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The Nautilus Siphuncle As an Ion Pump·

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The Nautilus Siphuncle As an Ion Pump· Pacific Science (1982), vol. 36, no. 3 © 1983 by the University of Hawaii Press. All rights reserved The Nautilus Siphuncle as an Ion Pump· CHARLOTTE P. MANGUM 2 and DAVID W. TOWLE3 ABSTRACT: The siphuncle, which is believed to empty the newly formed chambers ofthe shell by a process involving the active transport ofNaCl, has the metabolic, enzymatic, and morphological features ofa transporting epithelium. It is capable of removing monovalent ions from solutions containing only Na+ and no Cl- or divalent ions, or only Cl- and no Na+ or divalent ions, indicating no obligatory coupling. The Na+ and Cl- are removed from native cameral fluid at approximately the same ratio. The levels ofK + and the divalent ions are also lowered, but at slightly different rates. Neither H+ nor NH1 accumulate in cameral fluid to an appreciable extent. IN THE CEPHALOPOD MOLLUSKS there is no evi­ secretion of a hypersaline solution of NaCl dence of an ability to maintain blood salts from cameral fluid into the blood by the and water out of osmotic balance with the siphuncle, a long tube that extends into the medium, even in euryhaline species (Hendrix uninhabited chambers. Although no reliable 1980, see also Mangum 1981). The net move­ information is available on the hydrostatic ment of fluids across epithelia within the pressure and osmolality of the blood, blood animal, which in a number of species plays a pressure must be higher than ambient (see part in the regulation of buoyancy, can be Bourne, Redmond, and Johansen 1978 for explained by mechanisms that do not require data on N. pompilius), and blood osmolality a hypothesis of active ion transport (Denton would be expected to be at least as high as and and Gilpin-Brown 1973). Perhaps for these probably slightly higher than ambient, as in reasons, serious consideration has been given other cephalopods. Ifcameral fluid is initially to hypotheses invoking passive mechanisms composed of ambient seawater, then the os­ to explain the pumping of water out of newly motic gradient should drive permeant solutes formed chambers of the nautilus shell, even into cameral fluid. And yet, both the osmo­ though the outcome of the process is a net lality and the chlorinity of cameral fluid de­ osmotic change in the residual fluid (Denton crease as its total volume is lowered (Denton and Gilpin-Brown 1966, 1973; Greenwald, and Gilpin-Brown 1966, Ward and Martin Ward, and Greenwald 1980; Ward, Green­ 1978). wald, and Greenwald 1980). In addition, the siphuncular epithelium has However, several observations on Nautilus many ofthe morphological features that char­ macromphalus made by Denton and Gilpin­ acterize other ion transporting epithelia, in­ Brown (1966) strongly implicate the active cluding microvilli at the site of putative NaCl absorption into the cell and, most convincing, an elaborate infolding of the basement mem­ 1 This research was conducted as part of the Alpha brane at the site of NaCl extrusion from the Helix Cephalopod Expedition to the Republic of the cell (Denton and Gilpin-Brown 1966), extend­ Philippines, supported by National Science Foundation ing throughout the cytoplasm as a network grant PCM 77-16269 to J. Arnold. This study was also supported in part by National Science Foundation grant of "canaliculi" (Greenwald et al. 1980, Ward PCM 77-20159 (regulatory biology) to C. P. Mangum et al. 1980). Finally, unlike the body fluids and by a University ofRichmond Faculty Research grant of some cephalopods, cameral fluid contains to D. W. Towle. Na+ as the most abundant cation (Denton 2 College of William and Mary, Department of Biology, Williamsburg, Virginia 23185. and Gilpin-Brown 1966). 3University of Richmond, Department of Biology, The mechanism of active ion transport by Richmond, Virginia 23173. the siphuncle of nautilus seemed uniquely 273 "...... ",~ , " ',r, , "'. • _ '" r • eo -, " ", '", , , , •• , ,, _"~" "'~ r r , 274 PACIFIC SCIENCE, Volume 36, July 1982 interesting to us for two reasons: First, the Tissue Oxygen Uptake organ apparently survives exposure to very The oxygen uptake of minced tissues was dilute cameral fluid for long periods, which measured in 0.05 M Tris-maleate buffered is otherwise rare in cephalopods (Hendrix seawater (pH 6.99) with a Yellow Springs 1980). Therefore, it seemed possible that the Biological Oxygen Monitor Model 53. The siphuncle might also survive experimental tissue was halved; one half was added to the manipulation of the ionic composition of the fluid. Important aspects ofion transport such buffered seawater and the other to the same medium plus ouabain (10- 3 M). After 30-45 as the coupling of Na+ and Cl- movements (reviewed by Towle 1981) might be elucidated. min, ouabain was also added to the control (final concentration 2.0-2.5 x 10-4 M) and Second, cameral fluid is stagnant, ultimately as well as transiently. Unlike other ambient the measurement on both aliquots of tissue repeated, to control for deterioration. fluids with which animal bloods exchange in­ organic ions, cameral fluid is not flushed away from the transporting epithelium by convec­ Rate ofAmmonia Excretion tion. If electrochemical balance across the Animals were placed in containers with epithelium is maintained by the efflux ofcoun­ 0.05-6 liters of seawater, depending on body terions from the blood, they would be ex­ size, and the ammonia levels were assayed pected to accumulate to measurable levels before and after 30 min incubation, using in cameral fluid and thus might be clearly the phenol hypochlorite method (Gravitz and identified. Gleye 1975, Solorzano 1969). In this paper we report results that are difficult to reconcile with any mechanism of Ionic and Osmotic Composition of Blood and emptying newly formed chambers other than Cameral Fluid active ion transport. While the mechanism of maintaining electrochemical balance remains Osmolality was determined with an unknown, our findings eliminate one possi­ Advanced Instruments Model 3DII freezing bility, and they suggest an area for future point osmometer, pH with a Radiometer investigation. BMS3 Blood Gas System, and ammonia as above, using 0.5-ml samples diluted with sea­ water to 5 ml. The activities of Na+, K+, Ca2 +, Mg2 +, and Cl- were determined with METHODS AND MATERIALS ion-selective electrodes, using stirred, buffered Electron Microscopy dilutions of the unknown, as described by Mangum et al. (1978b). Due to malfunction of Siphuncles were removed intact by severing the Radiometer PHM4 on shipboard, it was the muscles attaching the animal to the shell, necessary to modify the apparatus by using extending two fingers into the inhabited cham­ a Radiometer PHM 64 for the electrodes ber to the most recently formed septum, and equipped with European plugs, and a Model pulling gently and slightly downward on the 8040 A Fluke Multimeter connected to the posterior mantle. They were fixed for 45 min input circuit of a Chemtrix 60 A electrometer at room temperature in 2.6% gluteraldehyde for the electrodes equipped with American in seawater (pH 7.2, osmolality 1003 mOsm). plugs. Then the tissue was rinsed with filtered sea­ Blood samples were obtained from cathe­ water for 30 min, with two changes, and post­ terized vessels (see Lykkeboe and Johansen, fixed at room temperature with 1% OS04 this issue), and cameral fluid from small holes in 70% local seawater for 19 min. The tissue drilled into the shell at the sites of the two was dehydrated with 50, 70, and 95% ethyl most recently formed chambers. Those cham­ alcohol, and left overnight in 95%. It was then bers were aspirated until no more fluid could embedded in Epon 812, sectioned, and stained be obtained with a syringe fitted with a short with lead citrate. The sections were examined length of polyethylene tubing (No. 60) while with a Zeiss 9S-2 electron microscope. holding the animal in the air for 30-60 sec so Siphuncle as Ion Pump-MANGUM AND TOWLE 275 that the hole was at the lowest point of the presumably, in contact with venous blood shell, and the hole was blotted with absorbent across a thick layer of contractile elements paper. A test solution was then added to the (Figure 1). These cells are joined in the apical chamber and the hole sealed with dental wax region by extensive junctional complexes (Surgident), after the surrounding 5-10 mm (Figure IA), but are separated laterally in was abraded. In no instance did the seal fail. groups of two or three cells to form large intercellular drainage channels, as previously reported in light-microscopic studies of N. Enzymology macromphalus siphuncle (Denton and Gilpin­ Tissues were frozen in homogenizing Brown 1966). The channels contain ameb­ medium (0.25 M sucrose, 6 mM disodium ocytes and other wandering cells. The blind ethylenediamine tetraacetic acid, 20 mM end of each channel may lie within 15 /-lm of imidazole, pH 6.8) and shipped frozen to the horny siphuncle tube, whereas the channel Virginia. Tissue samples were thawed in ice­ itself measures as much as 100 /-lm in length. cold homogenizing medium, briefly blotted, Leading into the channel are many small ducts weighed, and homogenized in 20 volumes of ("canaliculi") formed by invagination of the fresh homogenizing medium containing 0.1 % basolateral plasma membranes of the epithe­ sodium deoxycholate (wt/vol) (Towle, lial cells (Figure lA, B). Adjacent to these Palmer, and Harris 1976). Homogenates were invaginations are numerous densely staining filtered through two layers ofcheesecloth and mitochondria. The base ofthe channel is sepa­ were assayed immediately for Na++ K +­ rated from the central blood vessel by a layer ATPase activity and protein. ofcontractile elements; the layer may be up to The Na++ K +-ATPase activity was mea­ 70 /-lm thick (Figure 1C). sured at 25°C by a coupled spectrophoto­ A comparison of the arrangement of the metric system in a medium containing 0.1 ml canaliculi in Nautilus pompilius with those filtered homogenate, 20 mM imidazole (pH also observed in the siphuncle of N.
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