Abstract

BackgroundProvision of long-chain polyunsaturated fatty acids (LC-PUFA) in vertebrates occurs through the diet or via endogenous production from C18 precursors through consecutive elongations and desaturations. It has been postulated that the abundance of LC-PUFA in the marine environment has remarkably modulated the gene complement and function of Fads in marine teleosts. In vertebrates two fatty acyl desaturases, namely Fads1 and Fads2, encode ∆5 and ∆6 desaturases, respectively. To fully clarify the evolutionary history of LC-PUFA biosynthesis in vertebrates, we investigated the gene repertoire and function of Fads from species placed at key evolutionary nodes.ResultsWe demonstrate that functional Fads1Δ5 and Fads2∆6 arose from a tandem gene duplication in the ancestor of vertebrates, since they are present in the Arctic lamprey. Additionally, we show that a similar condition was retained in ray-finned fish such as the Senegal bichir and spotted gar, with the identification of fads1 genes in these lineages. Functional characterisation of the isolated desaturases reveals the first case of a Fads1 enzyme with ∆5 desaturase activity in the Teleostei lineage, the Elopomorpha. In contrast, in Osteoglossomorpha genomes, while no fads1 was identified, two separate fads2 duplicates with ∆6 and ∆5 desaturase activities respectively were uncovered.ConclusionsWe conclude that, while the essential genetic components involved LC-PUFA biosynthesis evolved in the vertebrate ancestor, the full completion of the LC-PUFA biosynthesis pathway arose uniquely in gnathostomes.

Highlights

  • Provision of long-chain polyunsaturated fatty acids (LC-Polyunsaturated fatty acids (PUFA)) in vertebrates occurs through the diet or via endogenous production from C18 precursors through consecutive elongations and desaturations

  • In the Fads1 group, in addition to the described gene orthologues from various lobe-finned fish (e.g. Latimeria chalumnae) and Chondrichthyes species (C. milii and S. canicula) [9], we find a putative Fads1 from the Arctic lamprey (L. camtschaticum), the Senegal bichir (P. senegalus), spotted gar (L. oculatus) and the teleost Japanese eel (A. japonica), but not in the Osteoglossomorpha or any other teleost examined (Fig. 1)

  • Gene orthologues of fads1 and fads2 emerged in the ancestor of vertebrates To address the orthology of the identified fatty acyl desaturase (Fads)-like sequences an Maximum Likelihood (ML) phylogenetic analysis was conducted with a total of 86 amino acid sequences, including species from cyclostomes (e.g. Arctic lamprey L. camtschaticum), tetrapods, Chondrichthyes, ray-finned fishes (e.g. P. senegalus, L. oculatus, A. japonica and P. buchholzi), as well as Fads sequences from several protostomes (Capitella teleta, Lingula anatina and Lottia gigantea) and the

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Summary

Introduction

Provision of long-chain polyunsaturated fatty acids (LC-PUFA) in vertebrates occurs through the diet or via endogenous production from C18 precursors through consecutive elongations and desaturations. Long-chain (≥C20) polyunsaturated fatty acids (LC-PUFA) and their derivatives are biologically active molecules that are involved in neural function, signalling and regulation of lipid metabolism, inflammation and cell division [1]. Δ5 and Δ6 desaturation reactions are catalysed by FADS1 and FADS2 enzymes, respectively [2]. Orthologues of both fads1Δ5 and fads2Δ6 were previously identified in the cartilaginous fish Scyliorhinus canicula, an indication that they emerged before gnathostome origin [9]. Many Teleostei Fads retain the Δ6 desaturase phenotype but, interestingly, they exhibit a more varied spectrum of activities including bifunctional Δ6Δ5 desaturase [10,11,12,13] and Δ4 desaturase [7] as a result of a functionalisation process hypothesised to have occurred in response to dietary availability in natural prey [9]

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