Molecular and functional bases of coordination in early branching metazoans – insights from physiology and investigations of potassium channels in the Porifera

Abstract

Sponges are filter feeders that lack nerves and muscle but are nonetheless able to respond to changes in the ambient environment to control their feeding current. Cellular sponges undergo coordinated contractions that effectively expel debris. Syncytial sponges propagate action potentials through their tissue, causing immediate flagellar arrest. Understanding the basis of this coordination in sponges is of interest for the insight it provides on mechanisms of coordination in early branching animals. However, when I began this thesis no ion channels had been described from the Porifera. I adopted a multifaceted approach to studying the conduction system of sponges. This included cloning and characterizing potassium channels as a means to understanding the underlying ionic currents, and monitoring regulation of the sponge feeding current in response to environmental stimuli. The latter experiments provided a functional context. The glass sponges Rhabdocalyptus dawsoni and Aphrocallistes vastus arrest feeding in response to mechanical disturbance and to sediment in the incurrent water – suggesting a protective role. Monitoring patterns of feeding current arrests also revealed several features of the glass sponge conduction system: pacemaker activity, mechanosensitivity, distinct excitability thresholds, and tolerance to repeated stimuli. With access to the genome of the demosponge Amphimedon queenslandica I have also cloned and characterized the first sponge ion channels. Inward rectifier potassium (Kir) channels were prioritized for their role in regulating excitability. Kir channels cloned from A. queenslandica shared critical residues and a strong rectifying phenotype with Kir channels typically expressed in excitable cells. A variety of potassium channels from A. queenslandica indicate great diversity and a foundation for coordination at the dawn of the Metazoa