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First published online January 27, 2004
Journal of Experimental Biology 207, 787-801 (2004)
Published by The Company of Biologists 2004
doi: 10.1242/jeb.00788

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The giant mudskipper Periophthalmodon schlosseri facilitates active NH₄⁺ excretion by increasing acid excretion and decreasing NH₃ permeability in the skin

Yuen K. Ip^1,*, David J. Randall², Timothy K. T. Kok¹, Cristiana Barzaghi¹, Patricia A. Wright³, James S. Ballantyne³, Jonathan M. Wilson⁴ and Shit F. Chew⁵

¹ Department of Biological Sciences, National University of Singapore, 10 Kent Ridge Road, Singapore 117543, Republic of Singapore
² Department of Biology and Chemistry, City University of Hong Kong, Tat Chee Avenue, Hong Kong, China
³ Department of Zoology, University of Guelph, Guelph, Ontario, Canada NIG 2W1
⁴ Centro Interdisciplinar de Investigação Marinha e Ambiental-CIIMAR, Rua do Campo Alegre 823, 4150-180 Porto, Portugal
⁵ Natural Sciences, National Institute of Education, Nanyang Technological University, 1 Nanyang Walk, Singapore 637616, Republic of Singapore

^* Author for correspondence (e-mail: dbsipyk{at}nus.edu.sg)

Accepted 7 November 2003

Periophthalmodon schlosseri is an amphibious and obligatory air-breathing teleost, which is extremely tolerant to environmental ammonia. It actively excretes NH₄⁺ in ammonia loading conditions. For such a mechanism to operate efficaciously the fish must be able to prevent back flux of NH₃. P. schlosseri could lower the pH of 50 volumes (w/v) of 50% seawater in an artificial burrow from pH 8.2 to pH 7.4 in 1 day, and established an ambient ammonia concentration of 10 mmol l^-1 in 8 days. It could alter the rate of titratable acid efflux in response to ambient pH. The rate of net acid efflux (H⁺ excretion) in P. schlosseri was pH-dependent, increasing in the order pH 6.0<7.0<8.0<8.5. Net acid flux in neutral or alkaline pH conditions was partially inhibited by bafilomycin, indicating the possible involvement of a V-type H⁺-ATPase. P. schlosseri could also increase the rate of H⁺ excretion in response to the presence of ammonia in a neutral (pH 7.0) external medium. Increased H⁺ excretion in P. schlosseri occurred in the head region where active excretion of NH₄⁺ took place. This would result in high concentrations of H⁺ in the boundary water layer and prevent the dissociation of NH₄⁺, thus preventing a back flux of NH₃ through the branchial epithelia. P. schlosseri probably developed such an `environmental ammonia detoxification' capability because of its unique behavior of burrow building in the mudflats and living therein in a limited volume of water. In addition, the skin of P. schlosseri had low permeability to NH₃. Using an Ussing-type apparatus with 10 mmol l^-1 NH₄Cl and a 1 unit pH gradient (pH 8.0 to 7.0), the skin supported only a very small flux of NH₃ (0.0095 µmol cm^-2 min^-1). Cholesterol content (4.5 µmol g^-1) in the skin was high, which suggests low membrane fluidity. Phosphatidylcholine, which has a stabilizing effect on membranes, constituted almost 50% of the skin phospholipids, with phosphatidyleserine and phsophatidylethanolamine contributing only 13% and 15%, respectively. More importantly, P. schlosseri increased the cholesterol level (to 5.5 µmol g^-1) and altered the fatty acid composition (increased total saturated fatty acid content) in its skin lipid after exposure to ammonia (30 mmol l^-1 at pH 7.0) for 6 days. These changes might lead to an even lower permeability to NH₃ in the skin, and reduced back diffusion of the actively excreted NH₄⁺ as NH₃ or the net influx of exogenous NH₃, under such conditions.

Key words: ammonia, excretion, permeability, cholesterol, fatty acid, gill, H⁺-ATPase, lipid, membrane, membrane fluidity, mudskipper, Periophthalmodon schlosseri, phospholipid, proton pump, skin

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