Lateral Transfer of a Lectin-Like Antifreeze Protein Gene in Fishes

Abstract

Fishes living in icy seawater are usually protected from freezing by endogenous antifreeze proteins (AFPs) that bind to ice crystals and stop them from growing. The scattered distribution of five highly diverse AFP types across phylogenetically disparate fish species is puzzling. The appearance of radically different AFPs in closely related species has been attributed to the rapid, independent evolution of these proteins in response to natural selection caused by sea level glaciations within the last 20 million years. In at least one instance the same type of simple repetitive AFP has independently originated in two distant species by convergent evolution. But, the isolated occurrence of three very similar type II AFPs in three distantly related species (herring, smelt and sea raven) cannot be explained by this mechanism. These globular, lectin-like AFPs have a unique disulfide-bonding pattern, and share up to 85% identity in their amino acid sequences, with regions of even higher identity in their genes. A thorough search of current databases failed to find a homolog in any other species with greater than 40% amino acid sequence identity. Consistent with this result, genomic Southern blots showed the lectin-like AFP gene was absent from all other fish species tested. The remarkable conservation of both intron and exon sequences, the lack of correlation between evolutionary distance and mutation rate, and the pattern of silent vs non-silent codon changes make it unlikely that the gene for this AFP pre-existed but was lost from most branches of the teleost radiation. We propose instead that lateral gene transfer has resulted in the occurrence of the type II AFPs in herring, smelt and sea raven and allowed these species to survive in an otherwise lethal niche.

Horizontal gene transfer between bacteria and animals

“…In animals, cases of eukaryote-to-eukaryote HGT include the recent acquisition of P elements by Drosophila melanogaster from Drosophila willistoni [4, 5], the horizontal transfer of lectin-like antifreeze proteins between fishes [6], and transfer of genes for carotenoid biosynthesis from fungi to pea aphids [7]. Recently, heritable HGT was even described in humans from the mitochondria-derived mini-circles in the eukaryote Trypanosoma cruzi , the causative agent of Chagas disease [8], suggesting HGT can occur in human germ cells.…”

A Review of Bacteria-Animal Lateral Gene Transfer May Inform Our Understanding of Diseases like Cancer

“…Yet, LGT can be detected in many animals, including vertebrates [11], [12]. For example, phylogenetically related antifreeze proteins in fish are scattered across disparate fish taxa, indicating a role for lateral gene transfer [13]. These proteins allow fish to survive at temperatures below freezing by preventing the formation of ice crystals [13].…”

“…For example, phylogenetically related antifreeze proteins in fish are scattered across disparate fish taxa, indicating a role for lateral gene transfer [13]. These proteins allow fish to survive at temperatures below freezing by preventing the formation of ice crystals [13]. Pea aphids and the two-spotted spider mite have both been found to synthesize carotenoids from an LGT that may have originated from fungi [14], [15].…”

Structural and functional diversity of the lectin repertoire in teleost fish: Relevance to innate and adaptive immunity

“…The type II antifreeze proteins (AFPs) present in plasma of arctic teleosts, such as herring (Atlantic herring Clupea harengus ), Pacific herring ( Clupea pallasii )) and sea raven ( Hemitripterus americanus ), are CTLs that have lost the capacity to bind sugars, instead disrupting the growth of ice crystals (Loewen et al, 1998). It has been recently proposed that the presence of AFPs in distantly related species such as herring, smelt ( Osmerus mordax ) and sea raven is the result of lateral gene transfer (Graham et al, 2008). Although FTLs have not been identified beyond the amphibians, the C1 and C2 domains of the human coagulation factor V (hCFV) not only share the FTL fold with the fish lectins, but also some of the key primary structure determinants that characterize this lectin family (Odom and Vasta, 2006; Bianchet et al, 2002).…”