Bacterial flagellar capping proteins adopt diverse oligomeric states

Postel, Sandra; Deredge, Daniel; Bonsor, Daniel A.; Yu, Xiong; Diederichs, Kay; Helmsing, Saskia; Vromen, Aviv; Friedler, Assaf; Hust, Michael; Egelman, Edward H.; Beckett, Dorothy; Wintrode, Patrick L.; Sundberg, Eric J.

doi:10.7554/eLife.18857

Bacterial flagellar capping proteins adopt diverse oligomeric states

Journal Article · Sat Sep 24 00:00:00 EDT 2016 · eLife

DOI:https://doi.org/10.7554/eLife.18857· OSTI ID:1357646

^[1]; Deredge, Daniel ^[2]; Bonsor, Daniel A. ^[1]; Yu, Xiong ^[3]; Diederichs, Kay ^[4]; Helmsing, Saskia ^[5]; Vromen, Aviv ^[6]; Friedler, Assaf ^[6]; Hust, Michael ^[5]; ^[3]; Beckett, Dorothy ^[7]; Wintrode, Patrick L. ^[2]; ^[1]

Univ. of Maryland School of Medicine, Baltimore, MD (United States)
Univ. of Maryland School of Pharmacy, Baltimore, MD (United States)
Univ. of Virginia, Charlottesville, VA (United States)
Univ. of Konstanz (Germany)
Technische Univ. Braunschweig (Germany)
The Hebrew Univ. of Jerusalem (Israel)
Univ. of Maryland College Park, Baltimore,MD (United States)

Flagella are crucial for bacterial motility and pathogenesis. The flagellar capping protein (FliD) regulates filament assembly by chaperoning and sorting flagellin (FliC) proteins after they traverse the hollow filament and exit the growing flagellum tip. In the absence of FliD, flagella are not formed, resulting in impaired motility and infectivity. Here, we report the 2.2 Å resolution X-ray crystal structure of FliD from Pseudomonas aeruginosa, the first high-resolution structure of any FliD protein from any bacterium. Using this evidence in combination with a multitude of biophysical and functional analyses, we find that Pseudomonas FliD exhibits unexpected structural similarity to other flagellar proteins at the domain level, adopts a unique hexameric oligomeric state, and depends on flexible determinants for oligomerization. Considering that the flagellin filaments on which FliD oligomers are affixed vary in protofilament number between bacteria, our results suggest that FliD oligomer stoichiometries vary across bacteria to complement their filament assemblies.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: National Center for Research Resources

OSTI ID:: 1357646

Journal Information:: eLife, Journal Name: eLife Journal Issue: 9 Vol. 5; ISSN 2050-084X

Publisher:: eLife Sciences Publications, Ltd.Copyright Statement

Country of Publication:: United States

Language:: ENGLISH

References (65)

Sequence complexity of disordered protein Romero, Pedro; Obradovic, Zoran; Li, Xiaohong Proteins: Structure, Function, and Genetics, Vol. 42, Issue 1 https://doi.org/10.1002/1097-0134(20010101)42:1<38::AID-PROT50>3.0.CO;2-3	journal	January 2000
Flagella and bacterial pathogenicity: Flagella and bacterial pathogenicity Duan, Qiangde; Zhou, Mingxu; Zhu, Liqian Journal of Basic Microbiology, Vol. 53, Issue 1 https://doi.org/10.1002/jobm.201100335	journal	February 2012
The Utility of Hydrogen/Deuterium Exchange Mass Spectrometry in Biopharmaceutical Comparability Studies Houde, Damian; Berkowitz, Steven A.; Engen, John R. Journal of Pharmaceutical Sciences, Vol. 100, Issue 6 https://doi.org/10.1002/jps.22432	journal	June 2011
Atomic Structures of the Human Immunophilin FKBP-12 Complexes with FK506 and Rapamycin Van Duyne, Gregory D.; Standaert, Robert F.; Karplus, P. Andrew Journal of Molecular Biology, Vol. 229, Issue 1 https://doi.org/10.1006/jmbi.1993.1012	journal	January 1993
Assembly characteristics of flagellar cap protein HAP2 of Salmonella : decamer and pentamer in the ph-sensitive equilibrium 1 1Edited by M. F. Moody Imada, Katsumi; Vonderviszt, Ferenc; Furukawa, Yukio Journal of Molecular Biology, Vol. 277, Issue 4 https://doi.org/10.1006/jmbi.1998.1662	journal	April 1998
Plugging interactions of HAP2 pentamer into the distal end of flagellar filament revealed by electron microscopy 1 1Edited by M. F. Moody Maki, Saori; Vonderviszt, Ferenc; Furukawa, Yukio Journal of Molecular Biology, Vol. 277, Issue 4 https://doi.org/10.1006/jmbi.1998.1663	journal	April 1998
Mechanism of self-association and filament capping by flagellar HAP2 1 1Edited by M. F. Moody Vonderviszt, Ferenc; Imada, Katsumi; Furukawa, Yukio Journal of Molecular Biology, Vol. 284, Issue 5 https://doi.org/10.1006/jmbi.1998.2274	journal	December 1998
Gene Transfer: Transformation/Electroporation Cadoret, Frédéric; Soscia, Chantal; Voulhoux, Romé Methods in Molecular Biology https://doi.org/10.1007/978-1-4939-0473-0_2	book	January 2014
Plate-Based Assay for Swimming Motility in Pseudomonas aeruginosa Ha, Dae-Gon; Kuchma, Sherry L.; O’Toole, George A. Methods in Molecular Biology https://doi.org/10.1007/978-1-4939-0473-0_7	book	January 2014
Construction of Human Antibody Gene Libraries and Selection of Antibodies by Phage Display Frenzel, André; Kügler, Jonas; Wilke, Sonja Methods in Molecular Biology https://doi.org/10.1007/978-1-62703-586-6_12	book	August 2013
Accurate Prediction of Protein Disordered Regions by Mining Protein Structure Data Cheng, Jianlin; Sweredoski, Michael J.; Baldi, Pierre Data Mining and Knowledge Discovery, Vol. 11, Issue 3 https://doi.org/10.1007/s10618-005-0001-y	journal	July 2005
Analysis of Overlapped and Noisy Hydrogen/Deuterium Exchange Mass Spectra Guttman, Miklos; Weis, David D.; Engen, John R. Journal of The American Society for Mass Spectrometry, Vol. 24, Issue 12 https://doi.org/10.1007/s13361-013-0727-5	journal	September 2013
Boundary analysis in sedimentation transport experiments: A procedure for obtaining sedimentation coefficient distributions using the time derivative of the concentration profile Stafford, Walter F. Analytical Biochemistry, Vol. 203, Issue 2 https://doi.org/10.1016/0003-2697(92)90316-Y	journal	June 1992
Determination of Domain Structure of Proteins from X-Ray Solution Scattering Svergun, Dmitri I.; Petoukhov, Maxim V.; Koch, Michel H. J. Biophysical Journal, Vol. 80, Issue 6 https://doi.org/10.1016/S0006-3495(01)76260-1	journal	June 2001
Sedimentation velocity spins a new weave for an old fabric Stafford, Walter F. Current Opinion in Biotechnology, Vol. 8, Issue 1 https://doi.org/10.1016/S0958-1669(97)80152-8	journal	February 1997
Seeds to crystals Bergfors, Terese Journal of Structural Biology, Vol. 142, Issue 1 https://doi.org/10.1016/S1047-8477(03)00039-X	journal	April 2003
From motility to virulence: sensing and responding to environmental signals in Vibrio cholerae Krukonis, Eric S.; DiRita, Victor J. Current Opinion in Microbiology, Vol. 6, Issue 2 https://doi.org/10.1016/S1369-5274(03)00032-8	journal	April 2003
Improved methods for fitting sedimentation coefficient distributions derived by time-derivative techniques Philo, John S. Analytical Biochemistry, Vol. 354, Issue 2 https://doi.org/10.1016/j.ab.2006.04.053	journal	July 2006
Small-Molecule Inhibitors of Protein-Protein Interactions: Progressing toward the Reality Arkin, Michelle R.; Tang, Yinyan; Wells, James A. Chemistry & Biology, Vol. 21, Issue 9 https://doi.org/10.1016/j.chembiol.2014.09.001	journal	September 2014
Identification and characterization of EX1 kinetics in H/D exchange mass spectrometry by peak width analysis Weis, David D.; Wales, Thomas E.; Engen, John R. Journal of the American Society for Mass Spectrometry, Vol. 17, Issue 11 https://doi.org/10.1016/j.jasms.2006.05.014	journal	November 2006
Flagellar Filaments of the Deep-sea Bacteria Idiomarina loihiensis Belong to a Family Different from those of Salmonella typhimurium Shibata, Satoshi; Alam, Maqsudul; Aizawa, Shin-Ichi Journal of Molecular Biology, Vol. 352, Issue 3 https://doi.org/10.1016/j.jmb.2005.07.023	journal	September 2005
EMAN2: An extensible image processing suite for electron microscopy Tang, Guang; Peng, Liwei; Baldwin, Philip R. Journal of Structural Biology, Vol. 157, Issue 1 https://doi.org/10.1016/j.jsb.2006.05.009	journal	January 2007
Interaction of pathogenic bacteria with rabbit appendix M cells: bacterial motility is a key feature in vivo Marchetti, Marta; Sirard, Jean Claude; Sansonetti, Philippe Microbes and Infection, Vol. 6, Issue 6 https://doi.org/10.1016/j.micinf.2004.02.009	journal	May 2004
Protein Disorder Prediction Linding, Rune; Jensen, Lars Juhl; Diella, Francesca Structure, Vol. 11, Issue 11 https://doi.org/10.1016/j.str.2003.10.002	journal	November 2003
The role of fimbriae and flagella in the colonization, invasion and persistence of Escherichia coli O78[ratio ]K80 in the day-old-chick model La Ragione, R. M.; Sayers, A. R.; Woodward, M. J. Epidemiology and Infection, Vol. 124, Issue 3 https://doi.org/10.1017/S0950268899004045	journal	June 2000
Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy Yonekura, Koji; Maki-Yonekura, Saori; Namba, Keiichi Nature, Vol. 424, Issue 6949 https://doi.org/10.1038/nature01830	journal	August 2003
Domain movements of HAP2 in the cap-filament complex formation and growth process of the bacterial flagellum Maki-Yonekura, S.; Yonekura, K.; Namba, K. Proceedings of the National Academy of Sciences, Vol. 100, Issue 26 https://doi.org/10.1073/pnas.2534343100	journal	December 2003
Principles of protein-protein interactions. Jones, S.; Thornton, J. M. Proceedings of the National Academy of Sciences, Vol. 93, Issue 1 https://doi.org/10.1073/pnas.93.1.13	journal	January 1996
SPINE-D: Accurate Prediction of Short and Long Disordered Regions by a Single Neural-Network Based Method Zhang, Tuo; Faraggi, Eshel; Xue, Bin Journal of Biomolecular Structure and Dynamics, Vol. 29, Issue 4 https://doi.org/10.1080/073911012010525022	journal	February 2012
Small-angle scattering studies of biological macromolecules in solution Svergun, Dmitri I.; Koch, Michel H. J. Reports on Progress in Physics, Vol. 66, Issue 10 https://doi.org/10.1088/0034-4885/66/10/R05	journal	September 2003
RONN: the bio-basis function neural network technique applied to the detection of natively disordered regions in proteins Yang, Z. R.; Thomson, R.; McNeil, P. Bioinformatics, Vol. 21, Issue 16 https://doi.org/10.1093/bioinformatics/bti534	journal	June 2005
FoldIndex(C): a simple tool to predict whether a given protein sequence is intrinsically unfolded Prilusky, J.; Felder, C. E.; Zeev-Ben-Mordehai, T. Bioinformatics, Vol. 21, Issue 16 https://doi.org/10.1093/bioinformatics/bti537	journal	June 2005
IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content Dosztanyi, Z.; Csizmok, V.; Tompa, P. Bioinformatics, Vol. 21, Issue 16 https://doi.org/10.1093/bioinformatics/bti541	journal	June 2005
OnD-CRF: predicting order and disorder in proteins conditional random fields Wang, L.; Sauer, U. H. Bioinformatics, Vol. 24, Issue 11 https://doi.org/10.1093/bioinformatics/btn132	journal	April 2008
Improved sequence-based prediction of disordered regions with multilayer fusion of multiple information sources Mizianty, Marcin J.; Stach, Wojciech; Chen, Ke Bioinformatics, Vol. 26, Issue 18 https://doi.org/10.1093/bioinformatics/btq373	journal	September 2010
Experimental Campylobacter jejuni Infection in Humans Black, R. E.; Levine, M. M.; Clements, M. L. Journal of Infectious Diseases, Vol. 157, Issue 3 https://doi.org/10.1093/infdis/157.3.472	journal	March 1988
GlobPlot: exploring protein sequences for globularity and disorder Linding, R. Nucleic Acids Research, Vol. 31, Issue 13 https://doi.org/10.1093/nar/gkg519	journal	July 2003
FoXS: a web server for rapid computation and fitting of SAXS profiles Schneidman-Duhovny, D.; Hammel, M.; Sali, A. Nucleic Acids Research, Vol. 38, Issue Web Server https://doi.org/10.1093/nar/gkq461	journal	May 2010
The Role of Flagella, But not Fimbriae, in the Adherence of Salmonella Enterica Serotype Enteritidis to Chick Gut Explant Allen-Vercoe, Emma; Woodward, Martin J. Journal of Medical Microbiology, Vol. 48, Issue 8 https://doi.org/10.1099/00222615-48-8-771	journal	August 1999
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
BioXTAS RAW , a software program for high-throughput automated small-angle X-ray scattering data reduction and preliminary analysis Nielsen, S. S.; Toft, K. Noergaard; Snakenborg, D. Journal of Applied Crystallography, Vol. 42, Issue 5 https://doi.org/10.1107/S0021889809023863	journal	August 2009
Determination of the regularization parameter in indirect-transform methods using perceptual criteria Svergun, D. I. Journal of Applied Crystallography, Vol. 25, Issue 4, p. 495-503 https://doi.org/10.1107/S0021889892001663	journal	August 1992
Maximum-likelihood density modification Terwilliger, Thomas C. Acta Crystallographica Section D Biological Crystallography, Vol. 56, Issue 8 https://doi.org/10.1107/S0907444900005072	journal	August 2000
Substructure solution with SHELXD Schneider, Thomas R.; Sheldrick, George M. Acta Crystallographica Section D Biological Crystallography, Vol. 58, Issue 10 https://doi.org/10.1107/S0907444902011678	journal	September 2002
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
An automated microseed matrix-screening method for protein crystallization D'Arcy, Allan; Villard, Frederic; Marsh, May Acta Crystallographica Section D Biological Crystallography, Vol. 63, Issue 4 https://doi.org/10.1107/S0907444907007652	journal	March 2007
Rapid shape determination of tissue transglutaminase using high-throughput computing Lammie, Donna; Osborne, James; Aeschlimann, Daniel Acta Crystallographica Section D Biological Crystallography, Vol. 63, Issue 9 https://doi.org/10.1107/S0907444907032933	journal	August 2007
Integration, scaling, space-group assignment and post-refinement Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 133-144 https://doi.org/10.1107/S0907444909047374	journal	January 2010
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
How good are my data and what is the resolution? Evans, Philip R.; Murshudov, Garib N. Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 7 https://doi.org/10.1107/S0907444913000061	journal	June 2013
Automated MAD and MIR structure solution Terwilliger, Thomas C.; Berendzen, Joel Acta Crystallographica Section D Biological Crystallography, Vol. 55, Issue 4 https://doi.org/10.1107/S0907444999000839	journal	April 1999
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/s0907444909047337	journal	January 2010
Divergence of Quaternary Structures Among Bacterial Flagellar Filaments Galkin, V. E.; Yu, X.; Bielnicki, J. Science, Vol. 320, Issue 5874 https://doi.org/10.1126/science.1155307	journal	April 2008
The Bacterial Flagellar Cap as the Rotary Promoter of Flagellin Self-Assembly Yonekura, K.; Maki, S.; Morgan, D. G. Science, Vol. 290, Issue 5499 https://doi.org/10.1126/science.290.5499.2148	journal	December 2000
The Pseudomonas aeruginosa Flagellar Cap Protein, FliD, Is Responsible for Mucin Adhesion Arora, Shiwani K.; Ritchings, Bruce W.; Almira, Ernesto C. Infection and Immunity, Vol. 66, Issue 3 https://doi.org/10.1128/IAI.66.3.1000-1007.1998	journal	March 1998
Role of Motility and Flagellin Glycosylation in the Pathogenesis of Pseudomonas aeruginosa Burn Wound Infections Arora, S. K.; Neely, A. N.; Blair, B. Infection and Immunity, Vol. 73, Issue 7 https://doi.org/10.1128/IAI.73.7.4395-4398.2005	journal	June 2005
Locations of hook-associated proteins in flagellar structures of Salmonella typhimurium. Homma, M.; Iino, T. Journal of Bacteriology, Vol. 162, Issue 1 https://doi.org/10.1128/JB.162.1.183-189.1985	journal	January 1985
Molecular Cloning and Characterization of theHelicobacter pylori fliD Gene, an Essential Factor in Flagellar Structure and Motility Seong Kim, Jang; Hoon Chang, Ji; Il Chung, Soo Journal of Bacteriology, Vol. 181, Issue 22 https://doi.org/10.1128/JB.181.22.6969-6976.1999	journal	November 1999
The Rotary Motor of Bacterial Flagella Berg, Howard C. Annual Review of Biochemistry, Vol. 72, Issue 1 https://doi.org/10.1146/annurev.biochem.72.121801.161737	journal	June 2003
MetaDisorder: a meta-server for the prediction of intrinsic disorder in proteins Kozlowski, Lukasz P.; Bujnicki, Janusz M. BMC Bioinformatics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2105-13-111	journal	May 2012
Disulfide by Design 2.0: a web-based tool for disulfide engineering in proteins Craig, Douglas B.; Dombkowski, Alan A. BMC Bioinformatics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2105-14-346	journal	December 2013
High level transient production of recombinant antibodies and antibody fusion proteins in HEK293 cells Jäger, Volker; Büssow, Konrad; Wagner, Andreas BMC Biotechnology, Vol. 13, Issue 1 https://doi.org/10.1186/1472-6750-13-52	journal	January 2013
Generation and analysis of the improved human HAL9/10 antibody phage display libraries Kügler, Jonas; Wilke, Sonja; Meier, Doris BMC Biotechnology, Vol. 15, Issue 1 https://doi.org/10.1186/s12896-015-0125-0	journal	January 2015
The Role of the Bacterial Flagellum in Adhesion and Virulence Haiko, Johanna; Westerlund-Wikström, Benita Biology, Vol. 2, Issue 4 https://doi.org/10.3390/biology2041242	journal	October 2013

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