Gill Ion Transport ATPases and Ammonia Excretion in Aquatic Crustaceans

Leone, Francisco de Assis; Lucena, Malson N.; Garçon, Daniela P.; Pinto, Marcelo R.; McNamara, John Campbell

doi:10.1007/978-3-319-39617-0_3

Cited by 19 publications

(23 citation statements)

References 387 publications

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“…Studies employing ion-selective microelectrodes have indicated that the three-cell excretory system of the nematode Caenorhabditis elegans excretes H + and K + (Adlimoghaddam et al, 2014), which suggests that ammonia might also be excreted by this internal method through an acid-trapping mechanism. In this system, NH 4 + likely enters the excretory cells via basolateral K + transporters, such as Na + /K + -ATPase (NKA) (Adlimoghaddam et al, 2015;Leone et al, 2016) and K + channels (Choe et al, 2000;Fehsenfeld and Weihrauch, 2016b). NH 4 + could then be excreted across the apical membrane in a similar fashion to K + while simultaneous apical H + excretion occurs, creating an acidic boundary layer that traps ammonia as NH 4 + , preventing its back-flow into the excretory system.…”

Section: Internal Excretory Organsmentioning

confidence: 99%

Ammonia excretion in aquatic invertebrates: new insights and questions

Weihrauch

Allen

2018

Journal of Experimental Biology

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Invertebrates employ a variety of ammonia excretion strategies to facilitate their survival in diverse aquatic environments, including freshwater, seawater and the water film surrounding soil particles. Various environmental properties set innate challenges for an organism's ammonia excretory capacity. These include the availability of NaCl and the respective ion-permeability of the organism's transport epithelia, and the buffering capacity of their immediate surrounding medium. To this end, some transporters seem to be conserved in the excretory process. This includes the Na/K(NH)-ATPase (NKA), the NH/CO dual gas-channel Rhesus (Rh)-proteins and novel ammonia transporters (AMTs), which have been identified in several invertebrates but appear to be absent from vertebrates. In addition, recent evidence strongly suggests that the hyperpolarization-activated cyclic nucleotide-gated K channel (HCN) plays a significant role in ammonia excretion and is highly conserved throughout the animal kingdom. Furthermore, microtubule-dependent vesicular excretion pathways have been found in marine and soil-dwelling species, where, unlike freshwater systems, acid-trapping of excreted ammonia is difficult or absent owing to the high environmental buffering capacity of the surroundings. Finally, although ammonia is known to be a toxic nitrogenous waste product, certain marine species readily maintain potentially toxic hemolymph ammonia as a sort of ammonia homeostasis, which suggests that ammonia is involved in physiological processes and does not exist simply for excretion. Such findings are discussed within this Commentary and are hypothesized to be involved in acid-base regulation. We also describe excretory organs and processes that are dependent on environmental constraints and indicate gaps in the current knowledge in these topics.

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Section: Internal Excretory Organsmentioning

confidence: 99%

Ammonia excretion in aquatic invertebrates: new insights and questions

Weihrauch

Allen

2018

Journal of Experimental Biology

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“…Crustaceans are mostly ammoniotelic (Weihrauch, Becker, Postel, Riestenpatt, & Siebers, 1998) and their nitrogenous metabolic end products are excreted across the gill epithelia, mainly as ammonia-N (NH 3 + NH 4 + ) (Weihrauch, Becker, Postel, Luck-Kopp, & Siebers, 1999), a process in which the Na + /K + -ATPase plays a major role (Lucu & Towle, 2003;Péqueux, 1995;Weihrauch, Fehsenfeld, & Quijada-Rodriguez, 2017), and is particularly important in crustaceans like C. vittatus from ammonia-rich, benthic niches (Romano & Zeng, 2013;Weihrauch, Morris, & Towle, 2004). As also seen in the vertebrate enzyme (Skou & Esmann, 1992), NH 4 + can replace K + in sustaining ATP hydrolysis by the gill Na + /K + -ATPase (Gonçalves et al, 2006;Lucena et al, 2012;Masui, Furriel, McNamara, Mantelatto, & Leone, 2002), and activity is synergistically stimulated by K + and NH 4 + in crustaceans from diverse habitats, corroborating a physiological role in nitrogen excretion (Leone et al, 2014;Leone, Lucena, Garçon, Pinto, & McNamara, 2017).…”

Section: Introductionmentioning

confidence: 78%

Low salinity‐induced alterations in epithelial ultrastructure, Na⁺/K⁺‐ATPase immunolocalization and enzyme kinetic characteristics in the gills of the thinstripe hermit crab, Clibanarius vittatus (Anomura, Diogenidae)

et al. 2017

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Fresh caught Clibanarius vittatus [SW, 31‰ salinity (S)] were acclimated to a dilute medium (15‰ S) for 10 days, employing silver staining to locate gill ion transporting tissue, immunofluorescence to localize the Na/K-ATPase α-subunit in the lamellae, and electron microscopy to portray ultrastructural changes in the gill epithelia. Na/K-ATPase activity was characterized kinetically in a gill microsomal fraction, including synergistic stimulation by NH plus K. Silver staining revealed that all 26 phyllobranchiate arthro- and pleurobranchiae participate in ion transport. Na/K-ATPase α-subunit staining was weak in SW crabs and distributed exclusively and irregularly within the intralamellar septal cells, particularly at the septal-pillar cell body junctions, and septal cell cytoplasm facing the hemolymph space. In 15‰ S crabs, α-subunit localization was intense, occupying the entire thickened septum. Pillar cells and flanges did not stain. Mitochondria and membrane foldings increased in the pillar cell flanges and intralamellar septal cells, greatly amplifying surface area. Only a single ATP binding site (V = 130.8 ± 10.5 nmol min mg protein; K = 55.3 ± 1.7 μmol l) obeying Michaelis-Menten kinetics was disclosed. Na/K-ATPase activity was modulated by Mg, Na, and NH, exhibiting site-site interactions; K modulation showed Michaelis-Menten kinetics. K plus NH synergistically stimulated activity ≈ 1.7-fold. Ouabain inhibited total ATPase activity by ≈ 70% (K = 220-300 μmol l), revealing phosphohydrolytic activities other than the Na/K-ATPase. Despite ample phylogenetic separation, the phyllobranchiate lamellae of the Anomura and Caridea share many ultrastructural features, that is, an intralamellar septum and opposed abutting pillar cells, similar Na/K-ATPase distribution, and comparable kinetic characteristics. These findings suggest either convergent evolution at the structural and biochemical levels, or preservation of traits present in a remote common ancestor.

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“…The copyright holder for this preprint (which this version posted April 25, 2020. ; https://doi.org/10.1101/2020.04.24.058297 doi: bioRxiv preprint site increased 10-fold (Table 1). (Na + , K + )-ATPase isoforms showing high and low affinity ATP-binding sites are present in many crustacean gill epithelia (Masui et al, 2002;Lucu and Towle, 2003;Leone et al, 2017;Farias et al, 2017). The non-exposure of the high affinity site after acclimation of U. cordatus to dilute media is similar to findings for the hermit crab C. symmetricus (Faleiros et al, 2018;and Antunes et al, 2017 as C. vittatus), the blue crab Callinectes danae (Masui et al, 2009) and the rock crab Cancer pagurus (Gache et al, 1976).…”

Section: Discussionmentioning

confidence: 99%

Osmotic and ionic regulation, and modulation by protein kinases, FXYD2 peptide and ATP of gill (Na+, K+)-ATPase activity, in the swamp ghost crab Ucides cordatus (Brachyura, Ocypodidae)

Leone

Lucena

Fabri

et al. 2020

Comparative Biochemistry and Physiology Part B: Biochemistry an

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The gill (Na + , K + )-ATPase is the main enzyme that underpins osmoregulatory ability in crustaceans that occupy biotopes like mangroves, characterized by salinity variation. We evaluated osmotic and ionic regulatory ability in the semi-terrestrial mangrove crab Ucides cordatus after 10-days acclimation to different salinities. We also analyzed modulation by exogenous FXYD2 peptide and by endogenous protein kinases A and C, and Ca 2+calmodulin-dependent kinase of (Na + , K + )-ATPase activity. Hemolymph osmolality was strongly hyper-/hypo-regulated in crabs acclimated at 2 to 35 ‰S. Clwas well hyper-/hyporegulated although Na + much less so, becoming iso-natremic at high salinity. (Na + , K + )-ATPase activity was greatest in isosmotic crabs (26 ‰S), diminishing progressively from 18 and 8 ‰S (0.5 fold) to 2 ‰S (0.04-fold), and decreasing notably at 35 ‰S (0.07-fold). At low salinity, the (Na + , K + )-ATPase exhibited a low affinity ATP-binding site that showed Michaelis-Menten behavior. Above 18 ‰S, an additional, high affinity ATP-binding site, corresponding to 10-20% of total (Na + , K + )-ATPase activity appeared. Activity is stimulated by exogenous pig kidney FXYD2 peptide, while endogenous protein kinases A and C and Ca 2+ /calmodulin-dependent kinase all inhibit activity. This is the first demonstration of inhibitory phosphorylation of a crustacean (Na + , K + )-ATPase by Ca 2+ /calmodulin-dependent kinase. Curiously, hyper-osmoregulation in U. cordatus shows little dependence on gill (Na + , K + )-ATPase activity, suggesting a role for other ion transporters. These findings reveal that the salinity acclimation response in U. cordatus consists of a suite of osmoregulatory and enzymatic adjustments that maintain its osmotic homeostasis in a challenging, mangrove forest environment.

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Gill Ion Transport ATPases and Ammonia Excretion in Aquatic Crustaceans

Cited by 19 publications

References 387 publications

Ammonia excretion in aquatic invertebrates: new insights and questions

Ammonia excretion in aquatic invertebrates: new insights and questions

Low salinity‐induced alterations in epithelial ultrastructure, Na⁺/K⁺‐ATPase immunolocalization and enzyme kinetic characteristics in the gills of the thinstripe hermit crab, Clibanarius vittatus (Anomura, Diogenidae)

Osmotic and ionic regulation, and modulation by protein kinases, FXYD2 peptide and ATP of gill (Na+, K+)-ATPase activity, in the swamp ghost crab Ucides cordatus (Brachyura, Ocypodidae)

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Gill Ion Transport ATPases and Ammonia Excretion in Aquatic Crustaceans

Cited by 19 publications

References 387 publications

Ammonia excretion in aquatic invertebrates: new insights and questions

Ammonia excretion in aquatic invertebrates: new insights and questions

Low salinity‐induced alterations in epithelial ultrastructure, Na+/K+‐ATPase immunolocalization and enzyme kinetic characteristics in the gills of the thinstripe hermit crab, Clibanarius vittatus (Anomura, Diogenidae)

Osmotic and ionic regulation, and modulation by protein kinases, FXYD2 peptide and ATP of gill (Na+, K+)-ATPase activity, in the swamp ghost crab Ucides cordatus (Brachyura, Ocypodidae)

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Low salinity‐induced alterations in epithelial ultrastructure, Na⁺/K⁺‐ATPase immunolocalization and enzyme kinetic characteristics in the gills of the thinstripe hermit crab, Clibanarius vittatus (Anomura, Diogenidae)