Rapid transitions among functional states support efficient osmoregulatory acclimation: focus on “Functional plasticity of mitochondrion-rich cells in the skin of euryhaline medaka larvae (Oryzias latipes) subjected to salinity changes”

Abstract

THERE IS A DECADES-LONG HISTORY of research to understand the biology of mitochondrion-rich cells (MRCs; ionocytes) in the gills, skin, and other integumentary tissues of fishes that bear direct contact with the external environment. Beginning in the 1930s, experiments to partition whole-animal salt movements among exchange routes accessible to physiological measurement (gills, skin, alimentary tract and rectal gland, and kidney) revealed the apparent importance of branchial tissues to monovalent ion excretion in seawater, and uptake in fresh water.The key contributions of August Krogh, Homer Smith, and Ancel Keys to this early body of experimental work and to the development of descriptive, organ-level models for hypoosmotic and hyperosmotic regulation in teleost fishes that persist largely unchanged to this day, were recently reviewed (3). The discovery and histological description by Keys and Willmer (13) of special so-called "chloride-secreting cells," as MRCs were then known, in fish gills provided the first linkage between branchial salt extrusion and an identifiable cell type; the greater abundance of these cells in seawater fishes relative to freshwater species supported the proposed secretory function. And, presaging more recent findings, Keys and Willmer (13) also conjectured that these cells in smaller representation in freshwater fishes could be responsible for ion uptake.In the middle years of experimental study, MRCs as the branchial ion-transporting cells became characterized with respect to their ultrastructure and physiological functions that include not only salt transport but also pH regulation through H ϩ and HCO 3Ϫ exchange (4, 10, 15). Typically containing abundant mitochondria, and well-developed basolateral membrane invaginations and tubulovesicular system, MRC subtypes are distinguished by topology of the apical (outwardfacing) membrane and by neighbor associations with adjacent accessory cells [see review by Evans (4)]. Many in vitro techniques have been applied to probe the physiological and biophysical mechanisms of ion transport by MRCs [see the comprehensive historical reviews of techniques by Evans (3) and by Marshall and Bellamy (14)]. Because of the geometrical complexity of the gills, only some of these techniques (such as perfusion of gill and heart-gill tissue preparations) afforded useful study of mitochondrion-rich cells in that important site. Several other MRC-containing tissues are now developed as simpler epithelial sheet models for branchial ion transport studies. In adult fishes, these include opercular membrane and skin that are easily mounted in Ussing-type flux chambers for studies of electrophysiology and radiotracer fluxes. And in larval fishes, the yolk-sac membrane (an apparently important osmoregulatory tissue during early life when gills are still rudimentary in development) is accessible for morphological and functional examinations of MRC biology, including responses to salinity challenge in euryhaline species (8,17). From these very productive chamber studie...