Photosensitive Signal Transduction Induces Membrane Hyperpolarization in Paramecium bursaria

Abstract

The protozoan ciliate Paramecium bursaria exhibits membrane hyperpolarization in response to photostimulation, accompanied with an increased swimming speed. The external addition of cyclic nucleotide phosphodiesterase (PDE) inhibitors, either theophylline (1,3-dimethylxanthine) or 3-isobutyl-1-methylxanthin (IBMX), increased in both amplitudes of the membrane hyperpolarization and the increase in swimming speed. Moreover, the addition of membrane permeable cyclic nucleotide analogs, either 8-bromo-adenosine 3',5'-cyclic monophosphate (Br-cAMP) or 8-Br-guanosine 3',5'-cyclic monophosphate (Br-cGMP), increased these amplitudes. On the other hand, the addition of l-cis-diltiazem, known to block the conductance of cyclic nucleotide-gated channels, partially decreased both amplitudes of the membrane hyperpolarization and the increase in swimming speed. An enzyme immunoassay of cellular cyclic nucleotide contents showed that photostimulation induced a rapid increase in adenosine 3',5'-cyclic monophosphate (cAMP), but little increase in guanosine 3',5'-cyclic monophosphate (cGMP), raising the possibility that a rapid increase in cAMP mediates the light-induced hyperpolarization in P. bursaria.

Microtubule Disruption Without Learning Impairment in the Unicellular Organism, Paramecium: Implications for Information Processing in Microtubules

“…Interestingly, this membrane hyperpolarization increases the ciliary beat frequency ( Machemer, 1974 ). This effect is mediated through cyclic Adenosine Monophosphate (cAMP) molecules as measured by enzyme immunoassay of cellular cAMP contents ( Mitarai & Nakaoka, 2005 ). Although retinal has been extracted from P. bursaria as a possible chromophore molecule ( Tokioka, Matsuoka, Nakaoka, & Kito, 1991 ), the exact identity of the photosensor molecule in P. caudatum is still unknown.…”

“…This photosensitivity is independent from the symbiotic alga that exists in Paramecium bursaria as both chlorella-containing and chlorella free forms of the Paramecium bursaria show photosensitivity (Matsuoka & Nakaoka, 1988). On the other hand, its swimming speed increases upon normal light exposure due to the hyperpolarization of the membrane potential (Mitarai & Nakaoka, 2005). Interestingly, this membrane hyperpolarization causes an increased ciliary beat frequency (Machemer, 1974).…”

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“…For instance, Bursaria truncatella , shaped like a scoop, achieves top speeds of 1775 µm/s (or 11.8 body lengths/second) multiple times within an 18-minute track, covering a distance of 45 centimeters (Fig 3a). The mutualistic endosymbiotic relationship between Bursaria truncatella and green algae (Chlorella) triggers faster movements under light [18], a condition enhanced by Trackoscope ’s light microscopy setup, allowing Bursaria truncatella to reach peak speeds. Manually tracking such swift organisms without Trackoscope would be nearly impossible for extended periods.…”

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“…Swimming speed of this ciliate decreases upon exposure to strong bright light and its membrane depolarizes in this process [31]. On the other hand, its swimming speed increases upon normal light exposure due to hyperpolarization of its membrane potential [32]. Interestingly, it is known that this membrane hyperpolarization causes an increased ciliary beat frequency [33] mediated through cyclic adenosine monophosphate (cAMP) molecules [32].…”

“…On the other hand, its swimming speed increases upon normal light exposure due to hyperpolarization of its membrane potential [32]. Interestingly, it is known that this membrane hyperpolarization causes an increased ciliary beat frequency [33] mediated through cyclic adenosine monophosphate (cAMP) molecules [32]. While retinal was extracted from Paramecium bursaria as a possible chromophore molecule [34], the exact identity of photosensor molecule in P. caudatum is still unknown.…”