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Adaptation and Evolution in Marine Environments, Volume 1 pp 143–155Cite as

Aspects of Protein Cold Adaptation in Antarctic Fish

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Part of the book series: From Pole to Pole ((POLE))

Abstract

With the transition of Antarctica from seasonally cold to a permanently frozen state came a very significant transition in the surrounding waters. During the seasonal cold period the formation of sea ice and reduction of water temperature created a set of problems for marine organisms. Seasonal changes that could previously be avoided by behavioural adaptations became permanent and had a profound effect on the marine fauna and flora.

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References

  • Abele D, Puntarulo S (2004) Formation of reactive species and induction of antioxidant defence systems in polar and temperate marine invertebrates and fish. Comp Biochem Physiol 138:405–415. doi:10.1016/j.cbpb.2004.05.013

    Article  Google Scholar 

  • Acierno R, Maffia M, Rollo M, Storelli C (1997) Buffer capacity in the blood of the hemoglobinless antarctic fish Chionodraco hamatus. Comp Biochem Physiol A 118:989–992. doi:10.1016/S0300-9629(97)86787-4

    Article  Google Scholar 

  • Andersson AJ, Mackenzie FT, Bates NR (2008) Life on the margin: implications of ocean acidification on Mg-calcite, high latitude and cold-water marine calcifiers. Mar Ecol Progr Ser 373:265–273. doi:10.3354/meps07639

    Article  CAS  Google Scholar 

  • Axelsson M, Davison W, Forster ME, Farrell AP (1992) Cardiovascular responses of the red-blooded antarctic fishes Pagothenia bernacchii and P. borchgrevinki. J Exp Biol 167:179–201

    CAS  Google Scholar 

  • Becker K, Wöhrmann A, Rahmann H (1995) Brain gangliosides and cold-adaptation in high-antarctic fish. Biochem Syst Ecol 23:695–707. doi:10.1016/0305-1978(95)00086-0

    Article  CAS  Google Scholar 

  • Beers JM, Borley KA, Sidell BD (2010) Relationship among circulating hemoglobin, nitric oxide synthase activities and angiogenic poise in red- and white-blooded Antarctic notothenioid fishes. Comp Biochem Physiol A Mol Integr Physiol 156:422–429. doi:10.1016/j.cbpa.2010.03.027

    Article  Google Scholar 

  • Buckley BA, Somero GN (2009) cDNA microarray analysis reveals the capacity of the cold-adapted Antarctic fish Trematomus bernacchii to alter gene expression in response to heat stress. Polar Biol 32:403–415. doi:10.1007/s00300-008-0533-x

    Article  Google Scholar 

  • Buckley BA, Place SP, Hofmann GE (2004) Regulation of heat shock genes in isolated hepatocytes from an Antarctic fish, Trematomus bernacchii. J Exp Biol 207:3649–3656

    Article  CAS  Google Scholar 

  • Carpenter CM, Hofmann GE (2000) Expression of 70 kDa heat shock proteins in antarctic and New Zealand notothenioid fish. Comp Biochem Physiol A Mol Integr Physiol 125:229–238

    Article  CAS  Google Scholar 

  • Chapelle G, Peck LS (1999) Polar gigantism dictated by oxygen availability. Nature 399:114–115. doi:10.1038/20099

    Article  CAS  Google Scholar 

  • Chen W-J, Bonillo C, Lecointre G (1998) Phylogeny of the channichthyidae (Notothenioidei, Teleostei) based on two mitochondrial genes. In: di Prisco D, Pisano E, Clarke A (eds) Fishes of Antarctica: a biological overview. Springer, Milan, pp 287–298

    Google Scholar 

  • Clarke A, Johnston NM (1999) Scaling of metabolic rate with body mass and temperature in teleost fish. J Animal Ecol 68:893–905. doi:10.1046/j.1365-2656.1999.00337.x

    Article  Google Scholar 

  • Collins T, Roulling F, Piette F, Marx J-C, Feller G, Gerday C, D’Amico S (2008) Fundamentals of cold-adapted enzymes. In: Margesin R, Schinner F, Marx J-C, Gerday C (eds) Psychrophiles: from biodiversity to biotechnology. Springer, Berlin, pp 211–227. doi:10.1007/978-3-540-74335-4

    Chapter  Google Scholar 

  • Cossins AR, Macdonald AG (1989) The adaptation of biological membranes to temperature and pressure: fish from the deep and cold. J Bioenerg Biomembranes 21:115–135

    Article  CAS  Google Scholar 

  • Crockett EL, Sidell BD (1990) Some pathways of energy metabolism are cold adapted in antarctic fishes. Physiol Zool 63:472–488

    Google Scholar 

  • Davison W, Axelsson M, Forster ME, Nilsson S (1995) Cardiovascular responses to acute handling stress in the Antarctic fish Trematomus bernacchii are not mediated by circulatory catecholamines. Fish Physiol Biochem 14:253–257

    Article  CAS  Google Scholar 

  • Detrich HW, Parker SK, Williams RC, Nogales E, Downing KH (2000) Cold adaptation of microtubule assembly and dynamics—structural interpretation of primary sequence changes present in the alpha- and beta-tubulins of antarctic fishes. J Biol Chem 275:37038–37047. doi:10.1074/jbc.M005699200

    Article  CAS  Google Scholar 

  • DeVries AL, Cheng C-HC (2005) Antifreeze proteins and organismal freezing avoidance in polar fishes. In: Anthony PF, Steffensen JF (eds) Physiology of polar fishes, 22nd edn. Academic, New York, pp 155–201. doi:10.1016/S1546-5098(04)22004-0

    Google Scholar 

  • di Prisco G, Macdonald JA, Brunori M (1992) Antarctic fishes survive exposure to carbon monoxide. Experientia 48:473–485. doi:10.1007/BF01928166

    Article  Google Scholar 

  • Dill KA, Ozkan SB, Shell MS, Weikl TR (2008) The protein folding problem. Annu Rev Biophys 37:289–316. doi:10.1146/annurev.biophys.37.092707.153558

    Article  CAS  Google Scholar 

  • Eastman JT (1993) Antarctic fish biology: evolution in a unique environment. Academic, San Diego

    Google Scholar 

  • Eastman JT (2000) Antarctic notothenioid fishes as subjects for research in evolutionary biology. Antarct Sci 12:276–287

    Article  Google Scholar 

  • Eastman JT, Clarke A (1998) Radiations of Antarctic and non-Antarctic fish. In: di Prisco G, Pisano E, Clarke A (eds) Fishes of Antarctica: a biological overview. Springer, Milan, pp 3–26

    Google Scholar 

  • Egginton S (1997) A comparison of the response to induced exercise in red- and white-blooded antarctic fishes. Comp Biochem Physiol B 167:129–134

    CAS  Google Scholar 

  • Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282. doi:10.1146/annurev.physiol.61.1.243

    Article  CAS  Google Scholar 

  • Feller G (2003) Molecular adaptations to cold in psychrophilic enyzmes. Cell Mol Life Sci 60:648–662

    Article  CAS  Google Scholar 

  • Feller G, Gerday C (1997) Adaptations of the hemoglobinless antarctic icefish (Channichthyidae) to hypoxia tolerance. Comp Biochem Physiol 118A:981–987

    Article  CAS  Google Scholar 

  • Fields PA, Houseman DE (2004) Decreases in activation energy and substrate affinity in cold-adapted A4-lactate dehydrogenase: evidence from the Antarctic notothenioid fish Chaenocephalus aceratus. Mol Biol Evol 21:2246–2255

    Article  CAS  Google Scholar 

  • Fields PA, Somero GN (1998) Hot spots in cold adaptation: localized increases in conformational flexibility in lactate dehydrogenase A4 orthologs of antarctic notothenioid fishes. Proc Natl Acad Sci USA 95:11476–11481. doi:10.1073/pnas.95.19.11476

    Article  CAS  Google Scholar 

  • Georlette D, Blaise V, Collins T, D’Amico S, Gratia E, Hoyoux A, Marx JC, Sonan G, Feller G, Gerday C (2004) Some like it cold: biocatalysis at low temperatures. FEMS Microbiol Rev 28:25–42. doi:10.1016/j.femsre.2003.07.003

    Article  CAS  Google Scholar 

  • Glickman MH, Adir N (2004) The proteasome and the delicate balance between destruction and rescue. PLoS Biol 2:E13. doi:10.1371/journal.pbio.0020013

    Article  Google Scholar 

  • Gon O, Heemstra PC (1990) Fishes of the southern ocean. JLB Smith Institute of Ichthyology, Grahamstown

    Google Scholar 

  • Gonzalez-Cabrera PJ, Dowd F, Pedibhotla VK, Rosario R, Stanley-Samuelson D, Petzel D (1995) Enhanced hypo-osmoregulation induced by warm-acclimation in antarctic fish is mediated by increased gill and kidney Na+/K+-ATPase activities. J Exp Biol 198:2279–2291

    CAS  Google Scholar 

  • Grove TJ, Hendrickson JW, Sidell BD (2004) Two species of Antarctic icefishes (genus Champsocephalus) share a common genetic lesion leading to the loss of myoglobin expression. Polar Biol 27:579–585. doi:10.1007/s00300-004-0634-0

    Article  Google Scholar 

  • Haschemeyer AEV (1980) Temperature effects on protein metabolism in cold-adapted fishes. Antarctic J US 15:147–149

    Google Scholar 

  • Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, Oxford

    Google Scholar 

  • Hofmann GE, Buckley BA, Airaksinen S, Keen JE, Somero GN (2000) Heat-shock protein expression is absent in the Antarctic fish Trematomus bernacchii (Family Nototheniidae). J Exp Biol 203:2331–2339

    CAS  Google Scholar 

  • Holland LZ, McFall-Ngai M, Somero GN (1997) Evolution of lactate dehydrogenase-A homologs of barracuda fishes (genus Sphyraena) from different thermal environments: differences in kinetic properties and thermal stability are due to amino acid substitutions outside the active site. Biochemistry 36:3207–3215. doi:10.1021/bi962664k

    Article  CAS  Google Scholar 

  • Johnston IA, Calvo J, Guderley H, Fernandez D, Palmer L (1998) Latitudinal variation in the abundance and oxidative capacities of muscle mitochondria in perciform fishes. J Exp Biol 201:1–12

    CAS  Google Scholar 

  • Kassahn KS, Crozier RH, Portner H-O, Caley MJ (2009) Animal performance and stress: responses and tolerance limits at different levels of biological organisation. Biol Rev Camb Philos Soc 84:277–292. doi:10.1111/j.1469-185X.2008.00073.x

    Article  Google Scholar 

  • Kawall HG, Torres JJ, Sidell BD, Somero GN (2002) Metabolic cold adaptation in Antarctic fishes: evidence from enzymatic activities of brain. Mar Biol 140:279–286. doi:10.1007/s002270100695

    Article  Google Scholar 

  • Kelley JL, Aagaard JE, MacCoss MJ, Swanson WJ (2010) Functional diversification and evolution of antifreeze proteins in the antarctic fish Lycodichthys dearborni. J Mol Evol 71:111–118. doi:10.1007/s00239-010-9367-6

    Article  CAS  Google Scholar 

  • Krogh A (1914) The quantitative relation between temperature and standard metabolism in animals. Int Z Phys-Chem Biol 1:491–498

    CAS  Google Scholar 

  • Leonard GH, Langhorne PJ, Williams MJM, Vennell R, Purdie CR, Dempsey DE, Haskell TG, Frew RD (2011) Evolution of supercooling under coastal Antarctic sea ice during winter. Antarctic Sci 1:1–11. doi:10.1017/S0954102011000265

    Google Scholar 

  • Lin J-J, Somero GN (1995) Temperature-dependent changes in expression of thermostable and thermolabile isozymes of cytosolic malate dehydrogenase in eurythermal goby fish Gillicthys mirabilis. J Exp Biol 198:551–560

    CAS  Google Scholar 

  • Lindquist S (2010) Protein folding sculpting evolutionary change. Cold Spring Harb Symp Quant Biol 74:doi: 10.1101/sqb.2009.74.043

  • Marshall CJ (1997) Cold-adapted enzymes. Trends Biotechnol 15:359–364

    Article  CAS  Google Scholar 

  • Marshall CJ, Johnston NM, Murray BW, Brown PM, Verghese AI (2003) Does the enzyme citrate synthase from several Antarctic fish show evidence of cold adaptation? In: Huiskes AL, Gieskes WWC, Rozema J, Schorno RML, van der Vies SM, Wolff WJ (eds) Symposium of the VIII SCAR biology meeting. Backhuys Publishers, Leiden, pp 102–106

    Google Scholar 

  • Marx JC, Collins T, D’Amico S, Feller G, Gerday C (2007) Cold-adapted enzymes from marine Antarctic microorganisms. Mar Biotechnol (NY) 9:293–304. doi:10.1007/s10126-006-6103-8

    Article  CAS  Google Scholar 

  • Nakamura I, Inada T, Takeda M, Hatanaka H (1986) Important fishes trawled off Patagonia. Japan Marine Fishery Resource, Tokyo

    Google Scholar 

  • Near TJ, Cheng C-HC (2008) Phylogenetics of notothenioid fishes (Teleostei: Acanthomorpha): inferences from mitochondrial and nuclear gene sequences. Mol Phylogenet Evol 47:832–840. doi:10.1016/j.ympev.2007.11.027

    Article  CAS  Google Scholar 

  • Near TJ, Pesavento JJ, Cheng C-HC (2003) Mitochondrial DNA, morphology, and the phylogenetic relationships of Antarctic icefishes (Notothenioidei: Channichthyidae). Mol Phylogen Evol 28:87–98. doi:10.1016/S1055-7903(03),00029-0

    Article  CAS  Google Scholar 

  • Near TJ, Parker SK, Detrich III HW (2006) A genomic fossil reveals key steps in hemoglobin loss by the antarctic icefishes. Mol Biol Evol 23:2008–2016. doi:10.1093/molbev/msl071

    Article  CAS  Google Scholar 

  • Nogales E (2000) Structural insights into microtubule function. Annu Rev Biochem 69:277–302. doi:10.1146/annurev.biochem.69.1.277

    Article  CAS  Google Scholar 

  • Nogales E, Downing KH (2008) Tubulin and microtubule structures. In: Fojo T (ed) The role of microtubules in cell biology, neurobiology, and oncology. Humana Press, Totowa, pp 211–225. doi:10.1007/978-1-59745-336-3

    Chapter  Google Scholar 

  • O’Brien KM (2011) Mitochondrial biogenesis in cold-bodied fishes. J Exp Biol 214:275–285. doi:10.1242/jeb.046854

    Article  Google Scholar 

  • O’Brien KM, Sidell BD (2000) The interplay among cardiac ultrastructure, metabolism and the expression of oxygen-binding proteins in Antarctic fishes. J Exp Biol 203:1287

    Google Scholar 

  • Patarnello T, Verde C, di Prisco G, Bargelloni L, Zane L (2011) How will fish that evolved at constant sub-zero temperatures cope with global warming? Notothenioids as a case study. BioEssays 33:260–268. doi:10.1002/bies.201000124

    Article  Google Scholar 

  • Pellegrino D, Palmerini CA, Tota B (2004) No hemoglobin but NO: the icefish (Chionodraco hamatus) heart as a paradigm. J Exp Biol 207:3855–3864. doi:10.1242/jeb.01180

    Article  CAS  Google Scholar 

  • Peters SE, Carlson AE, Kelly DC, Gingerich PD (2010) Large-scale glaciation and deglaciation of Antarctica during the late eocene. Geology 38:723–726. doi:10.1130/G31068.1

    Article  CAS  Google Scholar 

  • Petricorena ZL, Somero GN (2007) Biochemical adaptations of notothenioid fishes: comparisons between cold temperate South American and New Zealand species and Antarctic species. Comp Biochem Physiol A Mol Integr Physiol 147:799–807. doi:10.1016/j.cbpa.2006.09.028

    Article  Google Scholar 

  • Rodnick KJ, Sidell BD (1997) Structural and biochemical analyses of cardiac ventricular enlargement in cold-acclimated striped bass. Am J Physiol 273R:252–258

    Google Scholar 

  • Scudiero R, Carginale V, Riggio M, Capasso C, Capasso A, Kille P, di Prisco G, Parisi E (1997) Difference in hepatic metallothionein content in Antarctic red-blooded and haemoglobinless fish: undetectable metallothionein levels in haemoglobinless fish is accompanied by accumulation of untranslated metallothionein mRNA. Biochem J 322:207–211

    CAS  Google Scholar 

  • Seebacher F, Davison W, Lowe CJ, Franklin CE (2005) A falsification of the thermal specialization paradigm: compensation for elevated temperatures in Antarctic fishes. Biol Lett 1:151–154. doi:10.1098/rsbl.2004.0280

    Article  Google Scholar 

  • Sharpe M, Love C, Marshall C (2001) Lactate dehydrogenase from the Antarctic eelpout, Lycodichthys dearborni. Polar Biol 24:258–269. doi:10.1007/s003000000206

    Article  Google Scholar 

  • Sidell BD (1991) The physiological roles of high lipid content in tissues of Antarctic fish species. In: di Prisco G, Maresca B, Tota B (eds) Biology of Antarctic fish. Springer, Berlin, pp 220–231

    Chapter  Google Scholar 

  • Sidell BD (1998) Intracellular oxygen diffusion: the roles of myoglobin and lipid at cold body temperature. J Exp Biol 201:1119–1128

    CAS  Google Scholar 

  • Sidell BD, O’Brien KM (2006) When bad things happen to good fish: the loss of hemoglobin and myoglobin expression in Antarctic icefishes. J Exp Biol 209:1791–1802. doi:10.1242/jeb.02091

    Article  CAS  Google Scholar 

  • Sokolova IM, Portner H-O (2003) Metabolic plasticity and critical temperatures for aerobic scope in a eurythermal marine invertebrate (Littorina saxatilis, Gastropoda: Littorinidae) from different latitudes. J Exp Biol 206:195–207

    Article  Google Scholar 

  • Somero GN (1995) Proteins and temperature. Annu Rev Physiol 57:43–68. doi:10.1146/annurev.ph.57.030195.000355

    Article  CAS  Google Scholar 

  • Somero GN (2011) Invited review: comparative physiology: a “crystal ball” for predicting consequences of global change. Am J Physiol Regul Integr Comp Physiol. doi:10.1152/ajpregu.00719.2010

    Google Scholar 

  • Somero GN, DeVries AL (1967) Temperature tolerance of some antarctic fishes. Science 156:257–258. doi:10.1126/science.156.3772.257

    Article  CAS  Google Scholar 

  • Temussi PA (2011) Cold denaturation and protein stability. In: Brnjas-Kraljević J, Pifat-Mrzljak G (eds) Supramolecular structure and function 10. Springer Netherlands, Dordrecht, pp 75–85. doi:10.1007/978-94-007-0893-8

    Chapter  Google Scholar 

  • Todgham AE, Hoaglund EA, Hofmann GE (2007) Is cold the new hot? Elevated ubiquitin-conjugated protein levels in tissues of Antarctic fish as evidence for cold-denaturation of proteins in vivo. J Comp Physiol B 177:857–866. doi:10.1007/s00360-007-0183-2

    Article  CAS  Google Scholar 

  • Tota B, Angelone T, Mancardi D, Cerra MC (2011) Hypoxia and anoxia tolerance of vertebrate hearts: an evolutionary perspective. Antioxid Redox Signal 14:851–862. doi:10.1089/ars.2010.3310

    Article  CAS  Google Scholar 

  • Urschel MR, O’Brien KM (2008) High mitochondrial densities in the hearts of Antarctic icefishes are maintained by an increase in mitochondrial size rather than mitochondrial biogenesis. J Exp Biol 211:2638–2646. doi:10.1242/jeb.018598

    Article  CAS  Google Scholar 

  • Weinstein RB, Somero GN (1998) Effects of temperature on mitochondrial function in the Antarctic fish Trematomus bernacchii. J Comp Physiol B: Biochem, Systemic Environ Physiol 168:190–196. doi:10.1007/s003600050136

    Article  CAS  Google Scholar 

  • Williams WP (1990) Cold-induced lipid phase transitions. Phil Trans R Soc London Ser B 326:555–570. doi:10.1098/rstb.1990.0031

    Article  CAS  Google Scholar 

  • Wittenberg JB, Wittenberg BA (1990) Mechanisms of cytoplasmic hemoglobin and myoglobin function. Annu Rev Biophys Biophys Chem 19:217–241

    Article  CAS  Google Scholar 

  • Woods HA, Moran AL, Arango CP, Mullen L, Shields C (2009) Oxygen hypothesis of polar gigantism not supported by performance of Antarctic pycnogonids in hypoxia. Proc Biol Sci 276:1069–1075. doi:10.1098/rspb.2008.1489

    Article  Google Scholar 

  • Zachos J, Pagani M, Sloan L, Thomas E, Billups K (2001) Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292:686–693. doi:10.1126/science.1059412

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Biochemistry and Genetics Otago, University of Otago, PO Box 56, Dunedin, New Zealand

    Craig Marshall

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  1. Craig Marshall
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Correspondence to Craig Marshall .

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  1. Institute of Protein Biochemistry, CNR, Via Pietro Castellino 111, Napoli, 80131, Italy

    Guido di Prisco

  2. Institute of Protein Biochemistry, CNR, Via Pietro Castellino 111, Napoli, 80131, Italy

    Cinzia Verde

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Marshall, C. (2012). Aspects of Protein Cold Adaptation in Antarctic Fish. In: di Prisco, G., Verde, C. (eds) Adaptation and Evolution in Marine Environments, Volume 1. From Pole to Pole. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-27352-0_8

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