Abstract
BackgroundThe mollusk statocyst is a mechanosensing organ detecting the animal's orientation with respect to gravity. This system has clear similarities to its vertebrate counterparts: a weight-lending mass, an epithelial layer containing small supporting cells and the large sensory hair cells, and an output eliciting compensatory body reflexes to perturbations.Methodology/Principal FindingsIn terrestrial gastropod snail we studied the impact of 16- (Foton M-2) and 12-day (Foton M-3) exposure to microgravity in unmanned orbital missions on: (i) the whole animal behavior (Helix lucorum L.), (ii) the statoreceptor responses to tilt in an isolated neural preparation (Helix lucorum L.), and (iii) the differential expression of the Helix pedal peptide (HPep) and the tetrapeptide FMRFamide genes in neural structures (Helix aspersa L.). Experiments were performed 13–42 hours after return to Earth. Latency of body re-orientation to sudden 90° head-down pitch was significantly reduced in postflight snails indicating an enhanced negative gravitaxis response. Statoreceptor responses to tilt in postflight snails were independent of motion direction, in contrast to a directional preference observed in control animals. Positive relation between tilt velocity and firing rate was observed in both control and postflight snails, but the response magnitude was significantly larger in postflight snails indicating an enhanced sensitivity to acceleration. A significant increase in mRNA expression of the gene encoding HPep, a peptide linked to ciliary beating, in statoreceptors was observed in postflight snails; no differential expression of the gene encoding FMRFamide, a possible neurotransmission modulator, was observed.Conclusions/SignificanceUpregulation of statocyst function in snails following microgravity exposure parallels that observed in vertebrates suggesting fundamental principles underlie gravi-sensing and the organism's ability to adapt to gravity changes. This simple animal model offers the possibility to describe general subcellular mechanisms of nervous system's response to conditions on Earth and in space.
Highlights
Of all the environmental parameters under which a living organism has been exposed in the course of its evolution only gravity has remained constant
Less is available in the fossil record on invertebrate sensory structures, recent gene expression studies suggest that gravisensing statocyst system in eumetazoans is in the same way elemental and highly conserved [2]
In gastropods the statocyst is the predominant gravisensing organ, and it has clear similarities to its vertebrate counterparts: a weightlending mass comprised of calcium carbonate particles called statoconia, and an epithelial layer containing small supporting cells carrying microvilli and giant sensory hair cells carrying, in some species such as land snails, true (9+2)-type kinocilia
Summary
Of all the environmental parameters under which a living organism has been exposed in the course of its evolution only gravity has remained constant. Most if not all invertebrate species can orient their bodies’ axis with respect to gravity, but only in a few crustaceans, insects and mollusks has gravireception been more thoroughly studied. In insects it is remarkably robust, but complex in design. The mollusk statocyst is a mechanosensing organ detecting the animal’s orientation with respect to gravity This system has clear similarities to its vertebrate counterparts: a weight-lending mass, an epithelial layer containing small supporting cells and the large sensory hair cells, and an output eliciting compensatory body reflexes to perturbations
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