Galvanotaxis of ciliates: spatiotemporal dynamics of Coleps hirtus under electric fields

Abstract

Galvanotaxis describes the functional response of organisms to electric fields. In ciliates, the electric field influences the electrophysiology, and thus, the cilia beat dynamics. This leads to a change of the swimming direction toward the cathode. The dynamical response to electric fields of Coleps hirtus has not been studied since the observations of Verworn in 1890 Pflüger Arch. 46 267–303. While galvanotaxis has been studied in other ciliates, C. hirtus exhibit properties not found elsewhere, such as biomineralization processes of alveolar plates with impact on the intracellular calcium regulation and a bimodal resting membrane potential, which leads to unique electrophysiological driven bimodal swimming dynamics. Here, we statistically analyze the galvanotactic dynamics of C. hirtus by automated cell tracking routines. We found that the number of cells that show a galvanotactic response, increases with the increase of the applied electric field strength with a mean at about 2.1 V cm−1. The spatiotemporal swimming dynamics change and lead to a statistical increase of linear elongated cell trajectories that point toward the cathode. Further, the increase of the electric fields decreases the mean velocity variance for electric fields larger than about 1.3 V cm−1, while showing no significant change in the absolute velocity for any applied electric field. Fully functional galvanotactic responses were observed at a minimum extracellular calcium concentration of about 5 μM. The results add important insights to the current understanding of cellular dynamics of ciliates and suggest that the currently accepted model lacks the inclusion of the swimming dynamics and the complex calcium regulatory system of the cell. The results of this study not only extend the fundamental understanding of current physical models for galvanotaxis and C. hirtus dynamics, but also open possibilities for technical applications, such as biosensors or microrobots in the future.