Abstract
The biosynthesis of long-chain polyunsaturated fatty acids (LC-PUFA) provides an intriguing example on how multi-enzymatic cascades evolve. Essential LC-PUFA, such as arachidonic, eicosapentaenoic, and docosahexaenoic acids (DHA), can be acquired from the diet but are also endogenously retailored from C18 precursors through consecutive elongations and desaturations catalyzed, respectively, by fatty acyl elongase and desaturase enzymes. The molecular wiring of this enzymatic pathway defines the ability of a species to biosynthesize LC-PUFA. Exactly when and how in animal evolution a functional LC-PUFA pathway emerged is still elusive. Here we examine key components of the LC-PUFA cascade, the Elovl2/Elovl5 elongases, from amphioxus, an invertebrate chordate, the sea lamprey, a representative of agnathans, and the elephant shark, a basal jawed vertebrate. We show that Elovl2 and Elovl5 emerged from genome duplications in vertebrate ancestry. The single Elovl2/5 from amphioxus efficiently elongates C18 and C20 and, to a marked lesser extent, C22 LC-PUFA. Lamprey is incapable of elongating C22 substrates. The elephant shark Elovl2 showed that the ability to efficiently elongate C22 PUFA and thus to synthesize DHA through the Sprecher pathway, emerged in the jawed vertebrate ancestor. Our findings illustrate how non-integrated “metabolic islands” evolve into fully wired pathways upon duplication and neofunctionalization.
Highlights
The origin of complexity in living systems is a central question in evolution[1,2]
We analyzed the repertoire of Elovl[2] and
The retrieved sequence dataset was used for phylogenetic reconstruction employing two methods, Bayesian analysis (BA) and Maximum likelihood (ML)
Summary
The origin of complexity in living systems is a central question in evolution[1,2]. Pairwise interactions between molecules (e.g. ligand and receptors; enzymes and their substrates) and the impact of gene duplication on protein function have provided crucial insight into the understanding of physiological diversity[3]. An elovl[2] orthologue has been identified only in Atlantic salmon[10] (Salmo salar), zebrafish[27] (Danio rerio) and rainbow trout[28] (Oncorhynchus mykiss), and with ray-finned fishes (including most marine species) appearing to lack elovl[2] in their genomes[11] Similar to their tetrapod counterparts, teleost elovl[2] demonstrated the capacity to elongate DPA and contribute to DHA production through the so-called “Sprecher pathway”[29] (Fig. 1A). The desaturase abilities in mollusks are markedly different when compared to mammals and teleosts, since only Δ 5 desaturases have been described so far[33,34,35] (Fig. 1A) These results suggest a complex scenario regarding the evolutionary emergence of a complete LC-PUFA biosynthetic pathway. By examining three species, including the European amphioxus (Branchiostoma lanceolatum, cephalochordate), the sea lamprey (Petromyzon marinus, agnathan) and the elephant shark (Callorhinchus milii, basal gnathostome), we provide an insightful snapshot into the evolution of critical enzymes dictating the LC-PUFA biosynthetic pathways in chordates
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