Optimal ciliary locomotion of axisymmetric microswimmers

Many biological microswimmers locomote by periodically beating the densely packed cilia on their cell surface in a wave-like fashion. While the swimming mechanisms of ciliated microswimmers have been extensively studied both from the analytical and the numerical point of view, optimisation of the ciliary motion of microswimmers has received limited attention, especially for non-spherical shapes. In this paper, using an envelope model for the microswimmer, we numerically optimise the ciliary motion of a ciliate with an arbitrary axisymmetric shape. Forward solutions are found using a fast boundary-integral method, and the efficiency sensitivities are derived using an adjoint-based method. Our results show that a prolate microswimmer with a $2\,{:}\,1$ aspect ratio shares similar optimal ciliary motion as the spherical microswimmer, yet the swimming efficiency can increase two-fold. More interestingly, the optimal ciliary motion of a concave microswimmer can be qualitatively different from that of the spherical microswimmer, and adding a constraint to the cilia length is found to improve, on average, the efficiency for such swimmers.

Interstitial Annelida

Members of the following marine annelid families are found almost exclusively in the interstitial environment and are highly adapted to move between sand grains, relying mostly on ciliary locomotion: Apharyngtidae n. fam., Dinophilidae, Diurodrilidae, Nerillidae, Lobatocerebridae, Parergodrilidae, Polygordiidae, Protodrilidae, Protodriloididae, Psammodrilidae and Saccocirridae. This article provides a review of the evolution, systematics, and diversity of these families, with the exception of Parergodrilidae, which was detailed in the review of Orbiniida by Meca, Zhadan, and Struck within this Special Issue. While several of the discussed families have previously only been known by a few described species, recent surveys inclusive of molecular approaches have increased the number of species, showing that all of the aforementioned families exhibit a high degree of cryptic diversity shadowed by a limited number of recognizable morphological traits. This is a challenge for studies of the evolution, taxonomy, and diversity of interstitial families as well as for their identification and incorporation into ecological surveys. By compiling a comprehensive and updated review on these interstitial families, we hope to promote new studies on their intriguing evolutionary histories, adapted life forms and high and hidden diversity.

Neuronal coordination of motile cilia in locomotion and feeding

Efficient ciliary locomotion and transport require the coordination of motile cilia. Short-range coordination of ciliary beats can occur by biophysical mechanisms. Long-range coordination across large or disjointed ciliated fields often requires nervous system control and innervation of ciliated cells by ciliomotor neurons. The neuronal control of cilia is best understood in invertebrate ciliated microswimmers, but similar mechanisms may operate in the vertebrate body. Here, we review how the study of aquatic invertebrates contributed to our understanding of the neuronal control of cilia. We summarize the anatomy of ciliomotor systems and the physiological mechanisms that can alter ciliary activity. We also discuss the most well-characterized ciliomotor system, that of the larval annelid Platynereis . Here, pacemaker neurons drive the rhythmic activation of cholinergic and serotonergic ciliomotor neurons to induce ciliary arrests and beating. The Platynereis ciliomotor neurons form a distinct part of the larval nervous system. Similar ciliomotor systems likely operate in other ciliated larvae, such as mollusc veligers. We discuss the possible ancestry and conservation of ciliomotor circuits and highlight how comparative experimental approaches could contribute to a better understanding of the evolution and function of ciliary systems. This article is part of the Theo Murphy meeting issue ‘Unity and diversity of cilia in locomotion and transport’.

Ciliomotor circuitry underlying whole-body coordination of ciliary activity in the Platynereis larva

Ciliated surfaces harbouring synchronously beating cilia can generate fluid flow or drive locomotion. In ciliary swimmers, ciliary beating, arrests, and changes in beat frequency are often coordinated across extended or discontinuous surfaces. To understand how such coordination is achieved, we studied the ciliated larvae of Platynereis dumerilii, a marine annelid. Platynereis larvae have segmental multiciliated cells that regularly display spontaneous coordinated ciliary arrests. We used whole-body connectomics, activity imaging, transgenesis, and neuron ablation to characterize the ciliomotor circuitry. We identified cholinergic, serotonergic, and catecholaminergic ciliomotor neurons. The synchronous rhythmic activation of cholinergic cells drives the coordinated arrests of all cilia. The serotonergic cells are active when cilia are beating. Serotonin inhibits the cholinergic rhythm, and increases ciliary beat frequency. Based on their connectivity and alternating activity, the catecholaminergic cells may generate the rhythm. The ciliomotor circuitry thus constitutes a stop-and-go pacemaker system for the whole-body coordination of ciliary locomotion.

Ciliomotor circuitry underlying whole-body coordination of ciliary activity in the Platynereis larva

Ciliated surfaces harbouring synchronously beating cilia can generate fluid flow or drive locomotion. In ciliary swimmers, ciliary beating, arrests, and changes in beat frequency are often coordinated across extended or discontinuous surfaces. To understand how such coordination is achieved, we studied the ciliated larvae of Platynereis dumerilii, a marine annelid. Platynereis larvae have segmental multiciliated cells that regularly display spontaneous coordinated ciliary arrests. We used whole-body connectomics, activity imaging, transgenesis, and neuron ablation to characterize the ciliomotor circuitry. We identified cholinergic, serotonergic, and catecholaminergic ciliomotor neurons. The synchronous rhythmic activation of cholinergic cells drives the coordinated arrests of all cilia. The serotonergic cells are active when cilia are beating. Serotonin inhibits the cholinergic rhythm, and increases ciliary beat frequency. Based on their connectivity and alternating activity, the catecholaminergic cells may generate the rhythm. The ciliomotor circuitry thus constitutes a stop-and-go pacemaker system for the whole-body coordination of ciliary locomotion.

Network interneurons underlying ciliary locomotion in Hermissenda

In the nudibranch mollusk Hermissenda, ciliary locomotion contributes to the generation of two tactic behaviors. Light elicits a positive phototaxis, and graviceptive stimulation evokes a negative gravitaxis. Two classes of light-responsive premotor interneurons in the network contributing to ciliary locomotion have been recently identified in the cerebropleural ganglia. Aggregates of type I interneurons receive monosynaptic excitatory (Ie) or inhibitory (Ii) input from identified photoreceptors. Type II interneurons receive polysynaptic excitatory (IIe) or inhibitory (IIi) input from photoreceptors. The ciliary network also includes type III inhibitory (IIIi) interneurons, which form monosynaptic inhibitory connections with ciliary efferent neurons (CENs). Illumination of the eyes evokes a complex inhibitory postsynaptic potential, a decrease of Ii spike activity, a complex excitatory postsynaptic potential, and an increase of Ie spike activity. Here, we characterized the contribution of identified I, II, and IIIi interneurons to the neural network supporting visually guided locomotion. In dark-adapted preparations, light elicited an increase in the tonic spike activity of IIe interneurons and a decrease in the tonic spike activity of IIi interneurons. Fluorescent dye-labeled type II interneurons exhibited diverse projections within the circumesophageal nervous system. However, a subclass of type II interneurons, IIe(cp) and IIi(cp) interneurons, were shown to terminate within the ipsilateral cerebropleural ganglia and indirectly modulate the activity of CENs. Type II interneurons form monosynaptic or polysynaptic connections with previously identified components of the ciliary network. The identification of a monosynaptic connection between Ie and IIIi interneurons shown here suggest that they provide a major role in the light-dependent modulation of CEN spike activity underlying ciliary locomotion.