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The Mechanism of Low-Temperature Tolerance in Fish

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Survival Strategies in Extreme Cold and Desiccation

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1081))

Abstract

In this chapter, we cover the life history of fish in low-temperature environments, including their overwintering behavior and the physiological mechanisms by which they maintain life in cold environments, based on research to date. There is relatively little research on low-temperature tolerance of fish, compared with research on this phenomenon in mammals and birds, which are also vertebrates, and the mechanisms in fish have not been fully elucidated. First, we cover the life history of fish that overwinter by entering dormancy or hibernation. Next, we describe the mechanism that controls body temperature in fish that survive low-temperature environments. Finally, we introduce the physiological mechanisms for survival in extremely low-temperature environments, particularly antifreeze proteins.

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Abbreviations

ACTH:

Adrenocorticotropic hormone

AFGP:

Antifreeze glycoprotein

AFP:

Antifreeze protein

CDC48:

Cell division cycle protein 48

GH:

Growth hormone

GTH:

Gonadotropic hormone

LDLR:

Low density lipoprotein receptor

MO2 :

Muscle oxygen consumption

MSH:

Melanophore-stimulating hormone

PRL:

Prolactin

SERCA:

Sarco-endoplasmic reticulum Ca2+ ATPase

SL:

Somatolactin

TH:

Thyroid hormone

TSH:

Thyroid-stimulating hormone

References

  • Baardsnes J, Davies PL (2001) Sialic acid synthase: the origin of fish type III antifreeze protein? Trends Biochem Sci 26:468–469

    Article  CAS  Google Scholar 

  • Barton BA (2002) Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integ Comp Biol 42:517–525

    Article  CAS  Google Scholar 

  • Bernal D, Sepulveda C, Graham JB (2001) Water-tunnel studies of heat balance in swimming mako sharks. J Exp Biol 204:4043–4054

    CAS  PubMed  Google Scholar 

  • Block BA, Dewar H, Blackwell SB, Williams TD, Prince ED, Farwell CJ, Boustany A, Teo SL, Seitz A, Walli A, Fudge D (2001) Migratory movements, depth preferences, and thermal biology of Atlantic bluefin tuna. Science 293:1310–1314

    Article  CAS  Google Scholar 

  • Boulant JA (2000) Role of the preoptic-anterior hypothalamus in thermoregulation and fever. Clin Infect Dis 31:S157–S161

    Article  Google Scholar 

  • Boyd RB, DeVries AL (1983) The seasonal distribution of anionic binding sites in the basement membrane of the kidney glomerulus of the winter flounder Pseudopleuronectes americanus. Cell Tissue Res 234:271–277

    Article  CAS  Google Scholar 

  • Brett JR (1971) Energetic responses of salmon to temperature-study of some thermal relations in physiology and freshwater ecology of sockeye salmon (Oncorhynchus nerka). Am Zool 11:99–113

    Article  Google Scholar 

  • Brett JR (1979) Environmental factors and growth. In: Hore WS, Randall DJ, Brett JR (eds) Fish physiology. Academic, New Yolk, pp 599–675

    Google Scholar 

  • Burcham TS, Osuga DT, Chino H, Feeney RE (1984) Analysis of antifreeze glycoproteins in fish serum. Anal Biochem 139:197–120

    Article  CAS  Google Scholar 

  • Campbell HA, Fraser KPP, Bishop CM, Peck LS, Egginton S (2008) Hibernation in an Antarctic fish: on ice for winter. PLoS One 3:e1743

    Article  Google Scholar 

  • Carey FG, Lawson KD (1973) Temperature regulation in free-swimming bluefin tuna. Comp Biochem Physiol 44A:375–392

    Article  Google Scholar 

  • Carey FG, Robinson BH (1981) Daily patterns in the activities of swordfish, Xiphias gladius, observed by acoustic telemetry. Fish Bull US 79:277–292

    Google Scholar 

  • Carey FG, Scharold JV (1990) Movements of blue sharks (Prionace glauca) in depth and course. Mar Biol 106:329–342

    Article  Google Scholar 

  • Chen L, DeVries AL, Cheng CH (1997a) Evolution of antifreeze glycoprotein gene from a trypsinogen gene in Antarctic notothenioid fish. Proc Natl Acad Sci U S A 94:3811–3816

    Article  CAS  Google Scholar 

  • Chen L, DeVries AL, Cheng CH (1997b) Convergent evolution of antifreeze glycoproteins in Antarctic notothenioid fish and Arctic cod. Proc Natl Acad Sci U S A 94:3817–3822

    Article  CAS  Google Scholar 

  • Chen WH, Sun LT, Tsai CL, Song YL, Chang CF (2002) Cold-stress induced the modulation of catecholamines, cortisol, immunoglobulin M, and leukocyte phagocytosis in tilapia. Gen Comp Endocrinol 126:90–100

    Article  CAS  Google Scholar 

  • Cheng CH, Cziko PA, Evans CW (2006) Nonhepatic origin of notothenioid antifreeze reveals pancreatic synthesis as common mechanism in polar fish freezing avoidance. Proc Natl Acad Sci U S A 103:10491–10496

    Article  CAS  Google Scholar 

  • Choi YG, Park CJ, Kim HE, Seo YJ, Lee AR, Choi SR, Lee SS, Lee JH (2015) Comparison of backbone dynamics of the type III antifreeze protein and antifreeze-like domain of human sialic acid synthase. J Biomol NMR 61:137–150

    Article  CAS  Google Scholar 

  • Claireaux G, Webber DM, Kerr SR, Boutilier RG (1995) Physiology and behaviour of free-swimming Atlantic cod (Gadus morhua) facing fluctuating temperature conditions. J Exp Biol 198:49–60

    CAS  PubMed  Google Scholar 

  • Coggan R (1997) Seasonal and annual growth rates in the Antarctic fish Notothenia coriiceps R. J Exp Mar Biol Ecol 213:215–229

    Article  Google Scholar 

  • Crawshaw L, Grahn D, Wollmuth L, Spimson L (1985) Central nervous regulation of body temperature in vertebrates: comparative aspects. Pharmacol of body temperature in vertebrates: comparative aspect. Pharmacol Ther 30:19–30

    Article  CAS  Google Scholar 

  • Dantuma NP, Hoppe T (2012) Growing sphere of influence: Cdc48/p97 orchestrates ubiquitin-dependent extraction from chromatin. Trends Cell Biol 22:483–491

    Article  CAS  Google Scholar 

  • Deane EE, Woo NYS (2009) Modulation of fish growth hormone levels by salinity, temperature, pollutants and aquaculture related stress: a review. Rev Fish Biol Fish 19:97–120

    Article  Google Scholar 

  • Deng G, Laursen RA (1998) Isolation and characterization of an antifreeze protein from the longhorn sculpin, Myoxocephalus octodecimspinosis. Biochim Biophys Acta 1388:305–314

    Article  CAS  Google Scholar 

  • Deng G, Andrews DW, Laursen RA (1997) Amino acid sequence of a new type of antifreeze protein, from the longhorn sculpin Myoxocephalus octodecimspinosis. FEBS Lett 402:17–20

    Article  CAS  Google Scholar 

  • DeVries AL (1982) Biological antifreeze agents in coldwater fishes. Comp Biochem Physiol A 73:627–640

    Article  Google Scholar 

  • DeVries AL, Cheng CHC (2005) Antifreeze proteins and organismal freezing avoidance in polar fishes. In: Farrell AP, Steffenson JF (eds) The physiology of polar fishes. Fish physiology series, vol 22. Academic, San Diego, pp 155–201

    Chapter  Google Scholar 

  • Donaldson MR, Cooke SJ, Patterson DA, Macdonald JS (2008) Review paper, cold shock and fish. J Fish Biol 73:1491–1530

    Article  Google Scholar 

  • Duman JG, DeVries AL (1976) Isolation, characterization, and physical properties of protein antifreezes from the winter flounder, Pseudopleuronectes americanus. Comp Biochem Physiol B 54:375–380

    Article  CAS  Google Scholar 

  • Eastman JT, DeVries AL (1986) Renal glomerular evolution in Antarctic notothenioid fishes. J Fish Biol 29:649–662

    Article  Google Scholar 

  • Ewart KV, Rubinsky B, Fletcher GL (1992) Structural and functional similarity between fish antifreeze proteins and calcium-dependent lectins. Biochem Biophys Res Commun 185:335–340

    Article  CAS  Google Scholar 

  • Fletcher GL, Idler DR, Vaisius A, Hew CL (1989) Hormonal regulation of antifreeze protein gene expression in winter flounder. Fish Physiol Biochem 7:387–393

    Article  CAS  Google Scholar 

  • Fritsches KA, Brill RW, Warrant EJ (2005) Warm eyes provide superior vision in swordfishes. Curr Biol 15:55–58

    Article  CAS  Google Scholar 

  • Gallagher PS, Candadai SVC, Gardner RG (2014) The requirement for Cdc48/p97 in nuclear protein quality control degradation depends on the substrate and correlates with substrate insolubility. J Cell Sci 127:1980–1991

    Article  CAS  Google Scholar 

  • Gauthier SY, Scotter AJ, Lin FH, Baardsnes J, Fletcher GL, Davies PL (2008) A re-evaluation of the role of type IV antifreeze protein. Cryobiology 57:292–296

    Article  CAS  Google Scholar 

  • Gong Z, Ewart KV, Hu Z, Fletcher GL, Hew CL (1996) Skin antifreeze protein genes of the winter flounder, Pleuronectes americanus, encode distinct and active polypeptides without the secretory signal and prosequences. J Biol Chem 271:4106–4112

    Article  CAS  Google Scholar 

  • Graham JB, Dickson KA (2001) Anatomical and physiological specializations for endothermy. In: Block BA, Dtevens ED (eds) Tuna: physiology, ecology, and evolution. Academic, San Diego, pp 121–168

    Chapter  Google Scholar 

  • Graham LA, Li J, Davidson WS, Davies PL (2012) Smelt was the likely beneficiary of an antifreeze gene laterally transferred between fishes. BMC Evol Biol 12:190

    Article  CAS  Google Scholar 

  • Gronwald W, Loewen MC, Lix B, Daugulis AJ, Sonnichsen FD, Davies PL, Sykes BD (1998) The solution structure of type II antifreeze protein reveals a new member of the lectin family. Biochemistry 37:4712–4721

    Article  CAS  Google Scholar 

  • Guderley H (2004) Metabolic responses to low temperature in fish muscle. Biol Rev 79:409–427

    Article  Google Scholar 

  • Harding MM, Anderberg P, Haymet AD (2003) ‘Antifreeze’ glycoproteins from polar fish. Eur J Biochem 270:1381–1392

    Article  CAS  Google Scholar 

  • Hemmingsen EA (1991) Respiratory and cardiovascular adaptations in hemoglobin-free fish: resolved and unresolved problems. In: di Prisco G, Maresca B, Tota B (eds) Biology of Antarctic fish. Springer-Verlag, Berlin, pp 191–203

    Chapter  Google Scholar 

  • Hew CL, Fletcher GL (1979) The role of pituitary in regulating antifreeze protein synthesis in the winter flounder. FEBS Lett 99:337–339

    Article  CAS  Google Scholar 

  • Hew CL, Fletcher GL, Ananthanarayanan VS (1980) Antifreeze proteins from the shorthorn sculpin, Myoxocephalus scorpius: isolation and characterization. Can J Biochem 58:377–383

    Article  CAS  Google Scholar 

  • Hew CL, Slaughter D, Joshi SB, Fletcher GL, Ananthanarayanan VS (1984) Antifreeze polypeptides from the Newfoundland ocean pout, Macrozoarces americanus: presence of multiple and compositionally diverse components. J Comp Physiol B 155:81–88

    Article  CAS  Google Scholar 

  • Hew CL, Wang NC, Joshi S, Fletcher GL, Scott GK, Hayes PH, Buettner B, Davies PL (1988) Multiple genes provide the basis for antifreeze protein diversity and dosage in the ocean pout, Macrozoarces americanus. J Biol Chem 263:12049–12055

    CAS  PubMed  Google Scholar 

  • Holland KN, Sibert JR (1994) Physiological thermoregulation in bigeye tuna, Thunnus obesus. Environ Biol Fish 40:319–327

    Article  Google Scholar 

  • Holland KN, Brill RW, Chang RK, Sibert JR, Fournier DA (1992) Physiological and behavioural thermoregulation in bigeye tuna (Thunnus obesus). Nature 358:410–412

    Article  CAS  Google Scholar 

  • Hoppe T, Matuschewski K, Rape M, Schlenker S, Ulrich HD, Jentsch S (2000) Activation of a membrane-bound transcription factor by regulated ubiquitin/proteasome-dependent processing. Cell 102:577–586

    Article  CAS  Google Scholar 

  • Hubold G (1991) Ecology of notothenioid fishes in the Weddell Sea. In: di Prisco G, Maresca B, Tota B (eds) Biology of Antarctic fish. Springer-Verlag, Berlin Heidelberg, pp 3–22

    Chapter  Google Scholar 

  • Idler DR, Fletcher GL, Belkhode S, King MJ, Hwang SJ (1989) Regulation of antifreeze protein production in winter flounder: a unique function of growth hormone. Gen Comp Endocrinol 74:327–334

    Article  CAS  Google Scholar 

  • Imamura S, Ojima N, Yamashita M (2002) Molecular cloning and cold-inducible gene expression of the cell division cycle gene CDC48 in zebrafish cells. Fish Sci 68:1291–1292

    Article  Google Scholar 

  • Imamura S, Ojima N, Yamashita M (2003) Cold-inducible expression of the cell division cycle gene CDC48 and its promotion of cell proliferation during cold acclimation in zebrafish. FEBS Lett 549:14–20

    Article  CAS  Google Scholar 

  • Imamura S, Yabu T, Yamashita M (2012) Protective role of cell division cycle 48 (CDC48) protein against neurodegeneration via ubiquitin-proteasome system dysfunction during zebrafish development. J Biol Chiem 287:23047–23056

    Article  CAS  Google Scholar 

  • Kitagawa Y, Ogawa M, Fukuchi M (1990) On the kidney of the saffron cod, Eleginus gracilis and its cold adaptation. Proc NIPR Symp Polar Biol 3:71–75

    Google Scholar 

  • Kitagawa T, Kimura S, Nakata H, Yamada H (2006) Thermal adaptation of Pacific bluefin tuna Thunnus orientalis to temperate waters. Fish Sci 72:149–156

    Article  CAS  Google Scholar 

  • Knox GA (2006) Biology of the Southern Ocean, 2nd edn. CRC Press, London

    Book  Google Scholar 

  • Ko TP, Robinson H, Gao YG, Cheng CH, DeVries AL, Wang AH (2003) The refined crystal structure of an eel pout type III antifreeze protein RD1 at 0.62-A resolution reveals structural microheterogeneity of protein and solvation. Biophys J 84:1228–1237

    Article  CAS  Google Scholar 

  • Latterich M, Frohlich KU, Schekman R (1995) Membrane fusion and the cell cycle: Cdc48p participates in the fusion of ER membranes. Cell 22:885–893

    Article  Google Scholar 

  • Li XM, Trinh KY, Hew CL, Buettner B, Baenziger J, Davies P (1985) Structure of an antifreeze polypeptide and its precursor from the ocean pout, Macrozoarces americanus. J Biol Chem 260:12904–12909

    CAS  PubMed  Google Scholar 

  • Little AG, Seebacher F (2013) Thyroid hormone regulates muscle function during cold acclimation in zebrafish (Danio rerio). J Exp Biol 216:3514–3521

    Article  CAS  Google Scholar 

  • Little AG, Seebacher F (2014) Thyroid hormone regulates cardiac performance during cold acclimation in zebrafish (Danio rerio). J Exp Biol 217:718–725

    Article  CAS  Google Scholar 

  • Little AG, Kunisue T, Kannan K, Seebacher F (2013) Thyroid hormone actions are temperature-specific and regulate thermal acclimation in zebrafish (Danio rerio). BMC Biol 11:26

    Article  CAS  Google Scholar 

  • Liu Y, Li Z, Lin Q, Kosinski J, Seetharaman J, Bujnicki JM, Sivaraman J (2007) Structure and evolutionary origin of Ca2+-dependent herring type II antifreeze protein. PLoS One 2:e548

    Article  Google Scholar 

  • Low WK, Miao M, Ewart KV, Yang DS, Fletcher GL, Hew CL (1998) Skin-type antifreeze protein from the shorthorn sculpin, Myoxocephalus scorpius. Expression and characterization of a Mr 9, 700 recombinant protein. J Biol Chem 273:23098–23103

    Article  CAS  Google Scholar 

  • Marshall CB, Chakrabartty A, Davies PL (2005) Hyperactive antifreeze protein from winter flounder is a very long rod-like dimer of alpha-helices. J Biol Chem 280:17920–17929

    Article  CAS  Google Scholar 

  • Martin KLM, Ishimatus A (2017) Review of reproductive strategies. In: Jaafar Z, Murdy EO (eds) Fishes out of water, biology and ecology of mudskippers. CBC Press, New York, pp 209–236

    Google Scholar 

  • Meyer H, Bug M, Bremer S (2012) Emerging functions of the VCP/p97 AAA-ATPase in the ubiquitin system. Nat Cell Biol 14:117–123

    Article  CAS  Google Scholar 

  • Moir D, Stewart SE, Osmond BC, Botstein D (1982) Cold-sensitive cell-division-cycle mutants of yeast: isolation, properties, and pseudoreversion studies. Genetics 100:547–563

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nakamura I, Goto Y, Sato K (2015) Ocean sunfish rewarm at the surface after deep excursions to forage for siphonophores. J Anim Ecol 84:590–603

    Article  Google Scholar 

  • Nishimiya Y, Kondo H, Takamichi M, Sugimoto H, Suzuki M, Miura A, Tsuda S (2008) Crystal structure and mutational analysis of Ca2+-independent type II antifreeze protein from longsnout poacher, Brachyopsis rostratus. J Mol Biol 382:734–746

    Article  CAS  Google Scholar 

  • Ogawa M, Sugai T, Murata J, Watanuki T (1997) Effects of salmon prolactin and growth hormone on plasma osmolality, Na+ concentration and protein content in the saffron cod. Fish Physiol Biochem 17:289–293

    Article  CAS  Google Scholar 

  • Pace C (2017) Aquatic and terrestrial locomotion. In: Jaafar Z, Murdy EO (eds) Fishes out of water, biology and ecology of mudskippers. CBC Press, New York, pp 195–208

    Google Scholar 

  • Quinn T (1999) Habitat characteristics of an intertidal aggregation of Pacific sandlance (Ammodytes hexapterus) at a North Puget Sound Beach in Washington. Northwest Sci 73:44–49

    Google Scholar 

  • Schurmann H, Christiansen JS (1994) Behavioral thermoregulation and swimming activity of two Arctic teleosts (subfamily gadinae) – the Polar cod (Boreogadus saida) and the navaga (Eleginus navaga). J Therm Biol 19:207–212

    Article  Google Scholar 

  • Scott GK, Hew CL, Davies PL (1985) Antifreeze protein genes are tandemly linked and clustered in the genome of the winter flounder. Proc Natl Acad Sci U S A 82:2613–2617

    Article  CAS  Google Scholar 

  • Slaughter D, Fletcher GL, Ananthanarayanan VS, Hew CL (1981) Antifreeze proteins from the sea raven, Hemitripterus americanus. Further evidence for diversity among fish polypeptide antifreezes. J Biol Chem 256:2022–2026

    CAS  PubMed  Google Scholar 

  • Sönnichsen FD, DeLuca C, Davies PL, Sykes BD (1996) Refined solution structure of type III antifreeze protein: hydrophobic groups may be involved in the energetics of the protein-ice interaction. Structure 4:1325–1337

    Article  Google Scholar 

  • Sorhannus U (2012) Evolution of type II antifreeze protein genes in teleost fish: a complex scenario involving lateral gene transfers and episodic directional selection. Evol Bioinforma 8:535–544

    Article  CAS  Google Scholar 

  • Stevens ED, Lam HM, Kendall J (1974) Vascular anatomy of the counter-current heat exchange of skipjack tuna. J Exp Biol 61:145–153

    CAS  PubMed  Google Scholar 

  • Stevens ED, Kanwisher JW, Carey FG (2000) Muscle temperature in free-swimming giant Atlantic bluefin tuna (Thunnus thynnus L.). J Therm Biol 25:419–423

    Article  CAS  Google Scholar 

  • Takegaki T, Fujii T, Ishimatsu A (2006) Overwintering habitat and low-temperature tolerance of the young mudskipper Boleophthalmus pectinirostris. Nippon Suisan Gakkaishi 72:880–885

    Article  Google Scholar 

  • Takei Y, Ando H, Tsutui K (2016) Handbook of hormones. Academic, Oxford

    Google Scholar 

  • Tomiyama M, Yanagibashi S (2004) Effect of temperature, age class, and growth on induction of aestivation in Japanese sandeel (Ammodytes personatus) in Ise Bay, central Japan. Fish Oceanogr 13:81–90

    Article  Google Scholar 

  • Tytler P, Vaughan T (1982) Thermal ecology of the mudskippers, Periophthalmus koelreuteri (Pallas) and Boleophthalmus boddarti (Pallas) of Kuwait Bay. J Fish Biol 23:327–337

    Article  Google Scholar 

  • Wegner NC, Snodgrass OE, Dewar H, Hyde JR (2015) Whole-body endothermy in a mesopelagic fish, the opah, Lampris guttatus. Science 348:786–789

    Article  CAS  Google Scholar 

  • Winslade P (1974) Behavioural studies on the lesser sandeel Ammodytes marinus (Raitt) III. The effect of temperature on activity and the environmental control of the annual cycle of activity. J Fish Biol 6:587–599

    Article  Google Scholar 

  • Wolf DH, Stolz A (2012) The Cdc48 machine in endoplasmic reticulum associated protein degradation. Biochem Biophys Acta 1823:117–124

    Article  CAS  Google Scholar 

  • Wootton RJ, Smith C (2015) Reproductive biology of teleost fish. Wiley Blackwell, West Sussex

    Google Scholar 

  • Yamashita M, Ojima N, Sakamoto T (1996) Induction of proteins in response to cold acclimation of rainbow trout cells. FEBS Lett 382:261–264

    Article  CAS  Google Scholar 

  • Yamashita Y, Miura R, Takemoto Y (2003) Type II antifreeze protein from a mid-latitude freshwater fish, Japanese smelt (Hypomesus nipponensis). Biosci Biotechnol Biochem 67:461–466

    Article  CAS  Google Scholar 

  • Ye Y, Meyer HH, Rapoport TA (2001) The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into cytosol. Nature 414:652–656

    Article  CAS  Google Scholar 

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Soyano, K., Mushirobira, Y. (2018). The Mechanism of Low-Temperature Tolerance in Fish. In: Iwaya-Inoue, M., Sakurai, M., Uemura, M. (eds) Survival Strategies in Extreme Cold and Desiccation. Advances in Experimental Medicine and Biology, vol 1081. Springer, Singapore. https://doi.org/10.1007/978-981-13-1244-1_9

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