(The FASEB Journal. 1999;13:S69-S75.)
© 1999 FASEB
Graviresponses of certain ciliates and flagellates
R. HEMMERSBACH*,1 and
D.-P. HÄDER
* Institute of Aerospace Medicine, German Aerospace Research Establishment, 51170 Köln; and
Institute for Botany and Pharmaceutical Biology, University of Erlangen, Germany
1Correspondence: Institute of Aerospace Medicine, DLR (German Aerospace Research Establishment), 51140 Köln, Under Höhe, Germany. E-mail: Ruth.Hemmersbach{at}DLR.DE
 |
ABSTRACT
|
|---|
Protozoa are eukaryotic cells and represent suitable model systems to
study the mechanisms of gravity perception and signal transduction due
to their clear gravity-induced responses (gravitaxis and gravikinesis).
Among protists, parallel evolution for graviperception mechanisms have
been identified: either sensing by distinct stato-organelles (e.g., the
Müller vesicles of the ciliate Loxodes) or by sensing
the density difference between the whole cytoplasm and the
extracellular medium (as proposed for Paramecium and
Euglena). These two models are supported by experiments in
density-adjusted media, as the gravitaxis of Loxodes was
not affected, whereas the orientation of Paramecium and
Euglena was completely disturbed. Both models include the
involvement of ion channels in the cell membrane. Diverse experiments
gave new information on the mechanism of graviperception in unicellular
systems, such as threshold values in the range of 10% of gravity,
relaxation of the responses after removal of the stimulus, and no
visible adaptation phenomena during exposure to hypergravity or
microgravity conditions for up to 12 days.—Hemmersbach, R.,
Häder, D.-P. Graviresponses of certain ciliates and flagellates.
Key Words: gravitaxis • gravikinesis • gravity sensing • microgravity • protists
|
INTRODUCTION
|
|---|
THROUGHOUT EVOLUTION gravitational acceleration has
been constantly present, thus representing one of the most important
stimuli acting on living systems. Therefore it is not astonishing that
knowing up and knowing down is not only restricted to complex organisms
but was already developed by unicellular organisms. Well-known examples
are the gravity-oriented behavior (gravitaxis) and the recently
identified gravity-induced velocity regulation (gravikinesis) of some
protists (1
, 2
). There is a long-lasting
discussion concerning the underlying mechanism of the graviresponses,
either postulating a pure physical one or a physiological one (for
review see refs. 1-4
). In the case of an asymmetrical
mass distribution, e.g., due to a heavier posterior part, a cell can be
passively aligned in the gravity field. In contrast, a physiological
mechanism is based on a signal transduction chain and thus on the
existence of a physiological receptor. With new experimental approaches
under changed gravitational stimulation (microgravity to hypergravity),
experiments in density-adjusted media, and analysis of high cell
numbers providing statistically secured data (5)
, a
discrimination between physics and physiology of the graviresponses
becomes possible (6)
. The results obtained so far are in
favor of a physiological guided mechanism of the graviresponses which,
however, do not exclude a coexisting physical mechanism (e.g., a
heavier posterior part of the cell equals a buoy effect). This report
gives an overview of our current knowledge on graviresponses in certain
protists.
|
METHODS FOR CHANGING THE GRAVITATIONAL STIMULATION
|
|---|
If one investigates the effect of light one can manipulate the
stimulus and the same can be done with gravity. Experiments under
1-G conditions can be easily performed in horizontal
microscopes. Fast-rotation of a horizontal microscope about its optical
(horizontal) axis leads to the principle of a fast-rotating clinostat
(7
, 8
, for review see ref. 9
).
It is assumed that a biological system is rotated (about its
horizontal rotation axis) at such an angular velocity that the
system can no longer perceive the rapidly turning gravity vector. The
principle is based on the fact that during rotation sedimenting
particles or masses (which are proposed as gravisensing structures, see
below) are forced to move on circular paths, the diameter of which
approaches zero at higher rotational velocities. Thus the
gravity-induced relative movement of masses (sedimentation) is
neutralized, which is also the fact under free-fall (microgravity)
conditions. As the centrifugal force follows a gradient along a radius,
it is assumed that a particle near the center of rotation is in the
status of functional weightlessness. At a rotational speed of 60 rpm,
which corresponds to the acceleration speed we normally apply in our
experiments, a maximal residual (centrifugal) acceleration of 3 x
10-3 G is calculated for the border of the
observed field (radius = 1 mm) and 4 x 10-2
G for the border of the whole observation chamber
(radius = 15 mm) (10)
. The validity of the simulation
method finally depends on the threshold for graviperception and the
perception time of the gravisensor (11)
. Some results from
simulation experiments could already be confirmed by experiments under
real free-fall conditions (also seen below in randomization of
previously gravitactic cells) (11
, for review see ref.
12
). We had access to clinostat experiments, microgravity
experiments on sounding rockets (5–12 min microgravity) and two
shuttle missions (9 and 14 days). In addition, hypergravity conditions
(up to 5 G) were achieved by using a centrifuge microscope
on the ground, distinct acceleration steps between microgravity and 1
G by using the same device in space (13)
.
|
GRAVIRESPONSES UNDER VARIABLE ACCELERATIONS
|
|---|
Observation under 1 g and under controlled
environmental conditions (e.g., isothermal conditions and homogeneous
illumination) reveal the two gravity-dependent responses of protists:
gravitaxis and gravikinesis. Gravitaxis is defined as an orientation
with respect to the gravity vector. Although most of the investigated
protists, such as Paramecium (14
, for review
see 1
, 2
), Didinium
(15)
, Tetrahymena (16)
,
Euglena (17-19)
, Cryptomonas
(20)
, and Chlamydomonas (21
,
22
), preferentially show negative gravitaxis, a few such
as Loxodes prefer a positive gravitaxis or bimodal
distribution, i.e. the occurrence of positive and negative gravitaxis
within the same culture (23-25)
(Fig. 1
). It is known that the precision of the gravitactic orientation of
Loxodes depends on the overall oxygen concentration within
the medium. Thus, the microaerophilic Loxodes, predominantly
found in the sediment of lakes, shows positive gravitaxis and bimodal
distributions under oxic conditions (>10% atmospheric
saturation), and negative gravitaxis under anaerobic conditions (<5%
atmospheric saturation) (23)
, indicating the ecological
significance of gravitaxis. A correlation between oxygen concentration
and the sign of gravitaxis does not exist for Euglena but is
conversely discussed for Paramecium (26
,
27
). Whereas Hemmersbach et al. showed that the
gravitactic response of Paramecium depends on the oxygen
tension (a precise negative gravitaxis in low-oxygen conditions, which
changes to a random distribution if the oxygen concentration is
increased) (26)
, this correlation was not supported by
Machemer et al. (27)
. It remains to be shown whether the
controversial results were due to a different gas permeability of the
materials of theobservation chambers. Switches in the sign
from negative to positive gravitaxis were observed for
Euglena by the influence of micromolar concentrations of
heavy metal ions such as copper or mercury (28)
, culture
age (29)
, and temperature (30)
and for
Paramecium by temperature (31)
and ultraviolet
radiation (32)
, without detectable changes in cell
morphology and via an as yet unknown mechanism. Besides these switches
in the sign of gravitaxis, a further argument against a pure physical
mechanism is the variable orientation of the longitudinal axis of
immobilized Paramecium cells during sedimentation
(33)
.
View larger version (11K):
[in this window]
[in a new window]
|
Figure 1. Circular histograms of spatial orientation: a) negative
gravitaxis of Paramecium biaurelia, b) positive
gravitaxis of Loxodes striatus, c) bimodal
distribution of Loxodes striatus. Each histogram represents
>1000 tracks.
|
|
Some protozoa have the additional ability to counterbalance
sedimentation due to a gravity-dependent modification of their swimming
velocity (gravikinesis). Cell sedimentation is compensated due to an
increase in propulsion in upward-swimming cells and a decrease in
downward swimming ones (34-36)
. Gravikinetic values can
be calculated from upward and downward swimming velocities and the
sedimentation velocity according to Machemer et al. (34)
.
Gravikinetic values have been identified so far for different ciliates
(e.g., Paramecium, Tetrahymena, and
Loxodes) (34
, 36
, 37
,
38
), whereas the gravitactic flagellate Euglena
does not show any gravikinesis (39)
.
In some cases graviresponses become more obvious under increased
gravitational stimulation (centrifugation) (13
,
15
, 40
). The response time to the increased
acceleration is in the second range, because already within the first
20 s [the minimum period for our image analysis system
(5)
needed for the registration of a sufficient number of
cells for statistical analysis] after onset of centrifugation an
increase in the precision of gravitaxis and in gravikinesis of
Paramecium is registered (13)
. The fact that
the gravikinetic response is slightly delayed compared to the
gravitactic response indicates different time courses of both events
and probably different mechanisms (13
, 15
).
Paramecium cells do not adapt to altered gravitational
stimulation. Repetitive stimulation between 1 and 5 G
maintained their reactivity and showed the above-mentioned
characteristic graviresponses (13)
.
Experiments in microgravity (free fall) on drop towers, sounding
rockets, or on board a space shuttle have indicated that indeed the
gravity vector on earth is an important guiding stimulus, especially in
darkness, for the orientation and speed regulation of gravisensitive
protists (2
, 10
, 37
,
39
, 41
). The results are supported by
experiments using a fast-rotating clinostat. After onset of
microgravity the protists continue to swim on straight swimming paths
and their graviresponses (gravitaxis and gravikinesis) relax after some
time. Although relaxation of the negative gravitaxis of
Paramecium was incomplete in the 4.6-s course of free fall
in a drop tower (37)
and even during 10 s of free
fall in a drop shaft (42)
, random swimming of the cells
was observed in a sounding rocket experiment after 80 s in
microgravity (Fig. 2
) (10)
. Straight swimming paths and lack of
directional turns or of backward swimming of Paramecium
indicate that no depolarization of the cell membrane to the amount of
an action potential is induced (10)
. The transiently
increased swimming velocity of Paramecium under the
conditions of microgravity indicate a hyperpolarization of the cell
membrane. After 3 min the mean swimming velocity in microgravity does
not differ from the mean swimming velocity of horizontally swimming
cells in 1 G (36
, 37
). This was
predicted by Bräucker et al. and Machemer et al.
(15
, 37
) because de- and hyperpolarizing
receptor responses neutralize under 1 G in horizontally
swimming cells (see Fig. 5
), thus corresponding to the
gravity-independent swimming velocity. In contrast to the comparable
gravitactic response in microgravity and on a fast-rotating clinostat,
the gravikinetic response of the cells differs as the mean swimming
velocity remains elevated during the clinostat experiments
(36)
. This might be an indication that
Paramecium is still mechanically stimulated and that the
cells can differentiate between fast rotation on a clinostat and real
microgravity. Further experiments will show whether the differences in
response are based on different mechanisms for gravitaxis and
gravikinesis. Cultivation of Paramecium, Euglena,
and Loxodes for several generations in space for a maximum
of 12 days did not affect the graviresponses, as shown by threshold
experiments in-flight (see below) and post-flight behavioral analyses,
thus indicating no adaptation to the microgravity environment within
this time frame (41
, 43
, 44
).
View larger version (14K):
[in this window]
[in a new window]
|
Figure 2. Circular histograms of spatial orientation of Paramecium:
negative gravitaxis under 1-G conditions (a,
b) and random distribution in microgravity (c)
and in simulated weightlessness on a fast-rotating clinostat
(d). Each histogram represents >500 tracks.
|
|
View larger version (9K):
[in this window]
[in a new window]
|
Figure 5. Model for explanation of the gravikinetic behavior of
Paramecium based on electrophysiological data. Symbols
represent the bipolar distribution of mechanosensitive ion channels in
the cell membrane: Ca2+ (diamonds) and K+
(parallel bars) channels. Arrows within the cell indicate the site of
deformation during upward (a), horizonal (b), and
downward swimming (c), thus leading to an enhanced
(a), no (b), or reduced gravikinetic response
(c). [Modified from Bräucker et al.
(15)
].
|
|
To gain the first information on the sensitivity of the model
systems, the minimal acceleration that induces the graviresponses was
determined. Such threshold experiments can only be performed in space
by using a centrifuge microscope for the application of acceleration
profiles. Thus, cell cultures were observed under increasing or
decreasing acceleration profiles between 1 x 10-4 and
1.5 G providing the following values: Paramecium
biaurelia, 0.35 G (43
, 45
);
Euglena gracilis, 0.16 G (41)
and
0.12 G (46)
; and Loxodes striatus,
0.15 G (45)
. Similar results were obtained
for cells independent of whether they were subjected to increasing or
decreasing acceleration profiles and for cells that had been cultivated
in microgravity for increasing periods of time (up to 12 days). Again,
these results indicate no adaptation of cells to microgravity, even
though they underwent several divisions under this condition. Of
special interest is the direct comparison between Paramecium
and Loxodes and thus the higher sensitivity of
Loxodes, as these ciliates were observed in parallel under
identical experimental conditions.
|
EXPERIMENTS IN DENSITY-ADJUSTED MEDIA
|
|---|
If gravity is perceived due to the density difference between the
cytoplasm and the surrounding medium, the response should disappear in
density-adjusted media (Fig. 3
). This is exactly observed with Paramecium and
Euglena under these experimental conditions
(45
, 47
, 48
). Increasing density
of the medium impaired their gravitaxis and orientation was completely
disturbed under isodensity conditions in Paramecium and
Euglena (1.04 g/cm3). The results indicate the
participation of the membrane in graviperception (35)
.
Exposing Loxodes to an increased density of the medium, no
change in gravitaxis can be observed, thus proving the existence of an
internal gravisensor (45)
. The development of a
stato-organelle is essential for Loxodes because it
preferentially lives in the sediment of lakes, where the density of the
medium often exceeds the density of the cell.
View larger version (72K):
[in this window]
[in a new window]
|
Figure 3. Models for gravisensing: (a, b) in the case of an
internal gravisensor (R) gravitaxis (shown here for negative
gravitaxis) persists in density-adjusted media; (c,
d) in the case that perception occurs on the level of the
cell membrane or in the case of a passive orientation mechanism,
gravitactic orientation disappears.
|
|
|
MODELS FOR GRAVISENSING
|
|---|
Loxodes received attention because it bears
statocyst-like organelles (Müller vesicles), three to six per
cell (Fig. 4
), already proposed by Penard (49)
to function as
mechanoreceptors due to their morphology. These organelles are
specialized vacuoles (7–10 µm in diameter) containing a heavy body
of BaSO4 (3–3.5 µm in diameter, density 4.5
g/cm3), the Müller body, fixed to a modified ciliary
stalk (50
, 51
). Concerning the mechanism, it
is proposed, in analogy to the graviperception of metazoa, that gravity
is perceived by bending of a ciliary complex, which changes the
membrane potential, which in turn determines the activity of the cilia
and thus the swimming activity of the cell (51
,
52
). Cultivation for up to 12 days in space did not affect
the general morphology of the Müller vesicles, although there
were first indications for less mineralization in Loxodes
cells under microgravity without impact on the graviresponse, which was
tested after the mission on the ground (44)
. Destruction
of the Müller vesicles by means of laser beams leads to a loss of
orientation capacity of Loxodes (45)
, clearly
demonstrating their role as organelles of gravisensing and thus analog
function to the gravisensor in vertebrates. Probably this type of
organelle is not widespread in protozoa and general cell structures are
discussed as gravisensors in other systems.
View larger version (175K):
[in this window]
[in a new window]
|
Figure 4. Scanning electron micrograph of a replica of a ruptured Loxodes
striatus. Arrows indicate the barium sulfate granula of three
Müller vesicles. Scale bar: 1 µm.
|
|
In the cases of Paramecium and Euglena it is
postulated that the hydrostatic pressure difference between cytoplasm
and medium induces opening of specific, unevenly distributed ion
channels in the cell membrane, which in turn (in consequence of the
changed membrane potential) regulate the direction and the frequency of
the ciliary (flagellar) beat. The postulated organization fits very
well in the characteristic, bipolar distribution of mechanosensitive
ion channels in Paramecium as revealed by
electrophysiological studies: mechanosensitive K+ channels
are located posterior and mechanosensitive Ca2+ channels
anterior (53
, 54
) (Fig. 5
). Stimulation of these channels leads to a
hyperpolarization-induced increased forward swimming velocity during
upward swimming, and to a depolarization-induced decreased swimming
velocity during downward swimming, which is exactly observed during
gravikinesis. No gravikinesis is observed in horizontally swimming
cells as de- and hyperpolarizing responses neutralize
(15)
. Whether gravitaxis is regulated by the same
mechanism is still unclear. Future studies have to show whether the
mechanosensitive ion channels in the plasma membrane are identical with
gravireceptor channels (55)
. So far, no gravireceptor
potential has been recorded.
Channel blockers specifically inhibiting mechanosensitive ion channels
need to be identified. Low concentrations of gadolinium (100 µM),
known to affect stretch-sensitive ion channels, inhibited negative
gravitaxis in Euglena (47
, 48
) but
had no effect on Paramecium (R. Hemmersbach, unpublished
observation). Manipulation of the membrane potential by the lipophilic
cation triphenylmethylphosphonium (TPMP+) resulted in a
loss of gravitaxis of Euglena, whereas phototaxis was not
affected, thus indicating the involvement of the membrane in the
gravity signal transduction chain (47
, 48
).
|
ENERGETIC CONSIDERATIONS
|
|---|
Regarding the high density of 4.5 g/cm3 in the
statoliths of the Müller body of Loxodes and assuming
that the vacuolar fluid has a density similar to water, the organelle
should be able to signal the cell its spatial orientation within
0.2 s (51)
. Using heavy minerals is a general concept
in gravisensors, such as barium sulfate in the statoliths of the
Chara rhizoid (56)
, strontium sulfate in the
Müller bodies of Remanella (seawater representative of
the family Loxodidae) (57)
, or calcium carbonate within
the vestibular system (58)
.
But what about other cell systems, which do not have such a specialized
gravireceptor? Is the pressure of the cytoplasm on the lower membrane
sufficient to open mechanosensitive ion channels? Regarding the cell
size of 200 µm of a Paramecium cell and its cell density
4% higher than the density of fresh water, a pressure of 0.1 Pa was
calculated to act on the lower plasma membrane (34)
. One
nanometer of membrane deformation corresponds to 10-19 J,
which is 50 times above the thermal noise and thus suitable as a
potential stimulus. However, in the case of smaller gravitactic cells
such as Euglena (30 µm) and Tetrahymena (75
µm) the work for channel gating comes close to thermal noise level
(10-21 J). The threshold experiments also revealed that
even 10% of gravity leads to a graviresponse. As a consequence, a
system, such as the Ca2+-sensitive filament system in the
cortex of a Paramecium, has to be postulated for focusing
the weak gravitational forces to transduction channels and
amplification of the signal (55)
.
|
SIGNAL TRANSDUCTION
|
|---|
A few studies showed changes in cyclic nucleotide levels in human
cell lines (59
, 60
). It was demonstrated that
alteration of the gravitational stimulation (microgravity to
hypergravity) has an important impact on intracellular cAMP production.
It would be interesting to know whether this effect is also found in a
cell system with obvious graviresponses, such as Paramecium,
also keeping in mind that a direct regulation of ion channels by cyclic
nucleotides might influence the mechanical properties of the cell
membrane (61)
. Second messengers might be involved in the
modulation of the ciliary beat in the gravity field. As a consequence,
second messenger levels might decrease the more cells are aligned in
the gravity field, which is in agreement with our first biochemical
data gathered under hypergravity conditions (62)
.
|
PERSPECTIVES
|
|---|
Protists represent suitable model systems to study the influence
of gravity on the cellular level. Considerable amounts of data have
been obtained revealing the evolution of two principles in
gravisensing. In addition to behavioral responses protists offer the
advantage to investigate further cellular events under changed
gravitational stimulation such as cell proliferation, mineralization,
aging, as well as interaction between organisms in ecosystems.
Short-term experiments in microgravity did not show any adaptation
phenomena within these gravisensitive systems. Experiments in prolonged
microgravity on the space station will offer the unique chance to
perform multi-generation experiments in a gravity-free environment. If
these experiments are supported by ground-based studies, our knowledge
on the impact of gravity on evolution, development, and signal
transduction pathways will be increased. Future experiments will
clarify whether only free-living cells can directly perceive gravity or
even every cell within our body. Further experiments and suitable test
parameters will show whether results in microgravity can be
extrapolated from hypergravity experiments. This cannot be predicted
per se because removal of a stimulus might represent a new,
unpredictable stimulus situation.
|
ACKNOWLEDGMENTS
|
|---|
The microgravity experiments were financially supported by
Deutsches Zentrum für Luft- und Raumfahrt (DARA, Grant no.
50WB9406-ZA).
|
REFERENCES
|
|---|
-
Machemer, H., Bräucker, R. (1992) Graviperception and graviresponses in ciliates. Acta Protozool 31,185-214[Medline]
-
Hemmersbach, R., Volkmann, D., Häder, D.-P. (1999) Graviorientation in protists and plants. J. Plant Physiol. 154,1-15[Medline]
-
Bean, B. (1984) Microbial geotaxis. Colombetti, G. Lenci, F. eds. Membranes and Sensory Transduction ,163-198 Plenum Press New York.
-
Häder, D.-P., Hemmersbach, R. (1997) Graviperception and graviorientation in flagellates. Planta 203,S7-S10[Medline]
-
Häder, D.-P., Vogel, K. (1991) Simultaneous tracking of flagellates in real time by image analysis. J. Math. Biol. 30,63-72
-
Machemer, H., Bräucker, R. (1996) Gravitaxis screened for physical mechanisms using g-modulated orientational cellular behaviour. Micrograv. Sci. Tech. 5,221-231
-
Muller, H. J. (1959) Approximation to a gravity-free situation for the human organism achievable at moderate expense. Science 128,772
-
Briegleb, W. (1988) Ground-borne methods and results in gravitational cell biology. Physiologist 31,44-47
-
Briegleb, W. (1992) Some qualitative and quantitative aspects of the fast-rotating clinostat as a research tool. ASGSB Bull 5,23-30[Medline]
-
Hemmersbach-Krause, R., Briegleb, W., Häder, D.-P., Vogel, K., Grothe, D., Meyer, I. (1993) Orientation of Paramecium under the conditions of weightlessness. J. Euk. Microbiol. 40,439-446[Medline]
-
Klaus, D. M., Todd, P., Schatz, A. (1998) Functional weightlessness during clinorotation of cell suspensions. Adv. Space Res. 21,1315-1318[Medline]
-
Cogoli, M. (1992) The fast-rotating clinostat: a history of its use in gravitational biology and a comparison of ground-based and flight experiment results. ASGSB Bull 5,59-68[Medline]
-
Hemmersbach, R., Voormanns, R., Häder, D.-P. (1996) Graviresponses in Paramecium biaurelia under different accelerations—studies on the ground and in space. J. Exp. Biol. 199,2199-2205[Abstract/Free Full Text]
-
Jennings, H. S. (1906) Behavior of the Lower Organisms Indiana University Press Bloomington.
-
Bräucker, R., Machemer-Röhnisch, S., Machemer, H. (1994) Graviresponses in Paramecium caudatum and Didinium nasutum examined under hypergravity conditions. J. Exp. Biol. 197,271-294[Abstract]
-
Winet, H., Jahn, T. L. (1974) Gravitaxis in protozoa. I. A propulsion-gravity model for Tetrahymena ciliata. J. Theor. Biol. 46,449-465[Medline]
-
Aderhold, R. (1888) Beiträge zur Kenntnis richtender Kräfte bei der Bewegung niederer Organismen. Jenaische Zeitschr. Med. Naturwiss. 22,311-342
-
Creutz, C., Diehn, B. (1976) Motor responses to polarized light and gravity sensing in Euglena gracilis. J. Protozool. 23,552-556
-
Häder, D.-P. (1987) Polarotaxis, gravitaxis and vertical phototaxis in the green flagellate, Euglena gracilis. Arch. Microbiol. 147,179-183[Medline]
-
Rhiel, E., Häder, D.-P., Wehrmeyer, W. (1988) Diaphototaxis and gravitaxis in a freshwater Cryptomonas. Plant Cell Physiol 29,755-760[Abstract/Free Full Text]
-
Bean, B. (1977) Geotactic behavior of Chlamydomonas. J. Protozool. 24,394-401[Medline]
-
Kessler, J. O. (1986) The external dynamics of swimming microorganisms. Round, F. E. Chapman, D. J. eds. Progress in Phycological Research ,258-307 Biopress Oxford.
-
Fenchel, T., Finlay, B. J. (1984) Geotaxis in the ciliated protozoon Loxodes. J. Exp. Biol. 110,17-33[Abstract/Free Full Text]
-
Machemer-Röhnisch, S., Bräucker, R., Machemer, H. (1993) Neutral gravitaxis of gliding Loxodes exposed to normal and raised gravity. J. Comp. Physiol. A 171,779-790
-
Hemmersbach-Krause, R., Briegleb, W. (1992) Gravitational effects on Paramecium and Loxodes. Physiologist 35,23-26
-
Hemmersbach-Krause, R., Briegleb, W., Häder, D.-P. (1991) Dependence of gravitaxis in Paramecium on oxygen. Eur. J. Protistol. 27,278-282
-
Machemer, H., Machemer-Röhnisch, S., Bräucker, R. (1993) Velocity and graviresponses in Paramecium during adaptation and varied oxygen concentrations. Arch. Protistenk. 143,285-296
-
Stallwitz, E., Häder, D.-P. (1994) Effects of heavy metals on motility and gravitactic orientation of the flagellate, Euglena gracilis. Eur. J. Protistol. 30,18-24[Medline]
-
Häder, D.-P., Lebert, M., DiLena, M. R. (1987) Effects of culture age and drugs on phototaxis in the green flagellate, Euglena gracilis. Plant Physiol. Life Sci. Adv. 6,169-174
-
Freiberger, N., and Hemmersbach, R. (1998)
Influence of low temperature on the graviresponses of protists.
J. Eukaryot. Microbiol. (Abstract). In press
-
Moore, A. (1903) Some facts concerning geotropic gatherings of paramecia. Am. J. Physiol. 9,238-244
-
Fox, H. M. (1925) The effect of light on the vertical movement of aquatic organisms. Proc. Camb. Phil. Soc. Biol. Sci. 1,219-224
-
Kuznicki, L. (1968) Behavior of Paramecium in the gravity field. I. Sinking of immobilized specimens. Acta Protozool 6,109-117
-
Machemer, H., Machemer-Röhnisch, S., Bräucker, R., Takahashi, K. (1991) Gravikinesis in Paramecium: theory and isolation of a physiological response to the natural gravity vector. J. Comp. Physiol. A 168,1-12
-
Ooya, M., Mogami, Y., Izumi-Kurotani, A., Baba, S. A. (1992) Gravity-induced changes in propulsion of Paramecium caudatum: A possible role of graviperception in protozoan behaviour. J. Exp. Biol. 163,153-167[Abstract/Free Full Text]
-
Hemmersbach-Krause, R., Briegleb, W., Vogel, K., Häder, D.-P. (1993) Swimming velocity of Paramecium under the conditions of weightlessness. Acta Protozool 32,229-236[Medline]
-
Machemer, H., Bräucker, R., Murakami, A., Yoshimura, K. (1993) Graviperception in unicellular organisms: a comparative behavioural study under short-term microgravity. Micrograv. Sci. Technol. 5,221-231
-
Bräucker, R., Machemer-Röhnisch, S., Machemer, H., Murakami, A. (1992) Gravity-controlled gliding velocity in Loxodes. Eur. J. Protistol. 28,238-245
-
Vogel, K., Hemmersbach-Krause, R., Kühnel, C., Häder, D. P. (1993) Swimming behavior of the unicellular flagellate, Euglena gracilis, in simulated and real microgravity. Micrograv. Sci. Technol. 4,232-237
-
Lebert, M, . D.-P. Häder (1997) Effects of hypergravity on the photosynthetic flagellate, Euglena gracilis. J. Plant Physiol. 150,153-159[Medline]
-
Häder, D.-P., Rosum, A., Schäfer, J., Hemmersbach, R. (1996) Graviperception in the flagellate Euglena gracilis during a shuttle space flight. J. Biotech. 47,261-269[Medline]
-
Bräucker, R., Murakami, A., Ikegaya, K., Takahashi, K., Machemer-Röhnisch, S., Machemer, H. (1998) Relaxation and activation of graviresponses in Paramecium. J. Exp. Biol. 201,2103-2113[Abstract]
-
Hemmersbach, R., Voormanns, R., Briegleb, W., Rieder, N., Häder, D.-P. (1996) Influence of accelerations on the spatial orientation of Loxodes and Paramecium. J. Biotech. 47,271-278[Medline]
-
Hemmersbach, R., Tairbekov, M., Gawrilowa, O., Rieder, N., Send, W., Bromeis, B., Wilczek, M., Mulisch, M. (1998) Morphology and physiology of Loxodes after cultivation in space. ESA SP (Special Publication 222)
-
Hemmersbach, R., Voormanns, R., Bromeis, B., Schmidt, N., Rabien, H., Ivanova, K. (1998) Comparative studies of the graviresponses of Paramecium and Loxodes. Adv. Space Res. 21,1285-1289[Medline]
-
Häder, D.-P, Porst, M., Tahedl, H., Richter, P., Lebert, M. (1997) Gravitactic orientation in the flagellate Euglena gracilis. Micrograv. Sci. Technol. 10,53-57
-
Lebert, M., Häder, D.-P. (1996) How Euglena tells up from down. Nature 379,590[Medline]
-
Lebert, M., Richter, P., Häder, D.-P. (1997) Signal perception and transduction of gravitaxis in the flagellate Euglena gracilis. J. Plant Physiol. 150,685-690
-
Penard, E. (1917) Le genre Loxodes. Rev. Suisse de Zool. 25,453-489
-
Rieder, N. (1977) Die Müllerschen
Körperchen von Loxodes magnus (Ciliata, Holotricha):
Ihr Bau und ihre mögliche Funktion als Schwererezeptor.
Verh. Dt. Zool. Ges., 254
-
Fenchel, T., Finlay, B. J. (1986) The structure and function of Müller vesicles in loxodid ciliates. J. Protozool. 33,69-76
-
Neugebauer, D.-C., Machemer, H. (1997) Is there an orientation-dependent excursion of the Müller body in the "statocystoid" of Loxodes?. Cell Tissue Res. 287,277-582
-
Machemer, H., Deitmer, J. W. (1985) Mechanoreception in ciliates. Autrum, H. Ottoson, D. Perl, E. R. Schmidt, R. F. Schimazu, H. Willis, H. D. eds. Progress in Sensory Physiology ,81-118 Springer-Verlag Berlin.
-
Naitoh, Y. (1984) Mechanosensory tranduction in protozoa. Colombetti, G. Lenci, F. eds. Membranes and Sensory Transduction ,113-134 Plenum Press New York.
-
Machemer-Röhnisch, S., Machemer, H., Bräucker, R. (1996) Electric-field effects on gravikinesis in Paramecium. J. Comp. Physiol. A 179,213-226
-
Sievers, A., Volkmann, D. (1979) Gravitropism in single cells. Encyclopedia of Plant Physiology, N S Vol. 7, Physiology of Movements (Haupt, W., and Feinleib, M. E., eds) pp. 567–572, Springer-Verlag, Berlin.
-
Bedini, C., Lanfranchi, A., Nobili, R. (1973) The ultrastructure of the Müller body in Remanella. J. Protozool. 24,394-401
-
Neubert, J., Schatz, A., Bromeis, B., Linke-Hommes, A. (1998) Effects of gravity on the early development. Adv. Space Res. 22,265-271[Medline]
-
Meli, A., Perella, G., Curcio, F., Hemmersbach, R.,
Neubert, J., and Ambesi Impiombato, F. S. (1998) Response of
thyrotropin of normal thyroid follicular cell strain FRTL5 in
hypergravity. Biochimie, in press
-
Kumei, Y., Whitson, P. A., Sato, A., Cintron, N. M. (1991) Hypergravity signal transduction in HeLa cells with concomitant phosphorylation of proteins immunoprecipitated with anti-microtubule-associated protein antibodies. Exp. Cell Res. 192,492-496[Medline]
-
Schultz, J. E., Guo, Y. L., Kleefeld, G., Völk, H. (1997) Hyperpolarization- and depolarization-activated Ca2+-currents in Paramecium trigger behavioral changes and cGMP formation independently. J. Membr. Biol. 156,251-259[Medline]
-
Hemmersbach, R., Voormanns, R., Rabien, R.,
Bromeis, B., and Ivanova, K. (1996) Graviperception and signal
transduction in unicellular organisms. ESA SP-390 (Special
Publication), 193–197
This article has been cited by other articles:
|
|
|
|
 
J. S. Tash, S. Kim, M. Schuber, D. Seibt, and W. H. Kinsey
Fertilization of Sea Urchin Eggs and Sperm Motility Are Negatively Impacted under Low Hypergravitational Forces Significant to Space Flight
Biol Reprod,
October 1, 2001;
65(4):
1224 - 1231.
[Abstract]
[Full Text]
[PDF]
|
|
|
TOP
ABSTRACT
INTRODUCTION
