 as a novel FtsZ inhibitor with anti-tuberculosis activity. Tuberculosis 110:79–85CrossRefGoogle Scholar
  31. Ma X, Ehrhardt DW, Margolin W (1996) Colocalization of cell division proteins FtsZ and FtsA to cytoskeletal structures in living Escherichia coli cells by using green fluorescent protein. Proc Natl Acad Sci USA 93:12998–13003CrossRefGoogle Scholar
  32. Merino F, Raunser S (2016) The mother of all actins. eLife 5:e23354Google Scholar
  33. Montababa E, Agard DA (2014) Bacterial tubulin TubZ-Bt transitions between a two-stranded intermediate and a four-stranded filament upon GTP hydrolysis. Proc Natl Acad Sci USA 111:3407–3412CrossRefGoogle Scholar
  34. Mukherjee A, Dai K, Lutkenhaus J (1993) Escherichia coli cell division protein FtsZ is a guanine nucleotide binding protein. Proc Natl Acad Sci USA 90:1053–1057CrossRefGoogle Scholar
  35. Pilhofer M, Jensen GJ (2013) The bacterial cytoskeleton: more than twisted filaments. Curr Opin Cell Biol 25:125–133CrossRefGoogle Scholar
  36. Pilhofer M, Ladinsky MS, McDowall AW, Petroni G, Jensen GJ (2011) Microtubules in Bacteria: ancient tubulins build a five-protofilament homolog of the eukaryotic cytoskeleton. PLoS Biol 9(12):e1001213CrossRefGoogle Scholar
  37. Pogliano J (2008) The bacterial cytoskeleton. Curr Opin Cell Biol 20:19–27CrossRefGoogle Scholar
  38. RayChaudhuri D, Park JT (1992) Escherichia coli cell-division gene ftsZ encodes a novel GTP-binding protein. Nature 359:251–254CrossRefGoogle Scholar
  39. Salje J, van den Ent F, de Boer P, Löwe J (2011) Direct membrane binding by bacterial actin MreB. Mol Cell 43:478–487CrossRefGoogle Scholar
  40. Schaffner-Barbero C, Martín-Fontecha M, Chacón P, Andreu JM (2012) Targeting the assembly of bacterial cell division protein FtsZ with small molecules. ACS Chem Biol 7:269–277CrossRefGoogle Scholar
  41. Shih Y-L, Rothfield L (2006) The bacterial cytoskeleton. Microbiol Mol Biol Rev 70:729–754CrossRefGoogle Scholar
  42. Souza W (2012) Prokaryotic cells: structural organization of the cytoskeleton and organelles. Mem Inst Oswaldo Cruz 107:283–293CrossRefGoogle Scholar
  43. Stokes NR, Baker N, Bennett JM, Berry J, Collins I, Czaplewski LG, Logan A, Macdonald R, MacLeod L, Peasley H, Mitchell JP, Nayal N, Yadav A, Srivastava A, Haydon DJ (2013) An improved small-molecule inhibitor of FtsZ with superior in vitro potency, drug-like properties, and in vivo efficacy. Antimicrob Agents Chemother 57:317–325CrossRefGoogle Scholar
  44. 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 194:6382–6386CrossRefGoogle Scholar
  45. Swulius MT, Chen S, Ding HJ, Li Z, Briegel A, Pilhofer M, Tocheva EI, Lybarger SR, Johnson TL, Sandkvist M, Jensen GJ (2011) Long helical filaments are not seen encircling cells in electron cryotomograms of rod-shaped bacteria. Biochem Biophys Res Commun 407:650–655CrossRefGoogle Scholar
  46. Trent JD, Kagawa HK, Yaoi T, Olle E, Zaluzec NJ (1997) Chaperonin filaments: the archaeal cytoskeleton? Proc Natl Acad Sci USA 94:5383–5388CrossRefGoogle Scholar
  47. Trent JD, Kagawa HK, Yaoi T (1998) The role of chaperonins in vivo: the next frontiers. Ann N Y Acad Sci 851:36–47CrossRefGoogle Scholar
  48. Usui K, Ishii N, Kawarabayasi Y, Yohda M (2004) Expression and biochemical characterization of two small heat shock proteins from the thermoacidophilic crenarchaeon Sulfolobus tokodaii strain 7. Prot Sci 13:134–144CrossRefGoogle Scholar
  49. Van den Ent F, Izoré T, Bharat TAM, Johnson CM, Löwe J (2014) Bacterial actin MreB forms antiparalle double filaments. eLife 3:e02634CrossRefGoogle Scholar
  50. Vats P, Rothfield L (2007) Duplication and segregation of the actin (MreB) cytoskeleton during the prokaryotic cell cycle. Proc Natl Acad Sci USA 104:17795–17800CrossRefGoogle Scholar
  51. Wagstaff J, Löwe J (2018) Prokaryotic cytoskeletons: protein filaments organizing small cells. Nat Rev Microbiol 16:187–201CrossRefGoogle Scholar
  52. Wettstein G, Bellaye PS, Micheau O, Bonniaud P (2012) Small heat shock proteins and the cytoskeleton: an essential interplay for cell integrity?. Int J Biochem Cell Biol 44:1680–1686CrossRefGoogle Scholar
  53. White CL, Gober JW (2012) MreB: pilot or passenger of cell wall synthesis?. Trends Microbiol 20:74–79CrossRefGoogle Scholar
  54. Wintrebert P (1913) La rotation immédiate de l’oeuf pondu et la rotation d’activation chez Discoglossus pictus. Otth C R Soc Biol 106:439–442Google Scholar
  55. Yao Q, Jewett AI, Chang Y-W, Oikonomou CM, Beeby M, Lancu CV, Briegel A, Ghosal D, Jensen GJ (2017) Short FtsZ filaments can drive asymmetric cell envelope constriction at the onset of bacterial cytokinesis. EMBO J 36:1577–1589CrossRefGoogle Scholar
  56. Yaoi T, Kagawa H, Trent JD (1998) Chaperonin filaments: their formation and an evaluation of methods for studying them. Arch Biochem Biophys 356:55–62CrossRefGoogle Scholar
  57. Zupan JR, Cameron TA, Anderson-Furgeson J, Zambryski PC (2013) Dynamic FtsA and FtsZ localization and outer membrane alterations during polar growth and cell division in Agrobacterium tumefaciens. Proc Natl Acad Sci USA 110:9060–9065CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.School of Ecology and Environmental SystemKyungpook National UniversitySangjuKorea
  2. 2.Tree Diagnostic CenterKyungpook National UniversitySangjuKorea

Personalised recommendations