Abstract
Salt tolerance reflects ecophysiological adaptation, and the wide-ranging distribution of the Brachyura mirrors their ability to adjust body fluid concentrations. The gill (Na+, K+)-ATPase underpins such hyper/hypo-regulatory mechanisms. We evaluate osmotic and chloride regulation in Callinectes danae after 10 days acclimation to a wide salinity range (5–50 ‰S), accompanying alterations in hemolymph osmolality and [Cl−] during hypo- (15 ‰S) or hyper- (45 ‰S) osmotic challenge. Further, we investigate posterior gill (Na+, K+)-ATPase kinetics, α-subunit immunolocalization and its mRNA and protein expression (15, 30 and 40 or 45 ‰S). The crab is a moderate, asymmetrical hyper/hypo-osmoregulator but is a strong, asymmetrical hyper/hypo-chloride regulator. Hyper-regulation at low salinity is sustained by a threefold increase in (Na+, K+)-ATPase activity, a 3.5-fold increase in α-subunit mRNA expression and 1.6-fold increase in protein expression. α-Subunit signal is highest in 15 ‰S-acclimated crabs, and is uniformly distributed throughout the ionocytes and pillar cells. Activity in 30- and 40% S-acclimated crabs is similar. Affinity for ATP and Na+ increases on high salinity acclimation but decreases for ouabain. K+ apparent affinity is independent of salinity, while that for Mg2+ decreases and for NH4+ increases with increasing salinity. A high-affinity ATP-binding site disappears on acclimation at any salinity. FOF1- and Na+- or K+-ATPase activities decrease with increased salinity. Hemolymph chloride hypo-regulation depends little on gill (Na+, K+)-ATPase activity. Hyper-, and hypo-osmotic and ionic regulatory capabilities in C. danae are intricate physiological processes underpinned by multifarious gill (Na+, K+)-ATPase kinetics and altered mRNA and protein expressions.
Similar content being viewed by others
Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Andrade LS, Antunes M, Lima PA, Furlan M, Frameschi IF, Fransozo A (2015) Reproductive features of the swimming crab Callinectes danae (Crustacea, Portunidae) on the subtropical coast of Brazil: a sampling outside the estuary. Braz J Biol 75:692–702. https://doi.org/10.1590/1519-6984.21513
Antunes CD, Lucena MN, Garçon DP, Leone FA, McNamara JC (2017) 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). J Exp Zool 327:380–397. https://doi.org/10.1002/jez.2109
Augusto A, Greene LJ, Laure HJ, McNamara JC (2007) Adaptive shifts in osmoregulatory strategy and the invasion of freshwater by brachyuran crabs: evidence from Dilocarcinus pagei (Trichodactylidae). J Exp Zool 307:688–698. https://doi.org/10.1002/jez.422
Babonis LS, Brischoux F (2012) Perspectives on the convergent evolution of tetrapod salt glands. Int Comp Biol 52:245–256. https://doi.org/10.1093/icb/ics073
Chacur MM, Negreiros-Fransozo ML (2001) Spatial and seasonal distributions of Callinectes danae (Decapoda, Portunidae) in Ubatuba Bay, São Paulo, Brazil. J Crust Biol 21:414–425. https://doi.org/10.1651/0278-0372(2001)021[0414:sasdoc]2.0.co;2
Clausen MV, Hilbers F, Poulsen H (2017) The Structure and Function of the Na, K-ATPase Isoforms in Health and Disease. Front Physiol 8:371. https://doi.org/10.3389/fphys.2017.00371
Copeland DE, Fitzjarrell AT (1968) The salt absorbing cells in the gills of the blue crab (Callinectes sapidus Rathbun) with notes on modified mitochondria. Z Zellforsch 92:1–22. https://doi.org/10.1007/BF00339398
D’Orazio SE, Holliday CW (1985) Gill Na, K-ATPase and osmorregulation in the sand fiddler crab, Uca pugilator. Physiol Zool 58:364–373. https://doi.org/10.1086/physzool.58.4.30156011
Fabri LM, Lucena MN, Garçon DP, Moraes CM, McNamara JC, Leone FA (2019) Kinetic characterization of the gill (Na+, K+)-ATPase in a hololimnetic population of the diadromous Amazon River shrimp Macrobrachium amazonicum (Decapoda, Palaemonidae). Comp Biochem Physiol 227B:64–74. https://doi.org/10.1016/j.cbpb.2018.09.004
Faleiros RO, Goldman MHS, Furriel RPM, McNamara JC (2010) Differential adjustment in gill Na+/K+- and V-ATPase activities and transporter mRNA expression during osmoregulatory acclimation in the cinnamon shrimp Macrobrachium amazonicum (Decapoda, Palaemonidae). J Exp Biol 213:3894–3905. https://doi.org/10.1242/jeb.046870
Faleiros RO, Furriel RPM, McNamara JC (2017) Transcriptional, translational, and systemic alterations during the time course of osmoregulatory acclimation in two palaemonid shrimps from distinct osmotic niches. Comp Biochem Physiol 212A:97–106. https://doi.org/10.1002/ece3.2741
Faleiros RO, Garçon DP, Lucena MN, McNamara JC, Leone FA (2018) Short- and long-term salinity challenge, osmoregulatory ability, and (Na+, K+)-ATPase kinetics and α-subunit mRNA expression in the gills of the thinstripe hermit crab Clibanarius symmetricus. Comp Biochem Physiol 225:16–25. https://doi.org/10.1016/j.cbpa.2018.06.016
Farias DL, Lucena MN, Garçon DP, Mantelatto FL, McNamara JC, Leone FA (2017) A kinetic characterization of the gill (Na+, K+)-ATPase from the semi-terrestrial mangrove crab Cardisoma guanhumi Latreille, 1825 (Decapoda, Brachyura). J Membr Biol 250:517–534. https://doi.org/10.1007/s00232-017-9978-6
Findley AM, Stickle WB (1978) Effects of salinity fluctuation on the hemolymph composition of the blue crab Callinectes sapidus. Mar Biol 46:9–15. https://doi.org/10.1007/BF00393814
França JL, Pinto MR, Lucena MN, Garçon DP, Valenti WC, McNamara JC, Leone FA (2013) Subcellular localization and kinetic characterization of a gill (Na+, K+)-ATPase from the giant freshwater prawn Macrobrachium rosenbergii. J Membr Biol 246:529–543. https://doi.org/10.1007/s00232-013-9565-4
Freire CA, Onken H, McNamara JC (2008) A structure–function analysis of ion transport in crustacean gills and excretory organs. Comp Biochem Physiol 151A:272–304. https://doi.org/10.1016/j.cbpa.2007.05.008
Furriel RPM, Firmino KCS, Masui DC, Faleiros RO, Torres AH, McNamara JC (2010) Structural and biochemical correlates of (Na+, K+)-ATPase driven ion uptake across the posterior gill epithelium of the true freshwater crab, Dilocarcinus pagei (Brachyura, Trichodactylidae). J Exp Zool 313A:508–523. https://doi.org/10.1002/jez.622
Gache C, Rossi B, Lazdunski M (1977) Mechanistic analysis of the (Na, K)-ATPase using new pseudo substrates. Biochem 16:2957–2965. https://doi.org/10.1021/bi00632a024
Garçon DP, Masui DC, Mantelatto FLM, McNamara JC, Furriel RPM, Leone FA (2007) K+ and NH4+ modulate gill (Na+ K+)-ATPase activity in the blue crab Callinectes ornatus: fine tuning of ammonia excretion. Comp Biochem Physiol 147A:145–155. https://doi.org/10.1016/j.cbpa.2006.12.020
Garçon DP, Masui DC, Mantelatto FLM, McNamara JC, Furriel RPM, Leone FA (2009) Hemolymph ionic regulation and adjustments in gill (Na+, K+)-ATPase activity during salinity acclimation in the swimming crab Callinectes ornatus (Decapoda, Brachyura). Comp Biochem Physiol 154A:44–55. https://doi.org/10.1016/j.cbpa.2009.04.624
Geering K (2008) Functional roles of Na, K-ATPase subunits. Curr Opinion Nephrol Hyperten 17:526–532. https://doi.org/10.1097/MNH.0b013e3283036cbf
Genovese G, Luchetti CG, Luquet CM (2004) Na+/K+–ATPase activity and gill ultrastructure in the hyper–hypo-regulating crab Neohelice granulatus acclimated to dilute, normal and concentrated seawater. Mar Biol 144:111–118. https://doi.org/10.1007/s00227-003-1169-6
Gerencser GA, Zhang J (2004) The Cl- pump. Int Congress Series 1275:104–113. https://doi.org/10.1016/j.ics.2004.09.033
Gilles R, Péqueux A, Bianchini A (1988) Physiological aspects of NaCl movements in the gills of the euryhaline crab, Eriocheir sinensis, acclimated to freshwater. Comp Biochem Physiol 90A:201–207. https://doi.org/10.1016/0300-9629(88)91028-6
Gonçalves RR, Masui DC, McNamara JC, Mantelatto FLM, Garçon DP, Furriel RPM, Leone FA (2006) A kinetic study of the gill (Na+, K+)-ATPase, and its role in ammonia excretion in the intertidal hermit crab, Clibanarius vittatus. Comp Biochem Physiol 145A:346–356. https://doi.org/10.1016/j.cbpa.2006.07.007
Halperin J, Genovese G, Tresguerres M, Luquet CM (2004) Modulation of ion uptake across posterior gills of the crab Chasmagnathus granulata by dopamine and cAMP. Comp Biochem Physiol 139A:103–109. https://doi.org/10.1016/j.cbpb.2004.07.001
Harris RR, Santos MCF (1993) Sodium uptake and transport (Na+, K+)-ATPase changes following Na+ depletion and low salinity acclimation in the mangrove crab Ucides cordatus. Comp Biochem Physiol 105A:35–42. https://doi.org/10.1016/0300-9629(93)90170-9
Havird JC, Mitchell RT, Henry RP, Santos SR (2016) Salinity-induced changes in gene expression from anterior and posterior gills of Callinectes sapidus (Crustacea: Portunidae) with implications for crustacean ecological genomics. Comp Biochem Physiol 1:34–44. https://doi.org/10.1016/j.cbd.2016.06.002
Henry RP, Garrelts EE, McCarty MM, Towle DW (2002) Differential induction of branchial carbonic anhydrase and Na+/K+ ATPase activity in the euryhaline crab, Carcinus maenas, in response to low salinity exposure. J Exp Zool 292:595–603. https://doi.org/10.1002/jez.10075
Henry RP, Lucu C, Onken H, Weihrauch D (2012) Multiple functions of the crustacean gill: osmotic/ionic regulation, acid-base balance, ammonia excretion, and bioaccumulation of toxic metals. Front Physiol 3:1–33. https://doi.org/10.3389/fphys.2012.00431
Heugens EHW, Hendriks AJ, Dekker T, Straalen NMV, Admiraal W (2001) A review of the effects of multiple stressors on aquatic organisms and analysis of uncertainty factors for use in risk assessment. Crit Rev Toxicol 31:247–284. https://doi.org/10.1080/20014091111695
Jiang Q, Garcia A, Han M, Cornelius F, Apell HJ, Khandelia H, Clarke RJ (2017) Electrostatic stabilization plays a central role in autoinhibitory regulation of the Na+, K+-ATPase. Biophys J 112:288–299. https://doi.org/10.1016/j.bpj.2016.12.008
Kanai R, Ogawa H, Vilsen B, Cornelius F, Toyoshima C (2013) Crystal structure of a Na+-bound Na+, K+-ATPase preceding the E1 state. Nature 502:201–207. https://doi.org/10.1038/nature12578
Kirschner LB (1980) Comparison of vertebrate salt-excreting organs. Am J Physiol 238:R219–R223. https://doi.org/10.1152/ajpregu.1980.238.3.R219
Kirschner LB (2004) The mechanism of sodium chloride uptake in hyperregulating aquatic animals. J Exp Biol 207:1439–1452. https://doi.org/10.1242/jeb.00907
Lee CA, Kiergaard M, Gelembiuk W, Eads BD, Posavi M (2011) Pumping ions: rapid parallel evolution of ionic regulation following habitat invasions. Evolution 65:2229–2244. https://doi.org/10.1111/j.1558-5646.2011.01308.x
Leone FA, Baranauskas JA, Furriel RPM, Borin IA (2005a) SigrafW: an easy-to-use program for fitting enzyme kinetic data. Biochem Mol Biol 33:399–403. https://doi.org/10.1002/bmb.2005.49403306399
Leone FA, Furriel RPM, McNamara JC, Mantelatto FLM, Masui DC, Alves LR, Gonçalves RR, Garçon DP (2005b) (Na+, K+)-ATPase from crustacean gill microsomes: a molecular marker to evaluate adaptation to biotopes of different salinity. Trends Comp Biochem Physiol 11:1–15
Leone FA, Garçon DP, Lucena MN, Faleiros RO, Azevedo SV, Pinto MR, McNamara JC (2015) Gill-specific (Na+, K+)-ATPase activity and α-subunit mRNA expression during low-salinity acclimation of the ornate blue crab Callinectes ornatus (Decapoda, Brachyura). Comp Biochem Physiol 186B:59–67. https://doi.org/10.1016/j.cbpb.2015.04.010
Leone FA, Lucena MN, Garçon DP, Pinto MR, McNamara JC (2017) Gill ion transport ATPases and ammonia excretion in aquatic crustaceans. In: Weihrauch D, O’Donnell MJ (eds) Acid-base balance and nitrogen excretion in invertebrates. Mechanisms and strategies in various invertebrate groups with considerations of challenges caused by ocean acidification. Springer, New York, pp 61–107 (10.1007%2F978-3-319-39617-0_3)
Leone FA, Lucena MN, Fabri LM, Garçon DP, Fontes CFL, Faleiros RO, Moraes CM, McNamara JC (2020) 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). Comp Biochem Physiol 250B:110507. https://doi.org/10.1016/j.cbpb.2020.110507
Li E, Wang S, Li C, Wang X, Chen K, Chen L (2014) Transcriptome revealed the genes and pathways involved in salinity stress of Chinese mitten crab, Eriocheir sinensis. Physiol Genomics 46:177–190. https://doi.org/10.1152/physiolgenomics.00191.2013
Lima AG, McNamara JC, Terra WR (1997) Regulation of hemolymph osmolytes and gill Na+/K+-ATPase activities during acclimation to saline media in the freshwater shrimp Macrobrachium olfersii (Wiegmann, 1836) (Decapoda, Palaemonidae). J Exp Mar Biol Ecol 215:81–91. https://doi.org/10.1016/S0022-0981(97)00016-6
López-Mañanes AAL, Meligeni CD, Goldemberg AL (2002) Response to environmental salinity of Na+, K+ATPase activity in individual gills of the euryhaline crab Crytograpsus angulatus. J Exp Mar Biol Ecol 274:75–85. https://doi.org/10.1016/S0022-0981(02)00166-1
Lovett DL, Colella T, Cannon AC, Lee H, Evangelisto A, Muller EM, Towle DW (2006) Effect of Salinity on osmoregulatory patch epithelia in gills of the blue crab Callinectes sapidus. Biol Bull 210:132–139. https://doi.org/10.2307/4134602
Lucena MN, Garçon DP, Mantelatto FLM, Pinto MR, McNamara JC, Leone FA (2012) Hemolymph ion regulation and kinetic characteristics of the gill (Na+, K+)-ATPase in the hermit crab Clibanarius vittatus (Decapoda, Anomura) acclimated to high salinity. Comp Biochem Physiol 161B:380–391. https://doi.org/10.1016/j.cbpb.2012.01.003
Lucu C, Flik G (1999) (Na+, K+)-ATPase and Na+, Ca2+ exchange activities in gills of hyperregulating Carcinus maenas. Am J Physiol 276:R490–R499. https://doi.org/10.1152/ajpregu.1999.276.2.R490
Lucu C, Towle DW (2003) (Na+, K+)-ATPase in gills of aquatic crustacea. Comp Biochem Physiol 135A:195–214. https://doi.org/10.1016/S1095-6433(03)00064-3
Lucu C, Pavicic J, Ivankovic D, Pavicic-Hamer D, Najdek M (2008) Changes in Na+/K+-ATPase activity, unsaturated fatty acids and metallothioneins in gills of the shore crab Carcinus aestuarii after dilute seawater acclimation. Comp Biochem Physiol 149A:362–372. https://doi.org/10.1016/j.cbpa.2008.01.026
Luquet CM, Genovese G, Rosa GA, Pellerano GN (2002) Ultrastructural changes in the gill epithelium of the crab Chasmagnathus granulatus (Decapoda: Grapsidae) in diluted and concentrated seawater. Mar Biol 141:753–760. https://doi.org/10.1007/s00227-002-0860-3
Luquet CM, Weihrauch D, Senek M, Towle DW (2005) Induction of branchial ion transporter mRNA expression during acclimation to salinity change in the euryhaline crab Chasmagnathus granulatus. J Exp Biol 208:3627–3636. https://doi.org/10.1242/jeb.01820
Mantel LH, Farmer LL (1983) Osmotic and ionic regulation. In: Bliss DE (ed) The Biology of Crustacea, 5: internal anatomy and physiological regulation. Academic Press, New York, pp 53–159. https://doi.org/10.1016/B978-0-12-106405-1.50013-8
Mantelatto FLM, Fransozo A (2000) Brachyuran community in Ubatuba Bay, Northern Coast of São Paulo State, Brazil. J Shelfish Res 19:701–709
Martinez CBR, Harris RR, Santos MCF (1998) Transepithelial potential differences and sodium fluxes in isolated perfused gills of the mangrove crab Ucides cordatus. Comp Biochem Physiol 120A:227–236. https://doi.org/10.1016/S1095-6433(98)00021-X
Masui DC, Furriel RPM, McNamara JC, Mantelatto FLM, Leone FA (2002) Modulation by ammonium ions of gill microsomal (Na+, K+)-ATPase in the swimming crab Callinectes danae: a possible mechanism for the regulation of ammonia excretion. Comp Biochem Physiol 132C:471–482. https://doi.org/10.1016/S1532-0456(02)00110-2
Masui DC, Furriel RPM, Silva ECC, Mantelatto FLM, McNamara JC, Barrabin H, Scofano HM, Fontes CFL, Leone FA (2005) Gill microsomal (Na+, K+)-ATPase from the blue crab Callinectes danae: interactions at cationic sites. Int J Biochem Cell Biol 37:2521–2535. https://doi.org/10.1016/j.biocel.2005.06.004
Masui DC, Silva ECC, Mantelatto FLM, McNamara JC, Barrabin H, Scofano HM, Fontes CFL, Furriel RPM, Leone FA (2008) The crustacean gill (Na+, K+)-ATPase: Allosteric modulation of high- and low-affinity ATP-binding sites by sodium and potassium. Arch Biochem Biophys 479:139–144. https://doi.org/10.1016/j.abb.2008.08.018
Masui DC, Mantelatto FLM, Furriel RPM, McNamara JC, Leone FA (2009) (Na+, K+)-ATPase activity in gill microsomes from the blue crab, Callinectes danae, acclimated to low salinity: novel perspectives on ammonia excretion. Comp Biochem Physiol 153A:141–148. https://doi.org/10.1016/j.cbpa.2009.01.020
McNamara JC, Faria SC (2012) Evolution of osmoregulatory patterns and gill ion transport mechanisms in the decapod Crustacea: a review. J Comp Physiol 182B:997–1014. https://doi.org/10.1007/s00360-012-0665-8
McNamara JC, Lima AG (1997) The route of ion water movements across the gill epithelium of the freshwater shrimp Macrobrachium olfersii (Decapoda. Palaemonidae): evidence from ultrastructural changes induced by acclimation to saline media. Biol Bull 192:321–331. https://doi.org/10.2307/1542725
McNamara JC, Freire CA, Torres AH, Faria SC (2015) The conquest of fresh water by the palaemonid shrimps: an evolutionary history scripted in the osmoregulatory epithelia of the gills and antennal glands. Biol J Lin Soc 114:673–688. https://doi.org/10.1111/bij.12443
Middleton DA, Fedosova NU, Esmann M (2015) Long-range effects of Na+ binding in Na, K-ATPase reported by ATP. Biochem 54:7041–7047. https://doi.org/10.1021/acs.biochem.5b00893
Morth JP, Pedersen BP, Toustrup-Jensen MS, Sorensen TLM, Petersen J, Andersen JP, Vilsen B, Nissen P (2007) Crystal structure of the sodium–potassium pump. Nature 450:1043–1050. https://doi.org/10.1038/nature06419
Morth JP, Poulsen H, Toustrup-Jensen MS, Shack VR, Egebjerg J, Andersen JP, Vilsen B, Nissen P (2009) The structure of the Na+, K+-ATPase and mapping of isoform differences and disease-related mutations. Philos Trans R Soc 364B:217–227. https://doi.org/10.1098/rstb.2008.0201
Nyblom M, Poulsen H, Gourdon P, Reinhard I, Andersson M (2013) Crystal structure of Na+, K+-ATPase in the Na+-bound state. Science 342:123–127
Palmgren MG, Nissen P (2011) P-Type ATPases. Annu Rev Biophys 40:243–266. https://doi.org/10.1146/annurev.biophys.093008.131331
Péqueux A (1995) Osmotic regulation in crustaceans. J Crust Biol 15:1–60. https://doi.org/10.2307/1549010
Peres PA, Mantelatto FL (2020) Salinity tolerance explains the contrasting phylogeographic patterns of two swimming crabs species along the tropical western Atlantic. Evol Ecol 34:589–609. https://doi.org/10.1007/s10682-020-10057-x
Peres PA, Lopes M, Negri M, Robles R, Santos CRM, Mantelatto FL (2020) Lack of population genetic structure among Brazilian populations of Callinectes danae (Brachyura: Portunidae): implication for management and conservation. Reg Stud Mar Sci. https://doi.org/10.1016/j.rsma.2020.101336
Piller SC, Henry RP, Doeller JE, Kraus DW (1995) A comparison of the gill physiology of two euryhaline crab species, Callinectes Sapidus and Callinectes similis: energy production, transport related enzymes and osmorregulation as a function of acclimation salinity. J Exp Biol 198:349–358
Pinto MR, Lucena MN, Faleiros RO, Almeida EA, McNamara JC, Leone FA (2016) Effects of ammonia stress in the Amazon River shrimp Macrobrachium amazonicum (Decapoda, Palaemonidae). Aquatic Toxicol 170:13–23. https://doi.org/10.1016/j.aquatox.2015.10.021
Poulsen H, Morth P, Egebjerg J, Nissen P (2010) Phosphorylation of the Na+, K+-ATPase and the H+, K+-ATPase. FEBS Lett 584:2589–2595. https://doi.org/10.1016/j.febslet.2010.04.035
Proverbio F, Marín R, Proverbio T (1991) The ouabain-insensitive sodium pump. Comp Biochem Physiol 99A:279–283. https://doi.org/10.1016/0300-9629(91)90002-T
Ramaglia AC, de Castro LM, Augusto A (2018) Effects of ocean acidification and salinity variations on the physiology of osmoregulating and osmoconforming crustaceans. J Comp Physiol B 188(5):729–738
Riestenpatt S, Onken H, Siebers D (1996) Active absorption of Na+ and Cl- across the gill epithelium of the shore crab Carcinus maenas: voltage-clamp and ion-flux studies. J Exp Biol 199:1545–1554
Romano N, Zeng C (2012) Osmoregulation in decapod crustaceans: implications to aquaculture productivity, methods for potential improvement and interactions with elevated ammonia exposure. Aquacult 334–337:12–23. https://doi.org/10.1016/j.aquaculture.2011.12.035
Santos FH, McNamara JC (1996) Neuroendocrine modulation of osmoregulatory parameters in the freshwater shrimp Macrobrachium olfersii (Wiegmann) (Crustacea, Decapoda). J Exp Mar Biol Ecol 206:109–120. https://doi.org/10.1016/S0022-0981(96)02599-3
Santos LCF, Belli NM, Augusto A, Masui DC, Leone FA, McNamara JC, Furriel RPM (2007) Gill (Na+, K+)-ATPase in diadromous, freshwater palaemonid shrimps: species-specific kinetic characteristics and alpha-subunit expression. Comp Biochem Physiol 148A:178–188. https://doi.org/10.1016/j.cbpa.2007.04.008
Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3:1101–1108. https://doi.org/10.1038/nprot.2008.73
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. https://doi.org/10.1038/nmeth.2089
Serrano L, Halanych KM, Henry RP (2007) Salinity-stimulated changes in expression and activity of two carbonic anhydrase isoforms in the blue crab Callinectes sapidus. J Exp Biol 210:2320–2332. https://doi.org/10.1242/jeb.005041
Severino-Rodrigues E, Soares FC, Graça-Lopes R, Souza KH, Canéo VO (2009) Diversidade e biologia de espécies de Portunidae (Decapoda, Brachyura) no estuário de Iguape, Ilha Comprida e Cananéia, São Paulo, Brasil. Bol. Inst Pesca, São Paulo 35:47–60
Shinoda T, Ogawa H, Cornelius F, Toyoshima C (2009) Crystal structure of the sodium-potassium pump at 2.4 A resolution. Nature 459:446–450. https://doi.org/10.1038/nature07939
Silva ECC, Masui DC, Furriel RPM, Mantelatto FLM, McNamara JC, Barrabin H, Leone FA, Scofano HM, Fontes CFL (2008) Regulation by the exogenous polyamine spermidine of Na, K-ATPase activity from the gills of the euryhaline swimming crab Callinectes danae (Brachyura, Portunidae). Comp Biochem Physiol 149B:622–629. https://doi.org/10.1016/j.cbpb.2007.12.010
Silva ECC, Masui DC, Furriel RP, McNamara JC, Barrabin H, Scofano HM, Perales J, Teixeira-Ferreira A, Leone FA, Fontes CFL (2012) Identification of a crab gill FXYD2 protein and regulation of crab microsomal Na, K-ATPase activity by mammalian FXYD2 peptide. Biochim Biophys Acta 1818:2588–2597. https://doi.org/10.1016/j.bbamem.2012.05.009
Towle DW, Kays WT (1986) Basolateral localization of Na+, K+-ATPase in gill epithelium of two osmoregulating crabs, Callinectes sapidus and Carcinus maenas. J Exp Zool 239:311–318. https://doi.org/10.1002/jez.1402390302
Towle DW, Paulsen RS, Weihrauch D, Kordylewski M, Salvador C, Lignot JH, Pierrot CS (2001) Na+/K+-ATPase in gills of the blue crab Callinectes sapidus: cDNA sequencing and salinity-related expression of α-subunit mRNA and protein. J Exp Biol 204:4005–4012
Tsai JR, Lin HC (2007) V-type H1-ATPase e Na+, K+-ATPase in the gills of 13 euryhaline crabs during salinity acclimation. J Exp Biol 210:620–627. https://doi.org/10.1242/jeb.02684
Weihrauch D, McNamara JC, Towle DW, Onken H (2004a) Ion-motive ATPases and active, transbranchial NaCl uptake in the red freshwater crab, Dilocarcinus pagei (Decapoda, Trichodactylidae). J Exp Biol 207:4623–4631. https://doi.org/10.1242/jeb.01333
Weihrauch D, Morris S, Towle DW (2004b) Ammonia excretion in aquatic terrestrial crabs. J Exp Biol 207:4491–4504. https://doi.org/10.1242/jeb.01308
Acknowledgements
JCM and CDA are grateful to the Centro de Biologia Marinha, USP for access to laboratory facilities (Project #687), and thank the Instituto Chico Mendes de Conservação da Biodiversidade, Ministério do Meio Ambiente (permit #29594-9), and CGREP/IBAMA (02027.002342/98-04, permit #012/2007) for authorizing crab collections. This study derives in part from an undergraduate monograph presented by CDA to the Departamento de Biologia, FFCLRP, USP. FAL is grateful for support from the Instituto Nacional de Ciência e Tecnologia para Adaptações da Biota Aquática da Amazônia (INCT-ADAPTA II) and the Rede de Camarão da Amazônia.
Funding
This investigation was financed by research grants from the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP 2007/04870-9, 2013/22625-1, 2015/00131-3 and 2016/25336-0), Conselho de Desenvolvimento Científico e Tecnológico (CNPq 445078/2014-6 and 458246/2014-0) and in part by INCT ADAPTA II (CNPq 465540/2014-7) and the Fundação de Amparo à Pesquisa do Estado do Amazonas (FAPEAM 062.1187/2017). FAL (302072/2019-7) and JCM (303613/2017-3) received Excellence in Research scholarships from CNPq. CDA received a research scholarship from FAPESP (2007/50216-9), ROF from CNPq (400920/2015-8), MRP from CNPq (159886/2010-4) and LMF from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Finance code 001).
Author information
Authors and Affiliations
Contributions
All authors contributed to the conception and design of the study. Preparation of biological material, data collection and data analyses were performed by CDA, CMM, LMF, MRP, ROF, JCM, FAL and DPG. FAL, JCM, and DPG wrote the first draft of the manuscript. All authors contributed to subsequent versions and read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interests
The authors have no financial relationships with commercial entities that might have interests in the subject of this manuscript.
Human and animal rights
This investigation complies with all local, state, federal and international guidelines as regards the use of invertebrate animals in scientific research.
Additional information
Responsible Editor: A.E. Todgham.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Reviewers: J. Brown, C. M. Luquet and an undisclosed expert.
Rights and permissions
About this article
Cite this article
Garçon, D.P., Leone, F.A., Faleiros, R.O. et al. Osmotic and ionic regulation, and kinetic characteristics of a posterior gill (Na+, K+)-ATPase from the blue crab Callinectes danae on acclimation to salinity challenge. Mar Biol 168, 79 (2021). https://doi.org/10.1007/s00227-021-03882-3
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-021-03882-3