Parasitic wasps do not lack lipogenesis

Abstract

Fatty acids are crucial primary metabolites for virtually all creatures on earth. Most organisms thus do not rely exclusively on a nutritional supply containing fatty acids, but have the ability to synthesize fatty acids and triacylglycerides de novo from carbohydrates in a process called lipogenesis. The ubiquity of lipogenesis has been questioned by a series of studies reporting that many parasitic wasps (parasitoids) do not accumulate lipid mass despite having unlimited access to sugar. This has been interpreted as an evolutionary metabolic trait loss in parasitoids. Here, we demonstrate de novo biosynthesis of fatty acids from 13 C-labelled α- d -glucose in 13 species of parasitoids from seven families. We furthermore show in the model organism Nasonia vitripennis that lipogenesis occurs even when lipid reserves are still intact, but relative 13 C-incorporation rates increase in females with widely depleted fat reserves. We therefore conclude that the presumed ‘lack of lipogenesis' in parasitoids needs to be re-evaluated.

Why do many parasitoids lack adult triglyceride accumulation, despite functioning fatty acid biosynthesis machinery?

“…Thus, we posit that it is important to consider the overall impact of lipid synthesis and accumulation. The very low amounts of fatty acid synthesis detected by Ruther et al (2021) are unlikely to play a critical role as an energy source or as an anabolic substrate for egg production, compared to the wasps' physiological requirements. In fact, a similar finding was proposed almost two decades ago by Giron and Casas (2003) who also found trace amounts of incorporation of glucose into fatty acids using radioactive labels, and concluded that there was no substantial lipogenesis occurring.…”

“…In a strictly chemical sense, the answer is no, but from the perspective of the accumulation of lipid stores for adult energetics and reproduction, we believe the answer is yes. Rather than a core conceptual disagreement between Ruther et al (2021) and us, this seems to be a semantic problem that we hope will be ameliorated by the use of term "lack of lipid accumulation" in future work.…”

“…Observing lack of lipid accumulation does not show absence of fatty acid synthesis (as clearly illustrated in foundational work by Giron & Casas 2003). This distinction is also important from a methodological point of view, because the gravimetric and colorimetric methods (based on weight, as in Visser et al, 2010, Visser et al, 2018, Visser et al, 2021, or conversion of chromophores measured by light absorbance, as in Muller et al, 2017, respectively) focus on bulk lipid accumulation, while the isotope method measures the synthesis of fatty acids (Giron & Casas, 2003;Prager et al, 2019;Ruther et al, 2021;Visser et al, 2012Visser et al, , 2017Visser et al, , 2021. Although the isotope tracing method provides valuable insights into fatty acid synthesis, some less sophisticated, but cost-effective methods, including gravimetry and colorimetry, still provide important biological insights about bulk lipid quantity, accumulation, and storage.…”

“…Second, there is a need for appropriate negative controls. Ruther et al (2021) compared incorporation rates of wasps that were fed with labeled glucose to wasps that were starved, meaning that two different and potentially confounding factors were varied at the same time: isotope labelling (yes or no) and feeding status (fed vs starved vs host-fed). An important control for incorporation of 13 C label from glucose into fatty acids in their study would be to measure wasps that were fed unlabeled glucose (as a negative control for the labeled glucose fed wasps).…”

“…The advantage of using deuterium is that it measures fatty acid synthesis from acetate, glucose or other precursors, and can provide insights also into other metabolic processes (Murphy, 2006). Therefore, Visser et al (2012Visser et al ( , 2017Visser et al ( , 2021 preferred to use deuterium over the fatty acid precursor ( 13 C labeled) glucose (Ruther et al 2021), and showed that tracing deuterium can detect a biologically relevant variation in fatty acid incorporation across treatments (Visser et al, 2021). Finally, when considering the synthesis of very small quantities of fatty acids within an insect, an alternative hypothesis to the insect synthesizing these fatty acids themselves is that microbes are involved.…”