Concurrence in the ability for lipid synthesis between life stages in insects

Visser, Bertanne; Willett, Denis S.; Harvey, Jeffrey A.; Alborn, Hans T.

doi:10.1098/rsos.160815

Cited by 26 publications

(33 citation statements)

References 47 publications

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“…Although this hypothesis seems weak based on the expected and obtained results for C:10D and C:12D, combined genomic and proteomic studies, such as the study of Li et al, are essential to improve our knowledge of fatty acid production in BSF 31 . Following this synthesis, C16:0 will be elongated to form longer-chain fatty acids (as C18:0D via the fatty acid elongase 6 /ELOVL 6 32 ), desaturated to generate unsaturated fatty acids or used for the synthesis of storage lipids 27 . The occurrence of C10 to C14 fatty acids can be explained by the action of an additional cytosolic thioesterase (e.g.…”

Section: Resultsmentioning

confidence: 99%

About lipid metabolism in Hermetia illucens (L. 1758): on the origin of fatty acids in prepupae

Hoc

Genva

Fauconnier

et al. 2020

Sci Rep

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Although increasingly targeted in animal nutrition, black soldier fly larvae or prepupae (BSF, Hermetia illucens L. 1758) require the characterization and modulation of their fatty acid profile to become fully integrated within the feed sector. This improvement will only be possible by the understanding of underlaying biochemical pathways of fatty acid synthesis in BSF. In this study, we hypothesized a labelling of de novo synthesized fatty acids in BSF by the incorporation of deuterated water (D 2 O) in their feed. Three batches of fifty larvae were reared on two diets with different polyunsaturated fatty acid profiles moistened with 40% of H 2 O or D 2 O: chicken feed or 40% of chicken feed and 60% of flax cake. Although the occurrence of D 2 O in insect feed increased the larval development time and decreased prepupal weight, it was possible to track the biosynthesis of fatty acids through deuterium labelling. Some fatty acids (decanoic, lauric or myristic acid) were exclusively present in their deuterated form while others (palmitic, palmitoleic or oleic acid) were found in two forms (deuterated or not) indicating that BSF can partially produce these fatty acids via biosynthesis pathways and not only by bioaccumulation from the diet. These results suggest the importance of carbohydrates as a source of acetyl-CoA in the constitution of the BSF fatty acid profile but also the potential importance of specific enzymes (e.g. thioesterase II or Δ12 fat2 desaturase) in BSF fatty acid metabolism. Finally, nearly no deuterated polyunsaturated fatty acids were found in BSF fed with deuterium confirming that BSF is not able to produce these types of fatty acids. Despite the high levels of linolenic acid in flax-enriched diets, BSF will simply bioaccumulate around 13% of this fatty acid and will metabolize approximately two-thirds of it into saturated fatty acids as lauric or myristic acid. Insects are increasingly identified as an environmentally sustainable source of proteins and lipids for food and feed but also for pharmaceutical or biodiesel applications 1-3. While yellow mealworm larvae (Tenebrio molitor L. 1758) appears to be the preferred model in human nutrition for environmental, nutritional and acceptability considerations 4-6 , larvae or prepupae of black soldier fly (BSF, Hermetia illucens L. 1758) emerges by their ability to develop rapidly and extensively on a wide range of decomposing material for the feed sector 7-9. Although possessing unquestionable nutritional qualities 9,10 , the incorporation of BSF into animal feed is still limited by several factors including their high lipid content (till approximately 40%) and their unbalanced fatty acid profile 10,11. As BSF fatty acid profile is known to be related with the one of their diet, several experiments have tried to manipulate their fatty acid profile with enriched feed formulation 8,12-14. By analysing the fatty acid profiles in BSF fed with different diets, it appeared that BSF larvae contain a high level of saturated fatty acids (SFAs, lauric acid...

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Section: Resultsmentioning

confidence: 99%

About lipid metabolism in Hermetia illucens (L. 1758): on the origin of fatty acids in prepupae

Hoc

Genva

Fauconnier

et al. 2020

Sci Rep

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“…The ability for lipid synthesis was lost repeatedly during the evolution of distinct parasitoid taxa, including beetles, flies, and wasps, as a consequence of the parasitic larval lifestyle (Visser et al., 2010). Parasitoid larvae can readily consume the lipid stores of their host, suggesting that lipid synthesis in parasitoids is redundant or even costly to maintain (Visser, Willett, Harvey, & Alborn, 2017). While the majority of parasitoids lack the ability for lipid synthesis, several phylogenetically distinct taxa were found capable of lipid synthesis (Visser et al., 2010).…”

Section: Introductionmentioning

confidence: 99%

“…Between-species variation in the ability for lipid synthesis became evident by testing a large number of taxonomically distinct parasitoid species (Visser et al, 2010), but only few species were tested repeatedly for the ability to synthesize lipids (Giron & Casas, 2003;Rivero & West, 2002;Visser et al, 2012Visser et al, , 2017). An exception are species in the genus Leptopilina, which have been popular model systems for a multitude of research fields, including, but not limited to, studies on (theoretical) ecology and behavior (e.g., foraging behavior), chemical communication (e.g., host-finding cues), life histories (e.g., time vs egg limitation), and physiology (e.g., host immunity) (Fleury, Gibert, Ris, & Allemand, 2009;Haccou, Vlas, Alphen, & Visser, 1991;Heavner et al, 2017;Janssen, van Alphen, Sabelis, & Bakker, 1995;Visser, van Alphen, & Hemerik, 1992;Wertheim, Vet, & Dicke, 2003).…”

Section: Introductionmentioning

confidence: 99%

Variation in lipid synthesis, but genetic homogeneity, among Leptopilina parasitic wasp populations

Visser

Hance

Noël

et al. 2018

Ecology and Evolution

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Lipid synthesis can have a major effect on survival and reproduction, yet most insect parasitoids fail to synthesize lipids. For parasitic wasps in the genus Leptopilina, however, studies have suggested that there is intraspecific variation in the ability for lipid synthesis. These studies were performed on only few populations, and a large‐scale investigation of both lipogenic ability and population genetic structure is now needed. Here, we first examined lipogenic ability of nine Leptopilina heterotoma populations collected in 2013 and found that five of nine populations synthesized lipids. The 2013 populations could not be used to determine genetic structure; hence, we obtained another 20 populations in 2016 that were tested for lipogenic ability. Thirteen of 20 populations (all Leptopilina heterotoma) were then used to determine the level of genetic differentiation (i.e., haplotype and nucleotide diversity) by sequencing neutral mitochondrial (COI) and nuclear (ITS2) markers. None of the 2016 populations synthesized lipids, and no genetic differentiation was found. Our results did reveal a nearly twofold increase in mean wasp lipid content at emergence in populations obtained in 2016 compared to 2013. We propose that our results can be explained by plasticity in lipid synthesis, where lipogenic ability is determined by environmental factors, such as developmental temperature and/or the amount of lipids carried over from the host.

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“…For example, several lineages of fungi are fatty acid auxotrophs, caused by loss or degradation 73 of the fatty acid synthase gene (Xu et al 2007;Luginbuehl et al 2017). Also, multiple insect lineages lack 74 lipogenesis as shown by labelling studies (Giron and Casas 2003;Visser et al 2012;Visser et al 2017) or 75 a lack of increase in adult fat reserves, despite feeding on sugar ad libitum (Ellers 1996; Visser and Ellers 76 2008). In insects, this recurrent loss of lipogenesis is phylogenetically linked to the parasitoid lifestyle: 77 parasitoid clades of flies, beetles and wasps have lost lipogenesis independently (Visser et al 2010).…”

Section: Introduction 40mentioning

confidence: 99%

Gene regulatory mechanisms underlying the evolutionary loss of a polygenic trait

Lammers

Kraaijeveld

Mariën

et al. 2018

Preprint

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Trait loss is a pervasive phenomenon in evolution, yet the underlying molecular causes have been identified in only a handful of cases. Most of these involve loss-of-function mutations in one or more trait-specific genes. Parasitoid insects are fatty acid auxotrophs: they lost the ability to convert dietary sugars into fatty acids, a trait that is ubiquitous among non-parasitoid animals and is enabled by a highly conserved set of genes. Earlier research suggests that lack of lipogenesis is caused by changes in gene regulation, rather than gene decay. We compared transcriptome-wide responses to sugar-feeding in the non-lipogenic parasitoid species Nasonia vitripennis and the lipogenic Drosophila melanogaster. Both species adjusted their metabolism within four hours after feeding, but there was little overlap at the gene level between the responses of the two species. Even at the pathway-level, there were sharp differences between the expression profiles of the two species, especially in carbohydrate and lipid metabolic pathways. Several genes coding for key enzymes in acetyl-CoA metabolism, such as malonyl-CoA decarboxylase (MCD) and HMG-CoA synthase differed in expression between the two species. Their combined action likely blocks lipogenesis in the parasitoid species. Network analysis indicates most genes involved in these pathways to be highly connected, which suggest they have pleiotropic effects and could explain the absence of gene degradation. Our results indicate that modification of expression levels of only a few non-connected genes, such as MCD, is sufficient to enable complete loss of lipogenesis in N. vitripennis.

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Concurrence in the ability for lipid synthesis between life stages in insects

Cited by 26 publications

References 47 publications

About lipid metabolism in Hermetia illucens (L. 1758): on the origin of fatty acids in prepupae

About lipid metabolism in Hermetia illucens (L. 1758): on the origin of fatty acids in prepupae

Variation in lipid synthesis, but genetic homogeneity, among Leptopilina parasitic wasp populations

Gene regulatory mechanisms underlying the evolutionary loss of a polygenic trait

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