Altered motility of Caulobacter Crescentus in viscous and viscoelastic media

BMC Microbiology

Jay X Tang¹  Guanglai Li¹  Michael Morse¹  Nathan Johnson¹  Alexander Yang¹  Marianna Neubauer¹  Yukun Gao¹ 

[1] Physics Department, Brown University, Providence 02192, RI, USA

关键词: Viscoelasticity;    Viscous agent;    Rheology;    Hyperosmolarity;    Hydrodynamics;    Bacterial motility;   

Others  :  1090287
DOI  :  10.1186/s12866-014-0322-3

 received in 2014-08-20, accepted in 2014-12-11,  发布年份 2014

【 摘 要 】

Background

Motility of flagellated bacteria depends crucially on their organelles such as flagella and pili, as well as physical properties of the external medium, such as viscosity and matrix elasticity. We studied the motility of wild-type and two mutant strains of Caulobacter crescentus swarmer cells in two different types of media: a viscous and hyperosmotic glycerol-growth medium mixture and a viscoelastic growth medium, containing polyethylene glycol or polyethylene oxide of different defined sizes.

Results

For all three strains in the medium containing glycerol, we found linear drops in percentage of motile cells and decreases in speed of those that remained motile to be inversely proportional to viscosity. The majority of immobilized cells lost viability, evidenced by their membrane leakage. In the viscoelastic media, we found less loss of motility and attenuated decrease of swimming speed at shear viscosity values comparable to the viscous medium. In both types of media, we found more severe loss in percentage of motile cells of wild-type than the mutants without pili, indicating that the interference of pili with flagellated motility is aggravated by increased viscosity. However, we found no difference in swimming speed among all three strains under all test conditions for the cells that remained motile. Finally, the viscoelastic medium caused no significant change in intervals between flagellar motor switches unless the motor stalled.

Conclusion

Hyperosmotic effect causes loss of motility and cell death. Addition of polymers into the cell medium also causes loss of motility due to increased shear viscosity, but the majority of immobilized bacteria remain viable. Both viscous and viscoelastic media alter the motility of flagellated bacteria without affecting the internal regulation of their motor switching behavior.

【 授权许可】

   
2014 Gao et al.; licensee BioMed Central.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

【 参考文献 】

• [1]Berg HC: The rotary motor of bacterial flagella. Annu Rev Biochem 2003, 72:19-54.
• [2]Lele PP, Hosu BG, Berg HC: Dynamics of mechanosensing in the bacterial flagellar motor. Proc Natl Acad Sci U S A 2013, 110(29):11839-11844.
• [3]Fahrner KA, Ryu WS, Berg HC: Biomechanics: bacterial flagellar switching under load. Nature 2003, 423(6943):938.
• [4]Son K, Guasto J, Stocker R: Bacteria can exploit a flagellar buckling instability to change direction. Nat Commun 2013, 9:494-498.
• [5]Xie L, Altindal T, Chattopadhyay S, Wu XL: Bacterial flagellum as a propeller and as a rudder for efficient chemotaxis. Proc Natl Acad Sci 2011, 108(6):2246-2251.
• [6]Greenberg EP, Canale-Parola E: Motility of flagellated bacteria in viscous environments. J Bacteriol 1977, 132(1):356-358.
• [7]Schneider WR, Doetsch RN: Effect of viscosity on bacterial motility. J Bacteriol 1974, 117(2):696-701.
• [8]Shoesmith JG: The measurement of bacterial motility. J Gen Microbiol 1960, 22(2):528-535.
• [9]Berg HC, Turner L: Movement of microorganisms in viscous environments. Nature 1979, 278(5702):349-351.
• [10]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):733-739.
• [11]Fu H, Wolgemuth CW, Powers TR: Swimming of filaments in nonlinearly viscoelastic fluids. Phys Fluids 2009, 21:033102.
• [12]Liu B, Powers TR, Breuer KS: Force-free swimming of a model helical flagellum in viscoelastic fluids. Proc Natl Acad Sci U S A 2011, 108(49):19516-19520.
• [13]Atsumi T, Maekawa Y, Yamada T, Kawagishi I, Imae Y, Homma M: Effect of viscosity on swimming by the lateral and polar flagella of vibrio alginolyticus. J Bacteriol 1996, 178(16):5024-5026.
• [14]Chen X, Berg HC: Torque-speed relationship of the flagellar rotary motor of escherichia coli. Biophys J 2000, 78(2):1036-1041.
• [15]Li G, Tang JX: Low flagellar motor torque and high swimming efficiency of caulobacter crescentus swarmer cells. Biophys J 2006, 91(7):2726-2734.
• [16]Ferry J: Viscoelastic Properties of Polymers. 3rd edition. John Wiley, New York; 1980.
• [17]Larson RG: The Structure and Rheology of Complex Fluids. Oxford University Press, New York; 1999.
• [18]Gode-Potratz CJ, Kustusch RJ, Breheny PJ, Weiss DS, McCarter LL: Surface sensing in vibrio parahaemolyticus triggers a programme of gene expression that promotes colonization and virulence. Mol Microbiol 2011, 79(1):240-263.
• [19]Anderson JK, Smith TG, Hoover TR: Sense and sensibility: flagellum-mediated gene regulation. Trends Microbiol 2010, 18(1):30-37.
• [20]Kearns DB: A field guide to bacterial swarming motility. Nat Rev Microbiol 2010, 8(9):634-644.
• [21]Rather PN: Swarmer cell differentiation in proteus mirabilis. Environ Microbiol 2005, 7(8):1065-1073.
• [22]Li G, Brown PJ, Tang JX, Xu J, Quardokus EM, Fuqua C, Brun YV: Surface contact stimulates the just-in-time deployment of bacterial adhesins. Mol Microbiol 2012, 83(1):41-51.
• [23]Poindexter JS: Biological properties and classification of the caulobacter crescentus group. Bacteriol Rev 1964, 28:231-295.
• [24]Boutte, CC, Crosson, S: Bacterial lifestyle shapes stringent response activation.Trends Microbiol 2013, 21(4):174–180.
• [25]Poindexter JS: The caulobacters: ubiquitous unusual bacteria. Microbiol Rev 1981, 45(1):123-179.
• [26]Lawler ML, Brun YV: Advantages and mechanisms of polarity and cell shape determination in caulobacter crescentus. Curr Opin Microbiol 2007, 10(6):630-637.
• [27]Wagner JK, Setayeshgar S, Sharon LA, Reilly JP, Brun YV: A nutrient uptake role for bacterial cell envelope extensions. Proc Natl Acad Sci U S A 2006, 103(31):11772-11777.
• [28]Li G, Smith CS, Brun YV, Tang JX: The elastic properties of the caulobacter crescentus adhesive holdfast are dependent on oligomers of N-Acetylglucosamine. J Bacteriol 2005, 187(1):257-265.
• [29]Merker RI, Smit J: Characterization of the adhesive holdfast of marine and freshwater caulobacters. Appl Environ Microbiol 1988, 54(8):2078-2085.
• [30]Bodenmiller D, Toh E, Brun YV: Development of surface adhesion in caulobacter crescentus. J Bacteriol 2004, 186(5):1438-1447.
• [31]Entcheva-Dimitrov P, Spormann AM: Dynamics and control of biofilms of the oligotrophic bacterium caulobacter crescentus. J Bacteriol 2004, 186(24):8254-8266.
• [32]Skerker JM, Shapiro L: Identification and cell cycle control of a novel pilus system in caulobacter crescentus. EMBO J 2000, 19(13):3223-3234.
• [33]Li G, Tam L-K, Tang JX: Amplified effect of brownian motion in bacterial near-surface swimming. Proc Natl Acad Sci 2008, 105(47):18355-18359.
• [34]Li GL, Bensson J, Nisimova L, Munger D, Mahautmr P, Tang JX, Maxey MR, Brun YV: Accumulation of swimming bacteria near a solid surface. Phys Rev E 2011, 84(4):041932.
• [35]Li, GL and JX Tang: Accumulation of microswimmers near a surface mediated by collision and rotational brownian motion, Phys Rev Lett 2009, 103(7):078101.
• [36]Beney L, Mille Y, Gervais P: Death of escherichia coli during rapid and severe dehydration is related to lipid phase transition. Appl Microbiol Biotechnol 2004, 65(4):457-464.
• [37]Howard DH: The preservation of bacteria by freezing in glycerol broth. J Bacteriol 1956, 71(5):625.
• [38]Morris GJ, Goodrich M, Acton E, Fonseca F: The high viscosity encountered during freezing in glycerol solutions: effects on cryopreservation. Cryobiology 2006, 52(3):323-334.
• [39]Liu B, Gulino M, Morse M, Tang JX, Powers TR, Breuer KS: Helical motion of the cell body enhances caulobacter crescentus motility. Proc Natl Acad Sci U S A 2014, 111(31):11252-11256.
• [40]Yuan J, Fahrner KA, Turner L, Berg HC: Asymmetry in the clockwise and counterclockwise rotation of the bacterial flagellar motor. Proc Natl Acad Sci U S A 2010, 107(29):12846-12849.
• [41]Braun TF, Al-Mawsawi LQ, Kojima S, Blair DF: Arrangement of core membrane segments in the mota/motb proton-channel complex of escherichia coli. Biochemistry 2004, 43(1):35-45.
• [42]Brown MT, Delalez NJ, Armitage JP: Protein dynamics and mechanisms controlling the rotational behaviour of the bacterial flagellar motor. Curr Opin Microbiol 2011, 14(6):734-740.
• [43]Lele PP, Branch RW, Nathan VS, Berg HC: Mechanism for adaptive remodeling of the bacterial flagellar switch. Proc Natl Acad Sci U S A 2012, 109(49):20018-20022.
• [44]Yuan J, Branch RW, Hosu BG, Berg HC: Adaptation at the output of the chemotaxis signalling pathway. Nature 2012, 484(7393):233-236.
• [45]Yuan J, Berg HC: Ultrasensitivity of an adaptive bacterial motor. J Mol Biol 2013, 425(10):1760-1764.
• [46]Teran J, Fauci L, Shelley M: Viscoelastic fluid response can increase the speed and efficiency of a free swimmer. Phys Rev Lett 2010, 104:038101.
• [47]Armitage JP, Schmitt R: Bacterial chemotaxis: rhodobacter sphaeroides and sinorhizobium meliloti--variations on a theme? Microbiology 1997, 143(Pt 12):3671-3682.
• [48]Morse M, Huang A, Li G, Maxey MR, Tang JX: Molecular adsorption steers bacterial swimming at the air/water interface. Biophys J 2013, 105:21-28.
• [49]Degnen ST, Newton A: Chromosome replication during development in caulobacter crescentus. J Mol Biol 1972, 64(3):671-680.
• [50]Holyst R, Bielejewska A, Szymanski J, Wilk A, Patkowski A, Gapinski J, Zywocinski A, Kalwarczyk T, Kalwarczyk E, Tabaka M, Ziebacz N, Wieczorek SA: Scaling form of viscosity at all length-scales in poly(Ethylene Glycol) solutions studied by fluorescence correlation spectroscopy and capillary electrophoresis. Phys Chem Chem Phys 2009, 11(40):9025-9032.
• [51]Doi M, Edwards SF: The Theory of Polymer Dynamics. Clarendon, Oxford; 1986.
• [52]Watanabe H: Viscoelasticity and dynamics of entangled polymers. Prog Polym Sci 1999, 24:1253-1403.
• [53]Smit J, Sherwood CS, Turner RF: Characterization of high density monolayers of the biofilm bacterium caulobacter crescentus: evaluating prospects for developing immobilized cell bioreactors. Can J Microbiol 2000, 46(4):339-349.