Effects of elevated seawater pCO2 on gene expression patterns in the gills of the green crab, Carcinus maenas

BMC Genomics

Volumn 12, Issue , 2011, Pages

  Fehsenfeld, Sandra ^a,b   Kiko, Rainer ^b   Appelhans, Yasmin ^b   Towle, David W ^c   Zimmer, Martin ^b,d   Melzner, Frank ^b  

^a UNIVERSITY OF MANITOBA   (Canada)

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

^c MOUNT DESERT ISLAND BIOLOGICAL LABORATORY   (United States)

^d UNIVERSITY OF SALZBURG   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ACTIVATED CHLORIDE CHANNEL; CARBON DIOXIDE; CHLORIDE CHANNEL; CYCLIC NUCLEOTIDE GATED CHANNEL; INTEGRIN; POTASSIUM CHANNEL; SEA WATER; SYNTAXIN; TETRASPANIN; UNCLASSIFIED DRUG; BICARBONATE CHLORIDE ANTIPORTER; MEMBRANE PROTEIN;

ACID BASE BALANCE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CARBON DIOXIDE TENSION; CARCINUS MAENAS; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; CRAB; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL IMPACT; ENVIRONMENTAL STRESS; EPITHELIUM CELL; GENE CONTROL; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE LOCATION; GENETIC TRANSCRIPTION; GILL; HYPERPOLARIZATION; HYPOOSMOTIC STRESS; NONHUMAN; NUCLEOTIDE SEQUENCE; OSMOREGULATION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; REGULATORY MECHANISM; TRANSCRIPTION REGULATION; ANIMAL; BRACHYURA; CHEMISTRY; GAS; GENETICS; METABOLISM;

CARCINUS MAENAS; DECAPODA (CRUSTACEA);

ANIMALS; BRACHYURA; CARBON DIOXIDE; CHLORIDE CHANNELS; CHLORIDE-BICARBONATE ANTIPORTERS; GASES; GENE EXPRESSION PROFILING; GILLS; INTEGRINS; MEMBRANE PROTEINS; POTASSIUM CHANNELS; SEAWATER; TETRASPANINS;

EID: 80053559458     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-12-488     Document Type: Article

References (83)

1. Caldeira K. Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. Journal of Geophysical Research 2005, 110(C9):1-12.
2. IPCC Climate Change 2007: The Physical Science Basis. Changes 2007, 1-21. IPCC.
3. Tripati AK, Roberts CD, Eagle RA. Coupling of CO2 and Ice Cheet Stability Over Major Climate Transitions of the Last 20 Million Years. Science 2009, 326:1394-1397. 10.1126/science.1178296, 19815724.
4. Fabry V, Seibel B, Feely R, Orr J. Impacts of ocean acidification on marine fauna and ecosystem processes. ICES Journal of Marine Science 2008, 65:414-432.
5. Melzner F, Gutowska M, Langenbuch M, et al. Physiological basis for high CO2 tolerance in marine ectothermic animals: pre-adaptation through lifestyle and ontogeny?. Biogeosciences 2009, 6:4993-4738.
6. Doney SC, Fabry VJ, Feely RA, Kleypas JA. Ocean acidification: the other CO2 problem. Annual Review of Marine Science 2009, 169-192.
7. Kroecker KJ, Kordas RL, Crim RN, Singh GG. Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecology Letters 2010, 13:1419-1434. 10.1111/j.1461-0248.2010.01518.x, 20958904.
8. Michaelidis B, Ouzounis C, Paleras A, Pörtner H. Effects of long-term moderate hypercapnia on acid-base balance and growth rate in marine mussels Mytilus galloprovincialis. Marine Ecology Progress Series 2005, 293:109-118.
9. Kurihara H. Effects of CO2-driven ocean acidification on the early developmental stages of invertebrates. Marine Ecology Progress Series 2008, 373:275-284.
10. Munday PL, Jones GP, Pratchett MS, Williams AJ. Climate change and the future for coral reef fishes. Fish and Fisheries 2008, 9:261-285.
11. Munday PL, Dixsona DL, Donelsona JM, Jonesa GP, Pratchett MS, Devitsina GV, Døving KB. Ocean acidification impairs olfactory discrimination and homing ability of a marine fish. PNAS 2009, 106(6):1848-1852. 10.1073/pnas.0809996106, 2644126, 19188596.
12. Ries JB, Cohen AL, McCorkle DC. Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 2009, 37(12):1131-1134.
13. Thomsen J, Melzner F. Moderate seawater acidification does not elicit long-term metabolic depression in the blue mussel Mytilus edulis. Mar Biol 2010, 157:2667-2676.
14. Dupont S, Ortega-Martinez O, Thorndyke MC. Impact of near-future ocean acidification on echinoderms. Ecotoxicology 2010, 19:449-462. 10.1007/s10646-010-0463-6, 20130988.
15. Gutowska M, Melzner F, Pörtner H, Meier S. Cuttlebone calcification increases exposure to elevated seawater pCO2 in the cephalopod Sepia officinales. Marine Biology 2010, 157(7):1653-1663.
16. Checkley DM, Dickson AG, Takahashi M, Radich A, Eisenkolb N, Asch R. Elevated CO2 Enhances Otolith Growth in Young Fish. Science 2009, 324:1683. 10.1126/science.1169806, 19556502.
17. Truchot J. Blood acid-base changes during experimental emersion and reimmersion of the intertidal crab Carcinus maenas (L.). Respiration Physiology 1975, 23:351-360. 10.1016/0034-5687(75)90086-9, 238271.
18. Dejours P, Beekenkamp H. Crayfish respiration as a function of water oxygenation. Respiration Physiology 1977, 30:241-251. 10.1016/0034-5687(77)90033-0, 17899.
19. Thomsen J, Gutowska MA, Saphörster J, Heinemann A, Trübenbach K, Fietzke J, Hiebenthal C, Eisenhauer A, Körtzinger A, Wahl M, Melzner F. Calcifying invertebrates succeed in a naturally CO2 enriched coastal habitat but are threatened by high levels of future acidification. Biogeosciences 2010, 7:5119-5156.
20. Larsen B, Pörtner H, Jensen F. Extra- and intracellular acid-base balance and ionic regulation in cod (Gadus morhua) during combined and isolated exposures to hypercapnia and copper. Marine Biology 1997, 128(2):337-346.
21. Spicer JI, Raffo A, Widdicombe S. Influence of CO2-related seawater acidification on extracellular acid-base balance in the velvet swimming crab Necora puber. Marine Biology 2007, 151(3):1117-1125.
22. Gutowska M, Melzner F, Langenbuch M, et al. Acid-base regulatory ability of the cephalopod (Sepia officinalis) in response to environmental hypercapnia. Journal of Comparative Physiology, Part B 2009, 180(3):323-335.
23. Hu MY, Tseng Y-C, Stumpp M, Gutowska MA, Kiko R, Lucassen M, Melzner F. Elevated seawater pCO2 differentially affects branchial acid-base transporters over the course of development in the cephalopod Sepia officinalis. Am J Physiol Regul Integr Comp Physiol 2011, 300(5):R1100-R1114. 10.1152/ajpregu.00653.2010, 21307359.
24. Gilmour KM, Perry SF. Carbonic anhydrase and acid-base regulation in fish. The Journal of Experimental Biology 2009, 212:1647-1661. 10.1242/jeb.029181, 19448075.
25. Truchot J. Mechanisms of the compensation of blood respiratory acid-base disturbances in the shore crab, Carcinus maenas (L.). The Journal of Experimental Zoology 1979, 210(3):407-416.
26. Siebers D, Leweck K, Markus H, Winkler A. Sodium Regulation in the Shore Crab Carcinus maenas as Related to Ambient Salinity. Marine Biology 1982, 69:37-43.
27. Cieluch U, Anger K, Aujoulat F, Buchholz F, Charmantier-Daures M, Charmantier G. Ontogeny of osmoregulatory structures and functions in the green crab Carcinus maenas (Crustacea, Decapoda). The Journal of Experimental Biology 2004, 207(2):325-336. 10.1242/jeb.00759, 14668316.
28. Storey KB. Suspended animation: the molecular basis of metabolic depression. Canadian Journal of Zoology 1988, 66(1):124-132.
29. Dalla Via J, Van den Thillart G, Cattani O, De Zwaan A. Influence of long-term hypoxia exposure on the energy metabolism of Solea solea. II. Intermediary metabolism in blood, liver and muscle. Mar ecol Prog Ser 1994, 111(1-2):17-27.
30. Hochachka PW. Oxygen -A key regulatory metabolite in metabolic defense against hypoxia. Amer Zool 1997, 37:595-603.
31. Wu RSS. Hypoxia: from molecular responses to ecosystem responses. Marine Pollution Bulletin 2002, 45(1-12):35-45. 10.1016/S0025-326X(02)00061-9, 12398365.
32. Towle DW, Weihrauch D. Osmoregulation by Gills of Euryhaline Crabs: Molecular Analysis of Transporters. American Zoology 2001, 41(4):770-780.
33. Freire C, Onken H, McNamara J. A structure-function analysis of ion transport in crustacean gills and excretory organs. Comparative Biochemistry and Physiology, Part A 2008, 151(3):272-304.
34. Storey KB. Phosphofructokinase from foot muscle of the whelk, Busycotypus canaliculatum: Evidence for covalent modification of the enzyme during anaerobiosis. Archives of Biochemistry and Biophysics 1984, 235(2):665-672. 10.1016/0003-9861(84)90242-X, 6240229.
35. Rahman MS, Storey KB. Role of covalent modification in the control of glycolytic enzymes in response to environmental anoxia in goldfish. J Comp Physiol B 1988, 157:813-820.
36. Kotlyar S, Weihrauch D, Paulsen RS, Towle DW. Expression of arginine kinase enzymatic activity and mRNA in gills of the euryhaline crabs Carcinus maenas and Callinectes sapidus. The Journal of Experimental Biology 2000, 203:2395-2404. 31.
37. Towle DW, Henry RP, Terwilliger NB. Microarray-detected changes in gene expression in gills of green crabs (Carcinus maenas) upon dilution of environmental salinity. Comparative Biochemistry and Physiology, Part D 2011, 6(2):115-25.
38. Kültz D. Molecular and Evolutionary Basis of the Cellular Stress Response. Annu Rev Physiol 2005, 67:225-57. 10.1146/annurev.physiol.67.040403.103635, 15709958.
39. Dickson AG, Millero FJ. A comparison of the equilibrium-constants for the dissociation of carbonic-acid in seawater media. Deep-Sea Res 1987, 34:1733-1743.
40. Lewis E, Wallace DWR. Program Developed for CO2 System Calculations. ORNL/CDIAC-105. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy, Oak Ridge, Tennessee 1998,
41. Roy RN, Roy LN, Vogel KM, Porter-Moore C, Pearson T, Good CE, Millero FJ, Campbell DM. The dissociation constants of carbonic acid in seawater at salinities 5 to 45 and temperatures 0 to 45°C. Marine Chemistry 1993, 44:249-267.
42. Dickson AG. Standard potential of the reaction AgCls+1/2H2g = Ags+HClaq and the standard acidity constant of the ion HSO4- in synthetic sea-water from 273.15 K to 318.15 K. J Chem Thermodyn 1990, 22:113-127.
43. Blast2GO. , http://www.blast2go.org/
44. Conesa A, Götz S. Blast2GO Tutorial. Interface 2009, Valencia, Spain.
45. Jensen J, Ørntoft T. Normalization of real-time quantitative RT-PCR data: a model based variance estimation approach to identify genes suited for normalization - applied to bladder- and colon-cancer data-sets. Cancer Research 2004, (64):5245-5250.
46. Andersen CL, Jensen JL, Ørntoft TF. Normalization of Real-Time Quantitative Reverse Transcription-PCR Data: A Model-Based Variance Estimation Approach to Identify Genes Suited for Normalization, Applied to Bladder and Colon Cancer Data Sets. Cancer Res 2004, 64:5245-5250. 10.1158/0008-5472.CAN-04-0496, 15289330.
47. Cui X, Hwang JT, Qiu J, Blades NJ, Churchill GA. Improved statistical tests for differential gene expression by shrinking variance components estimates. Biostatistics 2005, 6:59-75. 10.1093/biostatistics/kxh018, 15618528.
48. Storey JD. A direct approach to false discovery rates. J R Stat Soc B 2002, 64:479-498.
49. Theede H, Ponat A, Hiroki K, Schlieper C. Studies on the resistance of marine bottom invertebrates to oxygen-deficiency and hydrogen sulphide. Marine Biol 1969, 2:325-337.
50. Compere P, Wanson S, Pequeux A, Gilles R, Goffinet G. Ultrastructural Changes in the Gill Epithelium of the Green Crab Carcinus maenas in Relation to the External Salinity. Tissue & Cell 1989, 21(2):299-318.
51. Langenbuch M, Poertner HO. Energy budget of hepatocytes from Antarctic fish (Pachycara brachycephalum and Lepidonotothen kempi) as a function of ambient CO2: pH-dependent limitations of cellular protein biosynthesis?. The Journal of experimental biology 2003, 206:3895-3903. 10.1242/jeb.00620, 14555731.
52. Deigweiher K, Koschnick N, Pörtner H, Lucassen M. Acclimation of ion regulatory capacities in gills of marine fish under environmental hypercapnia. Am J Physiol Regulatory Integrative Comp Physiol 2008, 295:R1660-R1670.
53. O'Donnell MJ, Todgham AE, Sewell MA, Hammond LM, Ruggiero K, Fangue NA, Zippay ML, Hofmann GE. Ocean acidification alters skeletogenesis and gene expression in larval sea urchins. Mar Ecol Prog Ser 2010, 398:157-171.
54. Feder ME, Hofmann GE. Heat shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 1999, 61:243-282. 10.1146/annurev.physiol.61.1.243, 10099689.
55. Amrani M, Corbett J, Boateng SY, Dunn MJ, Yacoub MH. Kinetics of Induction and Protective Effect of Heat-Shock Proteins After Cardioplegic Arrest. Ann Thorac Surg 1996, 61:1407-1411. 10.1016/0003-4975(96)00085-9, 8633950.
56. Tomanek L, Somero GN. Time Course and Magnitude of Synthesis of Heat-Shock Proteins in Congeneric Marine Snails (Genus Tegula) from Different Tidal Height. Physiological and Biochemical Zoology 2000, 73(2):249-256. 10.1086/316740, 10801403.
57. Yáñez-Mó M, Tejedor R, Rousselle P, Sánchez -Madrid F. Tetraspanins in intercellular adhesion of polarized epithelial cells: spatial and functional relationship to integrins and cadherins. Journal of Cell Science 2001, 114(Pt 3):577-87.
58. Berditchevski F. Complexes of tetraspanins with integrins: more than meets the eye. Journal of Cell Science 2001, 114(Pt 23):4143-51.
59. Zhang F, Kotha1 J, Jennings LK, Zhang XA. Tetraspanins and vascular functions. Cardiovascular Research 2009, 83:7-15. 10.1093/cvr/cvp080, 2695701, 19251723.
60. Tiwari-Woodruff SK, Buznikov AG, Vu TQ, et al. OSP/claudin-11 forms a complex with a novel member of the tetraspanin super family and beta1 integrin and regulates proliferation and migration of oligodendrocytes. The Journal of Cell Biology 2001, 153(2):295-305. 10.1083/jcb.153.2.295, 2169454, 11309411.
61. Takada Y, Ye X, Simon S. The integrins. Genome Biology 2007, 8:215. 10.1186/gb-2007-8-5-215, 1929136, 17543136.
62. Benghezal M, Cornillon S, Gebbie L, et al. Synergistic Control of Cellular Adhesion by Transmembrane 9 Proteins. Molecular Biology of the Cell 2003, 14:2890-2899. 10.1091/mbc.E02-11-0724, 165684, 12857872.
63. Bergeret E, Perrin J, Williams M, Grunwald D, Engel E, Thevenon D, Taillebourg E, Bruckert F, Cosson P, Fauvarque MO. TM9SF4 is required for Drosophila cellular immunity via cell adhesion and phagocytosis. Journal of Cell Science 2008, 121:3325-3334. 10.1242/jcs.030163, 18796536.
64. Jayasundara N, Towle DW, Weihrauch D, Spanings-Pierrot C. Gill-specific transcriptional regulation of Na+/K+-ATPase -subunit in the euryhaline shore crab Pachygrapsus marmoratus: sequence variants and promoter structure. The Journal of Experimental Biology 2007, 210:2070-2081. 10.1242/jeb.004309, 17562880.
65. Tsai J, Lin H. V-type H+-ATPase and Na+, K+-ATPase in the gills of 13 euryhaline crabs during salinity acclimation. The Journal of Experimental Biology 2007, 210(Pt 4):620-627.
66. Henry R, Gehnrich S, Weihrauch D, Towle D. Salinity-mediated carbonic anhydrase induction in the gills of the euryhaline green crab, Carcinus maenas. Comparative Biochemistry and Physiology, Part A 2003, 136:243-258.
67. Ramnanan CJ, Storey KB. Suppression of Na+/K+-ATPase activity during estivation in the land snail Otala lactea. J Exp Biol 2006, 209:677-688. 10.1242/jeb.02052, 16449562.
68. Diaz E, Schimmoller F, Pfeffer SR. A novel Rab9 effector required for endosome-to-TGN transport. J Cell Biol 1997, 138:283-290. 10.1083/jcb.138.2.283, 2138197, 9230071.
69. Schimmöller F, Díaz E, Mühlbauer B, Pfeffer SR. Characterization of a 76 kDa endosomal, multispanning membrane protein that is highly conserved throughout evolution. Gene 1998, 216(2):311-318. 10.1016/S0378-1119(98)00349-7, 9729438.
70. Weihrauch D, Ziegler A, Siebers D, Towle D. Active ammonia excretion across the gills of the green shore crab Carcinus maenas: participation of Na +/K + -ATPase, V-type H + -ATPase and functional microtubules. The Journal of Experimental Biology 2002, 205:2765-2775.
71. Suzuki M. The Drosophila tweety family: molecular candidates for large-conductance Ca2+-activated Cl- channels. Exp Physiol 2006, 91:141-147.
72. Hartzell CH, Yu K, Xiao Q, Chien LT, Qu Z. Anoctamin/TMEM16 family members are Ca2+-activated Cl- channels. J Physiol 2009, 587(10):2127-2139. 10.1113/jphysiol.2008.163709, 2697287, 19015192.
73. Hartzell C, Putzier I, Arreola J. Calcium-activated chloride channels. Annual Review of Physiology 2005, 67:719-58. 10.1146/annurev.physiol.67.032003.154341, 15709976.
74. Abdel-Ghany M, Cheng HC, Elble RC, Pauli BU. The Breast Cancer β4 Integrin and Endothelial Human CLCA2 Mediate Lung Metastasis. The journal of biological chemistry 2001, 276(6):25438-25446.
75. Eggermont J. Calcium-activated Chloride Channels: (Un)known, (Un)loved?. Proc Am Thorac Soc 2004, 22-27.
76. Hwang PP, Perry SF. Ionic and acid-base regulation. Fish Physiology 2010, 29:311-344.
77. Stevens DR, Seifert R, Bufe B, Müller F, Kremmer E, Gauss R, Meyerhoff W, Kaupp UB, Lindemann B. Hyperpolarization-activated channels HCN1 and HCN4 mediate responses to sour stimuli. Nature 2001, 413:631-635. 10.1038/35098087, 11675786.
78. Munsch T, Pape HC. Modulation of the hyperpolarization-activated cation current of rat thalamic relay neurones by intracellular pH. Journal of Physiology 1999, 519(2):493-504. 10.1111/j.1469-7793.1999.0493m.x, 2269522, 10457065.
79. Todgham AE, Hofmann GE. Transcriptomic response of sea urchin larvae Strongylocentrotus purpuratus to CO2-driven seawater acidification. J Exp Biol 2009, 212:2579-2594. 10.1242/jeb.032540, 19648403.
80. Ahearn GA, Mandal PK, Mandal A. Calcium regulation in crustaceans during the molt cycle: a review and update. Comparative Biochemistry and Physiology Part A 2004, 137:247-257.
81. Lucu C, Towle D. Na+ + K+ -ATPase in gills of aquatic crustacea. Comparative Biochemistry and Physiology, Part A 2003, 135:195-214.
82. Serrano L, Henry R. Differential expression and induction of two carbonic anhydrase isoforms in the gills of the euryhaline green crab, Carcinus maenas, in response to low salinity. Comparative Biochemistry and Physiology, Part D 2008, 3(2):186-193.
83. Burnett L, Dunn T, Infantino R. The Function of Carbonic Anhydrase in Crustacean Gills. Transport Processes, Iono- and Osmoregulation Heidelberg: Springer-Verlag 1985, 159-1. Gilles R, Gilles-Baillien M.