A Dynamic Response Regulator Protein Modulates G-Protein–Dependent Polarity in the Bacterium

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Migrating cells employ sophisticated signal transduction systems to respond to their environment and polarize towards attractant sources. Bacterial cells also regulate their polarity dynamically to reverse their direction of movement. In Myxococcus xanthus, a GTP-bound Ras-like G-protein, MglA, activates the motility machineries at the leading cell pole. Reversals are provoked by pole-to-pole switching of MglA, which is under the control of a chemosensory-like signal transduction cascade (Frz). It was previously known that the asymmetric localization of MglA at one cell pole is regulated by MglB, a GTPase Activating Protein (GAP). In this process, MglB specifically localizes at the opposite lagging cell pole and blocks MglA localization at that pole. However, how MglA is targeted to the leading pole and how Frz activity switches the localizations of MglA and MglB synchronously remained unknown. Here, we show that MglA requires RomR, a previously known response regulator protein, to localize to the leading cell pole efficiently. Specifically, RomR-MglA and RomR-MglB complexes are formed and act complementarily to establish the polarity axis, segregating MglA and MglB to opposite cell poles. Finally, we present evidence that Frz signaling may regulate MglA localization through RomR, suggesting that RomR constitutes a link between the Frz-signaling and MglAB polarity modules. Thus, in Myxococcus xanthus, a response regulator protein governs the localization of a small G-protein, adding further insight to the polarization mechanism and suggesting that motility regulation evolved by recruiting and combining existing signaling modules of diverse origins.

Vyšlo v časopise: A Dynamic Response Regulator Protein Modulates G-Protein–Dependent Polarity in the Bacterium. PLoS Genet 8(8): e32767. doi:10.1371/journal.pgen.1002872
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002872

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Zdroje

1. TongZ, GaoX-D, HowellAS, BoseI, LewDJ, et al. (2007) Adjacent positioning of cellular structures enabled by a Cdc42 GTPase-activating protein-mediated zone of inhibition. J Cell Biol 179 : 1375–1384 doi:10.1083/jcb.200705160.

2. ZhangS, CharestPG, FirtelRA (2008) Spatiotemporal regulation of Ras activity provides directional sensing. Curr Biol 18 : 1587–1593 doi:10.1016/j.cub.2008.08.069.

3. ShapiroL, McAdamsHH, LosickR (2002) Generating and exploiting polarity in bacteria. Science 298 : 1942–1946.

4. BornensM (2008) Organelle positioning and cell polarity. Nat Rev Mol Cell Biol 9 : 874–886 doi:10.1038/nrm2524.

5. MaddockJR, ShapiroL (1993) Polar location of the chemoreceptor complex in the Escherichia coli cell. Science 259 : 1717–1723.

6. KomeiliA, LiZ, NewmanDK, JensenGJ (2006) Magnetosomes are cell membrane invaginations organized by the actin-like protein MamK. Science 311 : 242–245.

7. LamH, SchofieldWB, Jacobs-WagnerC (2006) A landmark protein essential for establishing and perpetuating the polarity of a bacterial cell. Cell 124 : 1011–1023.

8. HuitemaE, PritchardS, MattesonD, RadhakrishnanSK, ViollierPH (2006) Bacterial birth scar proteins mark future flagellum assembly site. Cell 124 : 1025–1037.

9. BowmanGR, ComolliLR, ZhuJ, EckartM, KoenigM, et al. (2008) A polymeric protein anchors the chromosomal origin/ParB complex at a bacterial cell pole. Cell 134 : 945–955 doi:10.1016/j.cell.2008.07.015.

10. EbersbachG, BriegelA, JensenGJ, Jacobs-WagnerC (2008) A self-associating protein critical for chromosome attachment, division, and polar organization in caulobacter. Cell 134 : 956–968 doi:10.1016/j.cell.2008.07.016.

11. RomantsovT, StalkerL, CulhamDE, WoodJM (2008) Cardiolipin controls the osmotic stress response and the subcellular location of transporter ProP in Escherichia coli. J Biol Chem 283 : 12314–12323 doi:10.1074/jbc.M709871200.

12. LópezD, KolterR (2010) Functional microdomains in bacterial membranes. Genes Dev 24 : 1893–1902 doi:10.1101/gad.1945010.

13. LenarcicR, HalbedelS, VisserL, ShawM, WuLJ, et al. (2009) Localisation of DivIVA by targeting to negatively curved membranes. EMBO J 28 : 2272–2282 doi:10.1038/emboj.2009.129.

14. RamamurthiKS, LecuyerS, StoneHA, LosickR (2009) Geometric cue for protein localization in a bacterium. Science 323 : 1354–1357 doi:10.1126/science.1169218.

15. IniestaAA, McGrathPT, ReisenauerA, McAdamsHH, ShapiroL (2006) A phospho-signaling pathway controls the localization and activity of a protease complex critical for bacterial cell cycle progression. Proc Natl Acad Sci USA 103 : 10935–10940 doi:10.1073/pnas.0604554103.

16. ZhangY, FrancoM, DucretA, MignotT (2010) A bacterial Ras-like small GTP-binding protein and its cognate GAP establish a dynamic spatial polarity axis to control directed motility. PLoS Biol 8: e1000430 doi:10.1371/journal.pbio.1000430.

17. LeonardyS, MiertzschkeM, BulyhaI, SperlingE, WittinghoferA, et al. (2010) Regulation of dynamic polarity switching in bacteria by a Ras-like G-protein and its cognate GAP. Embo J 29 : 2276–2289.

18. LiY, SunH, MaX, LuA, LuxR, et al. (2003) Extracellular polysaccharides mediate pilus retraction during social motility of Myxococcus xanthus. Proc Natl Acad Sci U S A 100 : 5443–5448.

19. NanB, ChenJ, NeuJC, BerryRM, OsterG, et al. (2011) Myxobacteria gliding motility requires cytoskeleton rotation powered by proton motive force. Proc Natl Acad Sci USA 108 : 2498–2503 doi:10.1073/pnas.1018556108.

20. LucianoJ, AgrebiR, Le GallAV, WartelM, FiegnaF, et al. (2011) Emergence and modular evolution of a novel motility machinery in bacteria. PLoS Genet 7: e1002268 doi:10.1371/journal.pgen.1002268.

21. SunM, WartelM, CascalesE, ShaevitzJW, MignotT (2011) Motor-driven intracellular transport powers bacterial gliding motility. Proc Natl Acad Sci USA 108 : 7559–7564 doi:10.1073/pnas.1101101108.

22. MignotT, MerlieJP, ZusmanDR (2005) Regulated pole-to-pole oscillations of a bacterial gliding motility protein. Science 310 : 855–857.

23. NudlemanE, WallD, KaiserD (2006) Polar assembly of the type IV pilus secretin in Myxococcus xanthus. Mol Microbiol 60 : 16–29.

24. BulyhaI, SchmidtC, LenzP, JakovljevicV, HöneA, et al. (2009) Regulation of the type IV pili molecular machine by dynamic localization of two motor proteins. Mol Microbiol 74 : 691–706 doi:10.1111/j.1365-2958.2009.06891.x.

25. MignotT, ShaevitzJW, HartzellPL, ZusmanDR (2007) Evidence that focal adhesion complexes power bacterial gliding motility. Science 315 : 853–856 doi:10.1126/science.1137223.

26. MiertzschkeM, KoernerC, VetterIR, KeilbergD, HotE, et al. (2011) Structural analysis of the Ras-like G protein MglA and its cognate GAP MglB and implications for bacterial polarity. EMBO J 30 : 4185–4197 doi:10.1038/emboj.2011.291.

27. MaurielloEM, MouhamarF, NanB, DucretA, DaiD, et al. (2010) Bacterial motility complexes require the actin-like protein, MreB and the Ras homologue, MglA. Embo J 29 : 315–326.

28. BulyhaI, HotE, HuntleyS, Søgaard-AndersenL (2011) GTPases in bacterial cell polarity and signalling. Curr Opin Microbiol 14 : 726–733 doi:10.1016/j.mib.2011.09.001.

29. LeonardyS, FreymarkG, HebenerS, EllehaugeE, Sogaard-AndersenL (2007) Coupling of protein localization and cell movements by a dynamically localized response regulator in Myxococcus xanthus. Embo J 26 : 4433–4444.

30. ShiW, ZusmanDR (1993) The two motility systems of Myxococcus xanthus show different selective advantages on various surfaces. Proc Natl Acad Sci USA 90 : 3378–3382.

31. BlackhartBD, ZusmanDR (1985) “Frizzy” genes of Myxococcus xanthus are involved in control of frequency of reversal of gliding motility. Proc Natl Acad Sci U S A 82 : 8767–8770.

32. AstlingDP, LeeJY, ZusmanDR (2006) Differential effects of chemoreceptor methylation-domain mutations on swarming and development in the social bacterium Myxococcus xanthus. Mol Microbiol 59 : 45–55.

33. CharestPG, FirtelRA (2007) Big roles for small GTPases in the control of directed cell movement. Biochem J 401 : 377–390.

34. WuSS, KaiserD (1995) Genetic and functional evidence that Type IV pili are required for social gliding motility in Myxococcus xanthus. Mol Microbiol 18 : 547–558.

35. NanB, MaurielloEMF, SunI-H, WongA, ZusmanDR (2010) A multi-protein complex from Myxococcus xanthus required for bacterial gliding motility. Mol Microbiol 76 : 1539–1554 doi:10.1111/j.1365-2958.2010.07184.x.

36. RennerLD, WeibelDB (2011) Cardiolipin microdomains localize to negatively curved regions of Escherichia coli membranes. Proc Natl Acad Sci USA 108 : 6264–6269 doi:10.1073/pnas.1015757108.

37. KeilbergD, WuichetK, DrescherF, Søgaard-AndersenL (2012) A response regulator interfaces between the Frz chemosensory system and the MglA/MglB GTPase/GAP module to regulate polarity in Myxococcus xanthus. Submitted

38. InclanYF, VlamakisHC, ZusmanDR (2007) FrzZ, a dual CheY-like response regulator, functions as an output for the Frz chemosensory pathway of Myxococcus xanthus. Mol Microbiol 65 : 90–102.

39. InclanYF, LaurentS, ZusmanDR (2008) The receiver domain of FrzE, a CheA-CheY fusion protein, regulates the CheA histidine kinase activity and downstream signalling to the A -⁠ and S-motility systems of Myxococcus xanthus. Mol Microbiol 68 : 1328–1339.

40. KirkpatrickCL, ViollierPH (2012) Decoding Caulobacter development. FEMS Microbiol Rev 36 : 193–205 doi:10.1111/j.1574-6976.2011.00309.x.

41. TsokosCG, PerchukBS, LaubMT (2011) A dynamic complex of signaling proteins uses polar localization to regulate cell-fate asymmetry in Caulobacter crescentus. Dev Cell 20 : 329–341 doi:10.1016/j.devcel.2011.01.007.

42. PaulR, WeiserS, AmiotNC, ChanC, SchirmerT, et al. (2004) Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Genes Dev 18 : 715–727 doi:10.1101/gad.289504.

43. AbelS, ChienP, WassmannP, SchirmerT, KaeverV, et al. (2011) Regulatory cohesion of cell cycle and cell differentiation through interlinked phosphorylation and second messenger networks. Mol Cell 43 : 550–560 doi:10.1016/j.molcel.2011.07.018.

44. JenalU, GalperinMY (2009) Single domain response regulators: molecular switches with emerging roles in cell organization and dynamics. Curr Opin Microbiol 12 : 152–160 doi:10.1016/j.mib.2009.01.010.

45. BustamanteVH, Martinez-FloresI, VlamakisHC, ZusmanDR (2004) Analysis of the Frz signal transduction system of Myxococcus xanthus shows the importance of the conserved C-terminal region of the cytoplasmic chemoreceptor FrzCD in sensing signals. Mol Microbiol 53 : 1501–1513.

46. DucretA, MaisonneuveE, NotareschiP, GrossiA, MignotT, et al. (2009) A microscope automated fluidic system to study bacterial processes in real time. PLoS ONE 4: e7282 doi:10.1371/journal.pone.0007282.