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PLOS ONE  2013 

Helical Antifreeze Proteins Have Independently Evolved in Fishes on Four Occasions

DOI: 10.1371/journal.pone.0081285

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Abstract:

Alanine-rich α-helical (type I) antifreeze proteins (AFPs) are produced by a variety of fish species from three different orders to protect against freezing in icy seawater. Interspersed amongst and within these orders are fishes making AFPs that are completely different in both sequence and structure. The origin of this variety of types I, II, III and antifreeze glycoproteins (AFGPs) has been attributed to adaptation following sea-level glaciations that occurred after the divergence of most of the extant families of fish. The presence of similar types of AFPs in distantly related fishes has been ascribed to lateral gene transfer in the case of the structurally complex globular type II lectin-like AFPs and to convergent evolution for the AFGPs, which consist of a well-conserved tripeptide repeat. In this paper, we examine the genesis of the type I AFPs, which are intermediate in complexity. These predominantly α-helical peptides share many features, such as putative capping structures, Ala-richness and amphipathic character. We have added to the type I repertoire by cloning additional sequences from sculpin and have found that the similarities between the type I AFPs of the four distinct groups of fishes are not borne out at the nucleotide level. Both the non-coding sequences and the codon usage patterns are strikingly different. We propose that these AFPs arose via convergence from different progenitor helices with a weak affinity for ice and that their similarity is dictated by the propensity of specific amino acids to form helices and to align water on one side of the helix into an ice-like pattern.

References

[1]  Fletcher GL, Hew CL, Davies PL (2001) Antifreeze proteins of teleost fishes. Annu Rev Physiol 63: 359–390.
[2]  Ewart KV, Lin Q, Hew CL (1999) Structure, function and evolution of antifreeze proteins. Cell Mol Life Sci 55: 271–283.
[3]  Cheng CH (1998) Evolution of the diverse antifreeze proteins. Curr Opin Genet Dev 8: 715–720.
[4]  DeVries AL, Wohlschlag DE (1969) Freezing resistance in some Antarctic fishes. Science 163: 1073–1075.
[5]  Duman JG, DeVries AL (1974) Freezing resistance in winter flounder. Nature 274: 237–238.
[6]  Duman JG, de Vries AL (1976) Isolation, characterization, and physical properties of protein antifreezes from the winter flounder, Pseudopleuronectes americanus. Comp Biochem Physiol B 54: 375–380.
[7]  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.
[8]  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. Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology 155: 81–88.
[9]  Li XM, Trinh KY, Hew CL, Buettner B, Baenziger J, et al. (1985) Structure of an antifreeze polypeptide and its precursor from the ocean pout, Macrozoarces americanus. J Biol Chem 260: 12904–12909.
[10]  Raymond JA, DeVries AL (1977) Adsorption inhibition as a mechanism of freezing resistance in polar fishes. Proc Natl Acad Sci USA 74: 2589–2593.
[11]  Maeso I, Roy SW, Irimia M (2012) Widespread recurrent evolution of genomic features. Genome Biol Evol 4: 486–500.
[12]  Mallet J (2005) Hybridization as an invasion of the genome. Trends Ecol Evol 20: 229–237.
[13]  Doolittle RF (1994) Convergent evolution: the need to be explicit. Trends Biochem Sci 19: 15–18.
[14]  Losos JB (2011) Convergence, adaptation, and constraint. Evolution 65: 1827–1840.
[15]  Andersson JO (2005) Lateral gene transfer in eukaryotes. Cell Mol Life Sci 62: 1–16.
[16]  Baardsnes J, Davies PL (2001) Sialic acid synthase: the origin of fish type III antifreeze protein? Trends Biochem Sci 26: 468–469.
[17]  Deng C, Cheng CH, Ye H, He X, Chen L (2010) Evolution of an antifreeze protein by neofunctionalization under escape from adaptive conflict. Proc Natl Acad Sci U S A.
[18]  Cheng CH, Chen L, Near TJ, Jin Y (2003) Functional antifreeze glycoprotein genes in temperate-water New Zealand nototheniid fish infer an Antarctic evolutionary origin. Mol Biol Evol 20: 1897–1908.
[19]  Chen L, DeVries AL, Cheng CH (1997) Evolution of antifreeze glycoprotein gene from a trypsinogen gene in Antarctic notothenioid fish. Proc Natl Acad Sci USA 94: 3811–3816.
[20]  Chen L, DeVries AL, Cheng CH (1997) Convergent evolution of antifreeze glycoproteins in Antarctic notothenioid fish and Arctic cod. Proc Natl Acad Sci USA 94: 3817–3822.
[21]  Liu Y, Li Z, Lin Q, Kosinski J, Seetharaman J, et al. (2007) Structure and evolutionary origin of Ca2+-dependent herring type II antifreeze protein. PLoS ONE 2: e548.
[22]  Graham LA, Lougheed SC, Ewart KV, Davies PL (2008) Lateral transfer of a lectin-like antifreeze protein gene in fishes. PLoS ONE 3: e2616.
[23]  Graham LA, Liou YC, Walker VK, Davies PL (1997) Hyperactive antifreeze protein from beetles. Nature 388: 727–728.
[24]  Ng NF, Trinh KY, Hew CL (1986) Structure of an antifreeze polypeptide precursor from the sea raven, Hemitripterus americanus. J Biol Chem 261: 15690–15695.
[25]  Low WK, Lin Q, Stathakis C, Miao M, Fletcher GL, et al. (2001) Isolation and characterization of skin-type, type I antifreeze polypeptides from the longhorn sculpin, Myoxocephalus octodecemspinosus. J Biol Chem 276: 11582–11589.
[26]  Hew CL, Joshi S, Wang NC, Kao MH, Ananthanarayanan VS (1985) Structures of shorthorn sculpin antifreeze polypeptides. Eur J Biochem 151: 167–172.
[27]  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 USA 82: 2613–2617.
[28]  Eyles N (2008) Glacio-epochs and the supercontinent cycle after ~3.0 Ga: Tectonic boundary conditions for glaciation. Palaeogeography Palaeoclimatology Palaeoecology 258: 89–129.
[29]  DeConto RM, Pollard D, Wilson PA, Palike H, Lear CH, et al. (2008) Thresholds for Cenozoic bipolar glaciation. Nature 455: 652–U652.
[30]  Hew CL, Fletcher GL, Ananthanarayanan VS (1980) Antifreeze proteins from the shorthorn sculpin, Myoxocephalus scorpius: isolation and characterization. Can J Biochem 58: 377–383.
[31]  Evans RP, Fletcher GL (2001) Isolation and characterization of type I antifreeze proteins from Atlantic snailfish (Liparis atlanticus) and dusky snailfish (Liparis gibbus). Biochim Biophys Acta 1547: 235–244.
[32]  Hobbs RS, Shears MA, Graham LA, Davies PL, Fletcher GL (2011) Isolation and characterization of type I antifreeze proteins from cunner, Tautogolabrus adspersus, order Perciformes. FEBS J 278: 3699–3710.
[33]  Gourlie B, Lin Y, Price J, DeVries AL, Powers D, et al. (1984) Winter flounder antifreeze proteins: a multigene family. J Biol Chem 259: 14960–14965.
[34]  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.
[35]  Marshall CB, Fletcher GL, Davies PL (2004) Hyperactive antifreeze protein in a fish. Nature 429: 153.
[36]  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.
[37]  Graham LA, Marshall CB, Lin FH, Campbell RL, Davies PL (2008) Hyperactive antifreeze protein from fish contains multiple ice-binding sites. Biochemistry 47: 2051–2063.
[38]  Baardsnes J, Jelokhani-Niaraki M, Kondejewski LH, Kuiper MJ, Kay CM, et al. (2001) Antifreeze protein from shorthorn sculpin: identification of the ice-binding surface. Protein Sci 10: 2566–2576.
[39]  Low WK, Miao M, Ewart KV, Yang DS, Fletcher GL, et al. (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.
[40]  Rice P, Longden I, Bleasby A (2000) EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16: 276–277.
[41]  Baardsnes J, Kondejewski LH, Hodges RS, Chao H, Kay C, et al. (1999) New ice-binding face for type I antifreeze protein. FEBS Lett 463: 87–91.
[42]  Evans RP, Fletcher GL (2005) Type I antifreeze proteins expressed in snailfish skin are identical to their plasma counterparts. Febs J 272: 5327–5336.
[43]  Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW (2011) GenBank. Nucleic Acids Res 39: D32–37.
[44]  Evans RP, Fletcher GL (2005) Type I antifreeze proteins: possible origins from chorion and keratin genes in Atlantic snailfish. J Mol Evol 61: 417–424.
[45]  Matschiner M, Hanel R, Salzburger W (2011) On the origin and trigger of the notothenioid adaptive radiation. PLoS One 6: e18911.
[46]  Peng Z, He S, Wang J, Wang W, Diogo R (2006) Mitochondrial molecular clocks and the origin of the major Otocephalan clades (Pisces: Teleostei): A new insight. Gene 370: 113–124.
[47]  Steinke D, Salzburger W, Meyer A (2006) Novel relationships among ten fish model species revealed based on a phylogenomic analysis using ESTs. J Mol Evol 62: 772–784.
[48]  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.
[49]  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 Bioinform Online 8: 535–544.
[50]  Gong Z, King MJ, Fletcher GL, Hew CL (1995) The antifreeze protein genes of the winter flounder, Pleuronectus americanus, are differentially regulated in liver and non-liver tissues. Biochem Biophys Res Commun 206: 387–392.
[51]  Kwan AH, Fairley K, Anderberg PI, Liew CW, Harding MM, et al. (2005) Solution structure of a recombinant type I sculpin antifreeze protein. Biochemistry 44: 1980–1988.
[52]  Sicheri F, Yang DS (1995) Ice-binding structure and mechanism of an antifreeze protein from winter flounder. Nature 375: 427–431.
[53]  Pace CN, Scholtz JM (1998) A helix propensity scale based on experimental studies of peptides and proteins. Biophys J 75: 422–427.
[54]  Chakrabartty A, Ananthanarayanan VS, Hew CL (1989) Structure-function relationships in a winter flounder antifreeze polypeptide. I. Stabilization of an alpha-helical antifreeze polypeptide by charged-group and hydrophobic interactions. J Biol Chem 264: 11307–11312.
[55]  Yang DS, Sax M, Chakrabartty A, Hew CL (1988) Crystal structure of an antifreeze polypeptide and its mechanistic implications. Nature 333: 232–237.
[56]  Liou YC, Tocilj A, Davies PL, Jia Z (2000) Mimicry of ice structure by surface hydroxyls and water of a beta-helix antifreeze protein. Nature 406: 322–324.
[57]  Graether SP, Kuiper MJ, Gagne SM, Walker VK, Jia Z, et al. (2000) Beta-helix structure and ice-binding properties of a hyperactive antifreeze protein from an insect. Nature 406: 325–328.
[58]  Leinala EK, Davies PL, Jia Z (2002) Crystal structure of beta-helical antifreeze protein points to a general ice binding model. Structure (Camb) 10: 619–627.
[59]  Garnham CP, Campbell RL, Davies PL (2011) Anchored clathrate waters bind antifreeze proteins to ice. Proc Natl Acad Sci U S A 108: 7363–7367.
[60]  Middleton AJ, Marshall CB, Faucher F, Bar-Dolev M, Braslavsky I, et al. (2012) Antifreeze protein from freeze-tolerant grass has a beta-roll fold with an irregularly structured ice-binding site. J Mol Biol 416: 713–724.
[61]  Kondo H, Hanada Y, Sugimoto H, Hoshino T, Garnham CP, et al. (2012) Ice-binding site of snow mold fungus antifreeze protein deviates from structural regularity and high conservation. Proc Natl Acad Sci U S A 109: 9360–9365.
[62]  Chao H, Houston ME Jr, Hodges RS, Kay CM, Sykes BD, et al. (1997) A diminished role for hydrogen bonds in antifreeze protein binding to ice. Biochemistry 36: 14652–14660.
[63]  Pentelute BL, Gates ZP, Tereshko V, Dashnau JL, Vanderkooi JM, et al. (2008) X-ray structure of snow flea antifreeze protein determined by racemic crystallization of synthetic protein enantiomers. J Am Chem Soc 130: 9695–9701.
[64]  Mok YF, Lin FH, Graham LA, Celik Y, Braslavsky I, et al. (2010) Structural basis for the superior activity of the large isoform of snow flea antifreeze protein. Biochemistry 49: 2593–2603.
[65]  Loh YH, Brenner S, Venkatesh B (2008) Investigation of loss and gain of introns in the compact genomes of pufferfishes (Fugu and Tetraodon). Mol Biol Evol 25: 526–535.
[66]  Evans RP, Fletcher GL (2004) Isolation and purification of antifreeze proteins from skin tissues of snailfish, cunner and sea raven. Biochim Biophys Acta 1700: 209–217.
[67]  Miya M, Takeshima H, Endo H, Ishiguro NB, Inoue JG, et al. (2003) Major patterns of higher teleostean phylogenies: a new perspective based on 100 complete mitochondrial DNA sequences. Mol Phylogenet Evol 26: 121–138.
[68]  Mabuchi K, Miya M, Azuma Y, Nishida M (2007) Independent evolution of the specialized pharyngeal jaw apparatus in cichlid and labrid fishes. BMC Evol Biol 7: 10.
[69]  Lavoue S, Miya M, Saitoh K, Ishiguro NB, Nishida M (2007) Phylogenetic relationships among anchovies, sardines, herrings and their relatives (Clupeiformes), inferred from whole mitogenome sequences. Mol Phylogenet Evol 43: 1096–1105.
[70]  Marqusee S, Baldwin RL (1987) Helix stabilization by Glu-…Lys+ salt bridges in short peptides of de novo design. Proc Natl Acad Sci U S A 84: 8898–8902.
[71]  Hobbs RS, Fletcher GL (2013) Epithelial dominant expression of antifreeze proteins in cunner suggests recent entry into a high freeze-risk ecozone. Comp Biochem Physiol A Mol Integr Physiol 164: 111–118.

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