Dietary routing of long-chain polyunsaturated fatty acids in soil food websand the importance of de novo synthesis by free-living nematodes and predatory mites

Abstract: Long-chain (≥ C20) polyunsaturated fatty acid (LC-PUFA) as content of foodsources are considered essential for growth, reproduction, and neural development of a widerange of animals. Partly, LC-PUFA derived signal molecules, as eicosanoids, are responsiblefor these effects. In contrast to aquatic ecosystems, LC-PUFAs seem not widely available interrestrial food webs. This applies in particular to ω3 LC-PUFA, where common opinion wasthat most animals cannot de novo synthesize them. Here we now experience a paradigm shift.Complete PUFA de novo synthesis requires the presence of Δ12 and ω3 fatty acid desaturase(FAD) enzymes. The free-living nematode Caenorhabditis elegans was the first animal inwhich these desaturates were found. This raises the question if soil dwelling nematodes as awhole offer substantial supply of these valuable nutritional compounds in terrestrial food webs.First, BLAST searches in available nematode genomes revealed the existence ofΔ12 FAD genes in almost all tested Chromadoria, but failed to identify orthologs in Dorylaimiaand Enoplia. Additionally, RT-PCR screens and functional FAD characterization screen acrossfree-living nematode species identified both novel Δ12 and ω3 FAD genes in several nematodetaxa. Second, this work followed the dietary routing of PUFA of different nematode strains,including mutants defective in its biosynthesis, to a predatory mite species, Hypoaspis aculeifer.The mites clearly reflected the PUFA-richness or -poorness of their nematode prey in theirneutral lipid fraction. Moreover, mites did benefit from LC-PUFA rich diet, as shown bysignificant weight gain and increased number of laid eggs. Interestingly, the comparatively highPUFA-content of mite’s phospholipid fraction remained rather unchanged, even in response toalmost PUFA-depleted nematode prey. This suggests that H. aculeifer also possesses themetabolic capability to de novo synthesize LC-PUFA. Third, eicosanoid pattern of the miteswas determined, revealing for the first time that H. aculeifer is able to produce LC-PUFAderived eicosanoids. Moreover, the production volume of these signaling molecules isassociated with the PUFA supply by the diet.