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First published online August 31, 2004
Journal of Experimental Biology 207, 3447-3462 (2004)
Published by The Company of Biologists 2004
doi: 10.1242/jeb.01157

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Cellular composition and ultrastructure of the gill epithelium of larval and adult lampreys : Implications for osmoregulation in fresh and seawater

Helmut Bartels^1,* and Ian C. Potter²

¹ Anatomische Anstalt, Ludwig-Maximilians-Universität München, Pettenkoferstr. 11, 80336 München, Germany
² School of Biological Sciences and Biotechnology, Murdoch University, Murdoch 6150, Western Australia

View larger version (31K): [in a new window]   Fig. 1. Diagrams showing osmoregulatory mechanisms employed by anadromous lampreys during the freshwater (A) and seawater (B) phases in their life cycles. Modified from Hardisty et al. (1989).

View larger version (129K): [in a new window]   Fig. 2. Mitochondria-rich (MR) cells in the lamprey gill epithelium. (A) Intercalated MR cell between two pavement cells in the gill epithelium of a downstream migrant (young adult) of Geotria australis. The apical surface is enlarged by slender microplicae and the apical cytoplasm contains large numbers of membranous tubules and vesicles. (B) Higher magnification of the membrane of the microplicae, showing a coat of studs on the cytoplasmic side (arrows). (C) Ammocoete MR cells in the gill epithelium of a Petromyzon marinus larva, which, in contrast to the intercalated MR cells, lack cytoplasmic vesicles and tubules and exhibit only a moderate enlargement of their apical surface. Scale bars, 2 µm (A), 0.2 µm (B) and 2 µm (C).

View larger version (229K): [in a new window]   Fig. 3. (A) Freeze fracture of an intercalated mitochondria-rich (MR) cell of a Petromyzon marinus larva. Rod-shaped particles are present in the apical membrane (top of the micrograph) and in the membranes of cytoplasmic tubules and vesicles (arrows), while the basolateral membrane (bottom of micrograph) contains only globular particles. (B) Higher magnification of the apical part of the intercalated MR cell shown in A. The apical and cytoplasmic membranes contain a few globular particles in addition to rod-shaped particles. (C) Scanning electron micrograph of an intercalated MR cell surrounded by ammocoete MR cells in the gill epithelium of a larval Geotria australis. Scale bars, 0.5 µm (A), 0.25 µm (B) and 2 µm (C).

View larger version (15K): [in a new window]   Fig. 4. Diagram showing the three subtypes (A–C) of the intercalated mitochondria-rich (MR) cell, based on the different distribution of the H+ V-ATPase, anion exchanger and Cl– channel. Thicker and narrower arrows denote active and passive transport, respectively. CA II, cytosolic carbonic anhydrase.

View larger version (150K): [in a new window]   Fig. 5. Pavement cells in the gill epithelium of an upstream migrant of Lampetra fluviatilis. (A) The two-layered lamellar epithelium contains an outer layer of pavement cells (PC) and an inner layer of basal cells (BC). The pavement cells contain numerous ovoid mucous granules (arrows) and a few mitochondria. Freeze fracture of the apical membrane of the pavement cell showing few particles on the P face (B) and numerous particles on the E face (C). Scale bars, 2 µm (A) and 0.25 µm (B,C).

View larger version (10K): [in a new window]   Fig. 6. A proposed model for Na+ and Cl– uptake by adult lampreys in freshwater. Thicker and narrower arrows denote active and passive transport, respectively. IMRC-A and IRMC-C, subtype A and C of intercalated MR cells, respectively; PC, pavement cell.

View larger version (215K): [in a new window]   Fig. 7. Chloride cells in the gill epithelium of an adult Geotria australis in seawater. (A) Cross section of the filament, showing a row of chloride cells on each side of the central blood space. (B) Freeze fracture of a bundle of parallel membranous tubules, showing the helicoidally arranged particles (arrowheads). (C) Zonula occludens between two chloride cells consisting of a single strand. The particles in the apical membrane of the chloride cell are clustered on the P face. (D) Clusters of particles on the E face. Scale bars, 3 µm (A), 0.5 µm (B,C) and 0.25 µm (D).

View larger version (213K): [in a new window]   Fig. 8. Apical surfaces of the chloride cells of young adult Geotria australis in freshwater (A) and after migration to seawater (B). Lateral views of the filament, showing at the bottom its base, where lamellae are absent. The chloride cells form rows (arrows) at the base of the filament, which continue into the interlamellar region. Note the changes of the apical surface of the chloride cell from a small circular region enlarged by microvilli in freshwater (A) to a comparably large rectangular region lacking microvilli in seawater (B). Intercalated MR cells are encircled in A and absent in B. L, lamellae. Scale bars, 30 µm (A,B). Reprinted from Bartels et al. (1996) with kind permission from the publishers.

View larger version (8K): [in a new window]   Fig. 9. A proposed model for Na+ and Cl– secretion by lampreys in seawater. Thicker and narrower arrows denote active and passive transport, respectively. CC, chloride cell; PC, pavement cell.