Structure and signaling at hydroid polyp-stolon junctions, revisited

Abstract

ABSTRACT The gastrovascular system of colonial hydroids is central to homeostasis, yet its functional biology remains poorly understood. A probe (2′,7′-dichlorodihydrofluorescein diacetate) for reactive oxygen species (ROS) identified fluorescent objects at polyp-stolon junctions that emit high levels of ROS. A nuclear probe (Hoechst 33342) does not co-localize with these objects, while a mitochondrial probe (rhodamine 123) does. We interpret these objects as mitochondrion-rich cells. Confocal microscopy showed that this fluorescence is situated in large columnar cells. Treatment with an uncoupler (2,4-dinitrophenol) diminished the ROS levels of these cells relative to background fluorescence, as did removing the stolons connecting to a polyp-stolon junction. These observations support the hypothesis that the ROS emanate from mitochondrion-rich cells, which function by pulling open a valve at the base of the polyp. The open valve allows gastrovascular fluid from the polyp to enter the stolons and vice versa. The uncoupler shifts the mitochondrial redox state in the direction of oxidation, lowering ROS levels. By removing the stolons, the valve is not pulled open, metabolic demand is lowered, and the mitochondrion-rich cells slowly regress. Transmission electron microscopy identified mitochondrion-rich cells adjacent to a thick layer of mesoglea at polyp-stolon junctions. The myonemes of these myoepithelial cells extend from the thickened mesoglea to the rigid perisarc on the outside of the colony. The perisarc thus anchors the myoepithelial cells and allows them to pull against the mesoglea and open the lumen of the polyp-stolon junction, while relaxation of these cells closes the lumen.