Insight into the assembly properties and functional organisation of the magnetotactic bacterial actin-like homolog, MamK

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Sonkaria, Sanjiv ^a   Fuentes, Gloria ^b   Verma, Chandra ^b,c,d   Narang, Ram ^e   Khare, Varsha ^a   Fischer, Anna ^f   Faivre, Damien ^a  

^a MAX PLANCK INSTITUTE OF COLLOIDS AND INTERFACES   (Germany)

^b BIOINFORMATICS INSTITUTE   (Singapore)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^e MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^f TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ADENOSINE TRIPHOSPHATASE; BACTERIAL PROTEIN; CYTOSKELETON PROTEIN; GUANOSINE TRIPHOSPHATASE; MAMK PROTEIN; METAL ION; MREB PROTEIN; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATE; GUANOSINE TRIPHOSPHATE;

ARTICLE; BACTERIAL GENE; BACTERIUM; CIRCULAR DICHROISM; CONTROLLED STUDY; ELECTRIC POTENTIAL; FLUORESCENCE MICROSCOPY; GENE DELETION; GENE EXPRESSION; IN VITRO STUDY; LIGHT SCATTERING; MAGNETOSOME; MAGNETOSPIRILLUM; MAGNETOSPIRILLUM GRYPHISWALDENSE; MAGNETOTACTIC BACTERIUM; MAMK GENE; MICROFILAMENT; MOLECULAR CLONING; NONHUMAN; PH; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; SEQUENCE HOMOLOGY; STRUCTURAL HOMOLOGY; TEMPERATURE DEPENDENCE; TRANSMISSION ELECTRON MICROSCOPY; ACTIN FILAMENT; AMINO ACID SEQUENCE; CHEMISTRY; ENZYMOLOGY; GENETICS; ISOLATION AND PURIFICATION; MAGNETIC FIELD; MOLECULAR GENETICS; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; ULTRASTRUCTURE;

BACTERIA (MICROORGANISMS);

ACTIN CYTOSKELETON; ACTINS; ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CIRCULAR DICHROISM; GENE DELETION; GUANOSINE TRIPHOSPHATE; MAGNETIC FIELDS; MAGNETOSOMES; MAGNETOSPIRILLUM; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN MULTIMERIZATION;

EID: 84860617794     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0034189     Document Type: Article

References (50)

1. Carballido-López R, (2006) The bacterial actin-like skeleton. Microbiol Mol Biol Rev 17: 266-272.
2. Michie KA, Löwe J, (2006) Dynamic filaments of the bacterial cytoskeleton. Ann Rev Biochem 75: 467-492.
3. Van den Ent F, Moller-Jensen J, Amos LA, Gerdes K, Lowe J, (2002) F-actin-like filaments formed by plasmid segregation protein ParM. EMBO J 21: 6935-6943.
4. Ding Y, Li J, Liu J, Yang J, Jiang W, et al. (2010) Deletion of the ftsZ-like gene results in the production of superparamagnetic magnetite magnetosomes in Magnetospirillum gryphiswaldense. J Bacteriol 192: 1097-1105.
5. Romberg L, Simon M, Erickson HP, (2001) Polymerization of FtsZ, a bacterial homolog of tubulin: Is assembly cooperative? J Biol Chem 276: 11743-11753.
6. Van den Ent F, Amos LA, Lowe J, (2001) Prokaryotic origin of the actin cytoskeleton. Nature 413: 39-44.
7. Schirner K, Errington J, (2009) Influence of the heterogonous MreB proteins on cell morphology of Bacillus subtilis. Microbiol 155: 36211-3621.
8. Margolin W, (2009) Sculpting the bacterial cell. Curr Biol 15: 812-822.
9. Graumann PL, (2007) Cytoskeletal elements in bacteria. Ann Rev Microbiol 61: 589-618.
10. Faivre D, Schüler D, (2008) Magnetotactic bacteria and magnetosomes. Chem Rev 108: 4875-4898.
11. Komeili A, Li Z, Newman DK, Jensen GJ, (2006) Magnetosomes are cell membrane invaginations organized by the actin-like protein MamK. Sci 311: 242-245.
12. Pradel N, Santini CL, Bernadac A, Fukumori Y, Wu LF, (2006) Biogenesis of actin-like bacterial cytoskeletal filaments destined for positioning prokaryotic magnetic organelles. Proc Natl Acad Sci U S A 103: 17485-17489.
13. Derman AI, Becker EC, Truong BD, Fujioka A, Tucey TM, 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: 532-534.
14. Mayer JA, Amann KJ, (2009) Assembly properties of the Bacillus subtilis actin, MreB. Cell Mot Cyto 66: 109-118.
15. Esue O, Cordero M, Writz D, Tseng Y, (2005) The assembly of MreB, a prokaryotic homolog of actin. J Biol Chem 280: 2628-2635.
16. Bean GJ, Amann KJ, (2008) Polymerization properties of the T. maritma actin, MreB: Roles of temperature, nucleotides and ions. Biochemistry 47: 826-835.
17. Schübbe S, Williams TJ, Xie G, Kiss HE, Brettin TS, et al. (2009) Complete genome sequence of the chemolithoautotrophic marine magnetotactic coccus strain MC-1. Appl Environ Microbiol 75: 4835-4852.
18. Faivre D, Fischer A, Garcia-Rubio I, Mastrogiacomo G, Gehring AU, (2010) Development of cellular magnetic dipoles in magnetotactic bacteria. Biophys J 99: 1268-1273.
19. Katzmann E, Scheffel A, Gruska M, Plitzko JM, Schüler D, (2010) Loss of the actin-like protein MamK has pleiotropic effects on magnetosome formation and chain assembly in Magnetospirillum gryphiswaldense. Mol Microbiol 77: 208-224.
20. Taoka A, Asada R, Wu LF, Fukumori Y, (2007) Polymerization of the actin-like protein MamK, which is associated with magnetosomes. J Bacteriol 189: 8737-8740.
21. Rioux JB, Philippe N, Pereira S, Pignol D, Wu LF, et al. (2010) A second actin-like MamK protein in Magnetospirillum magneticum AMB-1 encoded outside the genomic magnetosome Island. PLoS ONE 5: 1-12.
22. Ullrich S, Kube M, Schübbe S, Reinhardt R, Schüler D, (2005) A hypervariable 130-kilobase genomic region of Magnetospirillum gryphiswaldense comprises a magnetosome island which undergoes frequent rearrangements during stationary growth. J Bacteriol 187: 7176-7184.
23. Tobacman LS, Korn ED, (1983) The kinetics of actin nucleation and polymerization. J Biol Chem 258: 3207-3214.
24. Kasai M, Asakura S, Oosawa F, (1962) The cooperative nature of G-F transformation of actin. Biochim Bio Phys Acta 57: 22-31.
25. Oosawa F, Asakura S, (1975) Thermodynamics of the polymerization of protein. Academic Press, London 41-51.
26. Gershman LC, Selden LA, Kinosian HJ, Easts JE, (1989) Preparation and polymerisation properties of monomeric ADP-actin. Biochim Biophys Acta 995: 109-115.
27. Pollard TD, Goldberg I, Schwarz WH, (1992) Nucleotide exchange, structure and mechanical properties of filaments assembled from ATP-actin and ADP-actin. J Biol Chem 267: 20339-20345.
28. Suck D, Kabsch W, Mannherz HG, (1981) Three-dimensional structure of the complex of skeletal muscle actin and bovine pancreatic DNase I at 6Å resolution. Pro Nat Acad Sci 78: 4319-4323.
29. Lorenz M, Popp D, Holmes K, (1993) Refinement of the F-acin model against X-ray fiber diffraction data by the use of a directed mutation algorithm. J Mol Biol 234: 826-836.
30. Bettache N, Bertrand R, Kassab R, (1990) Maleimidobenzoyl-G-actin: structural properties and interaction with skeletal, myosin subfragment-1. Biochemistry 29: 9085-9091.
31. Tilney LG, Connelly PS, Vranich KA, Shaw MK, Guild GM, (2000) Regulation of actin filament cross-linking and bundle shape in Drosophila bristles. J Cell Biol 148: 87-100.
32. Claessens MMAE, Semmrich C, Ramos L, Bausch AR, (2008) Helical twist controls the thickness of F-actin bundles. Proc Nat Acad Sci 105: 8819-8822.
33. Eswar N, Marti-Renom MA, Webb B, Madhusudhan MS, Eramian D, et al. (2006) Comparative protein structure modeling with MODELLER. Current Protocols in Bioinformatics 15: 5.6.1-5.6.30.
34. Jaroszewski L, Rychlewski L, Li Z, Li W, Godzik A, (2005) FFAS03: a server for profile-profile sequence alignments. Nucleic Acid Res 33: W284-W288.
35. Peer B, Sander C, Valencia A, (1992) An ATPase domain common to prokaryotic cell cycle proteins, sugar kinases, actin, and hsp7O heat shock proteins Proc Natl Acad Sci U S A 89: 7290-7294.
36. Esue O, Writz D, Tseng Y, (2006) GTPase activity, structure and mechanical properties of filaments assembled from bacterial cytoskeleton protein MreB. J Bacteriol 188: 968-976.
37. Golaszewska HS, Drabikowski W, (1968) Studies on the exchange of G-actin bound calcium with bivalent calcium ions. Biochim Biophys Acta 162: 581-595.
38. 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.
39. Bartles JR, (2000) Parallel actin bundles and their multiple actin-bundling proteins. Current Opinion in Cell Biology 12: 72-78.
40. Lieleg O, Schmoller KM, Cyron CJ, Luan Y, Wall WA, et al. (2009) Structural polymorphism in heterogeneous cytoskeletal networks. Soft Matter 5: 1796-1803.
41. Bombardier H, Wong P, Gicquaud C, (1997) Effects of nucleotides on the denaturation of F-Actin: A differential scanning calorimetry and FTIR spectroscopy study. Biophys Res Comm 236: 798-803.
42. Combeau C, Carlier MF, (1988) Probing the mechanism of ATP Hydrolysis on F-actin using vanadate and the structural analogs of phosphate BeF and AlF. J Biol Chem 263: 17429-17436.
43. Takacs FP, Matula TI, Macleod RA, (1964) Nutrition and metabolism of marine bacteria. J Bact 87: 510-518.
44. Scheffel A, Manuela G, Faivre D, Schüler D, (2006) An acidic protein aligns magnetosomes along a filamentous structure in magnetotactic bacteria. Nature 440: 110-114.
45. Popp D, Narita A, Maeda K, Fujisawa T, Ghoshdastider U, et al. (2010) Filament structure, organization, and dynamics in MreB Sheets. J Biol Chem 285: 15858-15865.
46. Smith MJ, Sheehan PE, Perry LL, O'Connor K, Csonka LN, et al. (2006) Quantifying the magnetic advantage in magnetotaxis. Biophys J 91: 1098-1107.
47. Sael L, La D, Li B, Rustamov R, Kihara D, (2008) Rapid comparison of properties on protein surface. Proteins 73: 1-10.
48. Studier FW, (2005) Protein production by auto-induction in high-density shaking cultures. Prot Exp Purif 41: 207-234.
49. Abramoff MD, Magalhaes PJ, Ram SJ, (2004) Image processing with ImageJ Biophotonics International 11: 36-42.
50. Geladopoulos TP, Sotiroudis TG, Evangelopoulos A, (1991) A malachite green colorimetric assay for protein phosphatase activity. Anal Biochem 192: 112-116.