Scientia Marina, Vol 77, No 1 (2013)

Effect of environmental salinity and dopamine injections on key digestive enzymes in hepatopancreas of the euryhaline crab Cyrtograpsus angulatus (Decapoda: Brachyura: Varunidae)


https://doi.org/10.3989/scimar.03687.09D

María Soledad Michiels
Departamento de Biología, Facultad de Ciencias Exactas y Naturales, Instituto de Investigaciones Marinas y Costeras IIMyC-CONICET, Universidad Nacional de Mar del Plata - Consejo Nacional de Investigaciones Científicas y Tecnológias (CONICET) , Argentina

Juana Cristina del Valle
Departamento de Biología, Facultad de Ciencias Exactas y Naturales, Instituto de Investigaciones Marinas y Costeras IIMyC-CONICET, Universidad Nacional de Mar del Plata , Argentina

Alejandra Antonia López Mañanes
Departamento de Biología, Facultad de Ciencias Exactas y Naturales, Instituto de Investigaciones Marinas y Costeras IIMyC-CONICET, Universidad Nacional de Mar del Plata - Consejo Nacional de Investigaciones Científicas y Tecnológias (CONICET) , Argentina

Abstract


We studied the occurrence and characteristics of lipase activity and the response of lipase and proteolytic activity to salinity and dopamine injections in hepatopancreas of the euryhaline crab (Cyrtograpsus angulatus). Lipase activity was maximal at pH 8.5; it exhibited Michaelis-Menten kinetics (apparent Km=0.019 mM), was higher at 37°C and appeared to be cold tolerant, being also high at 4°C. In 10 psu (hyper-regulation conditions), lipase and proteolytic activity were about 3 and 5 times higher, respectively, than in 35 psu (osmoconformation). In 40 psu (hypo-regulation), lipase activity was about three times higher than in 35 psu, while proteolytic activity was similar. Lipase activity was inhibited in vivo by 10–4 M dopamine in 35 psu but not in 10 or 40 psu. Proteolytic activity was not affected by 10–4 M dopamine. The differential responses of lipase and proteolytic activity to salinity and dopamine suggest the occurrence of distinct digestive adjustments and mechanisms of regulation upon osmoregulatory conditions. This study contributes to a better understanding of the complexity of the biochemical adaptations to salinity in euryhaline crabs. The fact that higher digestive enzyme activities could be associated with a differential digestive capacity potentially leading to enhanced availability of energy substrates is discussed.

Keywords


Cyrtograpsus angulatus; euryhaline crabs; salinity; hepatopancreas; digestive enzymes; dopamine; Mar Chiquita lagoon

Full Text:


PDF

References


Anger K. 2001. The Biology of Decapod Crustacean Larvae. Crustacean issues 14: 1-420.

Asaro A., del Valle J.C., López Mañanes A. 2011. Amylase, maltase and sucrase activities in hepatopancreas of the euryhaline crab Neohelice granulata (Decapoda: Brachyura: Varunidae): partial characterization and response to low environmental salinity. Sci. Mar. 75(3): 517-524. http://dx.doi.org/10.3989/scimar.2011.75n3517

Asaro A., del Valle J.C., López Mañanes A.A.2012. Responses to salinity in Cyrtograpsus angulatus: Osmoregulation and energy stores XIII Congress – XXXI Annual Meeting Rosario Society Biology. Biocell. 35(1): 67.

Bianchini A., Machado Lauer M., Nery L., Pinto Colares E., Monserrat J.M., dos Santos Filho E.A. 2008. Biochemical and physiological adaptations in the estuarine crab Neohelice granulata during salinity acclimation. Comp. Biochem. Physiol. A. 151: 423-436 http://dx.doi.org/10.1016/j.cbpa.2007.12.001 PMid:18243742

Botto F., Valiela I., Iribarne O., Martinetto P, Alberti J. 2005. Impact of burrowing crabs on C and N sources, control and transformations in sediments and food webs of SW Atlantic estuaries. Mar. Ecol. Prog. Ser. 293: 155-164. http://dx.doi.org/10.3354/meps293155

Bradford M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein-dye binding. Anal. Biochem. 72: 248-254. http://dx.doi.org/10.1016/0003-2697(76)90527-3

Cherif S., Fendri A., Miled N., Trabelsi H., Mejdoub H., Gargouri Y., 2007. Crab digestive lipase acting at high temperature: purification and biochemical characterization. Biochimie 89(8): 1012-1018. http://dx.doi.org/10.1016/j.biochi.2007.02.005 PMid:17395356

Cherif S., Gargouri Y. 2009. Thermoactivity and effects of organic solvents on digestive lipase from hepatopancreas of the green crab. Food Chem. 116: 82-86 http://dx.doi.org/10.1016/j.foodchem.2009.02.009

Clark M.C., Khan R., Baro D.J. 2008. Crustacean dopamine receptors: localization and G protein coupling in the stomatogastric ganglion. J. Neurochem. 104: 1006-1019 http://dx.doi.org/10.1111/j.1471-4159.2007.05029.x PMid:17986222

Christie A.E. 2011. Crustacean neuroendocrine systems and their signaling agents. Cell Tissue Res. 345: 41-67. http://dx.doi.org/10.1007/s00441-011-1183-9 PMid:21597913

del Valle J.C., Panzeri A., López Mañanes A.A. 2012. Glucose homeostasis in the euryhaline crab Cyrtograpsus angulatus from Mar Chiquita coastal lagoon: regulation by dopamine XIII Congress – XXXI Annual Meeting Rosario Society Biology. Biocell. 35(1): 66.

Figueiredo M.S.R.B., Anderson A.J. 2009. Digestive enzyme spectra in crustacean decapods (Paleomonidae, Portunidae and Penaeidae) feeding in the natural habitat. Aquac. Res. 40(3): 282-291. http://dx.doi.org/10.1111/j.1365-2109.2008.02087.x

Fingerman M., Nagabhushanam R., Sarojini R., Palla Reddy, S. 1994. Biogenic Amines in Crustaceans: Identification, Localization, and Roles. J. Crustac. Biol. 14(3): 413-437 http://dx.doi.org/10.2307/1548990

Freese D., Kreibich T., Niehoff B. 2012. Characteristics of digestive enzymes of calanoid copepod species from different latitudes in relation to temperature, pH and food. Comp Biochem Physiol . B. 162(4): 66-72. http://dx.doi.org/10.1016/j.cbpb.2012.04.007 PMid:22561197

Freire C.A., Onken H., McNamara J.C. 2008. A structure function analysis of ion transport in crustacean gills and excretory or gans. Comp. Biochem. Physiol. A 151(3): 272-304. http://dx.doi.org/10.1016/j.cbpa.2007.05.008 PMid:17604200

Genovese G., Senek M., Ortiz N., Regueira M., Towle D.W., Tresguerres M., Luquet C.M. 2006. Dopaminergic regulation of ion transport in gills of the euryhaline semiterrestrial crab Chasmagnathus granulatus: interaction between D1- and D2- like receptors. J. Exp. Biol. 209: 2785-2793. http://dx.doi.org/10.1242/jeb.02308 PMid:16809469

Halperin J., Genovese G., Tresguerres M., Luquet C.M. 2004. Modulation of ion uptake across posterior gills of the crab Chasmagnathus granulatus by dopamine and cAMP. Comp. Biochem. Physiol. A 139: 103-109. http://dx.doi.org/10.1016/j.cbpb.2004.07.001 PMid:15471687

Hammer H.S., Bishop C.D, Watts S.A. 2003. The characterization of three digestive enzymes from the crayfish Procamabarus clarkii. J. Alabama Acad. Sci. 74(1): 47-59.

Hsieh S.L., Chen S.M., Yang Y.H., Ku C.M. 2006. Involvement of norepinephrine in the hyperglycemic responses of the freshwater giant prawn, Macrobrachium rosenbergii, under cold shock. Comp. Biochem. Physiol. A 143: 254-263. http://dx.doi.org/10.1016/j.cbpa.2005.12.009 PMid:16423547

Jahn M.P., Cavagni G.M., Kaiser D, Kucharski L.C. 2006. Osmotic effect of choline and glycine betaine on the gills and hepatopancreas of the Chasmagnathus granulata crab submitted to hyperosmotic stress J. Exp. Mar. Biol. Ecol. 334: 1-9. http://dx.doi.org/10.1016/j.jembe.2006.01.006

Kirschner L B. 2004. The mechanism of sodium chloride uptake in hyperregulating aquatic animals. J. Exp. Biol. 207: 1439-1452. http://dx.doi.org/10.1242/jeb.00907 PMid:15037638

Li E., Chen L., Zeng C., Yu N., Xiong Z., Chen X., Qin J.G. 2008. Comparison of digestive and antioxidant enzymes activities, haemolymph oxyhemocyanin contents and hepatopancreas histology of white shrimp, Litopenaeus vannamei, at various salinities. Aquaculture 274: 80-86. http://dx.doi.org/10.1016/j.aquaculture.2007.11.001

López Mañanes A.A. 2004. Effect of dopamine on glucose levels in hemolymph of Cyrtograpsus angulatus. Abstracts XXIII Annual Meeting Rosario Biology Society. Biocell. 28(2): 225.

López Mañanes A.A., Magnoni L.J., Goldemberg A.L. 2000. Branchial carbonic anhydrase (CA) of gills of Chasmagnathus granulata (Crustacea Decapoda). Comp. Biochem. Physiol. B 127(1): 85-95. http://dx.doi.org/10.1016/S0305-0491(00)00243-1

López Mañanes A.A., Meligeni C.D., Goldemberg A.L. 2002. Response to environmental salinity Na+/K+-ATPase activity in individual gills of the euryhaline crab Cyrtograpsus angulatus. J. Exp. Mar. Biol. Ecol. 274: 75-85. http://dx.doi.org/10.1016/S0022-0981(02)00166-1

Lorenzon S. 2005. Hyperglycemic stress response in Crustacea. ISJ 2: 132-141.

Luvizotto-Santos R., Lee J., Branco Z., Bianchini A., Nery L. 2003. Lipids as energy source during salinity acclimation in the euryhaline crab Chasmagnathus granulata (Crustacea-Grapsidae). J. Exp. Zool. A 295: 200-205.

Markweg H., Lang M.S., Wagner F. 1995. Decanoic acid inhibition of lipase from Acetinobacter sp. OPA 55. Enz. Microb. Tech. 17: 512-516. http://dx.doi.org/10.1016/0141-0229(94)00067-2

Martins T.L., Chittó A.L.F., Rossetti C.R., Brondani C.K., Kucharski L.C., Da Silva R.S.M. 2011. Effects of hypo- or hyperosmotic stress on lipid synthesis and gluconeogenic activity in tissues of the crab Neohelice granulate. Comp. Biochem. Physiol. A 158(4): 400-405. http://dx.doi.org/10.1016/j.cbpa.2010.11.023 PMid:21130893

McNamara J.C., Faria S.C. 2012. Evolution of osmoregulatory patterns and gill ion transport mechanisms in the decapod Crustacea: a review. J. Comp. Physiol. B. http://dx.doi.org/10.1007/s00360-012-0665-8 PMid:22534792

Michiels M.S., Pinoni S.A., del Valle J.C., López Mañanes A.A. 2011. Lipase activity in hepatopancreas of the euryhaline crab Neohelice granulata: response in relation to osmoregulatory status Abstracts XXVII Annual Scientific Meeting Tucumán Biology Association, Tucumán, Argentina. Biocell. 35(2): 163.

Mo J.L., Devos P., Trausch G.1998. Dopamine as a modulator of ionic transport and Na+/K+-ATPase activity in the gills of the Chinese crab Eriocheir sinensis. J. Crustac. Biol. 18: 442-448. http://dx.doi.org/10.2307/1549409

Morris S. 2001. Neuroendocrine regulation of osmoregulation and the evolution of air-breathing in decapod crustaceans. J. Exp. Biol. 204: 979-989. PMid:11171421

Pasquevich M.Y., Dreona M.S., Lavaría S., Heras H. 2011.Triacylglycerol catabolism in the prawn Macrobrachium borellii (Crustacea: Palaemoniade). Comp Biochem Physiol B. 160(4): 1-207. http://dx.doi.org/10.1016/j.cbpb.2011.08.006 PMid:21889599

Pavasovic A., Anderson A.J., Mather P.B., Richardson N.A. 2007. Influence of dietary protein on digestive enzyme activity, growth and tail muscle composition in redclaw crayfish, Cherax quadricarinatus. Aquac. Res. 38: 644-652. http://dx.doi.org/10.1111/j.1365-2109.2007.01708.x

Perera E., Rodríguez-Viera L., Rodríguez-Casariego J., Fraga I., Carrillo O., Martínez-Rodríguez G., Mancera J.M. 2012. Dietary protein quality differentially regulates trypsin enzymes at the secretion and transcription level in Panulirus argus by distinct signaling pathways. J Exp Biol. 215: 853-862 http://dx.doi.org/10.1242/jeb.063925 PMid:22323208

Pinoni S.A. 2009. Mecanismos de mantenimiento del medio interno en respuesta a estrés ambiental en crustáceos decápodos de interés regional. PhD thesis, Universidad Nacional de Mar del Plata. Mar del Plata.

Pinoni S.A., López Mañanes A.A. 2004. Alkaline Phosphatase activities with differential response to environmental salinity in muscle of Chasmagnathus granulata and Cyrtograpsus angulatus from Mar Chiquita coastal lagoon. Biocell. 28: 225.

Pinoni S.A., López Mañanes A.A. 2008. Partial characterization and response under hyperregulating conditions of Na+/K+-ATPase and levamisole-sensitive alkaline phosphatase activities in chela muscle of the euryhaline crab Cyrtograpsus angulatus. Sci. Mar. 72(1): 15-24

Pinoni S.A, López Mañanes A.A. 2009. Na+ATPase activities in chela muscle of the euryhaline crab Neohelice granulata: Differential response to environmental salinity. J. Exp. Mar. Biol. Ecol. 372(1-2): 91-97. http://dx.doi.org/10.1016/j.jembe.2009.02.012

Pinoni S.A., Iribarne O., López Mañanes A.A. 2011.Between-habitat comparison of digestive enzymes activities and energy reserves in the SW Atlantic euryhaline burrowing crab Neohelice granulata. Comp. Biochem. Physiol. A 158: 552-559. http://dx.doi.org/10.1016/j.cbpa.2010.12.020 PMid:21215323

Pinoni S.A., López Mañanes A.A. 2011. Biochemical and physiological flexibility in the euryhaline semiterrestrial crab Neohelice granulata from contrasting habitats. Abstracts XXVII Annual Scientific Meeting Tucumán Biology Association, Tucumán, Argentina Biocell. 134: 13-15.

Resch-Sedlmeier G., Sedlmeier D. 1999. Release of digestive enzymes from the crustacean hepatopancreas: effect of vertebrate gastrointestinal hormones. Comp. Biochem. Physiol. B 1(2): 187-192. http://dx.doi.org/10.1016/S0305-0491(99)00056-5

Romano N., Zeng C. 2012. Osmoregulation in decapod crustaceans: implications to aquaculture productivity, methods for potential improvement and interactions with elevated ammonia exposure. Aquaculture 334-337: 12-23. http://dx.doi.org/10.1016/j.aquaculture.2011.12.035

Sánchez-Paz A., García-Carreño F., Muhlia-Almazan A., Peregrino- Uriarte A., Yepiz-Plascencia J.Y.G. 2006. Usage of energy reserves in crustaceans during starvation: status and future directions. Insect. Biochem. Mol. Biol. 36: 241-249. http://dx.doi.org/10.1016/j.ibmb.2006.01.002 PMid:16551538

Schleich C.E., López Mañanes A.A., Goldemberg A.L. 1999. Regulación por mensajeros químicos de la actividad Na+-K+ ATPasa branquial de Chasmagnathus granulata (Crustacea Decápoda) de la laguna costera de Mar Chiquita (Pcia. de Buenos Aires) en condiciones de salinidad reducida. In: Trisierra, A.E., Aguilar, Z.G. (eds), COLACMAR, vol. 1. Culquichicón Malpica, Perú, pp. 529-530.

Schleich C.E., Goldemberg A.L., López Mañanes A.A. 2001. Salinity dependent Na+/K+-ATPase activity in gills of euryhaline crab Chasmagnathus granulatus. Gen. Physiol. Biophys. 20: 255-256. PMid:11765216

Smichi N., Fendri A., Zarai Z., Bouchaala E., Chérif S., Gargouri Y., Miled N. 2012. Lipolytic activity levels and colipase presence in digestive glands of some marine animals. Fish Physiol. Biochem. http://dx.doi.org/10.1007/s10695-012-9633-1 PMid:22457120

Spivak E. 1997. Cangrejos estuariales del Atlántico sudoccidental (25°-41°S) (Crustacea: Decapoda: Brachyura). Invest. Mar. Valparaíso. 25: 105-120.

Spivak E., Anger K., Luppi T., Bas C., Ismael D. 1994. Distribution and habitat preferences of two grapsid crab species in Mar Chiquita lagoon (Pcia. Bs As. Argentina). Helgolander Meeresun. 48: 59-78. http://dx.doi.org/10.1007/BF02366202




Copyright (c) 2013 Consejo Superior de Investigaciones Científicas (CSIC)

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.


Contact us scimar@icm.csic.es

Technical support soporte.tecnico.revistas@csic.es