The Kinetics of Gravitaxis and Gravikinesis Relaxation Following Step Transition to Microgravity

Mission: Drop Shaft (JAMIC, Kamisunagawa)

Investigators: (1) Machemer, H.; (2) Bräucker, R.; (3) Machemer-Röhnisch,S.; (4) Takahashi, K.; (5) Murakami, A.; (6) Yoshimura, K., kegaya, K.

Keywords: Gravitaxis, Gravikinesis, Microgravity, Swimming Rate, Relaxation Kinetics,  Ciliates 

Discipline: Life Sciences

Research Area: Gravitational Physiology of Single Cells

References: R. Bräucker, Murakami, A., Ikegaya, K., Yoshimura, K., Takahashi, K., Machemer- Röhnisch, S., Machemer, H., "relaxation and activation of graviresponses in  paramecium". J. Exp. Biol. 201: 2103-2113 (1998). 
S. Machemer-Röhnisch,  Bräucker, R., Machemer, H., "Graviresponses of gliding and swimming Loxodes using  step transition to weightlessness". J. Euk. Microbiol. 45: 411-418 (1998). 
S. Machemer- Röhnisch, Bräucker, R., Machemer, H., "Relaxation of graviresponses of the ciliate  Didinium following step transition to the weightless condition". Microgravity Sci.  Technol. 11: 35-43 (1998). 
S. Machemer-Röhnisch, Machemer H., Bräucker R.,  "Electric-field effects on gravikinesis in Paramecium". J. Comp. Physiol. A 179:  213-226 (1996).

Extended Abstract

Experiment Objectives:  The gradual relaxation of gravitaxis and gravikinesis under microgravity seen in previous experiments included an apparently paradoxical result: the gravikinesis, which opposed effects of sedimentation under 1 g, changed sign in the initial time of µg now mimicking effects of sedimentation. In order to have a more detailed knowledge of the relaxation kinetics during µg, we sought to extend the µg period, which is available in the 500 m drop shaft of JAMIC at Kamisunagawa/ Hokkaido providing 10 s of weightlessness.

Experiment Procedure:  The kinetics of gravitaxis and gravikinesis were investigated in Paramecium caudatum, Loxodes striatus, and Didinium nasutum.  Step transitions from normal gravity to micro-gravity in the 500 m drop shaft of JAMIC in Hokkaido, Japan included a microgravity quality of 10-3 g after 0.4 s, 10^-4 g after 0.6 s, and 10^-5 g after 1.3 s.  We used a newly developed scheme of data processing giving time resolutions of speed of >= 3 µm/s for Loxodes, >= 3.8 µm/s for Paramecium, and >= 119 µm/s for Didinium.

Experiment Results.  All three species of cells were gravitactic under 1 g conditions (upward orientation: Paramecium; Didinium; downward orientation: Loxodes at > 40% air saturation).  The instantaneous transition to microgravity left existing orientations primarily unchanged, but relaxation of negative gravitaxis under microgravity followed a negative exponential time course exceeding 10 s of microgravity.  Time constants of relaxation of gravitaxis differed in the species investigated and even varied depending on culture condition.  Gravitaxis relaxation of Loxodes was more pronounced in gliding cells than in swimming cells.  In fast swimming Didinium (> 2000 µm/s) the assessment of relaxation from gravitaxis was affected by the lateral dimension (35 mm x 35 mm) of the space for swimming.  Collision with the wall induced upward swimmers to turn downward, and downward swimmers to turn upward generating transition from negative to apparently paradoxical positive gravitaxis under microgravity.  Gravity-induced speed regulation (gravikinesis) of Paramecium at 1 g was at steady-state 1 min after turning the experimental chamber from horizontal to vertical position.  In all species investigated, gravikinesis counteracted the effects of sedimentation (Paramecium: -50 µm/s; Didinium: -109 µm/s; Loxodes, gliders: -12 µm/s; Loxodes, swimmers: -10.5 µm/s).  In Paramecium, the step transition to microgravity initially reversed the sign of the gravikinesis (from negative to positive gravikinesis: +18 µm/s).  The oscillation-type relaxation of this kinetic response was not fully completed during 10 s of microgravity, although it passed the zero line after 4 s and 7 s of µg.  The data suggest that gravikinesis is functionally unrelated to gravitaxis being strongly affected by the rate of change in acceleration.  Didinium changed sign from negative gravikinesis to positive gravikinesis between the first and fourth second of microgravity with gravikinesis rising to a peak value of +45 µm/s between the seventh and tenth second of µg.  As in Paramecium, the full relaxation from gravikinesis was not seen within the available 10 s of µg.  Gliding cells of Loxodes did not fully abandon kinesis during the microgravity period, whereas swimming cells gradually changed the sign from negative to positive gravikinesis during this time.

The complexity of relaxation of gravikinetic behaviour in ciliates is obviously due to structural and functional properties of cellular organization: (1) The viscoelastic cytoplasm including the cytoskeleton is a limiting factor in rapid changes of membrane deformation in agreement with the literature, where relaxation times of 1 min have been reported in mechanosensory hair cells of vertebrates.  (2) A step change in mechanical stress, as induced by the transition from 1 g to µg, can differerently affect mechanoreceptor channels of cells depending on their distribution in the plasma membrane.  We present a model using previous evidence suggesting that fibers of the cytoskeleton connect to gates of gravitationally sensitive channels (Machemer-Röhnisch et al. 1996).  Combining cellular viscoelasticity with topological channel distributions, the model explains why gravikinesis can transiently reverse sign upon transition from 1 g to microgravity.