Smelt was the likely beneficiary of an antifreeze gene laterally transferred between fishes

Abstract

BackgroundType II antifreeze protein (AFP) from the rainbow smelt, Osmerus mordax, is a calcium-dependent C-type lectin homolog, similar to the AFPs from herring and sea raven. While C-type lectins are ubiquitous, type II AFPs are only found in a few species in three widely separated branches of teleost fishes. Furthermore, several other non-homologous AFPs are found in intervening species. We have previously postulated that this sporadic distribution has resulted from lateral gene transfer. The alternative hypothesis, that the AFP evolved from a lectin present in a shared ancestor and that this gene was lost in most species, is not favored because both the exon and intron sequences are highly conserved.ResultsHere we have sequenced and annotated a 160 kb smelt BAC clone containing a centrally-located AFP gene along with 14 other genes. Quantitative PCR indicates that there is but a single copy of this gene within the smelt genome, which is atypical for fish AFP genes. The corresponding syntenic region has been identified and searched in a number of other species and found to be devoid of lectin or AFP sequences. Unlike the introns of the AFP gene, the intronic sequences of the flanking genes are not conserved between species. As well, the rate and pattern of mutation in the AFP gene are radically different from those seen in other smelt and herring genes.ConclusionsThese results provide stand-alone support for an example of lateral gene transfer between vertebrate species. They should further inform the debate about genetically modified organisms by showing that gene transfer between ‘higher’ eukaryotes can occur naturally. Analysis of the syntenic regions from several fishes strongly suggests that the smelt acquired the AFP gene from the herring.

Horizontal gene transfer: building the web of life

“…This model could potentially explain the fact that genes are frequently acquired in plants and animals that have eggs associated with endosymbionts or exposed to exterior environments (for example, mosses, Drosophila spp. and nematodes) 23,31,32 .…”

“…Sturgeons, lampreys, which have been known to feed on sturgeons, and paddle fishes all share a transposable element, probably the result of HGT mediated by the exchange of fluids during lamprey feeding 99 . The sporadic distribution of type II antifreeze protein (AFP) genes in herring, smelt and sea raven was also mediated by HGT, allowing these fish to adapt to icy water 31 .…”

Massive horizontal transfer of transposable elements in insects

“…The majority of genes horizontally acquired by eukaryotes come from bacteria, but the extent to which these transfers have contributed to eukaryote evolution is still unclear (3, 4). Gene transfers from eukaryote to eukaryote appear to be largely limited to filamentous organisms, such as oomycetes and fungi (5, 6).In animals and plants, very few cases of such horizontal gene transfers (HGTs) have been reported so far (7,8). In fact, most of the genetic material that is horizontally transferred in animals and plants consists of transposable elements (TEs) (9-11), which are pieces of DNA able to move from a chromosomal locus to another (12).…”

“…In animals and plants, very few cases of such horizontal gene transfers (HGTs) have been reported so far (7,8). In fact, most of the genetic material that is horizontally transferred in animals and plants consists of transposable elements (TEs) (9-11), which are pieces of DNA able to move from a chromosomal locus to another (12).…”

Rainbow smelt: the unusual case of cryoprotection by sustained glycerol production in an aquatic animal

“…There is only a single copy of the AFP gene, consistent with the relatively low levels of the protein compared to other fish that utilize the AFP strategy (Graham et al 2012). The seasonal level of AFP follows the same pattern as the increase in plasma glycerol, but does not decrease to the same extent as glycerol during the March to June period.…”