Changes in protein expression in the salt marsh mussel Geukensia demissa: Evidence for a shift from anaerobic to aerobic metabolism during prolonged aerial exposure

Journal of Experimental Biology

Volumn 217, Issue 9, 2014, Pages 1601-1612

  Fields, Peter A ^a   Eurich, Chris ^a,b   Gao, William L ^a   Cela, Bekim ^a  

^a FRANKLIN AND MARSHALL COLLEGE   (United States)

^b Science Department   (United States)

Author keywords

Air gaping; Emersion; Geukensia demissa; Hypoxia; Intertidal zone; Proteomics

Indexed keywords

PROTEIN; PROTEOME;

AEROBIC METABOLISM; ANAEROBIC GROWTH; ANIMAL; ANOXIA; BIVALVE; GILL; IMMERSION; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; TSUNAMI;

AEROBIOSIS; ANAEROBIOSIS; ANIMALS; ANOXIA; BIVALVIA; GILLS; IMMERSION; PROTEINS; PROTEOME; STRESS, PHYSIOLOGICAL; TIDAL WAVES;

EID: 84910001778     PISSN: 00220949     EISSN: 14779145     Source Type: Journal    
DOI: 10.1242/jeb.101758     Document Type: Article

References (72)

1. Almeida, E. A., Bainy, A. C. D., Dafre, A. L., Gomes, O. F., Medieros, M. H. G. and Di Mascio, P. (2005). Oxidative stress in digestive gland and gill of the brown mussel (Perna perna) exposed to air and re-submersed. J. Exp. Mar. Biol. Ecol. 318, 21-30.
2. Amos, L. A. (2008). The tektin family of microtubule-stabilizing proteins. Genome Biol. 9, 229.
3. Apraiz, I., Mi, J. and Cristobal, S. (2006). Identification of proteomic signatures of exposure to marine pollutants in mussels (Mytilus edulis). Mol. Cell. Proteomics 5, 1274-1285.
4. Arrigo, A. P. (1998). Small stress proteins: Chaperones that act as regulators of intracellular redox state and programmed cell death. Biol. Chem. 379, 19-26.
5. Barrett, J. (1991). Parasitic helminths. In Metazoan Life Without Oxygen (ed. C. Bryant), pp 146-164. London: Chapman and Hall.
6. Berth, M., Moser, F. M., Kolbe, M. and Bernhardt, J. (2007). The state of the art in the analysis of two-dimensional gel electrophoresis images. Appl. Microbiol. Biotechnol. 76, 1223-1243.
7. Bertness, M. D. (1984). Ribbed mussels and Spartina alterniflora production in a New England salt marsh. Ecology 65, 1794-1807.
8. Blackwell, J. F., Gainey, L. F., Jr and Greenbert, M. J. (1977). Shell ultrastructure in two subspecies of the ribbed mussel, Geukensia demissa (Dillwyn, 1817). Biol. Bull. 152, 1-11.
9. Calderwood, D. A. (2004). Integrin activation. J. Cell Sci. 117, 657-666.
10. Chuang, D. M., Hough, C. and Senatorov, V. V. (2005). Glyceraldehyde-3-phosphate dehydrogenase, apoptosis, and neurodegenerative diseases. Annu. Rev. Pharmacol. Toxicol. 45, 269-290.
11. Critchley, D. R. and Gingras, A. R. (2008). Talin at a glance. J. Cell Sci. 121, 1345-1347.
12. Dalle-Donne, I., Rossi, R., Milzani, A., Di Simplicio, P. and Colombo, R. (2001). The actin cytoskeleton response to oxidants: From small heat shock protein phosphorylation to changes in the redox state of actin itself. Free Radic. Biol. Med. 31, 1624-1632.
13. Danielsson, O., Atrian, S., Luque, T., Hjelmqvist, L., Gonzàlez-Duarte, R. and Jörnvall, H. (1994). Fundamental molecular differences between alcohol dehydrogenase classes. Proc. Natl. Acad. Sci. USA 91, 4980-4984.
14. Dawson, N. J. and Storey, K. B. (2011). Regulation of tail muscle arginine kinase by reversible phosphorylation in an anoxia-tolerant crayfish. J. Comp. Physiol. B 181, 851-859.
15. de Zwaan, A. and van Marrewijk, W. J. A. (1973). Anaerobic glucose degradation in the sea mussel Mytilus edulis L. Comp. Biochem. Physiol. 44B, 429-439.
16. De Zwaan, A. and Zandee, D. I. (1972). The utilization of glycogen and the accumulation of some intermediates during anaerobiosis in Mytilus edulis L. Comp. Biochem. Physiol. 43B, 47-54.
17. Dowd, W. W. and Somero, G. N. (2013). Behavior and survival of Mytilus congeners following episodes of elevated body temperature in air and seawater. J. Exp. Biol. 216, 502-514.
18. Ellington, W. R. (2001). Evolution and physiological roles of phosphagen systems. Annu. Rev. Physiol. 63, 289-325.
19. Fields, P. A., Zuzow, M. J. and Tomanek, L. (2012). Proteomic responses of blue mussel (Mytilus) congeners to temperature acclimation. J. Exp. Biol. 215, 1106-1116.
20. Fisher, A. B. (2011). Peroxiredoxin 6: A bifunctional enzyme with glutathione peroxidase and phospholipase A2 activities. Antioxid. Redox Signal. 15, 831-844.
21. Gäde, G. (1983). Energy metabolism of arthropods and mollusks during environmental and functional anaerobiosis. J. Exp. Zool. 228, 415-429.
22. Görg, A. (2004). 2-D Electrophoresis: Principles and Methods. Little Chalfont, UK: GE Healthcare.
23. Gosner, K. L. (1978). A Field Guide to the Atlantic Seashore. New York, NY: Houghton Mifflin Co.
24. Grieshaber, M. K., Hardewig, I., Kreutzer, U. and Pörtner, H.-O. (1994). Physiological and metabolic responses to hypoxia in invertebrates. Rev. Physiol. Biochem. Pharmacol. 125, 43-147.
25. Hara, M. R., Agrawal, N., Kim, S. F., Cascio, M. B., Fujimuro, M., Ozeki, Y., Takahashi, M., Cheah, J. H., Tankou, S. K., Hester, L. D. et al. (2005). Snitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding. Nat. Cell Biol. 7, 665-674.
26. Hayes, J. D., Flanagan, J. U. and Jowsey, I. R. (2005). Glutathione transferases. Annu. Rev. Pharmacol. Toxicol. 45, 51-88.
27. Helmuth, B., Mieszkowska, N., Moore, P. and Hawkins, S. J. (2006). Living on the edge of two changing worlds: Forecasting the responses of rocky intertidal ecosystems to climate change. Annu. Rev. Ecol. Evol. Syst. 37, 373-404.
28. Hermes-Lima, M. and Zenteno-Savín, T. (2002). Animal response to drastic changes in oxygen availability and physiological oxidative stress. Comp. Biochem. Physiol. 133C, 537-556.
29. Hilbish, T. J. (1987). Response of aquatic and aerial metabolic rates in the ribbed mussel Geukensia demissa (Dillwyn) to acute and prolonged changes in temperature. J. Exp. Mar. Biol. Ecol. 105, 207-218.
30. Ho, M.-S. and Zubkoff, P. L. (1982). Anaerobic metabolism of the ribbed mussel, Geukensia demissa. Comp. Biochem. Physiol. 73B, 931-936.
31. Hochachka, P. W. (1986). Defense strategies against hypoxia and hypothermia. Science 231, 234-241.
32. Hochachka, P. W. and Mustafa, T. (1972). Invertebrate facultative anaerobiosis. Science 178, 1056-1060.
33. Hochachka, P. W. and Somero, G. N. (2002). Biochemical Adaptation: Mechanism and Process in Physiological Evolution. Oxford: Oxford University Press.
34. Jordan, T. E. and Valiela, I. (1982). A nitrogen budget of the ribbed mussel, Geukensia demissa, and its significance in nitrogen flow in a New England salt marsh. Limnol. Oceanogr. 27, 75-90.
35. Jost, J. and Helmuth, B. (2007). Morphological and ecological determinants of body temperature of Geukensia demissa, the Atlantic ribbed mussel, and their effects on mussel mortality. Biol. Bull. 213, 141-151.
36. Kaiser, R., Fernández, M. R., Parés, X. and Jörnvall, H. (1993). Origin of the human alcohol dehydrogenase system: Implications from the structure and properties of the octopus protein. Proc. Natl. Acad. Sci. USA 90, 11222-11226.
37. Kanwisher, J. W. (1955). Freezing in intertidal animals. Biol. Bull. 109, 56-63.
38. Kluytmans, J. H., Bont, A. M. T. D., Janus, J. and Wijsman, T. C. M. (1977). Timedependent changes and tissue specificities in accumulation of anaerobic fermentation products in sea mussel Mytilus edulis L. Comp. Biochem. Physiol. 58B, 81-87.
39. Kotchoni, S. O., Kuhns, C., Ditzer, A., Kirch, H.-H. and Bartels, D. (2006). Overexpression of different aldehyde dehydrogenase genes in Arabidopsis thaliana confers tolerance to abiotic stress and protects plants against lipid peroxidation and oxidative stress. Plant Cell Environ. 29, 1033-1048.
40. Kuenzler, E. J. (1961). Structure and energy flow of a mussel population in a Georgia salt marsh. Limnol. Oceanogr. 6, 191-204.
41. Kültz, D. (2005). Molecular and evolutionary basis of the cellular stress response. Annu. Rev. Physiol. 67, 225-257.
42. Lent, C. M. (1968). Air-gaping by the ribbed mussel, Modiolus demissus (Dillwyn): Effects and adaptive significance. Biol. Bull. 134, 60-73.
43. Lent, C. M. (1969). Adaptations of the ribbed mussel, Modiolus demissus (Dillwyn), to the intertidal habitat. Am. Zool. 9, 283-292.
44. Lin, J. (1989). Influence of location in a salt marsh on survivorship of ribbed mussels. Mar. Ecol. Prog. Ser. 56, 105-110.
45. Lin, M.-C., Galletta, B. J., Sept, D. and Cooper, J. A. (2010). Overlapping and distinct functions for cofilin, coronin and Aip1 in actin dynamics in vivo. J. Cell Sci. 123, 1329-1342.
46. Liu, L., Hausladen, A., Zeng, M., Que, L., Heitman, J. and Stamler, J. S. (2001). A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature 410, 490-494.
47. Loomis, S. H. and Zinser, M. (2001). Isolation and identification of an ice-nucleating bacterium from the gills of the intertidal bivalve mollusc Geukensia demissa. J. Exp. Mar. Biol. Ecol. 261, 225-235.
48. Malanga, C. J. and Aiello, E. L. (1972). Succinate metabolism in the gills of the mussels Modiolus demissus and Mytilus edulis. Comp. Biochem. Physiol. 43B, 795-806.
49. Müller, M., Mentel, M., van Hellemond, J. J., Henze, K., Woehle, C., Gould, S. B., Yu, R. Y., van der Giezen, M., Tielens, A. G. M. and Martin, W. F. (2012). Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol. Mol. Biol. Rev. 76, 444-495.
50. Nicastro, K. R., Zardi, G. I., McQuaid, C. D., Stephens, L., Radloff, S. and Blatch, G. L. (2010). The role of gaping behaviour in habitat partitioning between coexisting intertidal mussels. BMC Ecol. 10, 17.
51. Nicchitta, C. V. and Ellington, W. R. (1983). Energy metabolism during air exposure and recovery in the high intertidal bivalve mollusk Geukensia demissa granosissima and the subtidal bivalve mollusc Modiolus squamosus. Biol. Bull. 165, 708-722.
52. Ono, S. (2003). Regulation of actin filament dynamics by actin depolymerizing factor/cofilin and actin-interacting protein 1: New blades for twisted filaments. Biochemistry 42, 13363-13370.
53. Pirner, M. A. and Linck, R. W. (1994). Tektins are heterodimeric polymers in flagellar microtubules with axial periodicities matching the tubulin lattice. J. Biol. Chem. 269, 31800-31806.
54. Sagarin, R. D., Barry, J. P., Gliman, S. E. and Baxter, C. H. (1999). Climate-related change in an intertidal community over short and long time scales. Ecol. Monogr. 69, 465-490.
55. Schremer, B., Manevisch, Y., Feinstein, S. I. and Fisher, A. B. (2007). Peroxiredoxins in the lung with emphasis on peroxiredoxin VI. In Subcellular Biochemistry: Peroxidredoxin Systems, Vol. 44 (ed. L. Flohé and J. R. Harris), pp. 317-344. Amsterdam: Springer.
56. Sen, N., Hara, M. R., Kornberg, M. D., Cascio, M. B., Bae, B.-I., Shahani, N., Thomas, B., Dawson, T. M., Dawson, V. L., Snyder, S. H. et al. (2008). Nitric oxide-induced nuclear GAPDH activates p300/CBP and mediates apoptosis. Nat. Cell Biol. 10, 866-873.
57. Seo, J., Jeong, J., Kim, Y. M., Hwang, N., Paek, E. and Lee, K.-J. (2008). Strategy for comprehensive identification of post-translational modifications in cellular proteins, including low abundant modifications: Application to glyceraldehyde-3-phosphate dehydrogenase. J. Proteome Res. 7, 587-602.
58. Smith, J. M. and Frey, R. W. (1985). Biodeposition by the ribbed mussel Geukensia demissa in a salt marsh, Sapelo Island, Georgia. J. Sediment. Petrol. 55, 817-828.
59. Somero, G. N. (2012). The physiology of global change: Linking patterns to mechanisms. Ann. Rev. Mar. Sci. 4, 39-61.
60. Stillman, J. H. (2002). Causes and consequences of thermal tolerance limits in rocky intertidal porcelain crabs, genus petrolisthes. Integr. Comp. Biol. 42, 790-796.
61. Stillman, J. H. (2003). Acclimation capacity underlies susceptibility to climate change. Science 301, 65-65.
62. Storey, K. B. and Storey, J. B. (2005). Oxygen limitation and metabolic rate depression. In Functional Metabolism: Regulation and Adaptation (ed. K. B. Storey), pp. 415-442. Hoboken, NJ: John Wiley & Sons, Inc.
63. Tisdale, E. J. (2002). Glyceraldehyde-3-phosphate dehydrogenase is phosphorylated by protein kinase Ciota/lambda and plays a role in microtubule dynamics in the early secretory pathway. J. Biol. Chem. 277, 3334-3341.
64. Tomanek, L. and Somero, G. N. (1999). Evolutionary and acclimation-induced variation in the heat-shock responses of congeneric marine snails (genus Tegula) from different thermal habitats: Implications for limits of thermotolerance and biogeography. J. Exp. Biol. 202, 2925-2936.
65. Tomanek, L. and Zuzow, M. J. (2010). The proteomic response of the mussel congeners Mytilus galloprovincialis and M. trossulus to acute heat stress: Implications for thermal tolerance limits and metabolic costs of thermal stress. J. Exp. Biol. 213, 3559-3574.
66. Van Hellemond, J. J. and Tielens, A. G. M. (1994). Expression and functional properties of fumarate reductase. Biochem. J. 304, 321-331.
67. Venkatesan, B., Mahimainathan, L., Das, F., Ghosh-Choudhury, N. and Ghosh Choudhury, G. (2007). Downregulation of catalase by reactive oxygen species via PI 3 kinase/Akt signaling in mesangial cells. J. Cell. Physiol. 211, 457-467.
68. Welker, A. F., Moreira, D. C., Campos, E. G. and Hermes-Lima, M. (2013). Role of redox metabolism for adaptation of aquatic animals to drastic changes in oxygen availability. Comp. Biochem. Physiol. 165A, 384-404.
69. Widdows, J., Bayne, B. L., Livingstone, D. R., Newell, R. I. E. and Donkin, P. (1979). Physiological and biochemical responses of bivalve molluscs to exposure to air. Comp. Biochem. Physiol. 62A, 301-308.
70. Zheng, L., Roeder, R. G. and Luo, Y. (2003). S phase activation of the histone H2B promoter by OCA-S, a coactivator complex that contains GAPDH as a key component. Cell 114, 255-266.
71. Zheng, Y., Zhao, L., Gao, J. and Fei, Z. (2011). iAssembler: A package for de novo assembly of Roche-454/Sanger transcriptome sequences. BMC Bioinformatics 12, 453-461.
72. Zhou, S., Lien, Y.-C., Shuvaeva, T., DeBolt, K., Feinstein, S. I. and Fisher, A. B. (2013). Functional interaction of glutathione S-transferase pi and peroxiredoxin 6 in intact cells. Int. J. Biochem. Cell Biol. 45, 401-407.