Elevated seawater pco2 differentially affects branchial acid-base transporters over the course of development in the cephalopod Sepia officinalis

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 300, Issue 5, 2011, Pages

  Hu, Marian Y ^a   Tseng, Yung Che ^b   Stumpp, Meike ^a   Gutowska, Magdalena A ^c   Kiko, Rainer ^a   Lucassen, Magnus ^d   Melzner, Frank ^a  

^a GEOMAR HELMHOLTZ CENTRE FOR OCEAN RESEARCH KIEL   (Germany)

^b INSTITUTE OF CELLULAR AND ORGANISMIC BIOLOGY   (Taiwan)

^c UNIVERSITY OF KIEL   (Germany)

^d ALFRED WEGENER INSTITUTE FOR POLAR AND MARINE RESEARCH   (Germany)

Author keywords

Acid base regulation; Embryonic development; Na+ K+ ATPase; Ocean acidification; SLC4 family

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ADENOSINE TRIPHOSPHATASE (POTASSIUM); MESSENGER RNA; SEA WATER; SODIUM CHLORIDE COTRANSPORTER;

ACCLIMATIZATION; ACID BASE BALANCE; ACIDIFICATION; ARTICLE; BLOOD PH; BODY GROWTH; CARBON DIOXIDE TENSION; CEPHALOPOD; CONTROLLED STUDY; CUTTLEFISH; DOWN REGULATION; EMBRYO (ANATOMY); GENE EXPRESSION; HATCHING; HOMEOSTASIS; HYPERCAPNIA; IMMUNOHISTOCHEMISTRY; LIFE CYCLE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SEA;

ACCLIMATIZATION; ACID-BASE EQUILIBRIUM; AGE FACTORS; ANIMALS; CARBON DIOXIDE; CARBONIC ANHYDRASE II; ELECTRON TRANSPORT COMPLEX IV; ENERGY METABOLISM; GILLS; HYDROGEN-ION CONCENTRATION; HYPERCAPNIA; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; ION TRANSPORT; PARTIAL PRESSURE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEAWATER; SEPIA; SODIUM-POTASSIUM-EXCHANGING ATPASE; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 79955766901     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00653.2010     Document Type: Article

References (89)

1. Arnold JM. Normal embryonic stages of the squid, Loligo pealii (Lesueur). Biol Bull 128: 24-32, 1965.
2. +-pump activity: pathways between receptors and effectors. News Physiol Sci 10: 253-259, 1995.
3. Boron WF. Acid-base transport by the renal proximal tubule. J Am Soc Nephrol 17: 2368-2382, 2006.
4. Boron WF. Regulation of intracellular pH. Adv Physiol Educ 28: 160-179, 2004.
5. 3 transport. J Gen Physiol 81: 53-94, 1983.
6. Caldeira K, Wickett ME. Anthropogenic carbon and ocean pH. Nature 425: 365, 2003.
7. Cameron JN, Iwama GK. Compensation of progressive hypercapnia in channel catfish and blue crabs. J Exp Biol 133: 183-197, 1987.
8. Chapelle S, Dandrifosse G, Zwingelstein G. Metabolism of phospholipids of anterior or posterior gills of the crab Eriocheir sinensis during the adaptation of this animal to media of various salinities. J Biochem 7: 343-351, 1976.
9. 2 enhances otolith growth in young fish. Science 324: 1683, 2009.
10. +-ATPase is initiated by phosphorylation of Ser-18 in the rat-subunit and is responsible for the decreased activity in epithelial cells. J Biol Chem 274: 1920-1927, 1999.
11. Choe KP, Evans DH. Compensation for hypercapnia by a euryhaline elasmobranch: effect of salinity and roles of gills and kidneys in fresh water. J Exp Zool A Comp Exp Biol 297: 52-63, 2003.
12. Claiborne JB, Evans DH. Acid-base balance and ion transfers in the spiny dogfish (Squalus acanthias) during hypercapnia-a role for ammonia excretion. J Exp Zool 261: 9-17, 1992.
13. Claiborne JB, Heisler N. Acid-base regulation and ion transfers in the carp (Cyprinus carpio) during and after exposure to environmental hypercapnia. J Exp Biol 108: 25-43, 1984.
14. Cronin ER, Seymour RS. Respiration of the eggs of the giant cuttlefish Sepia apama. Mar Biol 136: 863-870, 2000.
15. Deigweiher K, Koschnick N, Pörtner HO, Lucassen M. Acclimation of ion regulatory capacities in gills of marine fish under environmental hypercapnia. Am J Physiol Regul Integr Comp Physiol 295: R1660- R1670, 2008.
16. Dickson A, Millero F. A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Res A 34: 1733-1743, 1987.
17. 2 analysis: a method for the certification of total alkalinity. Mar Chem 80: 185-197, 2003.
18. 2 measurements. PICES Special Publication 3: 1-191, 2007.
19. Donaubauer HH. Sodium- and potassium-activated adenosine triphosphatase in the excretory organs of Sepia officinalis (Cephalopoda). Mar Biol 63: 143-150, 1981.
20. 2-driven ocean acidification radically affect larval survival and development in the brittlestar Ophiothrix fragilis. Mar Ecol Prog Ser 373: 285-294, 2008.
21. Dupont S, Ortega-Martinez O, Thorndyke MC. Impact of near-future ocean acidification on echinoderms. Ecotoxycology 19: 449-462, 2010.
22. 2-driven ocean acidification on invertebrates early life history-what we know, what we need to know and what we can do. Biogeosci 6: 3109-3131, 2009.
23. Evans DH, Piermarini PM, Choe KP. The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol Rev 85: 97-177, 2005.
24. Fabry VJ, Seibel BA, Feely RA, Orr JC. Impacts of ocean acidification on marine fauna and ecosystem processes. J Mar Sci 65: 414-432, 2008.
25. Febry R, Lutz P. Energy partitioning in fish: the activity-related cost of osmoregulation in a euryhaline cichlid. J Exp Biol 128: 63-85, 1987.
26. Feder ME, Walser JC. The biological limitations of transcriptomics in elucidating stress and stress responses. J Evol Biol 18: 901-910, 2005.
27. Feely RA, Sabine CL, Hernandez-Ayon JM, Ianson D, Hales B. Evidence for upwelling of corrosive "acidified" water onto the continental shelf. Science 320: 1490-1492, 2008.
28. Fioroni P. Our recent knowledge of the development of the cuttlefish (Sepia officinalis). Zool Anz 224: 1-25, 1990.
29. Fivelstad S, Olsen AB, Asgard T, Baeverfjord G, Rasmussen T, Vindheim T, Staffanson S. Long-term sublethal effects on carbon dioxide on Atlantic salmon smolts (Salmo solar L.): ion regulation, haematology, element composition, nephrocalcinosis and growth parameters. Aquaculture 215: 301-319, 2003.
30. Forsythe J, Lee P, Walsh L, Clark T. The effects of crowding on growth of the European cuttlefish, Sepia officinalis Linnaeus, 1758 reared at two temperatures. J Exp Mar Biol Ecol 269: 173-185, 2002.
31. Foss A, Rosnes BA, Oiestad V. Graded environmental hypercapnia in juvenile spotted wolffish (Anarhichas minor Olafson): effects on growth, food conversion efficiency and nephrocalcinosis. Aquaculture 220: 607-617, 2003.
32. Georgalis T, Perry SF, Gilmour KM. The role of branchial carbonic anhydrase in acid-base regulation in rainbow trout (Oncorhynchus mykiss). J Exp Biol 209: 518-530, 2006.
33. +-adenosine triphosphatase activities in gills of marine teleost fishes: changes with depth, size and locomotory activity level. Mar Biol 106: 315-321, 1990.
34. Gilmour KM, Perry SF. Carbonic anhydrase and acid-base regulation in fish. J Exp Biol 212: 1647-1661, 2009.
35. 2 excretion during early development in zebrafish Danio rerio. J Exp Biol 212: 3837-3845, 2009.
36. Goyal S, Vanden Heuvel G, Aronson PS. Renal expression of novel Na/H exchanger isoform NHE8. Am J Physiol Renal Physiol 284: F467-F473, 2003.
37. Grigoriou P, Richardson CA. Aspects of the growth of cultured cuttlefish Sepia officinalis (Linnaeus 1758). Aquacult Res 35: 1141-1148, 2004.
38. Grigoriou P, Richardson CA. The effect of ration size, temperature and body weight on specific dynamic action of the common cuttlefish Sepia officinalis. Mar Biol 154: 1085-1095, 2008.
39. Grosell M. Intestinal anion exchange in marine fish osmoregulation. J Exp Biol 209: 2813-2817, 2006.
40. 2. Mar Biol 156: 515-519, 2009.
41. Gutowska MA, Melzner F, Langenbuch M, Bock C, Claireaux G, Pörtner HO. Acid-base regulatory ability of the cephalopod (Sepia officinalis) in response to environmental hypercapnia. J Comp Physiol B180: 323-335, 2010.
42. 2 in the cephalopod Sepia officinalis. Mar Biol 157: 1653-1663, 2010.
43. 2. Mar Ecol Prog Ser 373: 303-309, 2008.
44. Henry RP. Multiple functions of carbonic anhydrase in the crustacean gill. J Exp Zool 248: 19-24, 1988.
45. Henry RP, Cameron JN. The role of carbonic anhydrase in respiration, ion regulation and acid-base balance in the aquatic crab Callinectes sapidus and the terrestrial crab Gecarcinus lateralis. J Exp Biol 103: 205-223, 1983.
46. Henry RP, Swenson ER. The distribution and physiological significance on carbonic anhydrase in vertebrate gas exchange organs. Resp Physiol 121: 1-12, 2000.
47. Hoppema JMJ. Carbon dioxide and oxygen disequilibrium in a tidal basin (Dutch wadden sea). Neth J Sea Res 31: 221-229, 1993.
48. Horng JL, Lin LY, Huang JC, Katoh F, Kaneko T, Hwang PP. Knockdown of V-ATPase subunit A (atp6v1a) impairs acid secretion and ion balance in zebrafish (Danio rerio). Am J Physiol Regul Integr Comp Physiol 292: R2068-R2076, 2007.
49. Hu MY, Sucré E, Charmantier-Daures M, Charmantier G, Lucassen M, Melzner F. Localization of ion regulatory epithelia in embryos and hatchlings of two cephalopods. Cell Tiss Res 441: 571-583, 2010.
50. Hwang PP. Ion uptake and acid secretion in zebrafish (Danio rerio). J Exp Biol 212: 1745-1752, 2009.
51. Hwang PP, Lee TH. New insights into fish ion regulation and mitochondrion- rich cells. Comp Biochem Physiol A 148: 479-497, 2007.
52. 2 and acidification in Japanese flounder (Paralichthys olivaceus). Mar Poll Bull 49: 1062-1065, 2004.
53. +)ATPase activity: head-group specificity and fatty acid fluidity. Biochim Biophys Acta 282: 277-292, 1972.
54. 2 on early development of the oyster Crassostrea gigas. Aquat Biol 1: 91-98, 2007.
55. 2 concentration on the egg production rate and early development of two marine copepods (Acartia steueri and Acartia erythraea). Mar Poll Bull 49: 721-727, 2004.
56. 2 on sea urchin early development. Mar Ecol Prog Ser 274: 161-169, 2004.
57. Lämmli UK. Cleavage of structural proteins during the assembly of the head of Bacteriophage T4. Nature 227: 680-685, 1970.
58. Larsen BK, Pörtner HO, Jensen FB. Extra- and intracellular acid-base balance and ionic regulation in cod (Gadus morhua) during combined and isolated exposures to hypercapnia and copper. Mar Biol 128: 337-346, 1997.
59. Lemaire J. Table de développement embryonaire de Sepia officinalis L (Mollusque Céphalopode). Bull Soc Zool Fr 95: 773-782, 1970.
60. 2 system calculations (ORNL/.CDIAC-105). Oak Ridge, TN: Oak Ridge National Laboratory, 1998.
61. Marsh AG, Leong PKK, Manahan DT. Gene expression and enzyme activities of the sodium pump during sea urchin development: implications for indices of physiological state. Biol Bull 199: 100-107, 2000.
62. Mehrbach C, Culberso C, Hawley J, Pytkowic R. Measurement of apparent dissociation constants of carbonic acid in seawter at atmospheric pressure. Limnol Oceanogr 18: 897-907, 1973.
63. 2. Aqua Toxicol 92: 30-37, 2009.
64. 2 tolerance in marine ectothermic animals: pre-adaptation through lifestyle and ontogeny? Biogeosciences 6: 2313-2331, 2009.
65. Meunier B, De Visser SP, Shaik S. Mechanism of oxidation reactions catalyzed by cytochrome P450 enzymes. Chem Rev 104: 3947-3980, 2004.
66. Moyes CD, LeMoine CMR. Control of muscle bioenergetic gene expression: implications for allometric scaling relationships of glycolytic and oxidative enzymes. J Exp Biol 208: 1601-1610, 2005.
67. Palacios E, Racotta IS. Salinity stress test and its relation to future performance and different physiological responses in shrimp postlarvae. Aquaculture 268: 123-135, 2007.
68. Pane EF, Barry JP. Extracellular acid-base regulation during short-term hypercapnia is effective in a shallow-water crab, but ineffective in a deep-sea crab. Mar Ecol Prog Ser 334: 1-9, 2007.
69. Pecl GT, Steer MA, Hodgson KE. The role of hatchling size in generating the intrinsic size-at-age variability of cephalopods: extending the Forsythe hypothesis. Mar Freshw Res 55: 387-394, 2004.
70. 2 excretion in fish: unanswered questions and emerging models. Resp Physiol Neurobiol 154: 199-215, 2006.
71. 3 cotransporter from the squid giant fiber lobe. Am J Physiol Cell Physiol 292: C2023-C2045, 2007.
72. Pörtner HO, Webber DM, Boutilier RG, O'Dor RK. Acid-base regulation in exercising squid (Illex illecebrosus, Loligo pealei). Am J Physiol Regul Integr Comp Physiol 261: R239-R246, 1991.
73. 2 concentrations: lessons from animal physiology and earth history. J Oceanograph 60: 705-718, 2004.
74. +-ATPase activity during estivation in the land snail Otala lactea. J Exp Biol 209: 677-688, 2006.
75. Schipp R, Mollenhauer S, Boletzky S. Electron microscopical and histochemical studies of differentiation and function of the cephalopod gill (Sepia officinalis L.). Zoomorph 93: 193-207, 1979.
76. +-adenosine triphosphatase in the mechanism of action of cardiac glycosides. J Pharmacol Exp Ther 168: 31-41, 1969.
77. +-ATPase expression in gills of Atlantic salmon (Salmo salar) during isolated and combined exposure to hypoxia and hypercapnia in fresh water. Zool Sci 18: 1199-1205, 2001.
78. Somero GN, Childress JJ. A violation of the metabolism-size scaling paradigm: activities of glycolytic enzymes in muscle increase in larger fish. Physiol Zool 53: 322-337, 1980.
79. 2-related seawater acidification on extracellular acid-base balance in the velvet swimming crab Necora puber. Mar Biol 151: 1117-1125, 2007.
80. 2 enriched coastal habitat but are threatened by high levels of future acidification. Biogeosciences 7: 5119-5156, 2010.
81. Toews DP, Holeton GF, Heisler N. Regulation of the acid-base status during environmental hypercapnia in the marine teleost fish Conger conger. J Exp Biol 107: 9-20, 1983.
82. Towle DW. Sodium pump sites in teleost gill: unmasking by detergent (Abstract). Am Zool 177: 877, 1977.
83. Tseng YC, Huang CJ, Chang JCH, Teng WY, Baba O, Fann MJ, Hwang PP. Glycogen phosphorylase in glycogen-rich cells is involved in the energy supply for ion regulation in fish gill epithelia. Am J Physiol Regul Integr Comp Physiol 293: R482-R491, 2007.
84. Turner N, Hulbert AJ, Else PL. Sodium pump molecular activity and membrane lipid composition in two disparate ectotherms, and comparison with endotherms. J Comp Physiol B 175: 77-85, 2004.
85. 3- exchanger from squid giant fiber lobe. Am J Physiol Cell Physiol 285: C771-C780, 2003.
86. Wagner CA, Finberg KE, Breton S, Marshanski V, Brown D, Geibel JP. Renal vacuolar-ATPase. Physiol Rev 84: 1263-1314, 2003.
87. Wang T, Yang CL, Abbiati T, Schultheis PJ, Shull GE, Giebisch G, Aronson PS. Mechanism of proximal tubule bicarbonate absorption in NHE3 null mice. Am J Physiol Renal Physiol 277: F298-F302, 1999.
88. Yang TH, Somero G. Activity of lactate dehydrogenase but not its concentration of messenger RNA increases with body size in barred sand bass, Paralabrax nebulifer (Teleostei). Biol Bull 191: 155-158, 1996.
89. Young RE, Vecchione M. Cephalopod gills. Tree of Life Web Project: http://www.tolweb.org/articles/?article_id4200. 2004.