Unique fatty acid desaturase capacities uncovered in Hediste diversicolor illustrate the roles of aquatic invertebrates in trophic upgrading

Abstract

Omega-3 (ω3 or n-3) long-chain polyunsaturated fatty acids (PUFA), including eicosapentaenoic acid and docosahexaenoic acid (DHA), play physiologically important roles in vertebrates. These compounds have long been believed to have originated almost exclusively from aquatic (mostly marine) single-cell organisms. Yet, a recent study has discovered that many invertebrates possess a type of enzymes called methyl-end desaturases (ωx) that enables them to endogenously produce n-3 long-chain PUFA and could make a significant contribution to production of these compounds in the marine environment. Polychaetes are major components of benthic fauna and thus important to maintain a robust food web as a recycler of organic matter and a prey item for higher trophic level species like fish. In the present study, we investigated the ωx enzymes from the common ragworm, Hediste diversicolor, a common inhabitant in sedimentary littoral ecosystems of the North Atlantic. Functional assays of the H. diversicolorωx demonstrated unique desaturation capacities. An ω3 desaturase mediated the conversion of n-6 fatty acid substrates into their corresponding n-3 products including DHA. A further enzyme possessed unique regioselectivities combining both ω6 and ω3 desaturase activities. These results illustrate that the long-chain PUFA biosynthetic enzymatic machinery of aquatic invertebrates such as polychaetes is highly diverse and clarify that invertebrates can be major contributors to fatty acid trophic upgrading in aquatic food webs. This article is part of the theme issue 'The next horizons for lipids as 'trophic biomarkers': evidence and significance of consumer modification of dietary fatty acids'.

Keywords: biosynthesis; methyl-end desaturase; n-3 long-chain PUFA; polychaetes.

Figure 1.

General biosynthetic pathway of polyunsaturated fatty acids.

Figure 2.

Maximum-likelihood phylogenetic tree comparing the deduced aa sequence of H. diversicolor ωx1 and ωx2 with ωx desaturase from various animal species. The bootstrap support value (%) is given in each node. Clades 1–3 correspond to clusters established by Kabeya et al. [20].

Figure 3.

Representative chromatograms of FAME samples prepared from the transgenic yeast transformed with the H. diversicolor ωx1. Transgenic yeast expressing the coding region of the H. diversicolor ωx1 were grown in the absence (a) and presence of exogenously supplemented fatty acid substrates including 20:1n-9 (b), 20:3n-9 (c) and 20:4n-6 (d). The yeast endogenous fatty acids (16:0, 16:1 isomers, 18:0 and 18:1n-9) are indicated as 1–4 in all panels. Additional peaks corresponding to products resulting from Δ12 desaturation products of yeast endogenous fatty acids (16:2n-4 and 18:2n-6) and from Δ15 desaturation (18:3n-3) are indicated in all panels. Peaks corresponding to exogenously added fatty acids are indicated with an asterisk (*) (b–d).

Figure 4.

Representative chromatograms of FAME samples prepared from the transgenic yeast transformed with the H. diversicolor ωx2. Transgenic yeast expressing the coding region of the H. diversicolor ωx2 were grown in the presence of exogenously supplemented fatty acid substrates, including 18:2n-6 (a), 20:4n-6 (b), 22:4n-6 (c) and 22:5n-6 (d). Peaks corresponding to exogenously added fatty acids are indicated with an asterisk (*) in each panel. The yeast endogenous fatty acids (16:0, 16:1 isomers, 18:0 and 18:1n-9) are indicated as 1–4 in all panels.