Marine Biology

, Volume 126, Issue 1, pp 65–75 | Cite as

Interspecific variation in thermal denaturation of proteins in the congeneric musselsMytilus trossulus andM. galloprovincialis: evidence from the heat-shock response and protein ubiquitination

  • G. E. Hofmann
  • G. N. Somero


Individuals of two species of blue mussels,Mytilus trossulus (Gould, 1850) andM. galloprovincialis (Lamarck, 1819), that have different latitudinal distributions, were collected from two locations on the Pacific coast of the USA where their distributions do not overlap. To determine if the congeners were differentially sensitive to thermal stress, we first held individuals of each species at 13°C for 8 wk and then examined three biochemical indices of thermal damage to cellular proteins: relative levels of the stress protein hsp 70, quantities of ubiquitin conjugates and the induction of stress-protein synthesis. The results provide evidence that the northern species,M. trossulus, was more thermally sensitive than the southern species,M. galloprovincialis. Relative levels of hsp 70 and amounts of ubiquitin conjugates were higher in gill tissue fromM. trossulus than in gill fromM. galloprovincialis, which suggests thatM. trossulus was more susceptible to reversible and irreversible protein damage, respectively, thanM. galloprovincialis. In addition, the patterns of stress-protein expression as measured by in vitro radiolabeling experiments using isolated gill tissue, were significantly different, as follows: (1) the threshold induction temperatures for hsp 70 synthesis were 23 and 25°C forM. trossulus andM. galloprovincialis, respectively; (2) the overall intensity of synthesis and induction was greater inM. galloprovincialis than inM. trossulus, particularly at the higher incubation temperatures of 28 and 30°C; (3)M. galloprovincialis expressed a 30 kdalton, stress protein that was not induced in the northern species,M. trossulus. Thus, after an 8 wk exposure to a common temperature, the twoedulis-like mussel congeners appeared to be physiologically distinct with respect to thermal damage to proteins. Due to the energetic cost that is probably associated with environmentally-induced protein damage and maintaining pools of stress proteins, differential organismal thermotolerances and protein stabilites may contribute to setting species distribution-limits. Our data support conclusions of other workers thatM. trossulus is a more cold-adapted species thanM. galloprovincialis.


Stress Protein Thermal Damage Blue Mussel Gill Tissue Ubiquitin Conjugate 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Ananthan J, Goldberg AL, Voellmy R (1986) Abnormal proteins serve as eukaryotic stress signals and trigger the activation of heat shock genes. Science, NY 232: 522–524Google Scholar
  2. Becker J, Craig EA (1994) Heat-shock proteins as molecular chaperones. Eur J Biochem 219: 11–23Google Scholar
  3. Beckmann RP, Mizzen LE, Welch WJ (1990) Interaction of hsp70 with newly synthesized proteins: implications for protein folding and assembly. Science, NY 248: 850–854Google Scholar
  4. Beynon RJ, Bond JS (1986) Catabolism of intracellular proteins: molecular aspects. Am J Physiol 251: C141-C152Google Scholar
  5. Bond U, Agell N, Haas AL, Redman K, Schlesinger MJ (1988) Ubiquitin in stressed chicken embryo fibroblasts. J biol Chem 263: 2384–2388Google Scholar
  6. Bosch TCG, Krylow SM, Bode HR, Steele RE (1988) Thermotolerance and synthesis of heat shock proteins: these responses are present inHydra attenuata but absent inHydra oligactis. Proc natn Acad Sci USA 85: 7927–7931Google Scholar
  7. Chen Q, Lauzon LM, De Rocher AE, Vierling E (1990) Accumulation, stability and localisation of a major chloroplast heat-shock protein. J Cell Biol 110: 1873–1883Google Scholar
  8. Carlson N, Rogers S, Rechsteiner M (1987) Microinjection of ubiquitin: changes in protein degradation in HeLa cells subjected to heat-shock. J Cell Biol 104: 547–555Google Scholar
  9. Craig EA, Gross CA (1991) Is hsp70 the cellular thermometer? Trends biochem Sciences 16: 135–140Google Scholar
  10. Dahlhoff E, Somero GN (1993) Kinetic and structural adaptations of cytoplasmic malate dehydrogenases of eastern Pacific abalone (genusHaliotis) from different thermal habitats: biochemical correlates of biogeographical patterning. J exp Biol 185: 137–150Google Scholar
  11. Dietz TJ (1994) Acclimation of the threshold induction temperatures for 70-kDa and 90-kDa heat shock proteins in the fishGillichthys mirabilis. J exp Biol 188: 333–338Google Scholar
  12. Dietz TJ, Somero GN (1992) The threshold induction temperature of the 90-kDa heat shock protein is subject to acclimatization in eurythermal goby fishes (genusGillichthys). Proc natn Acad Sci USA 89: 3389–3393Google Scholar
  13. Ellis RJ, van der Vies SM (1991) Molecular chaperones. A Rev Biochem 60: 321–347Google Scholar
  14. Fader SC, Yu Z, Spotila JR (1994) Seasonal variation in heat shock proteins (hsp70) in stream fish under natural conditions. J therm Biol 19: 335–341Google Scholar
  15. Fields P, Graham JB, Rosenblatt RH, Somero GN (1993) Effects of expected global change on marine faunas. Trends Ecol Evolut 8: 361–366Google Scholar
  16. Frydman J, Hartl FU (1994) Molecular chaperone functions of hsp70 and hsp60 in protein folding. In: Morimoto RI, Tissieres A, Georgopoulos C (eds) The biology of heat shock proteins and molecular chaperones. Cold Spring Harbor Press, New York, pp 251–283Google Scholar
  17. Frydman J, Nimmesgern E, Ohtsuka E, Hartl FU (1994) Folding of nascent polypeptide chains in a high molecular mass assembly with molecular chaperones. Nature, Lond 370: 111–117Google Scholar
  18. Gehring WJ, Wehner R (1995) Heat shock protein synthesis and thermotolerance inCataglyphis, an ant from the Sahara desert. Proc natn Acad Sci USA 92: 2994–2998Google Scholar
  19. Geller JB, Carlton JT, Powers DA (1994) PCR-based detection of mtDNA haplotypes of native and invading mussels on the northeastern Pacific coast: latitudinal pattern of invasion. Mar Biol 119: 243–249Google Scholar
  20. Goff SA, Goldberg AL (1985) Production of abnormal proteins inE. coli stimulates transcription oflon and other heat shock genes. Cell 41: 587–595Google Scholar
  21. Gosling EM (1992) Systematics and geographic distribution ofMytilus. In: Gosling E (ed) The musselMytilus: ecology, physiology, genetics and culture. Elsevier Science Publishers B.V., Amsterdam, pp 1–20Google Scholar
  22. Graves JE, Somero GN (1982) Electrophoretic and functional enzymic evolution in four species of eastern Pacific barracudas from different thermal environments. Evolution 36: 97–106Google Scholar
  23. Haas AL, Bright PM (1985) The immunochemical detection and quantification of intracellular ubiquitin-protein conjugates. J biol Chem 260: 12464–12473Google Scholar
  24. Hawkins AJS (1991) Protein turnover: a functional appraisal. Funct Ecol 5: 222–233Google Scholar
  25. Hershko A, Ciechanover A (1992) The ubiquitin system for protein degradation. A Rev Biochem 61: 761–807Google Scholar
  26. Hightower LE (1980) Cultured animal cells exposed to amino acid analogues or puromycin rapidly synthesize several polypeptides. J Cell Physiol 102: 407–424Google Scholar
  27. Hilbish TJ, Bayne BL, Day A (1994) Genetics of physiological differentiation within the marine mussel genusMytilus. Evolution 48: 267–286Google Scholar
  28. Hochstrasser M (1995) Ubiquitin, proteasomes, and the regulation of intracellular protein degradation. Curr Opinion Cell Biol 7: 215–223Google Scholar
  29. Hofmann GE, Somero GN (1995) Evidence for protein damage at environmental temperatures: seasonal changes in levels of ubiquitin conjugates and hsp70 in the intertidal musselMytilus trossulus. J exp Biol 198: 1509–1518Google Scholar
  30. Hofmann GE, Somero GN (1996) Protein ubiquitination and stress protein synthesis inMytilus trossulus occurs during recovery from tidal emersion. Molec mar Biol Biotechnol (in press)Google Scholar
  31. Howarth CJ (1991) Molecular responses of plants to an increased incidence of heat shock. Pl, Cell Envir 14: 831–841Google Scholar
  32. Huey RB (1991) Physiological consequences of habitat selection. Am Nat 137: S91-S115Google Scholar
  33. Inoue K, Waite JH, Matsuoka M, Odo S, Harayama S (1995) Interspecific variations in adhesive protein sequences ofMytilus edulis, M. galloprovincialis, andM. trossulus. Biol Bull mar biol Lab, Woods Hole 189: 370–375Google Scholar
  34. Koehn RK (1991) The genetics and taxonomy of species in the genusMytilus. Aquaculture, Amsterdam 94: 125–145Google Scholar
  35. Krebs RA, Loeschcke V (1994a) Costs and benefits of activation of the heat shock response inDrosophila melanogaster. Funct Ecol 8: 730–737Google Scholar
  36. Krebs RA, Loeschcke V (1994b) Effects of exposure to short-term heat stress on fitness components inDrosophila melanogaster. J evolut Biol 7: 39–49Google Scholar
  37. Kurtz S, Rossi J, Petko L, Lindquist S (1986) An ancient developmental induction: heat-shock proteins induced in sporulation and oogenesis. Science, NY 231: 1154–1157Google Scholar
  38. Laemmli EK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, Lond 227: 680–685Google Scholar
  39. Landry J, Bernier D, Chretien P, Nicole LM, Tanguay RM, Marceau N (1982) Synthesis and degradation of heat shock proteins during development and decay of thermotolerance. Cancer Res 42: 2457–2461Google Scholar
  40. Langer T, Lu C, Echols H, Flanagan J, Hayer MK (1992) Successive action of Dnak, DnaJ and GroEL along the pathway of chaper-one-mediated protein folding. Nature, Lond 356: 683–689Google Scholar
  41. Li GC, Li LG, Liu YK, Mak JY, Chen LL (1991) Thermal response of rat fibroblasts stably transfected with the human 70-kDa heat shock protein-encoding gene. Proc natn Acad Sci USA 88: 1681–1685Google Scholar
  42. Lin JJ, Somero GN (1995) Thermal adaptation of cytoplasmic malate dehydrogenases of eastern Pacific barracuda (Sphyraena spp): the role of differential isoenzyme expression. J exp Biol 198: 551–560Google Scholar
  43. Lindquist S (1986) The heat-shock response. A Rev Biochem 55: 1151–1191Google Scholar
  44. Lubchenco J, Navarrete SA, Tissot BN, Castilla JC (1993) Possible ecological responses to global climate change: nearshore benthic biota of northeastern Pacific coastal ecosystems. In: Mooney HA, Fuentes ER, Kronberg BI (eds) Earth system responses to global change. Academic Press, New York, pp 147–166Google Scholar
  45. McDonald JH, Koehn RK (1988) The musselsMytilus galloprovincialis andM. trossulus on the Pacific coast of North America. Mar Biol 99: 111–118Google Scholar
  46. McDonald JH, Seed R, Koehn RK (1991) Allozymes and morphometric characters of three species ofMytilus in the Northern and Southern Hemispheres. Mar Biol 111: 323–333Google Scholar
  47. McFall-Ngai MJ, Horwitz J (1990) A comparative study of the thermal stability of the vertebrate eye lens: antarctic fish to the desert iguana. Expl Eye Res 50: 703–709Google Scholar
  48. Mizzen LA, Welch WJ (1988) Characterization of the thermotolerant cell. I. Effects on protein synthesis activity and the regulation of heat-shock protein 70 expression. J biol Chem 106: 1105–1116Google Scholar
  49. Morimoto RI (1993) Cells in stress: transcriptional activation of heat shock genes. Science, NY 259: 1409–1410Google Scholar
  50. Morimoto RI, Jurivich DA, Kroeger PE, Mathur SK, Murphy SP, Nakai A, Sarge K, Abravaya K, Sistonen LT (1994a) Regulation of heat shock gene transcription by a family of heat shock factors. In: Morimoto RI, Tissieres A, Georgopoulos C (eds) The biology of heat shock proteins and molecular chaperones. Cold Spring Harbor Press, New York, pp 417–455Google Scholar
  51. Morimoto RI, Tissieres A, Georgopoulos C (eds) (1994b) The biology of heat shock proteins and molecular chaperones. Cold Spring Harbor Press, New YorkGoogle Scholar
  52. Oda S, Mitani H, Naruse K, Shima A (1991) Synthesis of heat shock proteins in the isolated fin of the medaka,Oryzias latipes, acclimated to various temperatures. Comp Biochem Physiol 98B: 587–591Google Scholar
  53. Parag HA, Raboy B, Kulka RG (1987) Effect of heat shock on protein degradation in mammalian cells: involvement of the ubiquitin system. EMBO J 6: 55–61Google Scholar
  54. Parsell DA, Kowal AS, Singer MA, Lindquist S (1994) Protein disaggregation mediated by heat-shock protein Hsp104. Nature, Lond 372: 475–478Google Scholar
  55. Parsell DA, Lindquist S (1993) The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. A Rev Genet 27: 437–496Google Scholar
  56. Parsell DA, Lindquist S (1994) Heat shock proteins and stress tolerance. In: Morimoto RI, Tissieres A, Georgopoulos C (eds) The biology of heat shock proteins and molecular chaperones. Cold Spring Harbor Press, New York, pp 457–494Google Scholar
  57. Parsell DA, Taulien J, Lindquist S (1993) The role of heat-shock proteins in thermotolerance. Phil Trans R Soc (Ser B) 339: 279–286Google Scholar
  58. Rawson PD, Hilbish TJ (1995) Distribution of male and female mtDNA lineages in populations of blue mussels,Mytilus trossulus andM. galloprovincialis, along the Pacific coast of North America. Mar Biol 124: 245–250Google Scholar
  59. Rechsteiner M (1987) Ubiquitin-mediated pathways for intracellular proteolysis. A Rey Cell Biol 3: 1–30Google Scholar
  60. Roberts DA (1995) Heat-shock protein expression inMytilus californianus: seasonal and tidal height comparisons. M.S. thesis. Oregon State UniversityGoogle Scholar
  61. Sanchez Y, Lindquist SL (1990) Hsp104 required for induced thermotolerance. Science, NY 248: 1112–1115Google Scholar
  62. Sanders BM, Hope C, Pascoe VM, Martin LS (1991) Characterization of the stress protein response in two species ofCollisella limpets with different temperature tolerances. Physiol Zoöl 64: 1471–1489Google Scholar
  63. Sanders BM, Pascoe VM, Nakagawa PA, Martin, LS (1992) Persistence of the heat-shock response over time in a commonMytilus mussel. Molec mar Biol Biotechnol 1: 147–154Google Scholar
  64. Sarver SK, Foltz DW (1993) Genetic population structure of a species' complex of blue mussels (Mytilus spp.). Mar Biol 117: 105–112Google Scholar
  65. Sarver SK, Loudenslager EJ (1991) The genetics of California populations of the blue mussel: further evidence for the existense of electrophoretically distinguishable species or subspecies. Biochem Syst Ecol 19: 183–188Google Scholar
  66. Schröder H, Langer T, Hartl FU, Bukau B (1993) DnaK, DnaJ and GrpE form a cellular chaperone machinery capable of repairing heat-induced protein damage. EMBO J 12: 4137–4144Google Scholar
  67. Seed R (1992) Systematics, evolution and distribution of mussels belonging to the genusMytilus: an overview. Am malac Bull 9: 123–137Google Scholar
  68. Sharp VA, Miller D, Bythell JC, Brown BE (1994) Expression of low molecular weight HSP 70 related polypeptides from the symbiotic sea anemoneAnemonia viridis Forskall in response to heat shock. J exp mar Biol Ecol 179: 179–193Google Scholar
  69. Solomon JM, Rossi JM, Golic K, McGarry T, Lindquist S (1991) Changes in Hsp 70 alter thermotolerance and heat-shock regulation inDrosophila. New Biol 3: 1106–1120Google Scholar
  70. Somero GN (1995) Proteins and temperature. A Rev Physiol 57: 43–68Google Scholar
  71. Swezey RR, Somero GN (1982) Polymerization thermodynamics and structural stabilities of skeletal muscle actins from vertebrates adapted to different temperatures and pressures. Biochemistry (Am chem Soc) Easton, Pa 21: 4496–4503Google Scholar
  72. Vernberg FJ (1962) Latitudinal effects on physiological properties of animal populations. A Rev Physiol 24: 517–546Google Scholar

Copyright information

© Springer-Verlag 1996

Authors and Affiliations

  • G. E. Hofmann
    • 1
  • G. N. Somero
    • 1
  1. 1.Department of ZoologyOregon State UniversityCorvallisUSA

Personalised recommendations