Low Flagellar Motor Torque and High Swimming Efficiency of Caulobacter Crescentus Swarmer Cells

Overview

Journal Biophys J

Publisher Cell Press

Specialty Biophysics

Date 2006 Jul 18

PMID 16844761

Citations 38

Authors

Guanglai Li

Jay X Tang

Affiliations

Soon will be listed here.

Abstract

We determined the torque of the flagellar motor of Caulobacter crescentus for different motor rotation rates by measuring the rotation rate and swimming speed of the cell body and found it to be remarkably different from that of other bacteria, such as Escherichia coli and Vibrio alginolyticus. The average stall torque of the Caulobacter flagellar motor was approximately 350 pN nm, much smaller than the values of the other bacteria measured. Furthermore, the torque of the motor remained constant in the range of rotation rates up to those of freely swimming cells. In contrast, the torque of a freely swimming cell for V. alginolyticus is typically approximately 20% of the stall torque. We derive from these results that the C. crescentus swarmer cells swim more efficiently than both E. coli and V. alginolyticus. Our findings suggest that C. crescentus is optimally adapted to low nutrient aquatic environments.

Citing Articles

Torque-speed relationship of the flagellar motor with dual-stator systems in .

Wu H, Wu Z, Tian M, Zhang R, Yuan J mBio. 2024; 15(12):e0074524.

PMID: 39475228 PMC: 11633141. DOI: 10.1128/mbio.00745-24.

Decoding the hydrodynamic properties of microscale helical propellers from Brownian fluctuations.

Djutanta F, Brown P, Nainggolan B, Coullomb A, Radhakrishnan S, Sentosa J Proc Natl Acad Sci U S A. 2023; 120(22):e2220033120.

PMID: 37235635 PMC: 10235983. DOI: 10.1073/pnas.2220033120.

Synchronized Swarmers and Sticky Stalks: Caulobacter crescentus as a Model for Bacterial Cell Biology.

Barrows J, Goley E J Bacteriol. 2023; 205(2):e0038422.

PMID: 36715542 PMC: 9945503. DOI: 10.1128/jb.00384-22.

A one-dimensional three-state run-and-tumble model with a 'cell cycle'.

Breoni D, Schwarzendahl F, Blossey R, Lowen H Eur Phys J E Soft Matter. 2022; 45(10):83.

PMID: 36258055 PMC: 9579107. DOI: 10.1140/epje/s10189-022-00238-7.

Bacteria-on-a-bead: probing the hydrodynamic interplay of dynamic cell appendages during cell separation.

Sauter N, Sangermani M, Hug I, Jenal U, Pfohl T Commun Biol. 2022; 5(1):1093.

PMID: 36241769 PMC: 9568603. DOI: 10.1038/s42003-022-04026-z.

References

Koch A . Oligotrophs versus copiotrophs. Bioessays. 2001; 23(7):657-61. DOI: 10.1002/bies.1091. View

Manson M, Tedesco P, Berg H, Harold F, van der Drift C . A protonmotive force drives bacterial flagella. Proc Natl Acad Sci U S A. 1977; 74(7):3060-4. PMC: 431412. DOI: 10.1073/pnas.74.7.3060. View

Li G, Smith C, Brun Y, Tang J . The elastic properties of the caulobacter crescentus adhesive holdfast are dependent on oligomers of N-acetylglucosamine. J Bacteriol. 2004; 187(1):257-65. PMC: 538810. DOI: 10.1128/JB.187.1.257-265.2005. View

POINDEXTER J . The caulobacters: ubiquitous unusual bacteria. Microbiol Rev. 1981; 45(1):123-79. PMC: 281501. DOI: 10.1128/mr.45.1.123-179.1981. View

Sowa Y, Rowe A, Leake M, Yakushi T, Homma M, Ishijima A . Direct observation of steps in rotation of the bacterial flagellar motor. Nature. 2005; 437(7060):916-9. DOI: 10.1038/nature04003. View

Berg H, Turner L . Movement of microorganisms in viscous environments. Nature. 1979; 278(5702):349-51. DOI: 10.1038/278349a0. View

Berry R, Berg H . Absence of a barrier to backwards rotation of the bacterial flagellar motor demonstrated with optical tweezers. Proc Natl Acad Sci U S A. 1998; 94(26):14433-7. PMC: 25012. DOI: 10.1073/pnas.94.26.14433. View

Meister M, Lowe G, Berg H . The proton flux through the bacterial flagellar motor. Cell. 1987; 49(5):643-50. DOI: 10.1016/0092-8674(87)90540-x. View

Stallmeyer M, Aizawa S, Macnab R, DeRosier D . Image reconstruction of the flagellar basal body of Salmonella typhimurium. J Mol Biol. 1989; 205(3):519-28. DOI: 10.1016/0022-2836(89)90223-4. View

10.

Stallmeyer M, Hahnenberger K, Sosinsky G, Shapiro L, DeRosier D . Image reconstruction of the flagellar basal body of Caulobacter crescentus. J Mol Biol. 1989; 205(3):511-8. DOI: 10.1016/0022-2836(89)90222-2. View

11.

Turner L, Ryu W, Berg H . Real-time imaging of fluorescent flagellar filaments. J Bacteriol. 2000; 182(10):2793-801. PMC: 101988. DOI: 10.1128/JB.182.10.2793-2801.2000. View

12.

Koyasu S, Shirakihara Y . Caulobacter crescentus flagellar filament has a right-handed helical form. J Mol Biol. 1984; 173(1):125-30. DOI: 10.1016/0022-2836(84)90407-8. View

13.

Magariyama Y, Kudo S . A mathematical explanation of an increase in bacterial swimming speed with viscosity in linear-polymer solutions. Biophys J. 2002; 83(2):733-9. PMC: 1302182. DOI: 10.1016/S0006-3495(02)75204-1. View

14.

Nakamura S, Adachi Y, Goto T, Magariyama Y . Improvement in motion efficiency of the spirochete Brachyspira pilosicoli in viscous environments. Biophys J. 2006; 90(8):3019-26. PMC: 1414552. DOI: 10.1529/biophysj.105.074336. View

15.

Sowa Y, Hotta H, Homma M, Ishijima A . Torque-speed relationship of the Na+-driven flagellar motor of Vibrio alginolyticus. J Mol Biol. 2003; 327(5):1043-51. DOI: 10.1016/s0022-2836(03)00176-1. View

16.

Berg H . Chemotaxis in bacteria. Annu Rev Biophys Bioeng. 1975; 4(00):119-36. DOI: 10.1146/annurev.bb.04.060175.001003. View

17.

Berg H . The rotary motor of bacterial flagella. Annu Rev Biochem. 2002; 72:19-54. DOI: 10.1146/annurev.biochem.72.121801.161737. View

18.

Mitchell J . The influence of cell size on marine bacterial motility and energetics. Microb Ecol. 2013; 22(1):227-38. DOI: 10.1007/BF02540225. View

19.

Kashket E . The proton motive force in bacteria: a critical assessment of methods. Annu Rev Microbiol. 1985; 39:219-42. DOI: 10.1146/annurev.mi.39.100185.001251. View

20.

Mitchell J . The energetics and scaling of search strategies in bacteria. Am Nat. 2008; 160(6):727-40. DOI: 10.1086/343874. View