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First published online December 3, 2004
Journal of Experimental Biology 207, 4491-4504 (2004)
Published by The Company of Biologists 2004
doi: 10.1242/jeb.01308
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Ammonia excretion in aquatic and terrestrial crabs

Dirk Weihrauch1,*, Steve Morris2 and David W. Towle3

1 Department of Biology, Division of Animal Physiology, University of Osnabrück, D-49076 Osnabrück, Germany
2 Morlab, School of Biological Sciences, University of Bristol, BS8 1UG, UK
3 Mount Desert Island Biological Laboratory, Salsbury Cove, ME 04672, USA



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  		Fig. 1. Metabolic formation of nitrogen excretion products in Crustacea. Modified after Claybrook (1983Go). Existence of xanthine oxidase is unclear, as indicated by `?'.

 


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  		Fig. 2. Transporters and enzymes putatively involved in the process of ammonia excretion in crabs. Note: composition and localization of transporters may vary between crab species. (1) Na+/K+-ATPase; (2) K+ channels; (3) Na+/K+/2Cl– co-transporter; (4) Na+/H+ exchanger; (5) HCO3–/Cl– exchanger; (6) V-type H+-ATPase; (7) Carbonic anhydrase (CA); (8) amiloride-sensitive cation-permeable channel-like structures of the cuticle; (9) Rhesus-like protein (RhCM), putative ammonium transporter with unknown localization. For further information please refer to Table 2.

 


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  		Fig. 3. Fluxes of total ammonia (TAmm) across anterior (triangles) and posterior (squares) gills of seawater-adapted Cancer pagurus, brackish water-adapted Carcinus maenas, and freshwater-adapted Eriocheir sinensis. Gills were perfused with salines containing 100 µmol l–1 NH4Cl. Concentrations of NH4Cl in the bathing saline increased stepwise from 0 to 800 µmol l–1. Positive and negative values represent net effluxes and influxes from/into perfusate, respectively. Data represent means ±S.E.M. Carcinus maenas: N=7 (anterior) and N=9 (posterior gills). Cancer pagurus: N=7 (anterior) and N=8 (posterior gills). Eriocheir sinensis: N=7 (anterior) and N=6 (posterior gills). (Modified after Weihrauch et al., 1999Go.)

 


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  		Fig. 4. Transepithelial conductance in isolated half lamellae of gills of seawater-adapted Cancer pagurus, brackish water-adapted Carcinus maenas, and fresh water-adapted Eriocheir sinensis. For the electrophysiological measurements, half lamellae of anterior and posterior gills were mounted in a modified Ussing chamber. Data represent means ± S.E.M. with the number of experiments given in brackets. (From Weihrauch et al., 1999Go.)

 


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  		Fig. 5. Proposed hypothetical model of active ammonia excretion across gills of the shore crab Carcinus maenas. According to this model, NH4+ is pumped across the basolateral membrane by Na+/K+-ATPase (1) or traverses the membrane via Cs+-sensitive channels (2). Dissociation of cytosolic NH4+ to H+ and NH3 is accompanied by diffusion of NH3 into vesicles acidified by V-type H+-ATPase (3). The ammonia-loaded vesicles (4) then are moved via microtubules (5) to the apical membrane where vesicles fuse with the external membrane, releasing NH4+ into the subcuticular space. The NH4+ then is believed to diffuse across the cuticle, via amiloride-sensitive structures (6). Role and localization of the putative ammonia transporter (RhCM) identified in Carcinus maenas gill epithelium (GenBank Accession number: AF364404) are presently uncharacterized (7). Paracellular ammonia diffusion (8) and non-ionic transcellular diffusion of NH3 (9) is considered to be low under physiologically meaningful transepithelial ammonia gradients (Weihrauch et al., 1998Go). (Modified after Weihrauch et al., 2002Go.)

 


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  		Fig. 6. Localization of the 12 predicted transmembrane domains http://biowb.sdsc.edu (TMHMM) of putative Carcinus maenas (RhCM, GenBank Accession number: AF364404) and human (RhGK, also called PDRC2, GenBank Accession number: AF081497) ammonia transporter. Asterisk indicates identical predicted sites of transmembrane domains in RhCM and the human ammonia transporter RhGK.

 


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  		Fig. 7. Phylogenetic tree of published ammonia transporters. GenBank Accession numbers and type of ammonia transporter are given in parentheses. Anopheles gambiae (EAA01247 Rh-like protein); Azospirillum brasilense (AAC38548 AMT/MEP family); Carcinus maenas (AF364404, Rh-like protein); Danio rerio (AAM90586 Rh-like protein); Drosophila melanogaster (AF64673, Rh-like protein); Emericella nidulans (AAL73117 AMT/MEP family); Geodia cydonium (CAA73029 Rh-like protein); Hebeloma cylindrosporum 1 (AAK82417 AMT/MEP family); Hebeloma cylindrosporum 2 (AAM21926AMT/MEP family); Homo sapiens 50 KDa (CAA45883 Rh-like protein), Homo sapiens RhBG (AAL05978 Rh-like protein); Homo sapiens RhCG (AAH30965 Rh-like protein); Methanosarcina acetivorans (AAM07268 AMT/MEP family), Nostoc sp. (BAB72949 AMT/MEP family); Oryzias latipes (BAB13346 Rh-like protein); Pongo pygmaeus (AAG00305 Rh-like protein), Saccharomyces cerevisiae (P53390, AMT/MEP family), Tuber borchii (AAL11032 AMT/MEP family); Xenopus laevis (BAB13345 Rh-like protein). Tree was constructed with Multalin (Corpet, 1988Go). PAM, percent accepted mutations (a measure of phylogenetic distance).

 


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  		Fig. 8. Working model for ammonia excretion in the terrestrial crab Ocypode quadrata. (1) Na+/K+-ATPase; (2) NH4+-permeable K+ channels; (3) carbonic anhydrase (CA); (4) HCO3–/Cl– exchanger; (5) Na+/H+ exchanger; (6) Rhesus-like protein (RhCM), putative ammonium transporter; (7) cation-permeable channel-like structures of the cuticle; (8) transmembranous NH3 diffusion. For further details please refer to the text. Model compiled from data of DeVries and Wolcott (1993Go) and DeVries et al. (1994Go).

 


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  		Fig. 9. Working model for ammonia excretion in the terrestrial crab Geograpsus grayi. (1) Na+/K+-ATPase; (2) NH4+-permeable K+ channels; (3) carbonic anhydrase (CA); (4) Na+/H+/NH4+ exchanger; (5) HCO3–/Cl– exchanger; (6) Rhesus-like protein (RhCM), putative ammonium transporter; (7) cation-permeable channel-like structures of the cuticle. For further details please refer to the text. Model compiled from data of Varley and Greenaway (1994Go).

 

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© The Company of Biologists Ltd 2004