Helical antifreeze proteins have independently evolved in fishes on four occasions

PLoS One. 2013 Dec 6;8(12):e81285. doi: 10.1371/journal.pone.0081285. eCollection 2013.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alanine / genetics
  • Amino Acid Sequence
  • Animals
  • Antifreeze Proteins / chemistry*
  • Antifreeze Proteins / genetics*
  • Codon / genetics
  • DNA, Complementary / genetics
  • DNA, Intergenic / genetics
  • Databases, Protein
  • Evolution, Molecular*
  • Fish Proteins / chemistry
  • Fish Proteins / genetics
  • Fishes / genetics*
  • Molecular Sequence Data
  • Open Reading Frames / genetics
  • Protein Structure, Secondary
  • Species Specificity

Substances

  • Antifreeze Proteins
  • Codon
  • DNA, Complementary
  • DNA, Intergenic
  • Fish Proteins
  • antifreeze protein, Myoxocephalus scorpius
  • Alanine