Abstract
Evolution has generated a plethora of flagellate microswimmers. They populate all natural waters, from the deep sea to the ponds in our neighbourhood. But flagellates also thrive in the bodies of higher organisms, where they mostly remain undetected, but can also become pathogenic. Trypanosomes comprise a large group of mostly parasitic flagellates that cause many diseases, such as human sleeping sickness or the cattle plague nagana. We consider African trypanosomes as extremely versatile microswimmers, as they have to adapt to very diverse microenvironments. They swim efficiently in the blood of their mammalian hosts, but also in various tissue spaces and even in the human brain. Furthermore, in the transmitting tsetse fly, trypanosomes undergo characteristic morphological changes that are accompanied by amazing transitions between solitary and collective types of motion. In this review, we provide a basic introduction to trypanosome biology and then focus on the complex type of rotational movement that trypanosomes display. We relate their swimming performance to morphological parameters and the respective microenvironment, developing a contemporary view on the physics of trypanosome motility. The genetically programmed successions of life style-dependent motion patterns provide challenges and opportunities for interdisciplinary studies of microswimmers.
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U.B. Kaupp, L. Alvarez, Eur. Phys. J. Special Topics 225, 2119 (2016)
R. Jeanneret, M. Contino, M. Polin, Eur. Phys. J. Special Topics 225, 2141 (2016)
E.M. Purcell, Am. J. Phys. 45, 3 (1977)
I.H. Riedel, K. Kruse, J. Howard, Science 309, 300 (2005)
R. Brun, J. Blum, F. Chappuis, C. Burri, The Lancet 375, 148 (2010)
M. Engstler, T. Pfohl, S. Herminghaus, M. Boshart, G. Wiegertjes, N. Heddergott, et al., Cell. 131, 505 (2007)
R. Ross, D. Thomson, Br. Med. J. 1, 1544 (1910)
B.M. Mony, K.R. Matthews, Mol. Microbiol. 96, 220 (2015)
K. Vickerman, Br. Med. Bull. 41, 105 (1985)
R. Sharma, E. Gluenz, L. Peacock, W. Gibson, K. Gull, M. Carrington, Trends Parasitol. 25, 517 (2009)
N.A. Dyer, C. Rose, N.O. Ejeh, A. Acosta-Serrano, Trends Parasitol. 29, 188 (2013)
K.R. Matthews, Mol. Biochem. Parasitol. 200, 30 (2015)
K. Gull, Curr. Opin. Microbiol. 6, 365 (2003)
R. Broadhead, H.R. Dawe, H. Farr, S. Griffiths, S.R. Hart, N. Portman, et al., Nature 440, 224 (2006)
J.D. Sunter, K. Gull, Trends Parasitol. 32, 309 (2016)
P. Overath, M. Engstler, Mol. Microbiol. 53, 735 (2004)
J.D. Sunter, V. Varga, S. Dean, K. Gull, J. Cell. Sci. 128, 1580 (2015)
M. Engstler, L. Thilo, F. Weise, C.G. Grünfelder, H. Schwarz, M. Boshart, et al., J. Cell. Sci. 117, 1105 (2004)
E. Pays, L. Vanhamme, D. Pérez-Morga, Curr. Opin. Microbiol. 7, 369 (2004)
M.E. Dubois, K.P. Demick, J.M. Mansfield, Infect Immun. 73, 2690 (2005)
I. Roditi, H. Schwarz, T.W. Pearson, R.P. Beecroft, M.K. Liu, J.P. Richardson, et al., J. Cell. Biol. 108, 737 (1989)
D. Gruby, Comptes Rendus Hebd Séances Académie Sci. 17, 1134 (1843)
C.A. Hoare, The trypanosomes of mammals (Blackwell Scientific Publications, Edinburgh, 1972)
N. Heddergott, T. Krüger, S.B. Babu, A. Wei, E. Stellamanns, S. Uppaluri, et al., PLoS Pathog. 8, e1003023 (2012)
T.L. Jahn, J.R. Fonseca, J. Protozool. 10, 11 (1963)
T.L. Jahn, J.J. Votta, Annu. Rev. Fluid Mech. 4, 93 (1972)
M.E.J. Holwill, J. Exp. Biol. 42, 125 (1965)
C.J. Brokaw, Exp. Cell. Res. 19, 430 (1960)
M.E.J. Holwill, Physiol. Rev. 46, 696 (1966)
J. Gray, J. Exp. Biol. 32, 775 (1955)
J. Gray, G.J. Hancock, J. Exp. Biol. 32, 802 (1955)
E. Lauga, T.R. Powers, Rep. Prog. Phys. 72, 096601 (2009)
J. Elgeti, R.G. Winkler, G. Gompper, Rep. Prog. Phys. 78, 056601 (2015)
C. Gadelha, B. Wickstead, K. Gull, Cell. Motil. Cytoskeleton. 64, 629 (2007)
C. Branche, L. Kohl, G. Toutirais, J. Buisson, J. Cosson, P. Bastin, J. Cell Sci. 119, 3443 (2006)
D.M. Baron, Z.P. Kabututu, K.L. Hill, J. Cell. Sci. 120, 1513 (2007)
H. Weiße, N. Heddergott, M. Heydt, D. Pflästerer, T. Maier, T. Haraszti, et al., PLoS One. 7, e37296 (2012)
V. Zaburdaev, S. Uppaluri, T. Pfohl, M. Engstler, R. Friedrich, H. Stark. Phys. Rev. Lett. 106, 208103 (2011)
S. Uppaluri, J. Nagler, E. Stellamanns, N. Heddergott, S. Herminghaus, M. Engstler, et al., PLoS Comput. Biol. 7, e1002058 (2011)
D. Alizadehrad, T. Krüger, M. Engstler, H. Stark. PLoS Comput. Biol. 11, e1003967 (2015)
R.G. Winkler, Eur. Phys. J. Special Topics 225, 2079 (2016)
J. Carnes, A. Anupama, O. Balmer, A. Jackson, M. Lewis, R. Brown, et al., PLoS Negl Trop Dis. 9, e3404 (2015)
J.L. Bargul, J. Jung, F.A. McOdimba, C.O. Omogo, V.O. Adung’a, T. Krüger, et al., PLoS Pathog. 12, e1005448 (2016)
E. Stellamanns, S. Uppaluri, A. Hochstetter, N. Heddergott, M. Engstler, T. Pfohl, Sci. Rep. 4, (2014)
S. Uppaluri, N. Heddergott, E. Stellamanns, S. Herminghaus, A. Zöttl, H. Stark, et al., Biophys. J. 103, 1162 (2012)
H.C. Berg, L. Turner, Nature 278, 349 (1979)
Y. Magariyama, S. Kudo, Biophys. J. 83, 733 (2002)
S. Mogk, A. Meiwes, C.M. Boßelmann, H. Wolburg, M. Duszenko, Trends Parasitol. 30, 470 (2014)
T. Krüger, M. Engstler, Semin. Cell Dev. Biol. 46, 113 (2015)
J.C. Kirkman-Brown, D.J. Smith, Mol. Hum. Reprod. 17, 539 (2011)
E.A. Gaffney, H. Gadêlha, D.J. Smith, J.R. Blake, J.C. Kirkman-Brown, Annu. Rev. Fluid Mech. 43, 501 (2011)
R. Nosrati, A. Driouchi, C.M. Yip, D. Sinton, Nat. Commun. 6, 8703 (2015)
B. Rotureau, I. Subota, P. Bastin, Cell. Microbiol. 13, 705 (2011)
I. Subota, B. Rotureau, T. Blisnick, S. Ngwabyt, M. Durand-Dubief, M. Engstler, et al., Mol. Biol. Cell. 22, 4205 (2011)
B. Rotureau, I. Subota, J. Buisson, P. Bastin, Development 139, 1842 (2012)
A. Hochstetter, E. Stellamanns, S. Deshpande, S. Uppaluri, M. Engstler, T. Pfohl, Lab. Chip. 15, 1961 (2015)
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Krüger, T., Engstler, M. Trypanosomes – versatile microswimmers. Eur. Phys. J. Spec. Top. 225, 2157–2172 (2016). https://doi.org/10.1140/epjst/e2016-60063-5
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DOI: https://doi.org/10.1140/epjst/e2016-60063-5