De Novo Gene Evolution of Antifreeze Glycoproteins in Codfishes Revealed by Whole Genome Sequence Data

Abstract

New genes can arise through duplication of a pre-existing gene or de novo from non-coding DNA, providing raw material for evolution of new functions in response to a changing environment. A prime example is the independent evolution of antifreeze glycoprotein genes (afgps) in the Arctic codfishes and Antarctic notothenioids to prevent freezing. However, the highly repetitive nature of these genes complicates studies of their organization. In notothenioids, afgps evolved from an extant gene, yet the evolutionary origin of afgps in codfishes is unknown. Here, we demonstrate that afgps in codfishes have evolved de novo from non-coding DNA 13–18 Ma, coinciding with the cooling of the Northern Hemisphere. Using whole-genome sequence data from several codfishes and notothenioids, we find higher copy number of afgp in species exposed to more severe freezing suggesting a gene dosage effect. Notably, antifreeze function is lost in one lineage of codfishes analogous to the afgp losses in non-Antarctic notothenioids. This indicates that selection can eliminate the antifreeze function when freezing is no longer imminent. In addition, we show that evolution of afgp-assisting antifreeze potentiating protein genes (afpps) in notothenioids coincides with origin and lineage-specific losses of afgp. The origin of afgps in codfishes is one of the first examples of an essential gene born from non-coding DNA in a non-model species. Our study underlines the power of comparative genomics to uncover past molecular signatures of genome evolution, and further highlights the impact of de novo gene origin in response to a changing selection regime.

Stress-Induced Expression is Enriched for Evolutionarily Young Genes in Diverse Budding Yeasts

“…Previous works have linked some young genes to species and genus-specific adaptations, including movement on the surface of fast water in Rhagovelia water striders 37 , HIV-1 resistance in owl monkeys 38,39 , and the concurrent evolution of antifreeze proteins in several species [40][41][42] . Antifreeze protein genes are well-studied examples of young genes that arose via de novo gene origin events between 13 and 18 million years ago in codfishes and are present at variable copy number in some species 43 . Concurrently, the psychrophilic yeast G. antarctica, has evolved to encode nine antifreeze protein genes whose expression levels are induced by exposure to cold 15,44 .…”

Primordial emergence of a nucleic acid binding protein via phase separation and statistical ornithine to arginine conversion

“…If such polypeptides happen to provide some benefit, they may ultimately, through a series of duplications and fusions, and merging with other peptide fragments, yield a new folded and functional protein [2][3][4][5] . While also an ongoing process 6 , this mechanism of emergence foremost applies to the earliest proteins, regardless of whether the precursor polypeptides were formed by a primitive translation machinery, by other templatedriven processes 7 , or by spontaneous assembly 8 . However, crossing the peptide-protein divide remains a poorly-understood evolutionary process.…”

Universal and taxon-specific trends in protein sequences as a function of age

“…Although genes clearly originated de novo during the emergence of life, de novo gene birth after this unique event was once believed to be vanishingly rare (Jacob 1977;Keese & Gibbs 1992;Zuckerkandl 1975). Today, de novo gene birth is increasingly acknowledged to be real and important, with well-documented examples confirmed in diverse taxa (Baalsrud et al 2018;Cai et al 2008;Khalturin et al 2009;Milde et al 2009), despite the technical challenges associated with correctly identifying de novo genes (McLysaght & Hurst 2016). Compared to genes born early in the history of life, recently emerged de novo genes have had little time to evolve and adapt.…”