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Bacterial Actins and Their Interactors

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The Actin Cytoskeleton and Bacterial Infection

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 399))

Abstract

Bacterial actins polymerize in the presence of nucleotide (preferably ATP), form a common arrangement of monomeric interfaces within a protofilament, and undergo ATP hydrolysis-dependent change in stability of the filament—all of which contribute to performing their respective functions. The relative stability of the filament in the ADP-bound form compared to that of ATP and the rate of addition of monomers at the two ends decide the filament dynamics. One of the major differences between eukaryotic actin and bacterial actins is the variety in protofilament arrangements and dynamics exhibited by the latter. The filament structure and the polymerization dynamics enable them to perform various functions such as shape determination in rod-shaped bacteria (MreB), cell division (FtsA), plasmid segregation (ParM family of actin-like proteins), and organelle positioning (MamK). Though the architecture and dynamics of a few representative filaments have been studied, information on the effect of interacting partners on bacterial actin filament dynamics is not very well known. The chapter reviews some of the structural and functional aspects of bacterial actins, with special focus on the effect that interacting partners exert on the dynamics of bacterial actins, and how these assist them to carry out the functions within the bacterial cell.

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References

  • Abreu N, Mannoubi S, Ozyamak E et al (2014) Interplay between two bacterial actin homologs, MamK and MamK-Like, is required for the alignment of magnetosome organelles in Magnetospirillum magneticum AMB-1. J Bacteriol 196:3111–3121

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arbing MA, Handelman SK, Kuzin AP et al (2010) Crystal structures of Phd-Doc, HigA, and YeeU establish multiple evolutionary links between microbial growth-regulating toxin-antitoxin systems. Structure 18:996–1010

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Bharat TA, Murshudov GN, Sachse C et al (2015) Structures of actin-like ParM filaments show architecture of plasmid-segregating spindles. Nature 523:106–110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bork P, Sander C, Valencia A (1992) 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Braun T, Orlova A, ValegÃ¥rd K et al (2015) Archaeal actin from a hyperthermophile forms a single-stranded filament. Proc Natl Acad Sci USA 112:9340–9345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Breiher W (2013) Mechanisms of actin disassembly. Mol Biol Cell 24:2299–2302

    Article  Google Scholar 

  • Brown JM, Shaw KJ (2003) A novel family of Escherichia coli toxin–antitoxin gene pairs. J Bacteriol 185:6600–6608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bugalhão JN, Mota LJ, Franco IS (2015) Bacterial nucleators: actin’ on actin. Pathog Dis 73: ftv078

    Google Scholar 

  • Campellone KG, Welch MD (2010) A nucleator arms race: cellular control of actin assembly. Nat Rev Mol Cell Biol 11:237–251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chesarone MA, Goode BL (2009) Actin nucleation and elongation factors: mechanisms and interplay. Curr Opin Cell Biol 21:28–37

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cowles KN, Gitai Z (2010) Surface association and the MreB cytoskeleton regulate pilus production, localization and function in Pseudomonas aeruginosa. Mol Microbiol 76:1411–1426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Defeu Soufo HJ, Reimold C, Linne U et al (2010) Bacterial translation elongation factor EF-Tu interacts and colocalizes with actin-like MreB protein. Proc Natl Acad Sci USA 107:3163–3168

    Article  PubMed  PubMed Central  Google Scholar 

  • Defeu Soufo HJ, Reimold C, Breddermann H et al (2015) Translation elongation factor EF-Tu modulates filament formation of bacterial actin-like protein in vivo. J Mol Biol 427:1715–1727

    Article  CAS  PubMed  Google Scholar 

  • Derman AI, Becker EC, Truong BD et al (2009) Phylogenetic analysis identifies many uncharacterized actin-like proteins (Alps) in bacteria: regulated polymerization, dynamic instability and treadmilling in Alp7A. Mol Microbiol 73:534–552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dominguez R (2004) Actin-binding proteins—a unifying hypothesis. Trends Biochem Sci 29:572–578

    Article  CAS  PubMed  Google Scholar 

  • Dominguez R, Holmes KC (2011) Actin structure and function. Annu Rev Biophys 40:169–186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Draper O, Byrne ME, Li Z et al (2011) MamK, a bacterial actin, forms dynamic filaments in vivo that are regulated by the acidic proteins MamJ and LimJ. Mol Microbiol 82:342–354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ettema TJ, LindÃ¥s AC, Bernander R (2011) An actin-based cytoskeleton in archaea. Mol Microbiol 80:1052–1061

    Article  CAS  PubMed  Google Scholar 

  • Eun YJ, Kapoor M, Hussain S et al (2015) Bacterial filament systems: towards understanding their emergent behavior and cellular functions. J Biol Chem 290:17181–17189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garner EC, Campbell CS, Mullins RD (2004) Dynamic instability in a DNA-segregating prokaryotic actin homolog. Science 306:1021–1025

    Article  CAS  PubMed  Google Scholar 

  • Garner EC, Campbell CS, Weibel DB et al (2007) Reconstitution of DNA segregation driven by assembly of a prokaryotic actin homolog. Science 315:1270–1274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gayathri P, Fujii T, Møller-Jensen J et al (2012) A bipolar spindle of antiparallel ParM filaments drives bacterial plasmid segregation. Science 338:1334–1337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gitai Z, Dye NA, Reisenauer A et al (2005) MreB actin-mediated segregation of a specific region of a bacterial chromosome. Cell 120:329–341

    Article  CAS  PubMed  Google Scholar 

  • Gross SR, Kinzy TG (2005) Translation elongation factor 1A is essential for regulation of the actin cytoskeleton and cell morphology. Nat Struct Mol Biol 12:772–778

    Article  CAS  PubMed  Google Scholar 

  • Gunning PW, Ghoshdastider U, Whitaker S et al (2015) The evolution of compositionally and functionally distinct actin filaments. J Cell Sci 128:2009–2019

    Article  CAS  PubMed  Google Scholar 

  • Holm L, Rosenström P (2010) Dali server: conservation mapping in 3D. Nucl Acids Res 38:W545–W549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsu CY, Ko FY, Li CW et al (2007) Magnetoreception system in honeybees (Apis mellifera). PLoS ONE 2:e395

    Article  PubMed  PubMed Central  Google Scholar 

  • Ingerson-Mahar M, Gitai Z (2012) A growing family: the expanding universe of the bacterial cytoskeleton. FEMS Microbiol Rev 36:256–266

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Izoré T, Duman R, Kureisaite-Ciziene D et al (2014) Crenactin from Pyrobaculum calidifontis is closely related to actin in structure and forms steep helical filaments. FEBS Lett 588:776–782

    Article  PubMed  PubMed Central  Google Scholar 

  • Jiang S, Narita A, Popp D et al (2016) Novel actin filaments from Bacillus thuringiensis form nanotubules for plasmid DNA segregation. Proc Natl Acad Sci USA 89:7290–7294

    Google Scholar 

  • Jones LJ, Carballido-Lopez R, Errington J (2001) Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis. Cell 104:913–922

    Article  CAS  PubMed  Google Scholar 

  • Kim SY, Gitai Z, Kinkhabwala A et al (2006) Single molecules of the bacterial actin MreB undergo directed treadmilling motion in Caulobacter crescentus. Proc Natl Acad Sci 103:10929–10934

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Komeili A, Li Z, Newman DK et al (2006) Magnetosomes are cell membrane invaginations organized by the actin-like protein MamK. Science 311:242–245

    Article  CAS  PubMed  Google Scholar 

  • Kruse T, Møller-Jensen J, Løbner-Olesen A et al (2003) Dysfunctional MreB inhibits chromosome segregation in Escherichia coli. EMBO J 22:5283–5292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 446:927–932

    Article  CAS  PubMed  Google Scholar 

  • Kürner J, Frangakis AS, Baumeister W (2005) Cryo-electron tomography reveals the cytoskeletal structure of Spiroplasma melliferum. Science 307:436–438

    Article  PubMed  Google Scholar 

  • Lara B, Rico AI, Petruzzelli S et al (2005) Cell division in cocci: localization and properties of the Streptococcus pneumoniae FtsA protein. Mol Microbiol 55:699–711

    Article  CAS  PubMed  Google Scholar 

  • LindÃ¥s AC, Chruszcz M, Bernander R et al (2014) Structure of crenactin, an archaeal actin homologue active at 90 °C. Acta Crystallogr D Biol Crystallogr 70:492–500

    Article  PubMed  Google Scholar 

  • Loose M, Mitchison TJ (2014) The bacterial cell division proteins FtsA and FtsZ self-organize into dynamic cytoskeletal patterns. Nat Cell Biol 16:38–46

    Article  CAS  PubMed  Google Scholar 

  • Mann S, Sparks N, Walker M et al (1988) Ultrastructure, morphology and organization of biogenic magnetite from sockeye salmon, Oncorhynchus nerka: implications for magnetoreception. J Exp Biol 140:35–49

    CAS  PubMed  Google Scholar 

  • Masuda H, Tan Q, Awano N et al (2012) YeeU enhances the bundling of cytoskeletal polymers of MreB and FtsZ, antagonizing the CbtA (YeeV) toxicity in Escherichia coli. Mol Microbiol 84:979–989

    Article  CAS  PubMed  Google Scholar 

  • Mauriello EM, Nan B, Zusman DR (2009) AglZ regulates adventurous (A-) motility in Myxococcus xanthus through its interaction with the cytoplasmic receptor, FrzCD. Mol Microbiol 72:964–977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mauriello EM, Mouhamar F, Nan B et al (2010) Bacterial motility complexes require the actin-like protein, MreB and the Ras homologue, MglA. EMBO J 29:315–326

    Article  CAS  PubMed  Google Scholar 

  • Mignot T, Merlie JP Jr, Zusman DR (2005) Regulated pole-to-pole oscillations of a bacterial gliding motility protein. Science 310:855–857

    Article  CAS  PubMed  Google Scholar 

  • Mignot T, Shaevitz JW, Hartzell PL et al (2007) Evidence that focal adhesion complexes power bacterial gliding motility. Science 315:853–856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Møller-Jensen J, Jensen RB, Löwe J et al (2002) Prokaryotic DNA segregation by an actin-like filament. EMBO J 21:3119–3127

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 112:12510–12515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nan B, Zusman DR (2016) Novel mechanisms power bacterial gliding motility. Mol Microbiol. doi:10.1111/mmi.13389

    Google Scholar 

  • Nan B, Chen J, Neu JC et al (2011) Myxobacteria gliding motility requires cytoskeleton rotation powered by proton motive force. Proc Natl Acad Sci USA 108:2498–2503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nan B, Bandaria JN, Moghtaderi A et al (2013) Flagella stator homologs function as motors for myxobacterial gliding motility by moving in helical trajectories. Proc Natl Acad Sci USA 110:E1508–E1513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nan B, Bandaria JN, Guo KY et al (2015) The polarity of myxobacterial gliding is regulated by direct interactions between the gliding motors and the Ras homolog MglA. Proc Natl Acad Sci USA 112:E186–E193

    Article  CAS  PubMed  Google Scholar 

  • Ozyamak E, Kollman J, Agard DA et al (2013a) The bacterial actin MamK: in vitro assembly behavior and filament architecture. J Biol Chem 288:4265–4277

    Article  CAS  PubMed  Google Scholar 

  • Ozyamak E, Kollman JM, Komeili A (2013b) Bacterial actins and their diversity. Biochemistry 52:6928–6939

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pan W, Xie C, Lv J (2012) Screening for the interacting partners of the proteins MamK and MamJ by two-hybrid genomic DNA library of Magnetospirillum magneticum AMB-1. Curr Microbiol 64:515–523

    Article  CAS  PubMed  Google Scholar 

  • Pei J, Kim B-H, Grishin NV (2008) PROMALS3D: a tool for multiple sequence and structure alignment. Nuc Acids Res 36:2295–2300

    Article  CAS  Google Scholar 

  • Philippe N, Wu LF (2010) An MCP-like protein interacts with the MamK cytoskeleton and is involved in magnetotaxis in Magnetospirillum magneticum AMB-1. J Mol Biol 400:309–322

    Article  CAS  PubMed  Google Scholar 

  • Polka JK, Kollman JM, Agard DA et al (2009) The structure and assembly dynamics of plasmid actin AlfA imply a novel mechanism of DNA segregation. J Bacteriol 191:6219–6230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 111:2176–2181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Popp D, Xu W, Narita A et al (2010) Structure and filament dynamics of the pSK41 Actin-like ParM protein: implications for plasmid DNA segregation. J Biol Chem 285:10130–10140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Popp D, Narita A, Lee LJ et al (2012) Novel actin-like filament structure from Clostridium tetani. J Biol Chem 287:21121–21129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reuff AS, Chastanet A, Domínguez-Escobar J et al (2014) An early cytoplasmic step of peptidoglycan synthesis is associated to MreB in Bacillus subtilis. Mol Microbiol 91:348–362

    Article  Google Scholar 

  • Rivera CR, Kollman JM, Polka JK et al (2011) Architecture and assembly of a divergent member of the ParM family of bacterial actin-like proteins. J Biol Chem 286:14282–14290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salje J, van den Ent F, de Boer P et al (2011) Direct membrane binding by bacterial actin MreB. Mol Cell 43:478–487

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schirner K, Eun YJ, Dion M et al (2014) Lipid-linked cell wall precursors regulate membrane association of bacterial actin MreB. Nat Chem Biol 11:38–45

    Article  PubMed  PubMed Central  Google Scholar 

  • Shaevitz JW, Lee JY, Fletcher DA (2005) Spiroplasma swim by a processive change in body helicity. Cell 122:941–945

    Article  CAS  PubMed  Google Scholar 

  • Szwedziak P, Wang Q, Freund SM et al (2012) FtsA forms actin-like filaments. EMBO J 31:2249–2260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Szwedziak P, Wang Q, Bharat TA et al (2014) Architecture of the ring formed by the tubulin homologue FtsZ in bacterial cell division. eLife 10.04601

    Google Scholar 

  • Tan Q, Awano N, Inouye M (2011) YeeV is an Escherichia coli toxin that inhibits cell division by targeting the cytoskeletal proteins, FtsZ and MreB. Mol Microbiol 79:109–118

    Article  CAS  PubMed  Google Scholar 

  • Theriot JA (2013) Why are bacteria different from eukaryotes? BMC Biol 11:119

    Article  PubMed  PubMed Central  Google Scholar 

  • Treuner-Lange A, Macia E, Guzzo M et al (2015) The small G-protein MglA connects to the MreB actin cytoskeleton at bacterial focal adhesions. J Cell Biol 210:243–256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van den Ent F, Löwe J (2000) Crystal structure of the cell division protein FtsA from Thermotoga maritima. EMBO J 19:5300–5307

    Google Scholar 

  • van den Ent F, Møller-Jensen J, Amos LA et al (2002) F-actin-like filaments formed by plasmid segregation protein ParM. EMBO J 21:6935–6943

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • van den Ent F, Izoré T, Bharat TA et al (2014) Bacterial actin MreB forms antiparallel double filaments. eLife 3:e02634

    Google Scholar 

  • 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 108:15822–15827

    Article  PubMed  PubMed Central  Google Scholar 

  • Yakhnina AA, Gitai Z (2012) The small protein MbiA interacts with MreB and modulates shape in Caulobacter crescentus. Mol Microbiol 85:1090–1104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang F, Demma M, Warren V et al (1990) Identification of an actin-binding protein from Dictyostelium as elongation factor 1a. Nature 347:494–496

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The work in the lab is supported by INSPIRE Faculty Research Grant, Department of Science and Technology (DST), Government of India, and Innovative Young Biotechnologist Award, Department of Biotechnology, Government of India, Extra Mural Research Grant from DST and IISER Pune.

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Correspondence to Pananghat Gayathri .

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Gayathri, P. (2016). Bacterial Actins and Their Interactors. In: Mannherz, H. (eds) The Actin Cytoskeleton and Bacterial Infection. Current Topics in Microbiology and Immunology, vol 399. Springer, Cham. https://doi.org/10.1007/82_2016_31

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