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Phenotypic plasticity in gene expression and physiological response in red drum Sciaenops ocellatus exposed to a long-term freshwater environment

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Abstract

Red drum (Sciaenops ocellatus) is a euryhaline fish commonly found in the Gulf of Mexico and along the Atlantic coast of North America. Because of high commercial demand and its euryhaline characteristics, aquaculture of this species has diversified from marine to low-salinity aquaculture systems. In recent years, interest in the feasibility of producing red drum in inland freshwater systems has grown and this prompted us to investigate its osmoregulatory capacity after rearing for 8 months in a freshwater aquaculture system. We compared the activities of several genes and enzymes involved in the osmoregulatory process in freshwater-acclimatized (FW) and seawater (SW) red drum. The gene expression profiles were variable: the expression of genes encoding Na+/K+-ATPase (NKA) and the cystic fibrosis transmembrane regulator (CFTR) was slightly higher in SW than FW fish, while phosphoenolpyruvate carboxykinase (PEPCK) and the glucocorticoid receptor messenger RNA (mRNA) levels were higher in FW red drum. The total plasma K concentration was 60.3% lower, and gill NKA activity was 63.5% lower in FW than in SW fish. PEPCK activity was twofold higher in FW than in SW red drum. Similarly, liver glycogen was 60% higher in FW fish. In summary, both gene expression and the enzyme activity data support the phenotypic plasticity of red drum and suggest that the limited capacity for ion homeostasis observed, in particular the low plasma K concentration, was due to the composition of freshwater and does not necessarily reflect a physiological inability to osmoregulate.

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References

  • Araneda M, Pérez EP, Gasca-Leyva E (2008) White shrimp Penaeus vannamei culture in freshwater at three densities: condition state based on length and weight. Aquaculture 283:13–18. doi:10.1016/j.aquaculture.2008.06.030

    Article  Google Scholar 

  • Avarre JC, Dugué R, Alonso P, Diombokho A, Joffrois C, Faivre N, Cochet C, Durand JD (2014) Analysis of the black-chinned tilapia Sarotherodon melanotheron heudelotii reproducing under a wide range of salinities: from RNA-seq to candidate genes. Mol Ecol Res 14:139–149. doi:10.1111/1755-0998.12148

    Article  CAS  Google Scholar 

  • AVMA (American Veterinary Medical Association) (2013) Guidelines for the euthanasia of animals. American Veterinary Medical Association, Schaumburg

    Google Scholar 

  • Baginski ES, Slawa SM (1982) Calcium in biological fluids. In: Faulkner WR, Meites S (eds) Selected methods for the small clinical chemistry laboratory: selected methods of clinical chemistry. American Association for Clinical Chemistry, Washington, pp 125–129

    Google Scholar 

  • Barton BA, Iwama GK (1991) Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Annu Rev Fish Dis 1:3–26. doi:10.1016/0959-8030(91)90019-G

    Article  Google Scholar 

  • Barton BA, Ribas L, Acerete L, Tort L (2005) Effects of chronic confinement on physiological responses of juvenile gilthead sea bream, Sparus aurata L., to acute handling. Aquac Res 36:172–179. doi:10.1111/j.1365-2109.2004.01202.x

    Article  Google Scholar 

  • Bauer-Gottwein P, Gondwe BR, Charvet G, Marín LE, Rebolledo-Vieyra M, Merediz-Alonso G (2011) Review: the Yucatán Peninsula karst aquifer, Mexico. Hydrogeol J 19:507–524. doi:10.1007/s10040-010-0699-5

    Article  Google Scholar 

  • Beldade P, Mateus ARA, Keller RA (2011) Evolution and molecular mechanisms of adaptive developmental plasticity. Mol Ecol 20:1347–1363. doi:10.1111/j.1365-294X.2011.05016.x

    Article  PubMed  Google Scholar 

  • Berg PR, Jentoft S, Star B, Ring KH, Knutsen H, Lien S, Jakobsen KS, André C (2015) Adaptation to low salinity promotes genomic divergence in Atlantic cod (Gadus morhua L.) Genome Biol Evol 7:1644–1663. doi:10.1093/gbe/evv093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berry MN, Mazzachi RD, Pejakovic M, Peake MJ (1988) Enzymatic determination of sodium in serum. Clin Chem 34:2295–2298

    CAS  PubMed  Google Scholar 

  • Bilyk KT, DeVries AL (2011) Heat tolerance and its plasticity in Antarctic fishes. Comp Biochem Physiol A Mol Integr Physiol 158:382–390. doi:10.1016/j.cbpa.2010.12.010

    Article  PubMed  Google Scholar 

  • Bystriansky JS, Richards JG, Schulte PM, Ballantyne JS (2006) Reciprocal expression of gill Na+/K+-ATPase α- subunit isoforms α-1a and α-1b during seawater acclimation of three salmonid fishes that vary in their salinity tolerance. J Exp Zool 209:1848–1858. doi:10.1242/jeb.02188

    CAS  Google Scholar 

  • Bystriansky JS, Frick NT, Richards JG, Schulte PM, Ballantyne JS (2007) Wild Arctic char (Salvelinus alpines) upregulate gill Na+/K+-ATPase during freshwater migration. Physiol Biochem Zool 80:270–282. doi:10.1086/512982

    Article  CAS  PubMed  Google Scholar 

  • Chen K, Li E, Xu Z, Li T, Xu C, Qin JG, Chen L (2015) Comparative transcriptome analysis in the hepatopancreas tissue of Pacific white shrimp Litopenaeus vannamei fed different lipid sources at low salinity. PLoS One 10(12):e0144889. doi:10.1371/journal.pone.0144889

    Article  PubMed  PubMed Central  Google Scholar 

  • Cheng CJ, Kuo E, Huang CL (2013) Extracellular potassium homeostasis: insights from hypokalaemic periodic paralysis. Semin Nephrol 33:237–247. doi:10.1016/j.semnephrol.2013.04.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choi CY, Min BH, Jo PG, Chang YJ (2007) Molecular cloning of PEPCK and stress response of black porgy (Acanthopagrus schlegeli) to increased temperature in freshwater and seawater. Gen Comp Endocrinol 152:47–53. doi:10.1016/j.ygcen.2007.02.019

    Article  CAS  PubMed  Google Scholar 

  • Chomezynski P, Sacchi P (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156–159. doi:10.1006/abio.1987.9999

    Google Scholar 

  • Davis JT (1990) Red drum: biology and life history. Southern Regional Aquaculture Center, Publication 320, Stoneville, Mississippi

  • Duncan WP, Costa OTF, Araujo MLG, Fernandes MN (2009) Ionic regulation and Na+–K+-ATPase activity in gills and kidney of the freshwater stingray Paratrygon aiereba living in white and blackwaters in the Amazon basin. J Fish Biol 74:956–960. doi:10.1111/j.1095-8649.2008.02156.x

    Article  CAS  PubMed  Google Scholar 

  • Fast MD, Hosoya S, Johnson SC, Afonso LO (2008) Cortisol response and immune-related effects of Atlantic salmon (Salmo salar Linnaeus) subjected to short-and long-term stress. Fish Shellfish Immunol 24:194–204. doi:10.1016/j.fsi.2007.10.009

    Article  CAS  PubMed  Google Scholar 

  • Fordyce JA (2006) The evolutionary consequences of ecological interactions mediated through phenotypic plasticity. J ExpBiol 209:2377–2383. doi:10.1242/jeb.02271

    Google Scholar 

  • García-Tavera JL, Valdés-Lozano D, Poblete-Naredo I, Albores-Medina A, Zapata-Pérez O (2013) Bile benzo [a] pyrene concentration and hepatic CYP1A induction in hypoxic adult tilapia (Oreochromis niloticus). Chemosphere 92:16–23. doi:10.1016/j.chemosphere.2013.03.034

    Article  PubMed  Google Scholar 

  • Gullian M, Aramburu C, Sanders B, Lope R (2010) Viability of culturing pink shrimp Farfantepenaeus duorarum in low-salinity groundwater from the Yucatán Peninsula (SE, México). Aquaculture 302:202–207. doi:10.1016/j.aquaculture.2010.02.019

    Article  Google Scholar 

  • Gullian-Klanian M (2013) Physiological changes in the red drum after long-term freshwater acclimation. J Aquat Anim Health 25:131–141. doi:10.1080/08997659.2013.788582

    Article  CAS  PubMed  Google Scholar 

  • Gullian-Klanian M, Gerónimo-Alonso M (2015) Sensory characteristics and nutritional value of red drum Sciaenops ocellatus reared in freshwater and seawater conditions. Aquac Res 46:1550–1561. doi:10.1111/are.12307

    Article  CAS  Google Scholar 

  • Hanson RW, Reshef L (1997) Regulation of phosphoenolpyruvate carboxykinase (GTP) gene expression. Annu Rev Biochem 66:581–611. doi:10.1146/annurev.biochem.66.1.581

    Article  CAS  PubMed  Google Scholar 

  • Hasler CT, Donaldson MR, Sunder RP, Guimond E, Patterson DA, Mossop B, Hinch S, Cooke SJ (2011) Osmoregulatory, metabolic, and nutritional condition of summer-run male Chinook Salmon in relation to their fate and migratory behaviour in a regulated river. Endanger Species Res 14:79–89

    Article  Google Scholar 

  • Hsu HH, Lin LY, Tseng YC, Horng JL, Hwang PP (2014) A new model for fish ion regulation: identification of ionocytes in freshwater-and seawater-acclimated medaka (Oryzias latipes). Cell Tissue Res 357:225–243. doi:10.1007/s00441-014-1883-z

    Article  CAS  PubMed  Google Scholar 

  • Ip YK, Loong AM, Kuah JS, Sim EW, Chen XL, Wong WP, Lam SH, Delgado IL, Chew SF (2012) Roles of three branchial Na+-K+-ATPase α-subunit isoforms in freshwater adaptation, seawater acclimation, and active ammonia excretion in Anabas testudineus. Am J Physiol Regul Integr Comp Physiol 303:R112–R125. doi:10.1152/ajpregu.00618.2011

    Article  CAS  PubMed  Google Scholar 

  • Keppler D, Decker K (1974) Glycogen: determination with amyloglucosidase. In: Bergmeyer HU (ed) Methods of enzymatic Analysis. Verlag Chemie, Weinheim, pp 1127–1131

    Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J BiolChem 193:265–275

    CAS  Google Scholar 

  • Marshall WS (2002) Na+, Cl−, Ca2+ and Zn2+ transport by fish gills: retrospective review and prospective synthesis. J Exp Zool 293:264–283. doi:10.1002/jez.10127

    Article  CAS  PubMed  Google Scholar 

  • McCormick SD (1993) Methods for nonlethal gill biopsy and measurement of Na+,K+-ATPase activity. Can J Fish Aquat Sci 50:656–658

    Article  CAS  Google Scholar 

  • McCormick SD (1995) Hormonal control of gill Na+,K+-ATPase and chloride cell function. Fish Physiol 14:285–315. doi:10.1016/S1546-5098(08)60250-2

    Article  CAS  Google Scholar 

  • McCormick SD (2001) Endocrine control of osmoregulation in teleost fish. Am Zool 41:781–794. doi:10.1668/0003-1569(2001)041[0781:ECOOIT]2.0.CO;2

    CAS  Google Scholar 

  • McCormick SD, Regish AM, Christensen AK (2009) Distinct freshwater and seawater isoforms of Na+/K+-ATPase in gill chloride cells of Atlantic salmon. J. Exp Biol 212:3994–3400. doi:10.1242/jeb.037275

    Article  CAS  Google Scholar 

  • Miller SH, Morgan SG (2013) Phenotypic plasticity in larval swimming behaviour in estuarine and coastal crab populations. J Exp Mar Biol Ecol 449:45–50. doi:10.1016/j.jembe.2013.08.013

    Article  Google Scholar 

  • Mobasheri A, Avila J, Cózar-Castellano I, Brownleader MD, Trevan M, Francis MJ, Lamb JF, Martín-Vasallo P (2000) Na+,K+-ATPase isozyme diversity; comparative biochemistry and physiological implications of novel functional interactions. Biosci Rep 20:51–91. doi:10.1023/A:1005580332144

    Article  CAS  PubMed  Google Scholar 

  • Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish 9:211–268. doi:10.1023/A:1008924418720

    Article  Google Scholar 

  • Morgan JD, Iwama GK (1998) Salinity effects on oxygen consumption, gill Na+,K+-ATPase and ion regulation in juvenile coho salmon. J Fish Biol 53:1110–1119. doi:10.1111/j.1095-8649.1998.tb00467.x

    CAS  Google Scholar 

  • Nissling A, Kryvi H, Vallin L (1994) Variation in egg buoyancy of Baltic cod Gadus morhua and its implications for egg survival in prevailing conditions in the Baltic Sea. Mar Ecol Prog Ser 110:67–67

    Article  Google Scholar 

  • Perry SF (1997) The chloride cell: structure and function in the gills of freshwater fishes. Annu Rev Physiol 59:325–347. doi:10.1146/annurev.physiol.59.1.325

    Article  CAS  PubMed  Google Scholar 

  • Polakof S, Arjona FJ, Sangiao-Alvarellos S, Del Río MPM, Mancera JM, Soengas JL (2006) Food deprivation alters osmoregulatory and metabolic responses to salinity acclimation in gilthead sea bream Sparus auratus. J Comp Physiol B 176:441–452. doi:10.1007/s00360-006-0065-z

    Article  PubMed  Google Scholar 

  • Richards JG, Semple JW, Bystriansky JS, Schulte PM (2003) Na+/K+-ATPase α-isoform switching in gills of rainbow trout (Oncorhynchus mykiss) during salinity transfer. J Exp Biol 206:4475–4486. doi:10.1242/jeb.00701

    Article  CAS  PubMed  Google Scholar 

  • Scott GR, Schulte PM (2005) Intraspecific variation in gene expression after seawater transfer in gills of the euryhaline killifish Fundulus heteroclitus. Comp Biochem Physiol A Mol Integr Physiol 141:176–182. doi:10.1016/j.cbpb.2005.05.002

    Article  PubMed  Google Scholar 

  • Selvakumar S, Geraldine P (2003) Thermal modulation of pyruvate metabolism in the freshwater prawn Macrobrachium malcolmsonii: the role of lactate dehydrogenase. Fish Physiol Biochem 29:149–157. doi:10.1023/B:FISH.0000035935.33689.ea

    Article  CAS  Google Scholar 

  • Sigh J, Lindenstrøm T, Buchmann K (2004) Expression of pro-inflammatory cytokines in rainbow trout (Oncorhynchus mykiss) during an infection with Ichthyophthirius multifiliis. Fish Shellfish immunol 17:75–86. doi:10.1016/j.fsi.2003.12.005

    Article  CAS  PubMed  Google Scholar 

  • Singer TD, Raptis S, Sathiyaa R, Nichols JW, Playle RC, Vijayan MM (2007) Tissue-specific modulation of glucocorticoid receptor expression in response to salinity acclimation in rainbow trout. Comp Biochem Physiol B Biochem Mol Biol 146:271–278. doi:10.1016/j.cbpb.2006.11.010

    Article  PubMed  Google Scholar 

  • Snell-Rood EC, Van Dyken JD, Cruickshank T, Wade MJ, Moczek AP (2010) Toward a population genetic framework of developmental evolution: the costs, limits, and consequences of phenotypic plasticity. BioEssays 32:71–81. doi:10.1002/bies.200900132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sommer RJ, Ogawa A (2011) Hormone signaling and phenotypic plasticity in nematode development and evolution. Curr Biol 21:758–766. doi:10.1016/j.cub.2011.06.034

    Article  Google Scholar 

  • Taugbøl A, Junge C, Quinn TP, Herland A, Vøllestad LA (2014) Genetic and morphometric divergence in threespine stickleback in the Chignik catchment, Alaska. Ecol Evol 4:144–156. doi:10.1002/ece3.918

    Article  PubMed  Google Scholar 

  • Tietz NW (1995) Clinical guide to laboratory tests, 3rd edn. Saunders Company, Philadelphia

    Google Scholar 

  • Törnroos A, Bonsdorff E, Bremner J, Blomqvist M, Josefson AB, Garcia C, Warzocha J (2015) Marine benthic ecological functioning over decreasing taxonomic richness. J Sea Res 98:49–56. doi:10.1016/j.seares.2014.04.010

    Article  Google Scholar 

  • Tresguerres M, Katoh F, Orr E, Parks SK, Goss GG (2006) Chloride uptake and base secretion in freshwater fish: a transepithelial ion-transport metabolon? Physiol Biochem Zool 79:981–996. doi:10.1086/507658

    Article  CAS  PubMed  Google Scholar 

  • Vijayan MM, Leatherland JF (1990) High stocking density affects cortisol secretion and tissue distribution in brook charr, Salvelinus fontinalis. J Endocrinol 124:311–318

    Article  CAS  PubMed  Google Scholar 

  • Vijayan MM, Pereira C, Grau EG, Iwama GK (1997) Metabolic responses associated with confinement stress in tilapia: the role of cortisol. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 116:89–95. doi:10.1016/S0742-8413(96)00124-7

    Article  Google Scholar 

  • Vijayan MM, Raptis S, Sathiyaa R (2003) Cortisol treatment affects glucocorticoid receptor and glucocorticoid-responsive genes in the liver of rainbow trout. Gen Comp Endocrinol 132:256–263. doi:10.1016/S0016-6480(03)00092-3

    Article  CAS  PubMed  Google Scholar 

  • Watson CJ, Nordi WM, Esbaugh AJ (2014) Osmoregulation and branchial plasticity after acute freshwater transfer in red drum, Sciaenops ocellatus. Comp Biochem Physiol A Mol Integr Physiol 178:82–89. doi:10.1016/j.cbpa.2014.08.008

    Article  CAS  PubMed  Google Scholar 

  • Wendelaar-Bonga SE, Lock RAC (2008) The osmoregulatory system. In: Di Giulio RT, Hinton DE (eds) The toxicology of fishes. CRC Press-Taylor and Francis Group, Boca Raton, pp 401–415

    Chapter  Google Scholar 

  • Yokoi K (2002) Colorimetric determination of chloride in biological samples by using mercuric nitrate and diphenylcarbazone. Biol Trace Elem Res 85:87–94. doi:10.1385/BTER:85:1:87

    Article  CAS  PubMed  Google Scholar 

  • Young DS, Friedman RB (2001) Effects of disease on clinical laboratory tests, 4th edn. American Association for Clinical Chemistry Press, Washington, DC

    Google Scholar 

  • Zydlewski GB, Zydlewski J (2012) Gill Na+, K+-ATPase of Atlantic salmon smolts in freshwater is not a predictor of long-term growth in seawater. Aquaculture 362:121–126. doi:10.1016/j.aquaculture.2011.03.024

    Article  Google Scholar 

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Acknowledgements

I am grateful to Dr. J.C. Seijo from UMM for the support given to this research. This study followed the animal experimental use guidelines of the Mexican Official norm NOM-0.62-ZOO-1999 (http://www.fmvz.unam.mx/fmvz/principal/archivos/062ZOO.PDF) and the guidelines of the American Veterinary Medical Association (https://www.avma.org/KB/Policies/Documents/euthanasia.pdf).

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  1. Universidad Marista de Mérida, Periférico Norte Tablaje Catastral 13941 Carretera Mérida- Progreso, Post Office Box 97300, Mérida, Yucatán, Mexico

    Mariel Gullian Klanian & Miguel Angel Vela-Magaña

  2. CINVESTAV-IPN, Unidad Mérida Km 6 Antigua Carretera a Progreso, Cordemex, 97310, Mérida, Yucatán, Mexico

    Omar Zapata Pérez

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  1. Mariel Gullian Klanian
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Correspondence to Mariel Gullian Klanian.

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Gullian Klanian, M., Zapata Pérez, O. & Vela-Magaña, M.A. Phenotypic plasticity in gene expression and physiological response in red drum Sciaenops ocellatus exposed to a long-term freshwater environment. Fish Physiol Biochem 44, 73–85 (2018). https://doi.org/10.1007/s10695-017-0414-8

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