Abstract
How microorganisms interact with their environment and with their conspecifics depends strongly on their mechanical properties, on the hydrodynamic signatures they generate while swimming and on fluid flows in their environment. The rich fluid-structure interaction between flagella – the appendages microorganisms use for propulsion – and the surrounding flow, has broad reaching effects for both eukaryotic and prokaryotic microorganisms. Here, we discuss selected recent advances in our understanding of the physical ecology of microorganisms, which have hinged on the ability to directly interrogate the movement of individual cells and their swimming appendages, in precisely controlled fluid environments, and to image them at appropriately fast timescales. We review how a flagellar buckling instability can unexpectedly serve a fundamental function in the motility of bacteria, we elucidate the role of hydrodynamics and flexibility in the emergent properties of groups of eukaryotic flagella, and we show how fluid flows characteristic of microbial habitats can strongly bias the migration and spatial distribution of bacteria. The topics covered here are illustrative of the potential inherent in the adoption of experimental methods and conceptual frameworks from physics in understanding the lives of microorganisms.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
K. Son, D.R. Brumley, R. Stocker, Nat. Rev. Microbiol. 13, 761 (2015)
J. Elgeti, R.G. Winkler, G. Gompper, Rep. Prog. Phys. 78, 56601 (2015)
M.B. Short, C.A. Solari, S. Ganguly, T.R. Powers, J.O. Kessler, R.E. Goldstein, Proc. Natl. Acad. Sci. USA 103, 8315 (2006)
T. Ishikawa, M.P. Simmonds, T.J. Pedley, J. Fluid Mech. 568, 119 (2006)
R. Rusconi, S. Lecuyer, N. Autrusson, L. Guglielmini, H.A. Stone, Biophys. J. 100, 1392 (2011)
J. Brueckner, M. McGrath, Curr. Opin. Genet. Dev. 13, 385 (2003)
O.H. Shapiro, V.I. Fernandez, M. Garren, J.S. Guasto, F.P. Debaillon-Vesque, E. Kramarsky-Winter, A. Vardi, R. Stocker, Proc. Natl. Acad. Sci. USA 111, 13391 (2014)
R. Rusconi, R. Stocker, Curr. Opin. Microbiol. 25, 1 (2015)
K. Drescher,Y. Shen, B.L. Bassler, H.A. Stone, Proc. Natl. Acad. Sci. USA 110, 4345 (2013)
J. Li, G. Lykotrafitis, M. Dao, S. Suresh, Proc. Natl. Acad. Sci. USA 104, 4937 (2007)
J. Gore, Z. Bryant, M. Nöllmann, M.U. Le, N.R. Cozzarelli, C. Bustamante, Nature 442, 836 (2006)
K. Son, J.S. Guasto, R. Stocker, Nat. Phys. 9, 494 (2013)
D.R. Brumley, M. Polin, T.J. Pedley, R.E. Goldstein, J. R. Soc. Interface 12, 20141358 (2015)
R. Rusconi, J.S. Guasto, R. Stocker, Nat. Phys. 10, 212 (2014)
E.M. Purcell, Am. J. Phys. 45(1), 3 (1977)
H.C. Berg, R.A. Anderson, Nature 245, 380 (1973)
H.C. Berg, Annu. Rev. Biochem. 72, 19 (2003)
H.C. Berg, D.A. Brown, Nature 239, 500 (1972)
H.C. Berg, E. coli in Motion 1st edition (Springer-Verlag, New York, 2004)
E. Lauga (2015) [arXiv preprint] [arXiv:1509.02184] Annu. Rev. Fluid Mech, to appear (2016)
L. Turner, W.S. Ryu, H.C. Berg, J. Bacteriol. 182, 2793 (2000)
N.C. Darnton, L. Turner, S. Rojevsky, H.C. Berg, J. Bacteriol. 189, 1756 (2007)
S.E. Spagnolie, E. Lauga, Phys. Rev. Lett. 106, 58103 (2011)
M.T. Brown, B.C. Steel, C. Silvestrin, D.A. Wilkinson, N.J. Delalez, C.N. Lumb, B. Obara, J.P. Armitage, R.M. Berry, J. Bacteriol. 194, 3495 (2012)
E. Leifson, B.J. Cosenza, R. Murchelano, R.C. Cleverdon, J. Bacteriol. 87, 652 (1964)
L. Xie, T. Altindal, S. Chattopadhyay, X.-L. Wu, Proc. Natl. Acad. Sci. USA 108, 2246 (2011)
R. Stocker, J.R. Seymour, Microbiol. Mol. Bio. Rev. 76, 792 (2012)
E. Lauga, T.R. Powers, Rep. Prog. Phys. 72, 096601 (2009)
S.P. Timoshenko, Theory of elastic stability, 2nd edn. (McGraw-Hill, 1961)
G. Li, C.S. Smith, Y.V. Brun, J.X. Tang, J. Bacteriol. 187, 257 (2005)
E. Alipour-Assiabi, G. Li, T.R. Powers, J.X. Tang, Biophys. J. 90, 2206 (2006)
S. Nonaka, H. Shiratori, Y. Saijoh, H. Hamada, Nature 418, 96 (2002)
J. Gray, G.J. Hancock, J. Exp. Biol. 32, 802 (1955)
R. Shlomovitz, Y. Roongthumskul, S. Ji, D. Bozovic, R. Bruinsma, Interface Focus 4, 20140022 (2014)
K. Drescher, K.C. Leptos, I. Tuval, T. Ishikawa, T.J. Pedley, R.E. Goldstein, Phys. Rev. Lett. 102, 168101 (2009)
B. Button, L. Cai, C. Ehre, M. Kesimer, D.B. Hill, J.K. Sheehan, R.C. Boucher, M. Rubinstein, Science 337, 937 (2012)
J.H.E. Cartwright, O. Piro, I. Tuval, Proc. Natl. Acad. Sci. USA 101, 7234 (2004)
D.W. Fawcett, K.R. Porter, J. Morph. 94, 221 (1954)
A. Gennerich, R.D. Vale, Curr. Opin. Cell Biol. 21, 59 (2009)
R. Rikmenspoel, J. Cell Biol. 76, 310 (1978)
M.A. Sleigh, J. Exp. Biol. 37, 1 (1960)
J. Gray, Proc. R. Soc. B, 93, 104 (1922)
C.J. Brokaw, Nature 209, 161 (1966)
S. Camalet, F. Jülicher, J. Prost, Phys. Rev. Lett. 82, 1590 (1999)
C. Pozrikidis, Boundary integral and singularity methods for linearized viscous flow, (Cambridge University Press, Cambridge, 1992)
J.R. Blake, A.T. Chwang, J. Eng. Math. 8, 23 (1973)
G.J. Hancock, Proc. R. Soc. A. 217, 96 (1953)
J. Lighthill, SIAM Rev. 18, 161 (1976)
R.E. Johnson, C.J. Brokaw, Biophys. J. 25, 113 (1979)
D.R. Brumley, K.Y. Wan, M. Polin, R.E. Goldstein, eLife 3, e02750 (2014)
K.Y. Wan, R.E. Goldstein, Phys. Rev. Lett. 113, 238103 (2014)
P.V. Bayly, B.L. Lewis, P.S. Kemp, R.B. Pless, S.K. Dutcher, Cytoskeleton 67, 56 (2010)
P.V. Bayly, B.L. Lewis, E.C. Ranz, R.J. Okamoto, R.B. Pless, S.K. Dutcher, Biophys. J. 100, 2716 (2011)
H. Kurtuldu, D. Tam, A.E. Hosoi, K.A. Johnson, J.P. Gollub, Phys. Rev. E 88, 13015 (2013)
B.M. Friedrich, I.H. Riedel-Kruse, J. Howard, F. Jülicher, J. Exp. Biol. 213, 1226 (2010)
A. Vilfan, Eur. Phys. J. E 35, 1 (2012)
K. Drescher, R.E. Goldstein, N. Michel, M. Polin, I. Tuval, Phys. Rev. Lett. 105, 168101 (2010)
J.S. Guasto, K.A. Johnson, J.P. Gollub, Phys. Rev. Lett. 105, 168102 (2010)
T. Niedermayer, B. Eckhardt, P. Lenz, Chaos 18, 37128 (2008)
N. Uchida, R. Golestanian, Phys. Rev. Lett. 106, 58104 (2011)
D.R. Brumley, M. Polin, T.J. Pedley, R.E. Goldstein, Phys. Rev. Lett. 109, 268102 (2012)
K.Y. Wan, K.C. Leptos, R.E. Goldstein, J. R. Soc. Interface 11, 20131160 (2014)
R. Ma, G.S. Klindt, I.H. Riedel-Kruse, F. Jülicher, B.M. Friedrich, Phys. Rev. Lett. 113, 48101 (2014)
M. Bessen, R.B. Fay, G.B. Witman, J. Cell Biol. 86, 446 (1980)
S.L. Tamm, G.A. Horridge, Proc. R. Soc. B, 175, 219 (1970)
E.W. Knight-Jones, Quart. J. Microscop. Sci. 95, 503 (1954)
B.M. Friedrich, F. Jülicher, Phys. Rev. Lett. 109, 138102 (2012)
V.F. Geyer, F. Jülicher, J. Howard, B.M. Friedrich, Proc. Natl. Acad. Sci. USA 110, 18058 (2013)
R.E. Goldstein, M. Polin, I. Tuval, Phys. Rev. Lett. 103, 168103 (2009)
M. Polin, I. Tuval, K. Drescher, J.P. Gollub, R.E. Goldstein, Science 325, 487 (2009)
R.E. Goldstein, M. Polin, I. Tuval, Phys. Rev. Lett. 107, 148103 (2011)
R. Golestanian, J.M. Yeomans, N. Uchida, Soft Matter 7, 3074 (2011)
A. Vilfan, F. Jülicher, Phys. Rev. Lett. 96, 58102 (2006)
D.M. Woolley, R.F. Crockett, W.D.I. Groom, S.G. Revell, J. Exp. Biol. 212, 2215 (2009)
N. Uchida, R. Golestanian, Eur. Phys. J. E 35, 1 (2012)
M. Kim, T.R. Powers, Phys. Rev. E 69, 61910 (2004)
P. Lenz, A. Ryskin, Phys. Biol. 3, 285 (2006)
M. Reichert, H. Stark, Eur. Phys. J. E 17, 493 (2005)
J. Kotar, L. Debono, N. Bruot, S. Box, D. Phillips, S. Simpson, S. Hanna, P. Cicuta, Phys. Rev. Lett. 111, 228103 (2013)
K.C. Leptos, K.Y. Wan, M. Polin, I. Tuval, A.I. Pesci, R.E. Goldstein, Phys. Rev. Lett. 111, 158101 (2013)
D. Eshel, I.R. Gibbons, Cell Mot. Cytoskel. 14, 416 (1989)
M. Okuno, Y. Hiramoto, J. Exp. Biol. 65, 401 (1976)
S. Gueron, K. Levit-Gurevich, N. Liron, J.J. Blum, Proc. Natl. Acad. Sci. USA 94, 6001 (1997)
B. Guirao, J.-F. Joanny, Biophys. J. 92, 1900 (2007)
Y. Yang, J. Elgeti, G. Gompper, Phys. Rev. E 78, 61903 (2008)
J. Elgeti, G. Gompper, Proc. Natl. Acad. Sci. USA 110, 4470 (2013)
S. Gueron, K. Levit-Gurevich, Proc. Natl. Acad. Sci. USA 96, 12240 (1999)
S. Gueron, N. Liron, Biophys. J. 63, 1045 (1992)
S. Gueron, N. Liron, Biophys. J. 65, 499 (1993)
S. Michelin, E. Lauga, Phys. Fluids 22, 111901 (2010)
N. Osterman, Vilfan, Proc. Natl. Acad. Sci. USA 108, 15727 (2011)
C. Mettot, E. Lauga, Phys. Rev. E 84, 061905 (2011)
A. Dauptain, J. Favier, A. Bottaro, J. Fluids Struct. 24, 1156 (2008)
J.R. Blake, J. Fluid Mech. 55, 1 (1972)
X. Yang, R.H. Dillon, L.J. Fauci, Bull. Math. Biol. 70, 1192 (2008)
Rothschild, Nature 163, 358 (1949)
G.I. Taylor, Proc. R. Soc. Lond. A, Math. 209, 447 (1951)
G.J. Elfring, E. Lauga, J. Fluid Mech. 674, 163 (2011)
G.J. Elfring, E. Lauga, Phys. Fluids 23, 11902 (2011)
C. Brennen, H. Winet, Annu. Rev. Fluid Mech. 9, 339 (1977)
H. Machemer, J. Exp. Biol. 57, 239 (1972)
K.E. Machin, Proc. R. Soc. B 158, 88 (1963)
I.H. Riedel-Kruse, A. Hilfinger, J. Howard, F. Jülicher, HFSP J. 1, 192 (2007)
C.J. Brokaw, J. Exp. Biol. 53, 445 (1970)
C.J. Brokaw, Biophys. J. 12, 564 (1972)
R. Rikmenspoel, J. Exp. Biol. 108, 205 (1984)
M.C. Lagomarsino, P. Jona, B. Bassetti, Phys. Rev. E 68, 021908 (2003)
C. Wollin, H. Stark, Eur. Phys. J. E 34, 42 (2011)
B. Qian, H. Jiang, D.A. Gagnon, K.S. Breuer, T.R. Powers, Phys. Rev. E 80, 61919 (2009)
R. Di Leonardo, A. Búzás, L. Kelemen, G. Vizsnyiczai, L. Oroszi, P. Ormos, Phys. Rev. Lett. 109, 034104 (2012)
J. Kotar, M. Leoni, B. Bassetti, M.C. Lagomarsino, P. Cicuta, Proc. Natl. Acad. Sci. USA 107, 7669 (2010)
R.E. Goldstein, Annu. Rev. Fluid Mech. 47, 343 (2015)
J.R. Blake, Math. Proc. Camb. Phil. Soc. 70, 303 (1971)
J.S. Guasto, R. Rusconi, R. Stocker, Annu. Rev. Fluid Mech. 44, 373 (2012)
A. Persat, C.D. Nadell, M.K. Kim, F. Ingremeau, A. Siryaporn, K. Drescher, N.S. Wingreen, B.L. Bassler, Z. Gitai, H.A. Stone, Cell 161, 988 (2015)
L. Hall-Stoodley, J.W. Costerton, P. Stoodley, Nat. Rev. Microbiol. 2, 95 (2004)
F. Peters, C. Marrasé, H. Havskum, F. Rassoulzadegan, J. Dolan, M. Alcaraz, J. Gasol, J. Plankton Res. 24, 321 (2002)
J.R. Taylor, R. Stocker, Science 338, 675 (2012)
D. John, J. Rose, Environ. Sci. Techonol. 39, 7345 (2005)
H.J. Kim, D. Huh, G. Hamilton, D.E. Ingber, Lab on a Chip 12, 2165 (2012)
M.A. Bees, O.A. Croze, Biofuels 5, 53 (2014)
R.H. Luchsinger, B. Bergersen, J.G. Mitchell, Biophys. J. 77, 2377 (1999)
J.T. Locsei, Pedley, Bull. Math. Biol. 71, 1089 (2009)
W.E. Thomas, V. Vogel, E. Sokurenko, Annu. Rev. Biophys. 37, 399 (2008)
S. Lecuyer, R. Rusconi, Y. Shen, A. Forsyth, H. Vlamakis, R. Kolter, H.A. Stone, Biophys. J. 100, 341 (2011)
R. Nash, R. Adhikari, J. Tailleur, M. Cates, Phys. Rev. Lett. 104, 258101 (2010)
B.J. Nelson, I.K. Kaliakatsos, J.J. Abbott, Annu. Rev. Biomedical Eng. 12, 55 (2010)
A. Genin, J.S. Jaffe, R. Reef, C. Richter, P.J.S. Franks, Science 308, 860 (2005)
J.O. Kessler, Nature 313, 218 (1985)
W.M. Durham, J.O. Kessler, R. Stocker, Science 323, 1067 (2009)
T.J. Pedley, J.O. Kessler, Annu. Rev. Fluid Mech. 24, 313 (1992)
F.P. Bretherton, Rothschild, Proc. R. Soc. B 153, 490 (1961)
V. Kantsler, J. Dunkel, M. Blayney, R.E. Goldstein, eLife 3, e02403 (2014)
H. Winet, G.S. Bernstein, J. Head, J. Reprod. Fertil. 70, 511 (1984)
T. Kaya, H. Koser, Biophys. J. 102, 1514 (2012)
H. Marcos, T. Fu, Powers, R. Stocker, Proc. Natl. Acad. Sci. USA 109, 4780 (2012)
G.B. Jeffery, Proc. R. Soc. Lond. A 102, 161 (1922)
C. Torney, Z. Neufeld, Phys. Rev. Lett. 99, 078101 (2007)
N. Khurana, J. Blawzdziewicz, N. Ouellette, Phys. Rev. Lett. 106, 198104 (2011)
C. Zhan, G. Sardina, E. Lushi, L. Brandt, J. Fluid Mech. 739, 22 (2014)
B. ten Hagen, R. Wittkowski, H. Löwen, Phys. Rev. E 84, 031105 (2011)
A. Zöttl, H. Stark, Phys. Rev. Lett. 108, 218104 (2012)
A. Zöttl, H. Stark, Eur. Phys. J. E 36, 4 (2013)
M. Tournus, A. Kirshtein, L.V. Berlyand, I.S. Aranson, J. R. Soc. Interface 12, 20140904 (2014)
S. O’Malley, M.A. Bees, Bull. Math. Biol. 74, 232 (2012)
A. Chengala, M. Hondzo, J. Sheng, Phys. Rev. E 87, 52704 (2013)
S. Rafaï, L. Jibuti, P. Peyla, Phys. Rev. Lett. 104, 98102 (2010)
R.N. Bearon, A.L. Hazel, J. Fluid Mech. 771, R3 (2015)
M.T. Barry, R. Rusconi, J.S. Guasto, R. Stocker, J. R. Soc. Interface 12, 20150791 (2015)
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Brumley, D., Rusconi, R., Son, K. et al. Flagella, flexibility and flow: Physical processes in microbial ecology. Eur. Phys. J. Spec. Top. 224, 3119–3140 (2015). https://doi.org/10.1140/epjst/e2015-50138-9
Received:
Revised:
Published:
Issue Date:
DOI: https://doi.org/10.1140/epjst/e2015-50138-9