The Presence and Absence of Periplasmic Rings in Bacterial Flagellar Motors Correlates with Stator Type

Overview

Journal Elife

Specialty Biology

Date 2019 Jan 17

PMID 30648971

Citations 23

Authors

Mohammed Kaplan

Debnath Ghosal

Poorna Subramanian

Catherine M Oikonomou

Andreas Kjaer

Sahand Pirbadian

Davi R Ortega

Ariane Briegel

Mohamed Y El-Naggar

Grant J Jensen

Affiliations

Soon will be listed here.

Abstract

The bacterial flagellar motor, a cell-envelope-embedded macromolecular machine that functions as a cellular propeller, exhibits significant structural variability between species. Different torque-generating stator modules allow motors to operate in different pH, salt or viscosity levels. How such diversity evolved is unknown. Here, we use electron cryo-tomography to determine the in situ macromolecular structures of three Gammaproteobacteria motors: , , and , providing the first views of intact motors with dual stator systems. Complementing our imaging with bioinformatics analysis, we find a correlation between the motor's stator system and its structural elaboration. Motors with a single H-driven stator have only the core periplasmic P- and L-rings; those with dual H-driven stators have an elaborated P-ring; and motors with Na or Na/H-driven stators have both their P- and L-rings embellished. Our results suggest an evolution of structural elaboration that may have enabled pathogenic bacteria to colonize higher-viscosity environments in animal hosts.

Citing Articles

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Tetrameric PilZ protein stabilizes stator ring in complex flagellar motor and is required for motility in .

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How cells with diverse stator composition collectively swarm.

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Structure and Assembly of the Flagellar Motor by Cryo-Electron Tomography.

Kaplan M, Yao Q, Jensen G Int J Mol Sci. 2023; 24(9).

PMID: 37176000 PMC: 10179241. DOI: 10.3390/ijms24098292.

References

Oikonomou C, Jensen G . A new view into prokaryotic cell biology from electron cryotomography. Nat Rev Microbiol. 2017; 15(2):128. DOI: 10.1038/nrmicro.2016.195. View

Stock D, Namba K, Lee L . Nanorotors and self-assembling macromolecular machines: the torque ring of the bacterial flagellar motor. Curr Opin Biotechnol. 2012; 23(4):545-54. DOI: 10.1016/j.copbio.2012.01.008. View

Sowa Y, Berry R . Bacterial flagellar motor. Q Rev Biophys. 2008; 41(2):103-32. DOI: 10.1017/S0033583508004691. View

Terahara N, Krulwich T, Ito M . Mutations alter the sodium versus proton use of a Bacillus clausii flagellar motor and confer dual ion use on Bacillus subtilis motors. Proc Natl Acad Sci U S A. 2008; 105(38):14359-64. PMC: 2567154. DOI: 10.1073/pnas.0802106105. View

Terashima H, Kawamoto A, Morimoto Y, Imada K, Minamino T . Structural differences in the bacterial flagellar motor among bacterial species. Biophys Physicobiol. 2018; 14:191-198. PMC: 5774414. DOI: 10.2142/biophysico.14.0_191. View

Toutain C, Caizza N, Zegans M, OToole G . Roles for flagellar stators in biofilm formation by Pseudomonas aeruginosa. Res Microbiol. 2007; 158(5):471-7. DOI: 10.1016/j.resmic.2007.04.001. View

Zheng S, Keszthelyi B, Branlund E, Lyle J, Braunfeld M, Sedat J . UCSF tomography: an integrated software suite for real-time electron microscopic tomographic data collection, alignment, and reconstruction. J Struct Biol. 2006; 157(1):138-47. DOI: 10.1016/j.jsb.2006.06.005. View

Doyle T, Hawkins A, McCarter L . The complex flagellar torque generator of Pseudomonas aeruginosa. J Bacteriol. 2004; 186(19):6341-50. PMC: 516612. DOI: 10.1128/JB.186.19.6341-6350.2004. View

Kojima S . Dynamism and regulation of the stator, the energy conversion complex of the bacterial flagellar motor. Curr Opin Microbiol. 2015; 28:66-71. DOI: 10.1016/j.mib.2015.07.015. View

10.

Chaban B, Coleman I, Beeby M . Evolution of higher torque in Campylobacter-type bacterial flagellar motors. Sci Rep. 2018; 8(1):97. PMC: 5758724. DOI: 10.1038/s41598-017-18115-1. View

11.

Gan L, Jensen G . Electron tomography of cells. Q Rev Biophys. 2011; 45(1):27-56. DOI: 10.1017/S0033583511000102. View

12.

Chen S, Beeby M, Murphy G, Leadbetter J, Hendrixson D, Briegel A . Structural diversity of bacterial flagellar motors. EMBO J. 2011; 30(14):2972-81. PMC: 3160247. DOI: 10.1038/emboj.2011.186. View

13.

Belas R . Biofilms, flagella, and mechanosensing of surfaces by bacteria. Trends Microbiol. 2014; 22(9):517-27. DOI: 10.1016/j.tim.2014.05.002. View

14.

Jones C, Macnab R . Flagellar assembly in Salmonella typhimurium: analysis with temperature-sensitive mutants. J Bacteriol. 1990; 172(3):1327-39. PMC: 208602. DOI: 10.1128/jb.172.3.1327-1339.1990. View

15.

Feldman M, Bryan R, Rajan S, Scheffler L, Brunnert S, Tang H . Role of flagella in pathogenesis of Pseudomonas aeruginosa pulmonary infection. Infect Immun. 1998; 66(1):43-51. PMC: 107856. DOI: 10.1128/IAI.66.1.43-51.1998. View

16.

Macnab R . The bacterial flagellum: reversible rotary propellor and type III export apparatus. J Bacteriol. 1999; 181(23):7149-53. PMC: 103673. DOI: 10.1128/JB.181.23.7149-7153.1999. View

17.

Evans L, Hughes C, Fraser G . Building a flagellum outside the bacterial cell. Trends Microbiol. 2014; 22(10):566-72. PMC: 4183434. DOI: 10.1016/j.tim.2014.05.009. View

18.

Terashima H, Fukuoka H, Yakushi T, Kojima S, Homma M . The Vibrio motor proteins, MotX and MotY, are associated with the basal body of Na-driven flagella and required for stator formation. Mol Microbiol. 2006; 62(4):1170-80. DOI: 10.1111/j.1365-2958.2006.05435.x. View

19.

Subramanian P, Pirbadian S, El-Naggar M, Jensen G . Ultrastructure of MR-1 nanowires revealed by electron cryotomography. Proc Natl Acad Sci U S A. 2018; 115(14):E3246-E3255. PMC: 5889646. DOI: 10.1073/pnas.1718810115. View

20.

Myers C, Nealson K . Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor. Science. 1988; 240(4857):1319-21. DOI: 10.1126/science.240.4857.1319. View