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Lipidomics Reveals How the Endoparasitoid Wasp Pteromalus Puparum Manipulates Host Energy Stores for Its Young

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Lipidomics Reveals How the Endoparasitoid Wasp Pteromalus Puparum Manipulates Host Energy Stores for Its Young Lipidomics reveals how the endoparasitoid wasp Pteromalus puparum manipulates host energy stores for its young Item Type Article Authors Wang, Jiale; Jin, Hongxia; Schlenke, Todd; Yang, Yi; Wang, Fang; Yao, Hongwei; Fang, Qi; Ye, Gongyin Citation Wang, J., Jin, H., Schlenke, T., Yang, Y., Wang, F., Yao, H., ... & Ye, G. (2020). Lipidomics reveals how the endoparasitoid wasp Pteromalus puparum manipulates host energy stores for its young. Biochimica et Biophysica Acta (BBA)-Molecular and Cell Biology of Lipids, 158736. DOI 10.1016/j.bbalip.2020.158736 Publisher ELSEVIER Journal BIOCHIMICA ET BIOPHYSICA ACTA-MOLECULAR AND CELL BIOLOGY OF LIPIDS Rights Copyright © 2020 Elsevier B.V. All rights reserved. Download date 08/10/2021 08:45:24 Item License http://rightsstatements.org/vocab/InC/1.0/ Version Final accepted manuscript Link to Item http://hdl.handle.net/10150/648043 Lipidomics reveals how the endoparasitoid wasp Pteromalus puparum manipulates host energy stores for its young Jiale Wang 1,2, Hongxia Jin 1, Todd Schlenke 2, Yi Yang 1, Fang Wang1, Hongwei Yao1, Qi Fang1 and Gongyin Ye 1* 1State Key Laboratory of Rice Biology & Agricultural and Rural Affairs Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, China 2Department of Entomology, University of Arizona, Tucson AZ, USA *Corresponding author: Gongyin Ye, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, China (e-mail: [email protected]). 1 Highlights: After the infection by an endoparasitoid Pteromalus puparum, levels of 87 and 117 lipids significantly change in the fat body and hemolymph of the cabbage butterfly Pieris rapae, respectively. In host P. rapae fat body, levels of highly unsaturated triacylglycerides increased post-infection while more saturated forms decreased. Membrane phospholipid levels mostly decreased in host fat body but increased in hemolymph post-infection. Levels of the necessary dietary lipid for insects - cholesteryl esters - dramatically increased in host hemolymph following infection. Abstract: Endoparasitoid wasps inject venom along with their eggs to adjust the physiological and nutritional environment inside their hosts to benefit the development of their offspring. In particular, wasp venoms are known to modify host lipid metabolism, lipid storage in the fat body, and release of lipids into the hemolymph, but how venoms accomplish these functions remains unclear. Here, we use an UPLC-MS-based lipidomics approach to analyze the identities and concentrations of lipids in both fat body and hemolymph of host cabbage butterfly (Pieris rapae) infected by the pupal endoparasitoid Pteromalus puparum. During infection, host fat body levels of highly unsaturated, soluble triacylglycerides (TAGs) increased while less unsaturated, less soluble forms decreased. Furthermore, in infected host hemolymph, overall levels of TAG and phospholipids (the major component of cell membranes) increased, suggesting that fat body cells are destroyed and their contents are dispersed. Altogether, these data suggest that wasp venom induces host fat body TAGs to be transformed into lower melting point (more liquid) forms and released into the host hemolymph following infection, allowing simple absorption and nutritional acquisition by wasp larvae. Finally, cholesteryl esters (CEs, a dietary lipid derived from cholesterol) increased in host hemolymph following 2 infection with no concomitant decrease in host cholesterol, implying that the wasp may provide this necessary food resource to its offspring via its venom. This study provides novel insight into how parasitoid infection alters lipid metabolism in insect hosts, and begins to uncover the wasp venom proteins responsible for host physiological changes and offspring development. Keywords: Lipidomics; Hemolymph; Fat body; Pteromalus puparum; Pieris rapae; Lipid. 3 1 Introduction Parasitoid wasps are used in the biocontrol of insect pest populations around the world [1]. These wasps lay their eggs inside (endoparasitoids) or outside (ectoparasitoids) of their hosts’ bodies, and once hatched the wasp larvae consume their hosts as they proceed through development. Juvenile wasps are thus reliant on their hosts for most of their developmental nutrition needs. Many parasitoid wasp lineages have lost the ability to synthesize lipids themselves, instead evolving strategies for efficiently obtaining lipids from hosts [2-4]. For example, adult female wasps inject venom (virulence) proteins, which function to regulate host physiology, into their hosts while laying eggs [5-12]. Venom proteins can play important roles in modifying host lipid metabolism, like altering host lipid synthesis and accumulation, and causing hosts to release lipids from their main storage tissue, the fat body [13]. All of these effects are thought to help provision the developing wasp larvae. Although wasp venoms are essential for host manipulation and offspring development, we still lack a detailed understanding of how venoms actually regulate host lipid availability. Parasitoids have evolved multiple times in the wasps [14], as have the necessary virulence strategies and the parasitoid-associated factors that accomplish them. In some parasitoid wasp lineages (e.g. Braconidae, Ichneumonidae ), virulence factors are made up of individual venom proteins as well as supramolecular structures like polydnaviruses (PDVs) and virus-like particles (VLPs) [15, 16]. The proteins that make up these structures can be difficult to functionally characterize individually, and thus we have focused on a wasp species representing a lineage that mainly depends on venom but lacks those supramolecular factors PDVs or VLPs: Pteromalus puparum (Hymenoptera: Pteromalidae). P. puparum is a pupal endoparasitoid that regularly infects Pieris rapae (Lepidoptera: Pieridae), the “small white” butterfly or “cabbage 4 worm”, a worldwide pest of cabbage and other mustard family crops. After parasitization, infected P. rapae pupa stop developing and change color from green- gray to brown as the wasp larvae develop inside of them. The numerous single-protein venoms that P. puparum produces to enable successful infection have been identified, including lipases and phospholipases, but so far the venom constituents have only been functionally characterized in relation to their ability to suppress the host immune response against wasp eggs [6, 8]. Although P. puparum is one of the small proportion of parasitoids that have re-evolved the ability to synthesize some lipids [3], we assume that lipid acquisition from hosts remains a requisite of juvenile development. Thus, we believe that the P. puparum - P. rapae system is ripe for exploiting as a model system for how and why parasitoid infection alters lipid metabolism in insect hosts. Lipids are a class of organic compounds made up of fatty acids or their derivatives that have multiple roles in living organisms, including energy storage, signal transduction, and cell membrane building blocks. The past 25 years have seen a remarkable increase in our ability to differentiate and identify lipids from biological samples, leading to the new field of lipidomics [17-20]. The typical approach uses liquid chromatography and mass spectrometry to identify and quantify lipid species. Lipidomics data representing different biological treatments help illuminate the molecular biology of lipid metabolism as well as the functional roles that various lipids play in host physiology. Here, we used an ultra performance liquid chromatography-quadrupole time-of-flight mass spectrometry (UPLC-TOF-MS)-based lipidomics approach to analyze the identities and concentrations of lipids in P. rapae hosts parasitized by P. puparum wasps. We found that concentrations of 30 lipid components increased but 57 decreased in the host fat body post-infection, while 89 increased but 28 decreased in 5 the host hemolymph post-infection. Analysis of these data provides novel insight into how parasitoid wasp venom alters host lipid metabolism for the benefit of the developing wasp larvae. 2 Materials and Methods 2.1 Insect rearing Young P. rapae larvae were collected from greenhouse-grown cabbage in the suburbs of Hangzhou, China. Subsequently, larvae were maintained in the lab under the condition of 10 h: 14 h (light: darkness) photoperiod at 25 ± 1℃ and fed fresh cabbage until pupation. Adult P. puparum were reared as described by Cai et al. [21] under the same condition above and fed with 20% (v/v) honey solution to lengthen their life spans. 2.2 Samples collection For experimental infections, we selected P. rapae pupae of similar sizes that had pupated within the previous 6 h, and then independently exposed them to a two-day- old mated endoparasitoid P. puparum female. They were placed together in a plastic tube (18 × 82 mm). To minimize wasp superparasitism in hosts, we used a light parasitization method [22] where we ensured that only a single oviposition occurred within the period of 1 h. When this occurred, the parasitoid wasp was removed and the P. rapae pupae were left alone for 24 h (the parasitized groups). Uninfected control P. rapae were treated the same except without parasitization. Parasitoid larvae consume host hemolymph early on in development before feeding directly on the host fat body and other hard tissues later in development [23, 24]. Thus, we made lipid extractions from the host fat body and hemolymph, separately. Furthermore, P. puparum embryos hatch in
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