Functional consequences of the asymmetric architecture of the ctenophore statocyst.

Ctenophores, or comb jellies, are geotactic with a statocyst that controls the activity of the eight ciliary comb rows. If a ctenophore is tilted or displaced from a position of vertical balance, it rights itself by asymmetric frequencies of beating on the uppermost and lowermost comb rows, turning to swim up or down depending on its mood. I recently discovered that the statocyst of ctenophores has an asymmetric architecture related to the sagittal and tentacular planes along the oral-aboral axis. The four groups of pacemaker balancer cilia are arranged in a rectangle along the tentacular plane, and support a superellipsoidal statolith elongated in the tentacular plane. By controlled tilting of immobilized ctenophores in either body plane with video recording of activated comb rows, I found that higher beat frequencies occurred in the sagittal than in the tentacular plane at orthogonal orientations. Similar tilting experiments on isolated statocyst slices showed that statolith displacement due to gravity and the resulting deflection of the mechanoresponsive balancers are greater in the sagittal plane. Finally, tilting experiments on a mechanical model gave results similar to those of real statocysts, indicating that the geometric asymmetries of statolith design are sufficient to account for my findings. The asymmetric architecture of the ctenophore statocyst thus has functional consequences, but a possible adaptive value is not known.

Formation of the statolith in the ctenophore Mnemiopsis leidyi.

The aboral sensory organ (apical organ) of ctenophores contains a statocyst with a single large statolith. The statolith comprises living cells (lithocytes), each containing a large membrane-bound concretion. The statolith is supported on the distal ends of four compound motile mechanoresponsive cilia (balancers) which control the beat frequencies of the eight locomotory comb rows, and thereby the orientation of animals to gravity. In Mnemiopsis leidyi and Pleurobrachia pileus, lithocytes arise in the thickened epithelial floor of the apical organ on opposite sides along the tentacular plane. Lithocytes progressively differentiate and migrate toward the apical surface where they bud off next to the bases of the balancers. New lithocytes are transported up the balancers by ciliary surface motility to form the statolith (Noda, 2013). The statolith has a superellipsoidal shape due to the rectangular arrangement of the four balancers and the addition of new lithocytes to its ends via the balancers. The size of the statolith increases with animal size, starting at the highest rate of growth in younger stages and gradually decreasing in larger animals. The total number of developing lithocytes in the epithelial floor increases rapidly in smaller animals and reaches a plateau range in larger animals. Lithocytes are therefore produced continually throughout life for enlargement of the statolith and possibly for turnover and replacement of existing lithocytes. The dome cilia enclosing the statocyst were observed to propagate slow, low-ampitude waves distally. The dome cilia may act as an undulating screen to prevent foreign objects in the seawater from being transported non-specifically up the balancers to make a defective statolith.

Patterns of comb row development in young and adult stages of the ctenophores Mnemiopsis leidyi and Pleurobrachia pileus.

The development of comb rows in larval and adult Mnemiopsis leidyi and adult Pleurobrachia pileus is compared to regeneration of comb plates in these ctenophores. Late gastrula embryos and recently hatched cydippid larvae of Mnemiopsis have five comb plates in subsagittal rows and six comb plates in subtentacular rows. Subsagittal rows develop a new (sixth) comb plate and both types of rows add plates at similar rates until larvae reach the transition to the lobate form at ∼5 mm size. New plate formation then accelerates in subsagittal rows that later extend on the growing oral lobes to become twice the length of subtentacular rows. Interplate ciliated grooves (ICGs) develop in an aboral-oral direction along comb rows, but ICG formation itself proceeds from oral to aboral between plates. New comb plates in Mnemiopsis larvae are added at both aboral and oral ends of rows. At aboral ends, new plates arise as during regeneration: local widening of a ciliated groove followed by formation of a short split plate that grows longer and wider and joins into a common plate. At oral ends, new plates arise as a single tuft of cilia before an ICG appears. Adult Mnemiopsis continue to make new plates at both ends of rows. The frequency of new aboral plate formation varies in the eight rows of an animal and seems unrelated to body size. In Pleurobrachia that lack ICGs, new comb plates at aboral ends arise between the first and second plates as a single small nonsplit plate, located either on the row midline or off-axis toward the subtentacular plane. As the new (now second) plate grows larger, its distance from the first and third plates increases. Size of the new second plate varies within the eight rows of the same animal, indicating asynchronous formation of plates as in Mnemiopsis. New oral plates arise as in Mnemiopsis. The different modes of comb plate formation in Mnemiopsis versus Pleurobrachia are accounted for by differences in mesogleal firmness and mechanisms of ciliary coordination. In both cases, the body of a growing ctenophore is supplied with additional comb plates centripetally from opposite ends of the comb rows.

Regeneration of ciliary comb plates in the ctenophore Mnemiopsis leidyi. i. morphology.

Regeneration of missing body parts in model organisms provides information on the mechanisms underlying the regeneration process. The aim here is to use ctenophores to investigate regeneration of their giant ciliary swimming plates. When part of a row of comb plates on Mnemiopsis is excised, the wound closes and heals, greatly increasing the distance between comb plates near the former cut edges. Video differential interference contrast (DIC) microscopy of the regeneration of new comb plates between widely separated plates shows localized widenings of the interplate ciliated groove (ICG) first, followed by growth of two opposing groups of comb plate cilia on either side. The split parts of a new plate elongate as their bases extend laterally away from the ICG widening and continue ciliogenesis at both ends. The split parts of a new plate grow longer and move closer together into the ICG widening until they merge into a single plate that interrupts the ICG in a normal manner. Video DIC snapshots of dissected gap preparations 1.5-3-day postoperation show that ICG widenings and/or new plates do not all appear at the same time or with uniform spacing within a gap: the lengths and distances between young plates in a gap are quite variable. Video stereo microscopy of intact animals 3-4 days after the operation show that all the new plates that will form in a gap are present, fairly evenly spaced and similar in length, but smaller and closer together than normal. Normal development of comb plates in embryos and growing animals is compared to the pattern of comb plate regeneration in adults. Comb plate regeneration differs in the cydippid Pleurobrachia that lacks ICGs and has a firmer mesoglea than Mnemiopsis. This study provides a morphological foundation for histological, cellular, and molecular analysis of ciliary regeneration in ctenophores.

Unsolved motility looking for answer.

A rod-like axostyle complex turns the anterior end of a termite flagellate, including the plasma membrane, continually in the same direction relative to the rest of the cell at speeds up to approximately 1 Hz. This motility provides direct visual evidence for the fluid nature of cell membranes. Torque is generated along the length of the axostyle complex by an unknown mechanism. Here I describe findings not published before and promising experiments that may help to solve this remarkable motility.

Novel bridge of axon-like processes of epithelial cells in the aboral sense organ of ctenophores.

We describe by light and electron microscopy a novel structure in the aboral sense organ (apical organ) of cydippid (Pleurobrachia) and lobate (Mnemiopsis) ctenophores. An elevated bundle of long, thin, microtubule-filled processes arises from the apical ends of two groups of epithelial cells located on opposite sides of the apical organ along the tentacular plane of the body. This bundle of axon-like processes arches over the epithelial floor like a bridge, with branches at both ends running toward opposing pairs of ciliary balancers that are motile pacemakers for the rows of locomotory ciliary comb plates. The bridge in Pleurobrachia is approximately 40 microm long and 3-4 microm wide and consists of approximately 60 closely packed processes, 0.2-0.8 microm thick, containing vesicles and numerous microtubules running parallel to their long axes. There are approximately 30 epithelial cells in each of the two groups giving rise to the bridge and each cell forms a single process, so roughly half of the processes in the bridge must originate from cells on one side and diverge into branches to a pair of balancers on the opposite side of the apical organ. The 150-200 cilia in each balancer arise from morphologically complex cellular projections with asymmetric lateral extensions directed towards a fork of the bridge. Presynaptic triad structures and vesicles are found in this region but clear examples of synaptic contacts between bridge processes and balancer cells have not yet been traced. Cydippid larvae of Mnemiopsis have a conspicuous bridge along the tentacular plane of the apical organ. Beroid ctenophores that lack tentacles at all stages do not have a bridge. We discuss the possibility that the bridge is an electrical conduction pathway to balancers that coordinates tentacle-evoked swimming responses of ctenophores, such as global ciliary excitation.