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
Cellular composition and ultrastructure of the gill epithelium of larval and adult lampreys
:
Implications for osmoregulation in fresh and seawater
Helmut Bartels1,* 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
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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 ).
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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).
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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).
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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.
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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).
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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.
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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).
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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.
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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.
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© The Company of Biologists Ltd 2004
