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The Front-End Desaturase: Structure, Function, Evolution and Biotechnological Use

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The Front-End Desaturase: Structure, Function, Evolution and Biotechnological Use Lipids DOI 10.1007/s11745-011-3617-2 REVIEW The Front-end Desaturase: Structure, Function, Evolution and Biotechnological Use Dauenpen Meesapyodsuk • Xiao Qiu Received: 30 July 2011 / Accepted: 26 August 2011 Ó AOCS 2011 Abstract Very long chain polyunsaturated fatty acids engineer production of these fatty acids in transgenic oil- such as arachidonic acid (ARA, 20:4n-6), eicosapentaenoic seed plants for nutraceutical markets. acid (EPA, 20:5n-3), docosapentaenoic acid (DPA, 22:5n-3) and docosahexaenoic acid (DHA, 22:6n-3) are essential Keywords Desaturases Á n-3 fatty acids Á n-6 fatty acids Á components of cell membranes, and are precursors for a Polyunsaturated fatty acids (PUFA) Á Biotechnology Á group of hormone-like bioactive compounds (eicosanoids Lipid biochemistry Á General area and docosanoids) involved in regulation of various physi- ological activities in animals and humans. The biosynthesis of these fatty acids involves an alternating process of fatty Introduction acid desaturation and elongation. The desaturation is cat- alyzed by a unique class of oxygenases called front-end A desaturase is a special type of oxygenase that can remove desaturases that introduce double bonds between the pre- two hydrogens from a hydrocarbon chain, especially from a existing double bond and the carboxyl end of polyunsatu- fatty acyl chain, catalyzing the formation of a double bond rated fatty acids. The first gene encoding a front-end in the substrate [1, 2]. Unlike normal oxygenases which desaturase was cloned in 1993 from cyanobacteria. Since directly transfer molecular oxygen to a substrate; a desat- then, front-end desaturases have been identified and char- urase uses activated molecular oxygen to abstract hydro- acterized from a wide range of eukaryotic species including gens from the substrate creating a carbon/carbon double algae, protozoa, fungi, plants and animals including bond in a fatty acid and a molecule of water [1, 3]. humans. Unlike front-end desaturases from bacteria, those According to their regioselectivity, desaturases are typ- from eukaryotes are structurally characterized by the ically categorized as Dx desaturase that introduces a double presence of an N-terminal cytochrome b5-like domain bond at position x referred to from the carboxyl end of a fused to the main desaturation domain. Understanding the fatty acid; or xy desaturase that introduces a double bond structure, function and evolution of front-end desaturases, at position y referred to from the methyl end [4–6]. In as well as their roles in the biosynthesis of very long chain addition, desaturases can additionally be labelled as m?zor polyunsaturated fatty acids offers the opportunity to m-z desaturases. The m?z desaturase introduces a double bond at z carbons after the pre-existing double bond m,[7] i.e. towards the methyl end, while the m-z desaturase can D. Meesapyodsuk Á X. Qiu introduce a double bond at z carbons before the pre- Department of Food and Bioproduct Sciences, existing double bond m, i.e. towards the carboxyl end. An University of Saskatchewan, 51 Campus Drive, Saskatoon, SK S7N5A8, Canada example of a Dx desaturase is the acyl-ACP D9 desaturase from plants, a soluble enzyme introducing a first D9 double D. Meesapyodsuk Á X. Qiu (&) bond into saturated palmitoyl-ACP or stearoyl-ACP [8, 9]. Plant Biotechnology Institute, National Research The membrane-bound x3 desaturase from nematode Cae- Council of Canada, 110 Gymnasium Place, Saskatoon, SK S7N0W9, Canada norhabditis elegans is an example of a xy desaturase that e-mail: [email protected] inserts an x3 double bond into a polyunsaturated fatty acid 123 Lipids [10, 11]. An example of m?3 desaturase is the Claviceps purpurea ‘‘D12’’ desaturase that has a preference for introducing double bonds at the D12 position, three carbons after the pre-existing double bond at the ninth position [7], while the D4 desaturase from Thraustochytrium is cata- lytically a m-3 desaturase and can only introduce a double bond at position 4 which is three carbons before the pre- existing double bond at the seventh position [12]. Based on the position of the double bond insertion rel- ative to a pre-existing double bond in a fatty acyl chain, desaturases can also be referred to as front-end desaturases or methyl-end desaturases[13]. Unsaturated fatty acids are essential for all living species in which the initial de novo fatty acid synthesis generally results in production of sat- urated fatty acids with 18 carbons or 16 carbons in length. The first double bond is often inserted at approximately the middle position of a fatty acid chain. Fatty acids with different chain length and double bond position are gen- erated later by various fatty acid modifying enzymes, such as elongases and desaturases. A methyl-end desaturase introduces a double bond between the pre-existing double Fig. 1 Front-end desaturases involved in the biosynthesis of very bond and the methyl-end, while a front-end desaturase long chain polyunsaturated fatty acids. The dotted arrow indicates Sprecher’s pathway for DHA biosynthesis inserts a double bond between the pre-existing double bond and the carboxyl end of a fatty acid [14]. Commonly-found to dihomo-gamma-linolenic acid (DGLA, 20:3-8,11,14) membrane-bound xy and m?z desaturases such as ‘‘D12’’, and eicosatetraenoic acid (ETA, 20:4-8,11,14,17), which ‘‘D15’’ and x3 desaturases in plants are examples of are then desaturated by a second front-end desaturase—the methyl-end desaturases, while widely spread m-z desatu- D5 desaturase giving rise to arachidonic acid (ARA, 20:4- rases in microorganisms such as D4, D5, D6 and D8 5,8,11,14) and eicosapentaenoic acid (EPA, 20:5-5,8,11, desaturases belong to front-end desaturases. 14,17), respectively. EPA is elongated to docosapentaenoic Although both methyl-end desaturase and front-end acid (DPA, 22:5-7,10,13,16,19) which is then desaturated desaturase are involved in the biosynthesis of very long by a third front-end desaturase—the D4 desaturase, giving chain polyunsaturated fatty acids, their occurrence in living docosahexaenoic acid (DHA, 22:6-4,7,10,13,16,19) in the species is not identical. The former is widely present in x3 pathway. However, mammals including humans lack plants and microorganisms, while the latter mostly occur in the D4 desaturase. Biosynthesis of DHA in mammals takes animals and microorganisms, although certain types of ‘‘the retro-conversion pathway’’ [19] which involves two front-end desaturases have been identified in a small num- rounds of chain elongation of EPA and another D6 desat- ber of higher plants, such as borage [15], echium [16] and uration on the elongated product, followed by a single conifers [17]. Higher animals including humans lack the 2-carbon chain shortening of the D6 desaturated product in methyl-end desaturase such as ‘‘D12’’, ‘‘D15’’ and x3 the peroxisome, giving DHA. The D8 desaturase is another desaturase [18]. Consequently, they cannot synthesize lin- front-end desaturase involved in the biosynthesis of very oleic acid (LA, 18:2-9,12) and linolenic acid (ALA, 18:3- long chain polyunsaturated fatty acids [20–22]. This 9,12,15) from oleic acid (OA, 18:1-9), the two essential desaturase works on a branching pathway of the biosyn- fatty acids that have to be acquired from the diet. LA and thesis, introducing a D8 double bond into elongated prod- ALA are precursors for the biosynthesis of very long chain ucts LA or ALA, i.e. 20:2-11,14 or 20:3-11-14,17, giving polyunsaturated fatty acids such as arachidonic acid (20:4n- rise to DGLA and ETA, respectively, which can then be 6, ARA), eicosapentaenoic acid (20:5n-3, EPA) and doco- desaturated by a D5 desaturase, giving ARA and EPA as sahexaenoic acid (22:6n-3, DHA). As shown in Fig. 1,to described above (Fig. 1). The individual front-end desatu- synthesize these fatty acids, LA and ALA are desaturated by rases are described below. a first front-end desaturase—the D6 desaturase, introducing a D6 double bond into the substrates giving gamma-lino- D6 Desaturase lenic acid (GLA, 18:3-6,9,12) in the x6 pathway, and stearidonic acid (SDA, 18:4-6,9,12,15) in the x3 pathway, The first D-6 desaturase gene was cloned in 1993 from the respectively. GLA and SDA are elongated by a D6 elongase cyanobacterium Synechocystis using a gain-of-function 123 Lipids expression approach [23]. The protein sequence of this first who expressed the Synechocystis D6 desaturase under the front-end desaturase shows a similarity to other acyl-lipid control of a constitutive CaMV 35S promoter in tobacco. desaturases with different regioselectivity from cyanobac- Transgenic tobacco carrying the gene produced very small teria [23]. Like its homologous sequences, the D6 desat- amounts of GLA and SDA in leaves, but not in seeds [15, urase from Synechocystis does not contain a cytochrome 41]. That the prokaryotic D6 desaturase did not work well b5-like domain as was later found in eukaryotic D6 desat- in plants might be due to incompatible cofactors required urases. A similar D6 desaturase was later cloned from for the desaturation (see below). Production of high levels another cyanobacterium Spirulina platensis [24]. In 1997, of GLA and SDA, two D6 desaturated fatty acids, in the first eukaryotic D6 desaturase gene was cloned from transgenic oilseeds has since been achieved by several borage plant by two independent groups [15, 25]. Unlike other groups using eukaryotic D6 desaturases [42]. The bacterial D6 desaturases, the D6 desaturase encoded by this seed-specific expression of a fungal D6 desaturase and D12 gene is a modular protein that has a cytochrome b5-like desaturase from Mortierella alpina produced up to 43% domain fused to the N-terminus of the main desaturation GLA in seeds of Brassica napus [43].
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