Abstract
One of the well-known functions of the bacterial cytoskeleton is plasmid segregation. Type II plasmid segregation systems, among the best characterized with respect to the mechanism of action, possess an actin-like cytomotive filament as the motor component. This chapter describes the essential components of the plasmid segregation machinery and their mechanism of action, concentrating on the actin-like protein family of the bacterial cytoskeleton. The structures of the actin-like filaments depend on their nucleotide state and these in turn contribute to the dynamics of the filaments. The components that link the filaments to the plasmid DNA also regulate filament dynamics. The modulation of the dynamics facilitates the cytomotive filament to function as a mitotic spindle with a minimal number of components.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Becker E, Herrera NC, Gunderson FQ et al (2006) DNA segregation by the bacterial actin AlfA during Bacillus subtilis growth and development. EMBO J 25:5919–5931. doi:10.1038/sj.emboj.7601443
Bharat TAM, Murshudov GN, Sachse C, Löwe J (2015) Structures of actin-like ParM filaments show architecture of plasmid-segregating spindles. Nature 523:106–110. doi:10.1038/nature14356
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 U S A 89:7290–7294. doi:10.1073/pnas.89.16.7290
Campbell CS, Mullins RD (2007) In vivo visualization of type II plasmid segregation: bacterial actin filaments pushing plasmids. J Cell Biol 179:1059–1066. doi:10.1083/jcb.200708206
Dam M, Gerdes K (1994) Partitioning of plasmid R1 Ten direct repeats flanking the parA promoter constitute a centromere-like partition site parC, that expresses incompatibility. J Mol Biol 236:1289–1298. doi:10.1016/0022-2836(94)90058-2
Derman AI, Nonejuie P, Michel BC et al (2012) Alp7R regulates expression of the actin-like protein Alp7A in Bacillus subtilis. J Bacteriol 194:2715–2724. doi:10.1128/JB.06550-11
Dominguez R, Holmes KC (2011) Actin structure and function. Annu Rev Biophys 40:169–186. doi:10.1146/annurev-biophys-042910-155359
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 2–7:E1845–E1870. doi:10.1073/pnas.1423746112
Fujii T, Iwane AH, Yanagida T, Namba K (2010) Direct visualization of secondary structures of F-actin by electron cryomicroscopy. Nature 467:724–728. doi:10.1038/nature09372
Galkin VE, Orlova A, Rivera C et al (2009) Structural polymorphism of the ParM filament and dynamic instability. Structure 17:1253–1264. doi:10.1016/j.str.2009.07.008
Garner EC (2007) Reconstitution of DNA Segregation. Science 315:1270–1274. doi:10.1126/science.1138527
Garner EC, Campbell CS, Mullins RD (2004) Dynamic instability in a DNA-segregating prokaryotic actin homolog. Science 306:1021–1025. doi:10.1126/science.1101313
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. doi:10.1126/science.1229091
Gayathri P, Fujii T, Namba K, Löwe J (2013) Structure of the ParM filament at 8.5Å resolution. J Struct Biol 184:33–42. doi:10.1016/j.jsb.2013.02.010
Gerdes K, Molin S (1986) Partitioning of plasmid R1. J Mol Biol 190:269–279. doi:10.1016/0022-2836(86)90001-X
Gerdes K, Howard M, Szardenings F (2010) Pushing and pulling in prokaryotic DNA segregation. Cell 141:927–942. doi:10.1016/j.cell.2010.05.033
Gunning PW, Ghoshdastider U, Whitaker S et al (2015) The evolution of compositionally and functionally distinct actin filaments. J Cell Sci 128:2009–2019. doi:10.1242/jcs.165563
Jensen RB, Gerdes K (1997) Partitioning of plasmid R1. The ParM protein exhibits ATPase activity and interacts with the centromere-like ParR-parC complex. J Mol Biol 269:505–513. doi:10.1006/jmbi.1997.1061
Löwe J, Amos LA (2009) Evolution of cytomotive filaments: te cytoskeleton from prokaryotes to eukaryotes. Int J Biochem Cell Biol 41:323–329. doi:10.1016/j.biocel.2008.08.010
Møller-Jensen J, Jensen RB, Löwe J, Gerdes K (2002) Prokaryotic DNA segregation by an actin-like filament. EMBO J 21:3119–3127. doi:10.1093/emboj/cdf320
Møller-Jensen J, Borch J, Dam M et al (2003) Bacterial mitosis: ParM of plasmid R1 moves plasmid DNA by an actin-like insertional polymerization mechanism. Mol Cell 12:1477–1487. doi:10.1016/S1097-2765(03)00451-9
Møller-Jensen J, Ringgaard S, Mercogliano CP et al (2007) Structural analysis of the ParR/parC plasmid partition complex. EMBO J 26:4413–4422. doi:10.1038/sj.emboj.7601864
Orlova A, Garner EC, Galkin VE et al (2007) The structure of bacterial ParM filaments. Nat Struct Mol Biol 14:921–926
Ozyamak E, Kollman J, Agard DA, Komeili A (2013) The bacterial actin MamK: in vitro assembly behavior and filament architecture. J Biol Chem 288:4265–4277. doi:10.1074/jbc.M112.417030
Pei J, Tang M, Grishin NV (2008) PROMALS3D web server for accurate multiple protein sequence and structure alignments. Nucleic Acids Res 36:W30–W34. doi:10.1093/nar/gkn322
Petek NA, Mullins RD (2014) Bacterial actin-like proteins: purification and characterization of self-assembly properties. Methods Enzymol 540:19–34. doi:10.1016/B978-0-12-397924-7.00002-9
Polka JK, Kollman JM, Agard DA, Mullins RD (2009) The structure and assembly dynamics of plasmid actin AlfA imply a novel mechanism of DNA segregation. J Bacteriol 191:6219–6230. doi:10.1128/JB.00676-09
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. doi:10.1073/pnas.1304127111
Pollard TD (1986) Rate constants for the reactions of ATP-and ADP-actin with the ends of actin filaments. J Cell Biol 103:2747. doi:10.1083/jcb.103.6.2747
Popp D, Narita A, Oda T et al (2008) Molecular structure of the ParM polymer and the mechanism leading to its nucleotide-driven dynamic instability. EMBO J 27:570–579. doi:10.1038/sj.emboj.7601978
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. doi:10.1074/jbc.M109.071613
Popp D, Narita A, Lee LJ et al (2012) Novel actin-like filament structure from Clostridium tetani. J Biol Chem 287:21121–21129. doi:10.1074/jbc.M112.341016
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. doi:10.1074/jbc.M110.203828
Salje J, Löwe J (2008) Bacterial actin: architecture of the ParMRC plasmid DNA partitioning complex. EMBO J 27:2230–2238. doi:10.1038/emboj.2008.152
Salje J, Zuber B, Löwe J (2009) Electron cryomicroscopy of E. coli reveals filament bundles involved in plasmid DNA segregation. Science 323:509–512. doi:10.1126/science.1164346
Salje J, Gayathri P, Löwe J (2010) The ParMRC system: molecular mechanisms of plasmid segregation by actin-like filaments. Nat Rev Microbiol 8:683–692. doi:10.1038/nrmicro2425
Schumacher MA, Glover TC, Brzoska AJ et al (2007) Segrosome structure revealed by a complex of ParR with centromere DNA. Nature 450:1268–1271. doi:10.1038/nature06392
Schumacher MA, Tonthat NK, Lee J et al (2015) Structures of archaeal DNA segregation machinery reveal bacterial and eukaryotic linkages. Science 349:1120–1124. doi:10.1126/science.aaa9046
Szwedziak P, Wang Q, Freund SM, Löwe J (2012) FtsA forms actin-like protofilaments. EMBO J 31:2249–2260. doi:10.1038/emboj.2012.76
Tanaka T (2010) Functional analysis of the stability determinant AlfB of pBET131, a miniplasmid derivative of Bacillus subtilis (natto) plasmid pLS32. J Bacteriol 192:1221–1230. doi:10.1128/JB.01312-09
van den Ent F, Amos LA, Löwe J (2001) Prokaryotic origin of the actin cytoskeleton. Nature 413:39–44. doi:10.1038/35092500
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. doi:10.1093/emboj/cdf672
Acknowledgements
The work in the lab is supported by INSPIRE Faculty Research Grant, Department of Science and Technology (DST), India, and Innovative Young Biotechnologist Award, Department of Biotechnology, India. PG and SH acknowledge INSPIRE (DST) and IISER-Pune fellowships.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer International Publishing AG
About this chapter
Cite this chapter
Gayathri, P., Harne, S. (2017). Structure and Dynamics of Actin-Like Cytomotive Filaments in Plasmid Segregation. In: Löwe, J., Amos, L. (eds) Prokaryotic Cytoskeletons. Subcellular Biochemistry, vol 84. Springer, Cham. https://doi.org/10.1007/978-3-319-53047-5_10
Download citation
DOI: https://doi.org/10.1007/978-3-319-53047-5_10
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-53045-1
Online ISBN: 978-3-319-53047-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)