MinD-like ATPase FlhG effects location and number of bacterial flagella during C-ring assembly
10.1073/pnas.1419388112
Crossref journal-article
Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences (341)
Abstract

Significance Flagella are bacterial organelles of locomotion. The number and location of flagella (flagellation pattern) are species specific and represent one of the earliest taxonomic criteria in microbiology. During each round of cell division, bacteria reproduce their flagellation pattern. FlhG is essential to a variety of flagellation patterns (e.g., polar, lateral) by yet-unknown mechanisms. We show that FlhG is an MinD-like ATPase that interacts with the flagellar C-ring proteins FliM/FliY in a nucleotide-independent manner. FlhG activates FliM/FliY to assemble with the C-ring protein FliG. FlhG-driven assembly of the FliM/FliY/FliG complex is strongly enhanced by ATP and lipids. We identify an underappreciated structural diversity of flagellar building blocks that contribute to formation of different flagellation patterns.

Bibliography

Schuhmacher, J. S., Rossmann, F., Dempwolff, F., Knauer, C., Altegoer, F., Steinchen, W., Dörrich, A. K., Klingl, A., Stephan, M., Linne, U., Thormann, K. M., & Bange, G. (2015). MinD-like ATPase FlhG effects location and number of bacterial flagella during C-ring assembly. Proceedings of the National Academy of Sciences, 112(10), 3092–3097.

Authors 12
  1. Jan S. Schuhmacher (first)
  2. Florian Rossmann (additional)
  3. Felix Dempwolff (additional)
  4. Carina Knauer (additional)
  5. Florian Altegoer (additional)
  6. Wieland Steinchen (additional)
  7. Anja K. Dörrich (additional)
  8. Andreas Klingl (additional)
  9. Milena Stephan (additional)
  10. Uwe Linne (additional)
  11. Kai M. Thormann (additional)
  12. Gert Bange (additional)
References 47 Referenced 96
  1. FF Chevance, KT Hughes, Coordinating assembly of a bacterial macromolecular machine. Nat Rev Microbiol 6, 455–465 (2008). (10.1038/nrmicro1887) / Nat Rev Microbiol / Coordinating assembly of a bacterial macromolecular machine by Chevance FF (2008)
  2. F Altegoer, J Schuhmacher, P Pausch, G Bange, From molecular evolution to biobricks and synthetic modules: A lesson by the bacterial flagellum. Biotechnol Genet Eng Rev 30, 49–64 (2014). (10.1080/02648725.2014.921500) / Biotechnol Genet Eng Rev / From molecular evolution to biobricks and synthetic modules: A lesson by the bacterial flagellum by Altegoer F (2014)
  3. A Kusumoto, , Regulation of polar flagellar number by the flhF and flhG genes in Vibrio alginolyticus. J Biochem 139, 113–121 (2006). (10.1093/jb/mvj010) / J Biochem / Regulation of polar flagellar number by the flhF and flhG genes in Vibrio alginolyticus by Kusumoto A (2006)
  4. J Campos-García, R Nájera, L Camarena, G Soberón-Chávez, The pseudomonas aeruginosa motR gene involved in regulation of bacterial motility. FEMS Microbiol Lett 184, 57–62 (2000). (10.1016/S0378-1097(00)00019-7) / FEMS Microbiol Lett / The pseudomonas aeruginosa motR gene involved in regulation of bacterial motility by Campos-García J (2000)
  5. N Dasgupta, SK Arora, R Ramphal, fleN, a gene that regulates flagellar number in Pseudomonas aeruginosa. J Bacteriol 182, 357–364 (2000). (10.1128/JB.182.2.357-364.2000) / J Bacteriol / fleN, a gene that regulates flagellar number in Pseudomonas aeruginosa by Dasgupta N (2000)
  6. K van Amsterdam, A van der Ende, Helicobacter pylori HP1034 (ylxH) is required for motility. Helicobacter 9, 387–395 (2004). (10.1111/j.1083-4389.2004.00268.x) / Helicobacter / Helicobacter pylori HP1034 (ylxH) is required for motility by van Amsterdam K (2004)
  7. M Balaban, DR Hendrixson, Polar flagellar biosynthesis and a regulator of flagellar number influence spatial parameters of cell division in Campylobacter jejuni. PLoS Pathog 7, e1002420 (2011). (10.1371/journal.ppat.1002420) / PLoS Pathog / Polar flagellar biosynthesis and a regulator of flagellar number influence spatial parameters of cell division in Campylobacter jejuni by Balaban M (2011)
  8. SB Guttenplan, S Shaw, DB Kearns, The cell biology of peritrichous flagella in Bacillus subtilis. Mol Microbiol 87, 211–229 (2013). (10.1111/mmi.12103) / Mol Microbiol / The cell biology of peritrichous flagella in Bacillus subtilis by Guttenplan SB (2013)
  9. S Mukherjee, DB Kearns, The structure and regulation of flagella in Bacillus subtilis. Annu Rev Genet 48, 319–340 (2014). (10.1146/annurev-genet-120213-092406) / Annu Rev Genet / The structure and regulation of flagella in Bacillus subtilis by Mukherjee S (2014)
  10. G Bange, G Petzold, K Wild, RO Parlitz, I Sinning, The crystal structure of the third signal-recognition particle GTPase FlhF reveals a homodimer with bound GTP. Proc Natl Acad Sci USA 104, 13621–13625 (2007). (10.1073/pnas.0702570104) / Proc Natl Acad Sci USA / The crystal structure of the third signal-recognition particle GTPase FlhF reveals a homodimer with bound GTP by Bange G (2007)
  11. G Bange, , Structural basis for the molecular evolution of SRP-GTPase activation by protein. Nat Struct Mol Biol 18, 1376–1380 (2011). (10.1038/nsmb.2141) / Nat Struct Mol Biol / Structural basis for the molecular evolution of SRP-GTPase activation by protein by Bange G (2011)
  12. A Kusumoto, , Collaboration of FlhF and FlhG to regulate polar-flagella number and localization in Vibrio alginolyticus. Microbiology 154, 1390–1399 (2008). (10.1099/mic.0.2007/012641-0) / Microbiology / Collaboration of FlhF and FlhG to regulate polar-flagella number and localization in Vibrio alginolyticus by Kusumoto A (2008)
  13. M Schniederberend, K Abdurachim, TS Murray, BI Kazmierczak, The GTPase activity of FlhF is dispensable for flagellar localization, but not motility, in Pseudomonas aeruginosa. J Bacteriol 195, 1051–1060 (2013). (10.1128/JB.02013-12) / J Bacteriol / The GTPase activity of FlhF is dispensable for flagellar localization, but not motility, in Pseudomonas aeruginosa by Schniederberend M (2013)
  14. JR Parrish, , A proteome-wide protein interaction map for Campylobacter jejuni. Genome Biol 8, R130 (2007). (10.1186/gb-2007-8-7-r130) / Genome Biol / A proteome-wide protein interaction map for Campylobacter jejuni by Parrish JR (2007)
  15. JC Green, , Recruitment of the earliest component of the bacterial flagellum to the old cell division pole by a membrane-associated signal recognition particle family GTP-binding protein. J Mol Biol 391, 679–690 (2009). (10.1016/j.jmb.2009.05.075) / J Mol Biol / Recruitment of the earliest component of the bacterial flagellum to the old cell division pole by a membrane-associated signal recognition particle family GTP-binding protein by Green JC (2009)
  16. DD Leipe, YI Wolf, EV Koonin, L Aravind, Classification and evolution of P-loop GTPases and related ATPases. J Mol Biol 317, 41–72 (2002). (10.1006/jmbi.2001.5378) / J Mol Biol / Classification and evolution of P-loop GTPases and related ATPases by Leipe DD (2002)
  17. J Lutkenhaus, The ParA/MinD family puts things in their place. Trends Microbiol 20, 411–418 (2012). (10.1016/j.tim.2012.05.002) / Trends Microbiol / The ParA/MinD family puts things in their place by Lutkenhaus J (2012)
  18. J Lutkenhaus, S Pichoff, S Du, Bacterial cytokinesis: From Z ring to divisome. Cytoskeleton (Hoboken) 69, 778–790 (2012). (10.1002/cm.21054) / Cytoskeleton (Hoboken) / Bacterial cytokinesis: From Z ring to divisome by Lutkenhaus J (2012)
  19. W Wu, KT Park, T Holyoak, J Lutkenhaus, Determination of the structure of the MinD-ATP complex reveals the orientation of MinD on the membrane and the relative location of the binding sites for MinE and MinC. Mol Microbiol 79, 1515–1528 (2011). (10.1111/j.1365-2958.2010.07536.x) / Mol Microbiol / Determination of the structure of the MinD-ATP complex reveals the orientation of MinD on the membrane and the relative location of the binding sites for MinE and MinC by Wu W (2011)
  20. TH Szeto, SL Rowland, CL Habrukowich, GF King, The MinD membrane targeting sequence is a transplantable lipid-binding helix. J Biol Chem 278, 40050–40056 (2003). (10.1074/jbc.M306876200) / J Biol Chem / The MinD membrane targeting sequence is a transplantable lipid-binding helix by Szeto TH (2003)
  21. H Zhou, J Lutkenhaus, Membrane binding by MinD involves insertion of hydrophobic residues within the C-terminal amphipathic helix into the bilayer. J Bacteriol 185, 4326–4335 (2003). (10.1128/JB.185.15.4326-4335.2003) / J Bacteriol / Membrane binding by MinD involves insertion of hydrophobic residues within the C-terminal amphipathic helix into the bilayer by Zhou H (2003)
  22. A Dajkovic, G Lan, SX Sun, D Wirtz, J Lutkenhaus, MinC spatially controls bacterial cytokinesis by antagonizing the scaffolding function of FtsZ. Curr Biol 18, 235–244 (2008). (10.1016/j.cub.2008.01.042) / Curr Biol / MinC spatially controls bacterial cytokinesis by antagonizing the scaffolding function of FtsZ by Dajkovic A (2008)
  23. TA Leonard, PJ Butler, J Löwe, Bacterial chromosome segregation: Structure and DNA binding of the Soj dimer—a conserved biological switch. EMBO J 24, 270–282 (2005). (10.1038/sj.emboj.7600530) / EMBO J / Bacterial chromosome segregation: Structure and DNA binding of the Soj dimer—a conserved biological switch by Leonard TA (2005)
  24. G Stjepanovic, , Lipids trigger a conformational switch that regulates signal recognition particle (SRP)-mediated protein targeting. J Biol Chem 286, 23489–23497 (2011). (10.1074/jbc.M110.212340) / J Biol Chem / Lipids trigger a conformational switch that regulates signal recognition particle (SRP)-mediated protein targeting by Stjepanovic G (2011)
  25. H Szurmant, MW Bunn, VJ Cannistraro, GW Ordal, Bacillus subtilis hydrolyzes CheY-P at the location of its action, the flagellar switch. J Biol Chem 278, 48611–48616 (2003). (10.1074/jbc.M306180200) / J Biol Chem / Bacillus subtilis hydrolyzes CheY-P at the location of its action, the flagellar switch by Szurmant H (2003)
  26. BI Kazmierczak, DR Hendrixson, Spatial and numerical regulation of flagellar biosynthesis in polarly flagellated bacteria. Mol Microbiol 88, 655–663 (2013). (10.1111/mmi.12221) / Mol Microbiol / Spatial and numerical regulation of flagellar biosynthesis in polarly flagellated bacteria by Kazmierczak BI (2013)
  27. S Bubendorfer, , Specificity of motor components in the dual flagellar system of Shewanella putrefaciens CN-32. Mol Microbiol 83, 335–350 (2012). (10.1111/j.1365-2958.2011.07934.x) / Mol Microbiol / Specificity of motor components in the dual flagellar system of Shewanella putrefaciens CN-32 by Bubendorfer S (2012)
  28. S Bubendorfer, M Koltai, F Rossmann, V Sourjik, KM Thormann, Secondary bacterial flagellar system improves bacterial spreading by increasing the directional persistence of swimming. Proc Natl Acad Sci USA 111, 11485–11490 (2014). (10.1073/pnas.1405820111) / Proc Natl Acad Sci USA / Secondary bacterial flagellar system improves bacterial spreading by increasing the directional persistence of swimming by Bubendorfer S (2014)
  29. TS Murray, BI Kazmierczak, FlhF is required for swimming and swarming in Pseudomonas aeruginosa. J Bacteriol 188, 6995–7004 (2006). (10.1128/JB.00790-06) / J Bacteriol / FlhF is required for swimming and swarming in Pseudomonas aeruginosa by Murray TS (2006)
  30. KM Blair, L Turner, JT Winkelman, HC Berg, DB Kearns, A molecular clutch disables flagella in the Bacillus subtilis biofilm. Science 320, 1636–1638 (2008). (10.1126/science.1157877) / Science / A molecular clutch disables flagella in the Bacillus subtilis biofilm by Blair KM (2008)
  31. CR Courtney, LM Cozy, DB Kearns, Molecular characterization of the flagellar hook in Bacillus subtilis. J Bacteriol 194, 4619–4629 (2012). (10.1128/JB.00444-12) / J Bacteriol / Molecular characterization of the flagellar hook in Bacillus subtilis by Courtney CR (2012)
  32. LL Lackner, DM Raskin, PA de Boer, ATP-dependent interactions between Escherichia coli Min proteins and the phospholipid membrane in vitro. J Bacteriol 185, 735–749 (2003). (10.1128/JB.185.3.735-749.2003) / J Bacteriol / ATP-dependent interactions between Escherichia coli Min proteins and the phospholipid membrane in vitro by Lackner LL (2003)
  33. KT Park, , The Min oscillator uses MinD-dependent conformational changes in MinE to spatially regulate cytokinesis. Cell 146, 396–407 (2011). (10.1016/j.cell.2011.06.042) / Cell / The Min oscillator uses MinD-dependent conformational changes in MinE to spatially regulate cytokinesis by Park KT (2011)
  34. KT Park, W Wu, S Lovell, J Lutkenhaus, Mechanism of the asymmetric activation of the MinD ATPase by MinE. Mol Microbiol 85, 271–281 (2012). (10.1111/j.1365-2958.2012.08110.x) / Mol Microbiol / Mechanism of the asymmetric activation of the MinD ATPase by MinE by Park KT (2012)
  35. N Dasgupta, R Ramphal, Interaction of the antiactivator FleN with the transcriptional activator FleQ regulates flagellar number in Pseudomonas aeruginosa. J Bacteriol 183, 6636–6644 (2001). (10.1128/JB.183.22.6636-6644.2001) / J Bacteriol / Interaction of the antiactivator FleN with the transcriptional activator FleQ regulates flagellar number in Pseudomonas aeruginosa by Dasgupta N (2001)
  36. NE Correa, F Peng, KE Klose, Roles of the regulatory proteins FlhF and FlhG in the Vibrio cholerae flagellar transcription hierarchy. J Bacteriol 187, 6324–6332 (2005). (10.1128/JB.187.18.6324-6332.2005) / J Bacteriol / Roles of the regulatory proteins FlhF and FlhG in the Vibrio cholerae flagellar transcription hierarchy by Correa NE (2005)
  37. R Jain, BI Kazmierczak, A conservative amino acid mutation in the master regulator FleQ renders Pseudomonas aeruginosa aflagellate. PLoS ONE 9, e97439 (2014). (10.1371/journal.pone.0097439) / PLoS ONE / A conservative amino acid mutation in the master regulator FleQ renders Pseudomonas aeruginosa aflagellate by Jain R (2014)
  38. A Bren, M Eisenbach, The N terminus of the flagellar switch protein, FliM, is the binding domain for the chemotactic response regulator, CheY. J Mol Biol 278, 507–514 (1998). (10.1006/jmbi.1998.1730) / J Mol Biol / The N terminus of the flagellar switch protein, FliM, is the binding domain for the chemotactic response regulator, CheY by Bren A (1998)
  39. M Welch, K Oosawa, S Aizawa, M Eisenbach, Phosphorylation-dependent binding of a signal molecule to the flagellar switch of bacteria. Proc Natl Acad Sci USA 90, 8787–8791 (1993). (10.1073/pnas.90.19.8787) / Proc Natl Acad Sci USA / Phosphorylation-dependent binding of a signal molecule to the flagellar switch of bacteria by Welch M (1993)
  40. V Sourjik, JP Armitage, Spatial organization in bacterial chemotaxis. EMBO J 29, 2724–2733 (2010). (10.1038/emboj.2010.178) / EMBO J / Spatial organization in bacterial chemotaxis by Sourjik V (2010)
  41. TGG Battye, L Kontogiannis, O Johnson, HR Powell, AGW Leslie, iMOSFLM: A new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr D Biol Crystallogr 67, 271–281 (2011). (10.1107/S0907444910048675) / Acta Crystallogr D Biol Crystallogr / iMOSFLM: A new graphical interface for diffraction-image processing with MOSFLM by Battye TGG (2011)
  42. MD Winn, , Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr 67, 235–242 (2011). (10.1107/S0907444910045749) / Acta Crystallogr D Biol Crystallogr / Overview of the CCP4 suite and current developments by Winn MD (2011)
  43. AJ McCoy, , Phaser crystallographic software. J Appl Cryst 40, 658–674 (2007). (10.1107/S0021889807021206) / J Appl Cryst / Phaser crystallographic software by McCoy AJ (2007)
  44. P Emsley, K Cowtan, Coot: Model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60, 2126–2132 (2004). (10.1107/S0907444904019158) / Acta Crystallogr D Biol Crystallogr / Coot: Model-building tools for molecular graphics by Emsley P (2004)
  45. PD Adams, , PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66, 213–221 (2010). (10.1107/S0907444909052925) / Acta Crystallogr D Biol Crystallogr / PHENIX: A comprehensive Python-based system for macromolecular structure solution by Adams PD (2010)
  46. BD Pascal, , HDX workbench: Software for the analysis of H/D exchange MS data. J Am Soc Mass Spectrom 23, 1512–1521 (2012). (10.1007/s13361-012-0419-6) / J Am Soc Mass Spectrom / HDX workbench: Software for the analysis of H/D exchange MS data by Pascal BD (2012)
  47. CA Schneider, WS Rasband, KW Eliceiri, NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9, 671–675 (2012). (10.1038/nmeth.2089) / Nat Methods / NIH Image to ImageJ: 25 years of image analysis by Schneider CA (2012)
Dates
Type When
Created 10 years, 5 months ago (March 2, 2015, 5:13 p.m.)
Deposited 3 years, 2 months ago (June 7, 2022, 4:13 a.m.)
Indexed 2 months, 2 weeks ago (June 11, 2025, 9:26 a.m.)
Issued 10 years, 5 months ago (March 2, 2015)
Published 10 years, 5 months ago (March 2, 2015)
Published Online 10 years, 5 months ago (March 2, 2015)
Published Print 10 years, 5 months ago (March 10, 2015)
Funders 0

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@article{Schuhmacher_2015, title={MinD-like ATPase FlhG effects location and number of bacterial flagella during C-ring assembly}, volume={112}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.1419388112}, DOI={10.1073/pnas.1419388112}, number={10}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Schuhmacher, Jan S. and Rossmann, Florian and Dempwolff, Felix and Knauer, Carina and Altegoer, Florian and Steinchen, Wieland and Dörrich, Anja K. and Klingl, Andreas and Stephan, Milena and Linne, Uwe and Thormann, Kai M. and Bange, Gert}, year={2015}, month=mar, pages={3092–3097} }