The function of the ocelloid and piston in the dinoflagellate Erythropsidinium (Gymnodiniales, Dinophyceae)

Abstract

The marine dinoflagellate Erythropsidinium possesses an ocelloid, the most elaborate photoreceptor organelle known in a unicellular organism, and a piston, a fast contractile appendage unknown in any other organism. The ocelloid is able to rotate, often before the cell swims. The ocelloid contains lenses that function to concentrate light. The flagellar propulsion is atrophied, and the piston is responsible for locomotion through successive extensions and contractions. During the "locomotion mode", the contraction is ~4 times faster than the extension. The piston attained up to 50 mm · s and the cell jumps backwards at -4 mm · s , while during the piston extension the cell moves forwards. The net speed of ~-1 mm · s is faster than other dinoflagellates. The piston usually moved in the "static mode" without significant cell swimming. This study suggests that the piston is also a tactile organelle that scans the surrounding waters for prey. Erythropsidinium feeds on copepod eggs by engulfing. The end of the piston possesses a "suction cup" able to attach the prey and place it into the posterior cavity for engulfing. The cylindrical shape of Erythropsidinium, and the anterior position of the ocelloid and nucleus, are morphological adaptations that leave space for the large vacuole. Observations are provided on morphological development during cell division. Most of the described species of Erythropsidinium apparently correspond to distinct life stages of known species, and the genus Greuetodinium (=Leucopsis) corresponds to an earlier division stage.

Origins of eukaryotic excitability

“…In the warnowiid dinoflagellate Erythropsidinium, the design and sophistication of its eye suggests that they can do more than sense light gradients (as in most other protist photoreceptors) [76]. Ocelloid eyes are even capable of an active rolling or pivoting motion [77]. It is suggested that it can detect circularly-polarised light -a tell-tale sign of a prey dinoflagellates (polarotaxis).…”

Bioluminescence and Photoreception in Unicellular Organisms: Light-Signalling in a Bio-Communication Perspective

“…Indeed, dinoflagellates exhibit a rich real-time behavioural and morphological repertoire to adapt to their diverse and fluctuating environmental conditions [ 397 , 398 ]. For example, in addition to the high-resolution vision systems described above [ 96 , 376 ], some dinoflagellate species have developed complex organs such as a piston for efficient propulsion [ 198 ] or nematocysts for hunting [ 399 ] that require complex “sensorimotor” and coordination molecular processes. In bioluminescent dinoflagellates, excitable light emission is stimulated by mechanical forces that trigger an “action potential” and a subsequent signalling cascade leading to the activation of luciferase in the scintillon [ 34 , 72 , 328 , 331 , 332 , 400 ].…”

“…Conversely, as found in many bioluminescent organisms, the pigment of photoreceptors may be not synthetised by the organism but is acquired from the external environment [ 195 ]. To date, the ultimate stage of unicellular high-resolution vision is achieved by eye-spots or ocelloids organelles observed in some dinoflagellate or Chlamydomonas species [ 96 , 155 , 196 , 197 , 198 , 199 , 200 ].…”

“…Light also modulates the phototaxis and circadian rhythms of multiple eukaryotic algae [ 83 , 161 , 227 , 228 ] but also induces various behavioural responses from other, non-photosynthetic protists such as dinoflagellates [ 198 , 229 , 230 , 231 , 232 , 233 , 234 , 235 , 236 ], ciliates [ 237 , 238 , 239 ]; affects biofilm formation by Chlorella vulgaris [ 240 ]; controls the morphogenesis in green plants and stramenopiles [ 241 , 242 ] and the sexual cycle in Chlamydomonas [ 243 ]; and influences the phototactic swimming in sponge larvae [ 244 ]. Interestingly, light also mediates cross-kingdom communication: it has recently been demonstrated that the green fluorescence of the cnidarian host attracts symbiotic algae [ 245 ] ( Table 1 ) .…”