Exposure of the gill epithelial cells of larval lampreys to an ion-deficient environment: a stereological study

Abstract

Three kinds of epithelial cells comprise the surfaces of the gill filaments and lamellae of larval lampreys (ammocoetes): ammocoete mitochondria-rich cells (AMRCs), intercalated mitochondria-rich cells (IMRCs) and pavement cells. Selected characteristics of these cell types in ammocoetes of Geotria australis held in distilled water and in 10% sea water were compared using an ultrastructural stereological approach to determine which of those cell type(s) respond to exposure to an ion-deficient environment in a manner that indicates that they are involved in ion uptake. Particular focus was placed on the enigmatic AMRC, which comprises ca 60% of the cells and contains numerous mitochondria. The mean percentage contributions of both AMRCs and pavement cells to the total number of the three cell types in the two experimental groups were not significantly different, whereas that of IMRCs was >7% in distilled water and <1% in 10% sea water (P < 0.001). Furthermore, the mean apical surface areas of neither AMRCs nor pavement cells differed significantly between the two experimental groups, whereas that of IMRCs was nearly 3-fold greater in distilled water than in 10% sea water. The volume densities and size of mitochondria in AMRCs did not differ between the two exposure regimes. The above comparisons provide no indications that the uptake of Na + and Cl − in the gill epithelium of ammocoetes involves either the AMRC or pavement cell but, when considered in conjunction with data on ion-transporting cells in other vertebrates, they are consistent with the conclusion that the IMRC plays a crucial role in this process.

A cytosolic carbonic anhydrase molecular switch occurs in the gills of metamorphic sea lamprey

“…The high mitochondrial density of these cells would indicate a high metabolic activity and cytosolic carbonic anhydrase would have a role in modulating cellular acid-base demands 3 . A role in ion regulation seems unlikely since Bartels and co-workers 49 found no morphometric changes with ion poor water challenges and these cells are not present in adult freshwater migrants which also need to hyperosmoregulate. In addition, the ammocoete gill has very low NKA activity and neither NKA nor V-ATPase co-localize to these cells 50 .…”

Functional and evolutionary implications of the cellular composition of the gill epithelium of feeding adults of a freshwater parasitic species of lamprey, Ichthyomyzon unicuspis

“…In the epithelia of other vertebrates, the IMRC is involved in the uptake of Na + and Clby secreting H + and (or) HCO 3 -(for review see Bartels and Potter 2004;Reis-Santos et al 2008). It is thus assumed that as proposed for the freshwater stages of other lamprey species (Bartels and Potter 2004;Bartels et al 2009), the IMRC in the feeding adult of I. unicuspis is likewise engaged in the uptake of these ions.…”