ATP control of dynamic P1 ParA–DNA interactions: a key role for the nucleoid in plasmid partition

Abstract

Summary P1 ParA is a member of the Walker‐type family of partition ATPases involved in the segregation of plasmids and bacterial chromosomes. ATPases of this class interact with DNA non‐specifically in vitro and colocalize with the bacterial nucleoid to generate a variety of reported patterns in vivo . Here, we directly visualize ParA binding to DNA using total internal reflection fluorescence microscopy. This activity depends on, and is highly specific for ATP. DNA‐binding activity is not coupled to ATP hydrolysis. Rather, ParA undergoes a slow multi‐step conformational transition upon ATP binding, which licenses ParA to bind non‐specific DNA. The kinetics provide a time‐delay switch to allow slow cycling between the DNA binding and non‐binding forms of ParA. We propose that this time delay, combined with stimulation of ParA's ATPase activity by ParB bound to the plasmid DNA, generates an uneven distribution of the nucleoid‐associated ParA, and provides the motive force for plasmid segregation prior to cell division.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 46

1. 1.

   Atmakuri K, Cascales E, Burton OT, Banta LM, Christie PJ. Agrobacterium ParA/MinD-like VirC1 spatially coordinates early conjugative DNA transfer reactions. EMBO J. 2007;26:2540-2551.

   Not in our library10.1038/sj.emboj.7601696

2. 2.

   Barillà D, Rosenberg MF, Nobbmann U, Hayes F. Bacterial DNA segregation dynamics mediated by the polymerizing protein ParF. EMBO J. 2005;24:1453-1464.

   Not in our library10.1038/sj.emboj.7600619

3. 3.

   Berlatzky IA, Rouvinski A, Ben-Yehuda S. Spatial organization of a replicating bacterial chromosome. Proc Natl Acad Sci USA. 2008;105:14136-14140.

   Not in our library10.1073/pnas.0804982105

4. 4.

   Bouet J-Y, Funnell BE. P1 ParA interacts with the P1 partition complex at parS and an ATP-ADP switch controls ParA activities. EMBO J. 1999;18:1415-1424.

   Not in our library10.1093/emboj/18.5.1415

5. 5.

   Bouet J-Y, Ah-Seng Y, Benmeradi N, Lane D. Polymerization of SopA partition ATPase: regulation by DNA binding and SopB. Mol Microbiol. 2007;63:468-481.

   Not in our library10.1111/j.1365-2958.2006.05537.x

6. 6.

   Castaing J-P, Bouet J-Y, Lane D. F plasmid partition depends on interaction of SopA with non-specific DNA. Mol Microbiol. 2008;70:1000-1011.

   Not in our library10.1111/j.1365-2958.2008.06465.x

7. 7.

   Cremo CR, Yount RG. 2′-Deoxy-3′-O-(4-benzoylbenzoyl)- and 3′(2′)-O-(4-benzoylbenzoyl)-1,N6-ethenoadenosine 5′-diphosphate, fluorescent photoaffinity analogs of adenosine 5′-diphosphate. Synthesis, characterization, and interaction with myosin subfragment 1. Biochemistry. 1987;26:7524-7534.

   Not in our library10.1021/bi00397a048

8. 8.

   Davey M, Funnell BE. The P1 plasmid partition protein ParA: a role for ATP in site-specific DNA binding. J Biol Chem. 1994;269:29908-29913.

   Not in our library

9. 9.

   Davey M, Funnell BE. Modulation of the P1 plasmid partition protein ParA by ATP, ADP, and P1 ParB. J Biol Chem. 1997;272:15286-15292.

   Not in our library10.1074/jbc.272.24.15286

10. 10.

    Davis MA, Martin KA, Austin SJ. Biochemical activities of the ParA partition protein of the P1 plasmid. Mol Microbiol. 1992;6:1141-1147.

    Not in our library10.1111/j.1365-2958.1992.tb01552.x

11. 11.

    Davis MA, Radnedge L, Martin KA, Hayes F, Youngren B, Austin SJ. The P1 ParA protein and its ATPase activity play a direct role in the segregation of plasmid copies to daughter cells. Mol Microbiol. 1996;21:1029-1036.

    Not in our library10.1046/j.1365-2958.1996.721423.x

12. 12.

    Drew DA, Osborn MJ, Rothfield LI. A polymerization-depolymerization model that accurately generates the self-sustained oscillatory system involved in bacterial division site placement. Proc Natl Acad Sci USA. 2005;102:6114-6118.

    Not in our library10.1073/pnas.0502037102

13. 13.

    Dunham TD, Xu W, Funnell BE, Schumacher MA. Structural basis for ADP-mediated transcriptional regulation by P1 and P7 ParA. EMBO J. 2009;28:1792-1802.

    Not in our library10.1038/emboj.2009.120

14. 14.

    Ebersbach G, Gerdes K. Bacterial mitosis: partitioning protein ParA oscillates in spiral-shaped structures and positions plasmids at mid-cell. Mol Microbiol. 2004;52:385-398.

    Not in our library10.1111/j.1365-2958.2004.04002.x

15. 15.

    Ebersbach G, Ringgaard S, Moller-Jensen J, Wang Q, Sherratt DJ, Gerdes K. Regular cellular distribution of plasmids by oscillating and filament-forming ParA ATPase of plasmid pB171. Mol Microbiol. 2006;61:1428-1442.

    Not in our library10.1111/j.1365-2958.2006.05322.x

16. 16.

    Elowitz MB, Surette MG, Wolf P-E, Stock JB, Leibler S. Protein mobility in the cytoplasm of Escherichia coli. J Bacteriol. 1999;181:197-203.

    Not in our library10.1128/jb.181.1.197-203.1999

17. 17.

    Erdmann N, Petroff T, Funnell BE. Intracellular localization of P1 ParB protein depends on ParA and parS. Proc Natl Acad Sci USA. 1999;96:14905-14910.

    Not in our library10.1073/pnas.96.26.14905

18. 18.

    Ezaki B, Ogura T, Niki H, Hiraga S. Partitioning of a mini-F plasmid into anucleate cells of the mukB null mutant. J Bacteriol. 1991;173:6643-6646.

    Not in our library10.1128/jb.173.20.6643-6646.1991

19. 19.

    Fogel MA, Waldor MK. A dynamic, mitotic-like mechanism for bacterial chromosome segregation. Genes Dev. 2006;20:3269-3282.

    Not in our library10.1101/gad.1496506

20. 20.

    Fung E, Bouet J-Y, Funnell BE. Probing the ATP-binding site of P1 ParA: partition and repression have different requirements for ATP binding and hydrolysis. EMBO J. 2001;20:4901-4911.

    Not in our library10.1093/emboj/20.17.4901

21. 21.

    Funnell BE, Gagnier L. Partition of P1 plasmids in Escherichia coli mukB chromosomal partition mutants. J Bacteriol. 1995;177:2381-2386.

    Not in our library10.1128/jb.177.9.2381-2386.1995

22. 22.

    Garner EC, Campbell CS, Weibel DB, Mullins RD. Reconstitution of DNA segregation driven by assembly of a prokaryotic actin homolog. Science. 2007;315:1270-1274.

    Not in our library10.1126/science.1138527

23. 23.

    Gerdes K, Moller-Jensen J, Jensen RB. Plasmid and chromosome partitioning: surprises from phylogeny. Mol Microbiol. 2000;37:455-466.

    Not in our library10.1046/j.1365-2958.2000.01975.x

24. 24.

    Greene EC, Mizuuchi K. Direct observation of single MuB polymers: evidence for a DNA-dependent conformational change for generating an active target complex. Mol Cell. 2002;9:1079-1089.

    Not in our library10.1016/s1097-2765(02)00514-2

25. 25.

    Hatano T, Yamaichi Y, Niki H. Oscillating focus of SopA associated with filamentous structure guides partitioning of F plasmid. Mol Microbiol. 2007;64:1198-1213.

    Not in our library10.1111/j.1365-2958.2007.05728.x

26. 26.

    Hester CM, Lutkenhaus J. Soj (ParA) DNA binding is mediated by conserved arginines and is essential for plasmid segregation. Proc Natl Acad Sci USA. 2007;104:20326-20331.

    Not in our library10.1073/pnas.0705196105

27. 27.

    Ho TQ, Zhong Z, Aung S, Pogliano J. Compatible bacterial plasmids are targeted to independent cellular locations in Escherichia coli. EMBO J. 2002;21:1864-1872.

    Not in our library10.1093/emboj/21.7.1864

28. 28.

    Howard M, Rutenberg AD, de Vet S. Dynamic compartmentalization of bacteria: accurate division in E. coli. Phys Rev Lett. 2001;87:278102.

    Not in our library10.1103/physrevlett.87.278102

29. 29.

    Huang KC, Meir Y, Wingreen NS. Dynamic structures in Escherichia coli: spontaneous formation of MinE rings and MinD polar zones. Proc Natl Acad Sci USA. 2003;100:12724-12728.

    Not in our library10.1073/pnas.2135445100

30. 30.

    Ivanov V, Mizuuchi K. Multiple modes of interconverting dynamic pattern formation by bacterial cell division proteins. Proc Natl Acad Sci USA. 2010;107:8071-8078.

    Not in our library10.1073/pnas.0911036107

31. 31.

    Kruse K. A dynamic model for determining the middle of Escherichia coli. Biophys J. 2002;82:618-627.

    Not in our library10.1016/s0006-3495(02)75426-x

32. 32.

    Leonard TA, Butler PJ, Löwe J. Bacterial chromosome segregation: structure and DNA binding of the Soj dimer – a conserved biological switch. EMBO J. 2005;24:270-282.

    Not in our library10.1038/sj.emboj.7600530

33. 33.

    Lim GE, Derman AI, Pogliano J. Bacterial DNA segregation by dynamic SopA polymers. Proc Natl Acad Sci USA. 2005;102:17658-17663.

    Not in our library10.1073/pnas.0507222102

34. 34.

    Marston AL, Errington J. Dynamic movement of the ParA-like Soj protein of B. subtilis and its dual role in nucleoid organization and developmental regulation. Mol Cell. 1999;4:673-682.

    Not in our library10.1016/s1097-2765(00)80378-0

35. 35.

    Meinhardt H, deBoer PAJ. Pattern formation in Escherichia coli: a model for the pole-to-pole oscillations of Min proteins and the localization of the division site. Proc Natl Acad Sci USA. 2001;98:14202-14207.

    Not in our library10.1073/pnas.251216598

36. 36.

    Moller-Jensen J, Borch J, Dam M, Jensen RB, Roepstorff P, Gerdes K. Bacterial mitosis: ParM of plasmid R1 moves plasmid DNA by an actin-like insertional polymerization mechanism. Mol Cell. 2003;12:1477-1487.

    Not in our library10.1016/s1097-2765(03)00451-9

37. 37.

    Pratto F, Cicek A, Weihofen WA, Lurz R, Saenger W, Alonso JC. Streptococcus pyogenes pSM19035 requires dynamic assembly of ATP-bound ParA and ParB on parS DNA during plasmid segregation. Nucleic Acids Res. 2008;36:3676-3689.

    Not in our library10.1093/nar/gkn170

38. 38.

    Quisel JD, Lin DCH, Grossman AD. Control of development by altered localization of a transcription factor in B. subtilis. Mol Cell. 1999;4:665-672.

    Not in our library10.1016/s1097-2765(00)80377-9

39. 39.

    Raskin DM, deBoer PAJ. Rapid pole-to-pole oscillation of a protein required for directing division to the middle of Escherichia coli. Proc Natl Acad Sci USA. 1999;96:4971-4976.

    Not in our library10.1073/pnas.96.9.4971

40. 40.

    Ringgaard S, van Zon J, Howard M, Gerdes K. Movement and equipositioning of plasmids by ParA filament disassembly. Proc Natl Acad Sci USA. 2009;106:19369-19374.

    Not in our library10.1073/pnas.0908347106

Cited by papers we hold 3

• Bacterial chromosome segregation by the ParABS system · 2020
  No notice
• ParAB Partition Dynamics in Firmicutes: Nucleoid Bound ParA Captures and Tethers ParB-Plasmid Complexes. · 2015
  Not checked
• Evidence for a DNA-relay mechanism in ParABS-mediated chromosome segregation · 2014
  No notice

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.