Letter | Published:

Schistosoma mansoni cercariae swim efficiently by exploiting an elastohydrodynamic coupling

Nature Physics volume 13, pages 266271 (2017) | Download Citation

Abstract

The motility of many parasites is critical for infecting their host, as exemplified in the transmission cycle of the parasite Schistosoma mansoni1. In its human infectious stage, submillimetre-scale forms of the parasite known as cercariae swim in freshwater and infect humans by penetrating the skin1,2. This infection causes schistosomiasis, a disease comparable to malaria in global socio-economic impact3,4. Given that cercariae do not feed and hence have a lifetime of around 12 hours5,6, efficient motility is crucial for schistosomiasis transmission. Despite this, a first-principles understanding of how cercariae swim is lacking. Combining biological experiments, a novel theoretical model and its robotic realization, we show that cercariae use their forked tail to swim against gravity using a novel swimming gait, described here as a ‘T-swimmer gait’. During this gait, cercariae beat their tail periodically while maintaining an increased flexibility near their posterior and anterior ends. This flexibility allows an interaction between fluid drag and bending resistance—an elastohydrodynamic coupling, to naturally break time-reversal symmetry and enable locomotion at small length scales7. Finally, we find that cercariae maintain this flexibility at an optimal regime for efficient swimming. We anticipate that our work sets the ground for linking the swimming of cercariae to disease transmission, and could potentially enable explorations of novel strategies for schistosomiasis control and prevention.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

    Physiological analysis of cercarial behavior. Physiol. Anal. Cercarial Behav. 78, 243–255 (1992).

  2. 2.

    Parasitic worms: strategies of host finding, recognition and invasion. Zoology 106, 349–364 (2003).

  3. 3.

    & Neglected tropical diseases in sub-Saharan Africa: review of their prevalence, distribution, and disease burden. PLoS Negl. Trop. Dis. 3, e412 (2009).

  4. 4.

    & Schistosomiasis in Africa: an emerging tragedy in our new global health decade. PLoS Negl. Trop. Dis. 3, e485 (2009).

  5. 5.

    & The survival of the cercariae of Schistosoma mansoni in relation to water temperature and glycogen utilization. Parasitology 81, 337–348 (1980).

  6. 6.

    , , & Age-dependent survival and infectivity of Schistosoma mansoni cercariae. Parasitology 127, 29–35 (2003).

  7. 7.

    Life at low Reynolds number. Am. J. Phys. 45, 3–11 (1977).

  8. 8.

    , & Selection of the host’s habitat by cercariae: from laboratory experiments to the field. J. Parasitol. 94, 1233–1238 (2008).

  9. 9.

    , , & Behaviours in trematode cercariae that enhance parasite transmission: patterns and processes. Parasitology 109, S3 (1994).

  10. 10.

    , & Forked tail of the cercaria of Schistosoma mansonia rowing device. Nature 215, 207–208 (1967).

  11. 11.

    The Structure and Behaviour of the Cercaria of Schistosoma Mansoni PhD thesis, Univ. York (1975).

  12. 12.

    Random Walks in Biology (Princeton Univ. Press, 1993).

  13. 13.

    & The hydrodynamics of swimming microorganisms. Rep. Prog. Phys. 72, 96601 (2009).

  14. 14.

    & The fluid dynamics of swimming microorganisms and cells. J. Indian Inst. Sci. 91, 283–314 (2012).

  15. 15.

    Swimming behaviour of the cercaria of Transversotrema patialense. Parasitology 82, 319–334 (1981).

  16. 16.

    , , & Schistosoma mansoni: human skin ceramides are a chemical cue for host recognition of cercariae. Exp. Parasitol. 120, 94–97 (2008).

  17. 17.

    & Swimming behaviour of Schistosoma mansoni cercariae: responses to irradiance changes and skin attractants. Parasitol. Res. 102, 685–690 (2008).

  18. 18.

    et al. Recognition and invasion of human skin by Schistosoma mansoni cercariae: the key-role of L-arginine. Parasitology 124, 153–167 (2002).

  19. 19.

    Advanced Transport Phenomena: Fluid Mechanics and Convective Transport Processes Vol. 7 (Cambridge Univ. Press, 2007).

  20. 20.

    & Flexive and propulsive dynamics of elastica at low Reynolds number. Phys. Rev. Lett. 80, 3879–3882 (1998).

  21. 21.

    The motion of long slender bodies in a viscous fluid part 1. General theory. J. Fluid Mech. 44, 791–810 (1970).

  22. 22.

    Studies on the fine structure of cercarial tail muscle of Schistosoma sp. (Trematoda). J. Ultrastruct. Res. 57, 77–86 (1976).

  23. 23.

    The fine structure and organization of the tail musculature of the cercaria of Schistosoma mansoni. Parasitology 68, 147–154 (1974).

  24. 24.

    & Dynamics of Purcell’s three-link microswimmer with a passive elastic tail. Eur. Phys. J. E 35, 1–9 (2012).

  25. 25.

    , , & High-precision tracking of sperm swimming fine structure provides strong test of resistive force theory. J. Exp. Biol. 213, 1226–1234 (2010).

  26. 26.

    Locomotion of flagellates with mastigonemes. J. Mechanochem. Cell Motil. 3, 207–217 (1975).

  27. 27.

    , , & Schistosomiasis control: praziquantel forever? Mol. Biochem. Parasitol. 195, 23–29 (2014).

Download references

Acknowledgements

We thank all members of Prakash lab for fruitful discussions. D.K. is supported by a Stanford Bio-X Bowes fellowship. G.K. was supported by the Onassis Foundation and the A.G. Leventis Foundation. M.P. is supported by the Keck Foundation. This material is based on work supported by, or in part by, the US Army Research Laboratory and the US Army Research Office under contract/grant number W911NF-15-1-0358. This work was also supported by National Institute of Health Directors New Innovator Award (Grant number DP2-AI-124336) and Pew Scholars Program. We thank J. Sakanari and K. C. Lim of UCSF for providing lab space and live organisms. We thank M. Lanas for the scientific illustrations of cercariae in their natural habitat.

Author information

Affiliations

  1. Department of Mechanical Engineering, Stanford University, Stanford, California 94305, USA

    • Deepak Krishnamurthy
    •  & Georgios Katsikis
  2. Department of Applied Physics, Stanford University, Stanford, California 94305, USA

    • Arjun Bhargava
  3. Department of Bioengineering, Stanford University, Stanford, California 94305, USA

    • Manu Prakash

Authors

  1. Search for Deepak Krishnamurthy in:

  2. Search for Georgios Katsikis in:

  3. Search for Arjun Bhargava in:

  4. Search for Manu Prakash in:

Contributions

D.K. and M.P. designed the research. D.K., G.K. and M.P. performed experiments. G.K. and D.K. performed image analysis. D.K. and A.B. performed the scaled-up robotic experiments and D.K. performed numerical simulations. D.K., G.K. and M.P. analysed the results and wrote the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Manu Prakash.

Supplementary information

PDF files

  1. 1.

    Supplementary information

    Supplementary information

Videos

  1. 1.

    Supplementary Movie 1

    Supplementary Movie

  2. 2.

    Supplementary Movie 2

    Supplementary Movie

  3. 3.

    Supplementary Movie 3

    Supplementary Movie

  4. 4.

    Supplementary Movie 4

    Supplementary Movie

  5. 5.

    Supplementary Movie 5

    Supplementary Movie

  6. 6.

    Supplementary Movie 6

    Supplementary Movie

  7. 7.

    Supplementary Movie 7

    Supplementary Movie

  8. 8.

    Supplementary Movie 8

    Supplementary Movie

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nphys3924

Further reading