Advertisement

Overview of the Diverse Roles of Bacterial and Archaeal Cytoskeletons

  • Linda A. AmosEmail author
  • Jan LöweEmail author
Chapter
Part of the Subcellular Biochemistry book series (SCBI, volume 84)

Abstract

As discovered over the past 25 years, the cytoskeletons of bacteria and archaea are complex systems of proteins whose central components are dynamic cytomotive filaments. They perform roles in cell division, DNA partitioning, cell shape determination and the organisation of intracellular components. The protofilament structures and polymerisation activities of various actin-like, tubulin-like and ESCRT-like proteins of prokaryotes closely resemble their eukaryotic counterparts but show greater diversity. Their activities are modulated by a wide range of accessory proteins but these do not include homologues of the motor proteins that supplement filament dynamics to aid eukaryotic cell motility. Numerous other filamentous proteins, some related to eukaryotic IF-proteins/lamins and dynamins etc, seem to perform structural roles similar to those in eukaryotes.

Keywords

FtsZ Tubulin MreB ParM Actin TubZ ESCRT Bacterial cell division Archaea Cytomotive filaments Plasmid segregation Cell constriction Sliding filament motility Dynamic instability Treadmilling 

References

  1. Adams DW, Wu LJ, Errington J (2015) Nucleoid occlusion protein Noc recruits DNA to the bacterial cell membrane. EMBO J 34:491–501PubMedPubMedCentralCrossRefGoogle Scholar
  2. Agrebi R, Wartel M, Brochier-Armanet C, Mignot T (2015) An evolutionary link between capsular biogenesis and surface motility in bacteria. Nat Rev Microbiol 13:318–326PubMedCrossRefGoogle Scholar
  3. Agromayor M, Martin-Serrano J (2013) Knowing when to cut and run: mechanisms that control cytokinetic abscission. Trends Cell Biol 23:433–441PubMedCrossRefGoogle Scholar
  4. Alonso Y, Adell M, Migliano SM, Teis D (2016) ESCRT-III and Vps4: a dynamic multipurpose tool for membrane budding and scission. FEBS J 283(18):3288–3302CrossRefGoogle Scholar
  5. Amos LA (2008) The tektin family of microtubule-stabilizing proteins. Genome Biol 9:229PubMedPubMedCentralCrossRefGoogle Scholar
  6. Aylett CH, Löwe J (2012) Superstructure of the centromeric complex of TubZRC plasmid partitioning systems. Proc Natl Acad Sci U S A 109:16522–16527PubMedPubMedCentralCrossRefGoogle Scholar
  7. Aylett CH, Wang Q, Michie KA, Amos LA, Löwe J (2010) Filament structure of bacterial tubulin homologue TubZ. Proc Natl Acad Sci U S A 107:19766–19771PubMedPubMedCentralCrossRefGoogle Scholar
  8. Aylett CH, Löwe J, Amos LA (2011) New insights into the mechanisms of cytomotive actin and tubulin filaments. Int Rev Cell Mol Biol 292:1–71PubMedCrossRefGoogle Scholar
  9. Aylett CH, Izoré T, Amos LA, Löwe J (2013) Structure of the tubulin/FtsZ-like protein TubZ from Pseudomonas bacteriophage ΦKZ. J Mol Biol 425:2164–2173PubMedPubMedCentralCrossRefGoogle Scholar
  10. Bach JN, Albrecht N, Bramkamp M (2014) Imaging DivIVA dynamics using photo-convertible and activatable fluorophores in Bacillus subtilis. Front Microbiol 5:59PubMedPubMedCentralCrossRefGoogle Scholar
  11. Baek JH, Rajagopala SV, Chattoraj DK (2014) Chromosome segregation proteins of Vibrio cholerae as transcription regulators. MBio 5:e01061–e01014PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bagchi S, Tomenius H, Belova LM, Ausmees N (2008) Intermediate filament-like proteins in bacteria and a cytoskeletal function in Streptomyces. Mol Microbiol 70:1037–1050PubMedPubMedCentralGoogle Scholar
  13. Bailey MW, Bisicchia P, Warren BT, Sherratt DJ, Männik J (2014) Evidence for divisome localization mechanisms independent of the Min system and SlmA in Escherichia coli. PLoS Genet 10:e1004504PubMedPubMedCentralCrossRefGoogle Scholar
  14. Barry RM, Gitai Z (2011) Self-assembling enzymes and the origins of the cytoskeleton. Curr Opin Microbiol 14:704–711PubMedPubMedCentralCrossRefGoogle Scholar
  15. Baum DA, Baum B (2014) An inside-out origin for the eukaryotic cell. BMC Biol 12:76PubMedPubMedCentralCrossRefGoogle Scholar
  16. Beall B, Lutkenhaus J (1989) Nucleotide sequence and insertional inactivation of a Bacillus subtilis gene that affects cell division, sporulation, and temperature sensitivity. J Bacteriol 171:6821–6834PubMedPubMedCentralCrossRefGoogle Scholar
  17. Beuria TK et al (2009) Adenine nucleotide-dependent regulation of assembly of bacterial tubulin-like FtsZ by a hypermorph of bacterial actin-like FtsA. J Biol Chem 284:14079–14086PubMedPubMedCentralCrossRefGoogle Scholar
  18. Bharat TA, Murshudov GN, Sachse C, Löwe J (2015a) Structures of actin-like ParM filaments show architecture of plasmid-segregating spindles. Nature 523:106–110PubMedPubMedCentralCrossRefGoogle Scholar
  19. Bharat TA, Russo CJ, Löwe J, Passmore LA, Scheres SH (2015b) Advances in single-particle electron cryomicroscopy structure determination applied to sub-tomogram averaging. Structure 23:1743–1753PubMedPubMedCentralCrossRefGoogle Scholar
  20. Bisicchia P, Arumugam S, Schwille P, Sherratt D (2013) MinC, MinD, and MinE drive counter-oscillation of early-cell-division proteins prior to Escherichia coli septum formation. MBio 4:e00856–e00813PubMedPubMedCentralGoogle Scholar
  21. Bohuszewicz O, Liu J, Low HH (2016) Membrane remodelling in bacteria. J Struct Biol 196(1):3–14PubMedCrossRefGoogle Scholar
  22. Bramkamp M (2012) Structure and function of bacterial dynamin-like proteins. Biol Chem 393:1203–1214PubMedCrossRefGoogle Scholar
  23. Bramkamp M, Lopez D (2015) Exploring the existence of lipid rafts in bacteria. Microbiol Mol Biol Rev 79:81–100PubMedPubMedCentralCrossRefGoogle Scholar
  24. Braun T et al (2015) Archaeal actin from a hyperthermophile forms a single-stranded filament. Proc Natl Acad Sci U S A 112:9340–9345PubMedPubMedCentralCrossRefGoogle Scholar
  25. Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P (2008) Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol 6:245–252PubMedCrossRefGoogle Scholar
  26. Bush MJ, Tschowri N, Schlimpert S, Flärdh K, Buttner MJ (2015) c-di-GMP signalling and the regulation of developmental transitions in streptomycetes. Nat Rev Microbiol 13:749–760PubMedCrossRefGoogle Scholar
  27. Cabeen MT, Herrmann H, Jacobs-Wagner C (2011) The domain organization of the bacterial intermediate filament-like protein crescentin is important for assembly and function. Cytoskeleton (Hoboken) 68:205–219CrossRefGoogle Scholar
  28. Cavalier-Smith T (2010) Kingdoms Protozoa and Chromista and the eozoan root of the eukaryotic tree. Biol Lett 6:342–345PubMedCrossRefGoogle Scholar
  29. Chen S et al (2010) Electron cryotomography of bacterial cells. J Vis Exp 39:1943Google Scholar
  30. Chen Y, Milam SL, Erickson HP (2012) SulA inhibits assembly of FtsZ by a simple sequestration mechanism. Biochemistry 51:3100–3109PubMedPubMedCentralCrossRefGoogle Scholar
  31. Chen BW, Lin MH, Chu CH, Hsu CE, Sun YJ (2015) Insights into ParB spreading from the complex structure of Spo0J and parS. Proc Natl Acad Sci U S A 112:6613–6618PubMedPubMedCentralCrossRefGoogle Scholar
  32. Chernyatina AA, Nicolet S, Aebi U, Herrmann H, Strelkov SV (2012) Atomic structure of the vimentin central α-helical domain and its implications for intermediate filament assembly. Proc Natl Acad Sci U S A 109:13620–13625PubMedPubMedCentralCrossRefGoogle Scholar
  33. Chernyatina AA, Guzenko D, Strelkov SV (2015) Intermediate filament structure: the bottom-up approach. Curr Opin Cell Biol 32:65–72PubMedCrossRefGoogle Scholar
  34. Coltharp C, Buss J, Plumer TM, Xiao J (2016) Defining the rate-limiting processes of bacterial cytokinesis. Proc Natl Acad Sci U S A 113(8):E1044–E1053PubMedPubMedCentralCrossRefGoogle Scholar
  35. Cordell SC, Robinson EJ, Lowe J (2003) Crystal structure of the SOS cell division inhibitor SulA and in complex with FtsZ. Proc Natl Acad Sci U S A 100:7889–7894PubMedPubMedCentralCrossRefGoogle Scholar
  36. Dajkovic A, Mukherjee A, Lutkenhaus J (2008) Investigation of regulation of FtsZ assembly by SulA and development of a model for FtsZ polymerization. J Bacteriol 190:2513–2526PubMedPubMedCentralCrossRefGoogle Scholar
  37. Dajkovic A, Pichoff S, Lutkenhaus J, Wirtz D (2010) Cross-linking FtsZ polymers into coherent Z rings. Mol Microbiol 78:651–668PubMedCrossRefGoogle Scholar
  38. Davis BK (2002) Molecular evolution before the origin of species. Prog Biophys Mol Biol 79:77–133PubMedCrossRefGoogle Scholar
  39. Dobro MJ et al (2013) Electron cryotomography of ESCRT assemblies and dividing Sulfolobus cells suggests that spiraling filaments are involved in membrane scission. Mol Biol Cell 24:2319–2327PubMedPubMedCentralCrossRefGoogle Scholar
  40. Donovan C, Bramkamp M (2014) Cell division in Corynebacterineae. Front Microbiol 5:132PubMedPubMedCentralCrossRefGoogle Scholar
  41. Donovan C et al (2015) A prophage-encoded actin-like protein required for efficient viral DNA replication in bacteria. Nucleic Acids Res 43:5002–5016PubMedPubMedCentralCrossRefGoogle Scholar
  42. Draper O et al (2011) MamK, a bacterial actin, forms dynamic filaments in vivo that are regulated by the acidic proteins MamJ and LimJ. Mol Microbiol 82:342–354PubMedPubMedCentralCrossRefGoogle Scholar
  43. Duggin IG et al (2015) CetZ tubulin-like proteins control archaeal cell shape. Nature 519:362–365PubMedCrossRefGoogle Scholar
  44. Duman R et al (2013) Structural and genetic analyses reveal the protein SepF as a new membrane anchor for the Z ring. Proc Natl Acad Sci U S A 110:E4601–E4610PubMedPubMedCentralCrossRefGoogle Scholar
  45. Dupaigne P et al (2012) Molecular basis for a protein-mediated DNA-bridging mechanism that functions in condensation of the E. coli chromosome. Mol Cell 48:560–571PubMedCrossRefGoogle Scholar
  46. Durand D et al (2012) Expression, purification and preliminary structural analysis of Escherichia coli MatP in complex with the matS DNA site. Acta Crystallogr Sect F Struct Biol Cryst Commun 68:638–643PubMedPubMedCentralCrossRefGoogle Scholar
  47. Dye NA, Pincus Z, Fisher IC, Shapiro L, Theriot JA (2011) Mutations in the nucleotide binding pocket of MreB can alter cell curvature and polar morphology in Caulobacter. Mol Microbiol 81(2):368–394PubMedPubMedCentralCrossRefGoogle Scholar
  48. Egan AJ, Biboy J, van’t Veer I, Breukink E, Vollmer W (2015) Activities and regulation of peptidoglycan synthases. Philos Trans R Soc Lond Ser B Biol Sci 370Google Scholar
  49. El Andari J, Altegoer F, Bange G, Graumann PL (2015) Bacillus subtilis bactofilins are essential for flagellar Hook- and filament assembly and dynamically localize into structures of less than 100 nm diameter underneath the cell membrane. PLoS One 10:e0141546PubMedPubMedCentralCrossRefGoogle Scholar
  50. Erb ML et al (2014) A bacteriophage tubulin harnesses dynamic instability to center DNA in infected cells. Elife 3Google Scholar
  51. Erickson HP, Osawa M (2010) Cell division without FtsZ–a variety of redundant mechanisms. Mol Microbiol 78:267–270PubMedPubMedCentralCrossRefGoogle Scholar
  52. Erickson HP, Anderson DE, Osawa M (2010) FtsZ in bacterial cytokinesis: cytoskeleton and force generator all in one. Microbiol Mol Biol Rev 74:504–528PubMedPubMedCentralCrossRefGoogle Scholar
  53. Errington J (2013) L-form bacteria, cell walls and the origins of life. Open Biol 3:120143PubMedPubMedCentralCrossRefGoogle Scholar
  54. Errington JAJ-W (2015) Bacterial morphogenesis and the enigmatic MreB helix. Nat Rev Microbiol 13:241–248PubMedCrossRefGoogle Scholar
  55. Espéli O et al (2012) A MatP-divisome interaction coordinates chromosome segregation with cell division in E. coli. EMBO J 31:3198–3211PubMedPubMedCentralCrossRefGoogle Scholar
  56. Eun YJ, Kapoor M, Hussain S, Garner EC (2015) Bacterial filament systems: toward understanding their emergent behavior and cellular functions. J Biol Chem 290:17181–17189PubMedPubMedCentralCrossRefGoogle Scholar
  57. Faguy DM, Doolittle WF (1998) Cytoskeletal proteins: the evolution of cell division. Curr Biol 8:R338–R341PubMedCrossRefGoogle Scholar
  58. Fink G, Löwe J (2015) Reconstitution of a prokaryotic minus end-tracking system using TubRC centromeric complexes and tubulin-like protein TubZ filaments. Proc Natl Acad Sci U S A 112:E1845–E1850PubMedPubMedCentralCrossRefGoogle Scholar
  59. Fleurie A et al (2014) MapZ marks the division sites and positions FtsZ rings in Streptococcus pneumoniae. Nature 516:259–262PubMedPubMedCentralCrossRefGoogle Scholar
  60. Forterre P (2015) The universal tree of life: an update. Front Microbiol 6:717PubMedPubMedCentralCrossRefGoogle Scholar
  61. Gayathri P et al (2012) A bipolar spindle of antiparallel ParM filaments drives bacterial plasmid segregation. Science 338:1334–1337PubMedPubMedCentralCrossRefGoogle Scholar
  62. Gerdes K, Howard M, Szardenings F (2010) Pushing and pulling in prokaryotic DNA segregation. Cell 141:927–942PubMedCrossRefGoogle Scholar
  63. Ghosal D, Löwe J (2015) Collaborative protein filaments. EMBO J 34:2312–2320PubMedPubMedCentralCrossRefGoogle Scholar
  64. Ghosal D, Trambaiolo D, Amos LA, Lowe J (2014) MinCD cell division proteins form alternating copolymeric cytomotive filaments. Nat Commun 5:5341PubMedPubMedCentralCrossRefGoogle Scholar
  65. Glas M et al (2015) The Soluble periplasmic domains of Escherichia coli cell division proteins FtsQ/FtsB/FtsL form a trimeric complex with submicromolar affinity. J Biol Chem 290:21498–21509PubMedPubMedCentralCrossRefGoogle Scholar
  66. Goley ED et al (2011) Assembly of the caulobacter cell division machine. Mol Microbiol 80:1680–1698PubMedPubMedCentralCrossRefGoogle Scholar
  67. Graham TG et al (2014) ParB spreading requires DNA bridging. Genes Dev 28:1228–1238PubMedPubMedCentralCrossRefGoogle Scholar
  68. Griffith JD, Bonner JF (1973) Chromatin-like aggregates of uranyl acetate. Nat New Biol 244:80–81PubMedCrossRefGoogle Scholar
  69. Grüber G, Manimekalai MS, Mayer F, Müller V (2014) ATP synthases from archaea: the beauty of a molecular motor. Biochim Biophys Acta 1837:940–952PubMedCrossRefGoogle Scholar
  70. Guo P et al (2014) Common mechanisms of DNA translocation motors in bacteria and viruses using one-way revolution mechanism without rotation. Biotechnol Adv 32:853–872PubMedPubMedCentralCrossRefGoogle Scholar
  71. Holečková N et al (2015) LocZ is a new cell division protein involved in proper septum placement in Streptococcus pneumoniae. MBio 6:e01700–e01714Google Scholar
  72. Hu L, Vecchiarelli AG, Mizuuchi K, Neuman KC, Liu J (2015) Directed and persistent movement arises from mechanochemistry of the ParA/ParB system. Proc Natl Acad Sci U S A 112:E7055–E7064PubMedPubMedCentralCrossRefGoogle Scholar
  73. Hui MP et al (2010) ParA2, a Vibrio cholerae chromosome partitioning protein, forms left-handed helical filaments on DNA. Proc Natl Acad Sci U S A 107:4590–4595PubMedPubMedCentralCrossRefGoogle Scholar
  74. Ietswaart R, Szardenings F, Gerdes K, Howard M (2014) Competing ParA structures space bacterial plasmids equally over the nucleoid. PLoS Comput Biol 10:e1004009PubMedPubMedCentralCrossRefGoogle Scholar
  75. Ingerson-Mahar M, Gitai Z (2012) A growing family: the expanding universe of the bacterial cytoskeleton. FEMS Microbiol Rev 36:256–266PubMedCrossRefGoogle Scholar
  76. Islam ST, Mignot T (2015) The mysterious nature of bacterial surface (gliding) motility: a focal adhesion-based mechanism in Myxococcus xanthus. Semin Cell Dev Biol 46:143–154PubMedCrossRefGoogle Scholar
  77. Iyer LM, Makarova KS, Koonin EV, Aravind L (2004) Comparative genomics of the FtsK-HerA superfamily of pumping ATPases: implications for the origins of chromosome segregation, cell division and viral capsid packaging. Nucleic Acids Res 32:5260–5279PubMedPubMedCentralCrossRefGoogle Scholar
  78. 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 588:776–782PubMedPubMedCentralCrossRefGoogle Scholar
  79. Jacquier N, Viollier PH, Greub G (2015) The role of peptidoglycan in chlamydial cell division: towards resolving the chlamydial anomaly. FEMS Microbiol Rev 39:262–275PubMedCrossRefGoogle Scholar
  80. Jiang S et al (2016) Novel actin filaments from Bacillus thuringiensis form nanotubules for plasmid DNA segregation. Proc Natl Acad Sci U S A 113(9):E1200–E1205PubMedPubMedCentralCrossRefGoogle Scholar
  81. Jones LJ, Carballido-López R, Errington J (2001) Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis. Cell 104:913–922PubMedCrossRefGoogle Scholar
  82. Kabsch W, Holmes KC (1995) The actin fold. FASEB J 9:167–174PubMedGoogle Scholar
  83. Kawai Y, Daniel RA, Errington J (2009) Regulation of cell wall morphogenesis in Bacillus subtilis by recruitment of PBP1 to the MreB helix. Mol Microbiol 71:1131–1144PubMedCrossRefGoogle Scholar
  84. Kiekebusch D, Thanbichler M (2014) Spatiotemporal organization of microbial cells by protein concentration gradients. Trends Microbiol 22:65–73PubMedCrossRefGoogle Scholar
  85. Kiekebusch D, Michie KA, Essen LO, Löwe J, Thanbichler M (2012) Localized dimerization and nucleoid binding drive gradient formation by the bacterial cell division inhibitor MipZ. Mol Cell 46:245–259PubMedPubMedCentralCrossRefGoogle Scholar
  86. Koonin EV (1993) A superfamily of ATPases with diverse functions containing either classical or deviant ATP-binding motif. J Mol Biol 229:1165–1174PubMedCrossRefGoogle Scholar
  87. Koonin EV (2015) Origin of eukaryotes from within archaea, archaeal eukaryome and bursts of gene gain: eukaryogenesis just made easier. Philos Trans R Soc Lond Ser B Biol Sci 370:20140333CrossRefGoogle Scholar
  88. Kraemer JA et al (2012) A phage tubulin assembles dynamic filaments by an atypical mechanism to center viral DNA within the host cell. Cell 149:1488–1499PubMedPubMedCentralCrossRefGoogle Scholar
  89. Ku C, Lo WS, Kuo CH (2014) Molecular evolution of the actin-like MreB protein gene family in wall-less bacteria. Biochem Biophys Res Commun 446:927–932PubMedCrossRefGoogle Scholar
  90. Kühn J et al (2010) Bactofilins, a ubiquitous class of cytoskeletal proteins mediating polar localization of a cell wall synthase in Caulobacter crescentus. EMBO J 29:327–339PubMedCrossRefGoogle Scholar
  91. Laddomada F, Miyachiro MM, Dessen A (2016) Structural insights into protein-protein interactions involved in bacterial cell wall biogenesis. Antibiotics (Basel) 5:14CrossRefGoogle Scholar
  92. LaPointe LM et al (2013) Structural organization of FtsB, a transmembrane protein of the bacterial divisome. Biochemistry 52:2574–2585PubMedPubMedCentralCrossRefGoogle Scholar
  93. Larsen RA et al (2007) Treadmilling of a prokaryotic tubulin-like protein, TubZ, required for plasmid stability in Bacillus thuringiensis. Genes Dev 21:1340–1352PubMedPubMedCentralCrossRefGoogle Scholar
  94. Leger MM et al (2015) An ancestral bacterial division system is widespread in eukaryotic mitochondria. Proc Natl Acad Sci U S A 112:10239–10246PubMedPubMedCentralCrossRefGoogle Scholar
  95. Leonard TA, Butler PJ, Löwe J (2005) Bacterial chromosome segregation: structure and DNA binding of the Soj dimer–a conserved biological switch. EMBO J 24:270–282PubMedPubMedCentralCrossRefGoogle Scholar
  96. Lin L, Thanbichler M (2013) Nucleotide-independent cytoskeletal scaffolds in bacteria. Cytoskeleton (Hoboken) 70:409–423CrossRefGoogle Scholar
  97. Linck R et al (2014) Insights into the structure and function of ciliary and flagellar doublet microtubules: tektins, Ca2+-binding proteins, and stable protofilaments. J Biol Chem 289:17427–17444PubMedPubMedCentralCrossRefGoogle Scholar
  98. Lindås AC, Karlsson EA, Lindgren MT, Ettema TJ, Bernander R (2008) A unique cell division machinery in the Archaea. Proc Natl Acad Sci U S A 105(48):18942–18946PubMedPubMedCentralCrossRefGoogle Scholar
  99. Lindås AC, Chruszcz M, Bernander R, Valegård K (2014) Structure of crenactin, an archaeal actin homologue active at 90°C. Acta Crystallogr D Biol Crystallogr 70:492–500PubMedCrossRefGoogle Scholar
  100. Loose M, Mitchison TJ (2014) The bacterial cell division proteins FtsA and FtsZ self-organize into dynamic cytoskeletal patterns. Nat Cell Biol 16:38–46PubMedCrossRefGoogle Scholar
  101. Loose M, Fischer-Friedrich E, Ries J, Kruse K, Schwille P (2008) Spatial regulators for bacterial cell division self-organize into surface waves in vitro. Science 320:789–792PubMedCrossRefGoogle Scholar
  102. Loose M, Fischer-Friedrich E, Herold C, Kruse K, Schwille P (2011) Min protein patterns emerge from rapid rebinding and membrane interaction of MinE. Nat Struct Mol Biol 18:577–583PubMedCrossRefGoogle Scholar
  103. Low HH, Löwe J (2010) Dynamin architecture–from monomer to polymer. Curr Opin Struct Biol 20:791–798PubMedCrossRefGoogle Scholar
  104. Low HH, Sachse C, Amos LA, Löwe J (2009) Structure of a bacterial dynamin-like protein lipid tube provides a mechanism for assembly and membrane curving. Cell 139:1342–1352PubMedPubMedCentralCrossRefGoogle Scholar
  105. Löwe J, Amos LA (2009) Evolution of cytomotive filaments: the cytoskeleton from prokaryotes to eukaryotes. Int J Biochem Cell Biol 41:323–329PubMedCrossRefGoogle Scholar
  106. Löwe J, Li H, Downing KH, Nogales E (2001) Refined structure of alpha beta-tubulin at 3.5 A resolution. J Mol Biol 313:1045–1057PubMedCrossRefGoogle Scholar
  107. Lutkenhaus JF, Donachie WD (1979) Identification of the ftsA gene product. J Bacteriol 137:1088–1094PubMedPubMedCentralGoogle Scholar
  108. 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 U S A 93:12998–13003PubMedPubMedCentralCrossRefGoogle Scholar
  109. Martin WF, Sousa FL (2015) Early microbial evolution: the age of anaerobes. Cold Spring Harb Perspect Biol 8(2)Google Scholar
  110. Martin-Galiano AJ et al (2011) Bacterial tubulin distinct loop sequences and primitive assembly properties support its origin from a eukaryotic tubulin ancestor. J Biol Chem 286:19789–19803PubMedPubMedCentralCrossRefGoogle Scholar
  111. Mauriello EM et al (2010) Bacterial motility complexes require the actin-like protein, MreB and the Ras homologue, MglA. EMBO J 29:315–326PubMedCrossRefGoogle Scholar
  112. Mercier R, Kawai Y, Errington J (2014) General principles for the formation and proliferation of a wall-free (L-form) state in bacteria. Elife 3Google Scholar
  113. Michie KA, Boysen A, Low HH, Møller-Jensen J, Löwe J (2014) LeoA, B and C from enterotoxigenic Escherichia coli (ETEC) are bacterial dynamins. PLoS One 9:e107211PubMedPubMedCentralCrossRefGoogle Scholar
  114. Mim C, Unger VM (2012) Membrane curvature and its generation by BAR proteins. Trends Biochem Sci 37:526–533PubMedPubMedCentralCrossRefGoogle Scholar
  115. Minamino T, Imada K (2015) The bacterial flagellar motor and its structural diversity. Trends Microbiol 23:267–274PubMedCrossRefGoogle Scholar
  116. Miyagishima SY, Nakamura M, Uzuka A, Era A (2014) FtsZ-less prokaryotic cell division as well as FtsZ- and dynamin-less chloroplast and non-photosynthetic plastid division. Front Plant Sci 5:459PubMedPubMedCentralCrossRefGoogle Scholar
  117. Møller-Jensen J, Ringgaard S, Mercogliano CP, Gerdes K, Löwe J (2007) Structural analysis of the ParR/parC plasmid partition complex. EMBO J 26:4413–4422PubMedPubMedCentralCrossRefGoogle Scholar
  118. Montabana EA, 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 U S A 111:3407–3412PubMedPubMedCentralCrossRefGoogle Scholar
  119. Morgenstein RM et al (2015) RodZ links MreB to cell wall synthesis to mediate MreB rotation and robust morphogenesis. Proc Natl Acad Sci U S A 112:12510–12515PubMedPubMedCentralCrossRefGoogle Scholar
  120. Moriscot C et al (2011) Crenarchaeal CdvA forms double-helical filaments containing DNA and interacts with ESCRT-III-like CdvB. PLoS One 6:e21921PubMedPubMedCentralCrossRefGoogle Scholar
  121. Motallebi-Veshareh M, Rouch DA, Thomas CM (1990) A family of ATPases involv2ed in active partitioning of diverse bacterial plasmids. Mol Microbiol 4:1455–1463PubMedCrossRefGoogle Scholar
  122. Nan B, Zusman DR (2011) Uncovering the mystery of gliding motility in the myxobacteria. Annu Rev Genet 45:21–39PubMedPubMedCentralCrossRefGoogle Scholar
  123. Nan B, McBride MJ, Chen J, Zusman DR, Oster G (2014) Bacteria that glide with helical tracks. Curr Biol 24:R169–R173PubMedPubMedCentralCrossRefGoogle Scholar
  124. Ni L, Xu W, Kumaraswami M, Schumacher MA (2010) Plasmid protein TubR uses a distinct mode of HTH-DNA binding and recruits the prokaryotic tubulin homolog TubZ to effect DNA partition. Proc Natl Acad Sci U S A 107:11763–11768PubMedPubMedCentralCrossRefGoogle Scholar
  125. Nierzwicki-Bauer SA, Balkwill DL, Stevens SE (1983) Three-dimensional ultrastructure of a unicellular cyanobacterium. J Cell Biol 97:713–722PubMedCrossRefGoogle Scholar
  126. Oda T, Iwasa M, Aihara T, Maéda Y, Narita A (2009) The nature of the globular- to fibrous-actin transition. Nature 457:441–445PubMedCrossRefGoogle Scholar
  127. Oliva MA, Cordell SC, Lowe J (2004) Structural insights into FtsZ protofilament formation. Nat Struct Mol Biol 11:1243–1250PubMedCrossRefGoogle Scholar
  128. Oliva MA et al (2010) Features critical for membrane binding revealed by DivIVA crystal structure. EMBO J 29:1988–2001PubMedPubMedCentralCrossRefGoogle Scholar
  129. Oliva MA, Martin-Galiano AJ, Sakaguchi Y, Andreu JM (2012) Tubulin homolog TubZ in a phage-encoded partition system. Proc Natl Acad Sci U S A 109:7711–7716PubMedPubMedCentralCrossRefGoogle Scholar
  130. Ortiz C et al (2015) Crystal structure of the Z-ring associated cell division protein ZapC from Escherichia coli. FEBS Lett 589:3822–3828PubMedPubMedCentralCrossRefGoogle Scholar
  131. Osawa M, Erickson HP (2011) Inside-out Z rings–constriction with and without GTP hydrolysis. Mol Microbiol 81:571–579PubMedPubMedCentralCrossRefGoogle Scholar
  132. Osawa M, Erickson HP (2013) Liposome division by a simple bacterial division machinery. Proc Natl Acad Sci U S A 110:11000–11004PubMedPubMedCentralCrossRefGoogle Scholar
  133. Osteryoung KW, Pyke KA (2014) Division and dynamic morphology of plastids. Annu Rev Plant Biol 65:443–472PubMedCrossRefGoogle Scholar
  134. Ouellette SP, Karimova G, Subtil A, Ladant D (2012) Chlamydia co-opts the rod shape-determining proteins MreB and Pbp2 for cell division. Mol Microbiol 85:164–178PubMedCrossRefGoogle Scholar
  135. Ozyamak E, Kollman J, Agard DA, Komeili A (2013) The bacterial actin MamK: in vitro assembly behavior and filament architecture. J Biol Chem 288:4265–4277PubMedCrossRefGoogle Scholar
  136. Park KT, Du S, Lutkenhaus J (2015) MinC/MinD copolymers are not required for Min function. Mol Microbiol 98:895–909PubMedPubMedCentralCrossRefGoogle Scholar
  137. Pérez-Núñez D et al (2011) A new morphogenesis pathway in bacteria: unbalanced activity of cell wall synthesis machineries leads to coccus-to-rod transition and filamentation in ovococci. Mol Microbiol 79:759–771PubMedCrossRefGoogle Scholar
  138. Pilhofer M, Rosati G, Ludwig W, Schleifer KH, Petroni G (2007) Coexistence of tubulins and ftsZ in different Prosthecobacter species. Mol Biol Evol 24:1439–1442PubMedCrossRefGoogle Scholar
  139. 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:e1001213PubMedPubMedCentralCrossRefGoogle Scholar
  140. Polka JK, Kollman JM, Mullins RD (2014) Accessory factors promote AlfA-dependent plasmid segregation by regulating filament nucleation, disassembly, and bundling. Proc Natl Acad Sci U S A 111:2176–2181PubMedPubMedCentralCrossRefGoogle Scholar
  141. Popp D, Robinson RC (2012) Supramolecular cellular filament systems: how and why do they form. Cytoskeleton (Hoboken) 69:71–87CrossRefGoogle Scholar
  142. Ptacin JL et al (2010) A spindle-like apparatus guides bacterial chromosome segregation. Nat Cell Biol 12:791–798PubMedPubMedCentralCrossRefGoogle Scholar
  143. Ptacin JL et al (2014) Bacterial scaffold directs pole-specific centromere segregation. Proc Natl Acad Sci U S A 111:E2046–E2055PubMedPubMedCentralCrossRefGoogle Scholar
  144. Ramamurthi KS, Losick R (2009) Negative membrane curvature as a cue for subcellular localization of a bacterial protein. Proc Natl Acad Sci U S A 106:13541–13545PubMedPubMedCentralCrossRefGoogle Scholar
  145. 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 24:2340–2349PubMedPubMedCentralCrossRefGoogle Scholar
  146. Reyes-Lamothe R, Nicolas E, Sherratt DJ (2012) Chromosome replication and segregation in bacteria. Annu Rev Genet 46:121–143PubMedCrossRefGoogle Scholar
  147. Rivera CR, Kollman JM, Polka JK, Agard DA, Mullins RD (2011) Architecture and assembly of a divergent member of the ParM family of bacterial actin-like proteins. J Biol Chem 286:14282–14290PubMedPubMedCentralCrossRefGoogle Scholar
  148. Roeben A et al (2006) Crystal structure of an archaeal actin homolog. J Mol Biol 358:145–156PubMedCrossRefGoogle Scholar
  149. Samson RY, Obita T, Freund SM, Williams RL, Bell SD (2008) A role for the ESCRT system in cell division in archaea. Science 322(5908):1710–1713PubMedPubMedCentralCrossRefGoogle Scholar
  150. Samson RY et al (2011) Molecular and structural basis of ESCRT-III recruitment to membranes during archaeal cell division. Mol Cell 41:186–196PubMedPubMedCentralCrossRefGoogle Scholar
  151. Schlieper D, Oliva MA, Andreu JM, Löwe J (2005) Structure of bacterial tubulin BtubA/B: evidence for horizontal gene transfer. Proc Natl Acad Sci U S A 102:9170–9175PubMedPubMedCentralCrossRefGoogle Scholar
  152. Schuh AL, Audhya A (2014) The ESCRT machinery: from the plasma membrane to endosomes and back again. Crit Rev Biochem Mol Biol 49:242–261PubMedPubMedCentralCrossRefGoogle Scholar
  153. Schumacher MA, Zeng W, Huang KH, Tchorzewski L, Janakiraman A (2016) Structural and functional analyses reveal insights into the molecular properties of the Escherichia coli Z ring stabilizing protein, ZapC. J Biol Chem 291:2485–2498PubMedCrossRefGoogle Scholar
  154. Shaevitz JW, Gitai Z (2010) The structure and function of bacterial actin homologs. Cold Spring Harb Perspect Biol 2:a000364PubMedPubMedCentralCrossRefGoogle Scholar
  155. Shi C et al (2015) Atomic-resolution structure of cytoskeletal bactofilin by solid-state NMR. Sci Adv 1:e1501087PubMedPubMedCentralCrossRefGoogle Scholar
  156. Shimogonya Y et al (2015) Torque-induced precession of bacterial flagella. Sci Rep 5:18488PubMedPubMedCentralCrossRefGoogle Scholar
  157. Shrivastava A, Lele PP, Berg HC (2015) A rotary motor drives Flavobacterium gliding. Curr Biol 25:338–341PubMedPubMedCentralCrossRefGoogle Scholar
  158. Skau CT, Waterman CM (2015) Specification of architecture and function of actin structures by actin nucleation factors. Annu Rev Biophys 44:285–310PubMedCrossRefGoogle Scholar
  159. Skoog K, Daley DO (2012) The Escherichia coli cell division protein ZipA forms homodimers prior to association with FtsZ. Biochemistry 51:1407–1415PubMedCrossRefGoogle Scholar
  160. Spang A et al (2015) Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521:173–179PubMedPubMedCentralCrossRefGoogle Scholar
  161. 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 194:6382–6386PubMedPubMedCentralCrossRefGoogle Scholar
  162. Szardenings F, Guymer D, Gerdes K (2011) ParA ATPases can move and position DNA and subcellular structures. Curr Opin Microbiol 14:712–718PubMedCrossRefGoogle Scholar
  163. Szwedziak P, Löwe J (2013) Do the divisome and elongasome share a common evolutionary past. Curr Opin Microbiol 16:745–751PubMedCrossRefGoogle Scholar
  164. Szwedziak P, Wang Q, Freund SM, Löwe J (2012) FtsA forms actin-like protofilaments. EMBO J 31:2249–2260PubMedPubMedCentralCrossRefGoogle Scholar
  165. Szwedziak P, Wang Q, Bharat TA, Tsim M, Löwe J (2014) Architecture of the ring formed by the tubulin homologue FtsZ in bacterial cell division. Elife 3:e04601PubMedPubMedCentralCrossRefGoogle Scholar
  166. Tonthat NK et al (2013) SlmA forms a higher-order structure on DNA that inhibits cytokinetic Z-ring formation over the nucleoid. Proc Natl Acad Sci U S A 110:10586–10591PubMedPubMedCentralCrossRefGoogle Scholar
  167. Trachtenberg S, Schuck P, Phillips TM, Andrews SB, Leapman RD (2014) A structural framework for a near-minimal form of life: mass and compositional analysis of the helical mollicute Spiroplasma melliferum BC3. PLoS One 9:e87921PubMedPubMedCentralCrossRefGoogle Scholar
  168. Treuner-Lange A et al (2013) PomZ, a ParA-like protein, regulates Z-ring formation and cell division in Myxococcus xanthus. Mol Microbiol 87:235–253PubMedCrossRefGoogle Scholar
  169. Trip EN, Scheffers DJ (2015) A 1 MDa protein complex containing critical components of the Escherichia coli divisome. Sci Rep 5:18190PubMedPubMedCentralCrossRefGoogle Scholar
  170. Turner RD et al (2010) Peptidoglycan architecture can specify division planes in Staphylococcus aureus. Nat Commun 1:26PubMedCrossRefGoogle Scholar
  171. Typas A, Banzhaf M, Gross CA, Vollmer W (2012) From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nat Rev Microbiol 10:123–136Google Scholar
  172. Valas RE, Bourne PE (2011) The origin of a derived superkingdom: how a gram-positive bacterium crossed the desert to become an archaeon. Biol Direct 6:16PubMedPubMedCentralCrossRefGoogle Scholar
  173. van den Ent F, Amos LA, Löwe J (2001) Prokaryotic origin of the actin cytoskeleton. Nature 413:39–44PubMedCrossRefGoogle Scholar
  174. van den Ent F, Johnson CM, Persons L, de Boer P, Löwe J (2010) Bacterial actin MreB assembles in complex with cell shape protein RodZ. EMBO J 29:1081–1090PubMedPubMedCentralCrossRefGoogle Scholar
  175. van den Ent F, Izoré T, Bharat TA, Johnson CM, Löwe J (2014) Bacterial actin MreB forms antiparallel double filaments. Elife 3:e02634PubMedPubMedCentralGoogle Scholar
  176. van Teeffelen S et al (2011) The bacterial actin MreB rotates, and rotation depends on cell-wall assembly. Proc Natl Acad Sci U S A 108:15822–15827PubMedPubMedCentralCrossRefGoogle Scholar
  177. Vecchiarelli AG, Neuman KC, Mizuuchi K (2014) A propagating ATPase gradient drives transport of surface-confined cellular cargo. Proc Natl Acad Sci U S A 111:4880–4885PubMedPubMedCentralCrossRefGoogle Scholar
  178. Vecchiarelli AG, Lia M, Mizuuchia M, Hwanga LC, Seol Y, Neuman KC, Mizuuchia K (2016) Membrane-bound MinDE complex acts as a toggle switch that drives Min oscillation coupled to cytoplasmic depletion of MinD. Proc Natl Acad Sci U S A 113:E1479–E1488PubMedPubMedCentralCrossRefGoogle Scholar
  179. Villanelo F, Ordenes A, Brunet J, Lagos R, Monasterio O (2011) A model for the Escherichia coli FtsB/FtsL/FtsQ cell division complex. BMC Struct Biol 11:28PubMedPubMedCentralCrossRefGoogle Scholar
  180. Walsby AE (1994) Gas vesicles. Microbiol Rev 58:94–144PubMedPubMedCentralGoogle Scholar
  181. Wang X, Rudner DZ (2014) Spatial organization of bacterial chromosomes. Curr Opin Microbiol 22:66–72PubMedPubMedCentralCrossRefGoogle Scholar
  182. Weiss DS, Chen JC, Ghigo JM, Boyd D, Beckwith J (1999) Localization of FtsI (PBP3) to the septal ring requires its membrane anchor, the Z ring, FtsA, FtsQ, and FtsL. J Bacteriol 181:508–520PubMedPubMedCentralGoogle Scholar
  183. Wickstead B, Gull K (2011) The evolution of the cytoskeleton. J Cell Biol 194:513–525PubMedPubMedCentralCrossRefGoogle Scholar
  184. Wilde A, Mullineaux CW (2015) Motility in cyanobacteria: polysaccharide tracks and Type IV pilus motors. Mol Microbiol 98:998–1001PubMedCrossRefGoogle Scholar
  185. Wilkens S (2015) Structure and mechanism of ABC transporters. F1000Prime Rep 7:14Google Scholar
  186. Yang R et al (2004) AglZ is a filament-forming coiled-coil protein required for adventurous gliding motility of Myxococcus xanthus. J Bacteriol 186:6168–6178PubMedPubMedCentralCrossRefGoogle Scholar
  187. Yang B, Stjepanovic G, Shen Q, Martin A, Hurley JH (2015) Vps4 disassembles an ESCRT-III filament by global unfolding and processive translocation. Nat Struct Mol Biol 22:492–498PubMedPubMedCentralCrossRefGoogle Scholar
  188. Yooshida Y, Miyagishima SY, Kuroiwa H, Kuroiwa T (2012) The plastid-dividing machinery: formation, constriction and fission. Curr Opin Plant Biol 15:714–721CrossRefGoogle Scholar
  189. Yuan Y et al (2015) Effects of actin-like proteins encoded by two Bacillus pumilus phages on unstable lysogeny, revealed by genomic analysis. Appl Environ Microbiol 81:339–350PubMedCrossRefGoogle Scholar
  190. Yutin N, Koonin EV (2012) Archaeal origin of tubulin. Biol Direct 7:10PubMedPubMedCentralCrossRefGoogle Scholar
  191. Zehr EA et al (2014) The structure and assembly mechanism of a novel three-stranded tubulin filament that centers phage DNA. Structure 22:539–548PubMedPubMedCentralCrossRefGoogle Scholar
  192. Zheng M et al (2014) Self-assembly of MinE on the membrane underlies formation of the MinE ring to sustain function of the Escherichia coli Min system. J Biol Chem 289:21252–21266PubMedPubMedCentralCrossRefGoogle Scholar
  193. Zuckerman DM et al (2015) The bactofilin cytoskeleton protein BacM of Myxococcus xanthus forms an extended β-sheet structure likely mediated by hydrophobic interactions. PLoS One 10:e0121074PubMedPubMedCentralCrossRefGoogle Scholar

Website

  1. Slides (including some movies) can be downloaded from the Löwe group website: http://www2.mrc-lmb.cam.ac.uk/groups/jyl/slideshows/encyclopedia2014/index.html

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.MRC Laboratory of Molecular BiologyCambridgeUK

Personalised recommendations