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Amino Acid Synthesis Loss in Parasitoid Wasps and Other Hymenopterans

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Amino Acid Synthesis Loss in Parasitoid Wasps and Other Hymenopterans This article has been retracted. Read the retraction notice RESEARCH ARTICLE Amino acid synthesis loss in parasitoid wasps and other hymenopterans Xinhai Ye1,2†, Shijiao Xiong1†, Ziwen Teng1, Yi Yang1, Jiale Wang1, Kaili Yu1, Huizi Wu1, Yang Mei1, Zhichao Yan1, Sammy Cheng2, Chuanlin Yin1, Fang Wang1, Hongwei Yao1, Qi Fang1, Qisheng Song3, John H Werren2‡*, Gongyin Ye1‡*, Fei Li1‡* 1State Key Laboratory of Rice Biology & Ministry of Agricultural and Rural Affairs Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang University, Hangzhou, China; 2Department of Biology, University of Rochester, Rochester, United States; 3Division of Plant Sciences, College of Agriculture, Food and Natural Resources, University of Missouri, Columbia, United States Abstract Insects utilize diverse food resources which can affect the evolution of their genomic repertoire, including leading to gene losses in different nutrient pathways. Here, we investigate gene loss in amino acid synthesis pathways, with special attention to hymenopterans and parasitoid wasps. Using comparative genomics, we find that synthesis capability for tryptophan, phenylalanine, tyrosine, and histidine was lost in holometabolous insects prior to hymenopteran divergence, while valine, leucine, and isoleucine were lost in the common ancestor of Hymenoptera. *For correspondence: Subsequently, multiple loss events of lysine synthesis occurred independently in the Parasitoida [email protected] (JHW); and Aculeata. Experiments in the parasitoid Cotesia chilonis confirm that it has lost the ability to [email protected] (GY); synthesize eight amino acids. Our findings provide insights into amino acid synthesis evolution, and [email protected] (FL) specifically can be used to inform the design of parasitoid artificial diets for pest control. †These authors contributed equally to this work ‡These authors also contributed equally to this work Introduction Competing interests: The The Hymenoptera contain diverse insects (e.g. sawflies, wasps, bees, and ants) which utilize a wide authors declare that no variety of food resources (Quicke, 1997; Peters et al., 2017). Among the Hymenoptera, parasitoids competing interests exist. account for about 75% of species and 10 ~ 20% of all insect species (Pennacchio and Strand, 2006). Funding: See page 20 They are also important biological control agents in integrated pest management (IPM) (Bale et al., Received: 08 June 2020 2008). Female parasitoid wasps attack arthropod hosts and lay their eggs upon (ectoparasitoid) or Accepted: 17 October 2020 within (endoparasitoid) them, where the offspring feed and develop, eventually causing host death. Published: 19 October 2020 Therefore, parasitoids feed on a food resource rich in proteins, lipids, and other nutrients. In addi- tion, parasitoids can manipulate the nutritional value of the hosts through effectors injected into the Reviewing editor: Antonis Rokas, Vanderbilt University, host, such as venom proteins, polydnaviruses, and molecular factors produced by parasitoid cells United States (teratocytes) that are either injected into the host or produced by feeding larvae (Pennacchio and Strand, 2006; Pennacchio et al., 2014). As well as inhibiting host immunity and alterning host Copyright Ye et al. This article development, these mechanisms alter host metabolism in ways that mobilize nutrients from host tis- is distributed under the terms of sues to meet the demands of developing larvae (Mrinalini et al., 2015; Pennacchio et al., 1995; the Creative Commons Attribution License, which Rivers and Denlinger, 1994). permits unrestricted use and We originally began this project to investigate how the protein-rich diet of parasitoids and their redistribution provided that the ability to manipulate amino acid availability in hosts, has affected their genomic repertoire in amino original author and source are acid synthesis pathways. Our hypothesis was that parasitoids would show extensive loss of genes in credited. amino acid synthesis pathways due to the availability of amino acids in their diet. Ye, Xiong, et al. eLife 2020;9:e59795. DOI: https://doi.org/10.7554/eLife.59795 1 of 37 This article has been retracted. Read the retraction notice Research article Genetics and Genomics Gene loss in nutritional biosynthetic pathways has been described in several insect groups. For instance, some hemipteran insects have lost genes in amino acid biosynthetic pathways, apparently because they can obtain the nutrition from their endosymbionts (Douglas, 2006; Feldhaar, 2011). In some cases, this has been confirmed by annotation of the complete pathway of the endosymbiont and incomplete pathway of the insect, for instance in aphids (Richards et al., 2010), planthoppers (Xue et al., 2014), leafhoppers (McCutcheon and Moran, 2007), and mealybugs (Husnik and McCutcheon, 2016; Gil et al., 2018). Many of these studies involve herbivorous insects that feed on plant sap. However, hymenopteran insects have diverse food resources. Thus, it is reasonable to assume that changes involved in some biosynthetic pathways occurred during the evolution of hyme- nopteran insects. In particular, carnivorous parasitoid wasps feed on a protein and lipid-rich food resource of hosts, which could have resulted in genomic changes. This prompted us to investigate whether some gene losses occur in the nutritional biosynthetic pathways and how parasitoid wasps exploit the nutrition of hosts. The amino acid, carbohydrate, and lipid requirements of several parasitoid wasps have been eval- uated using the traditional nutrient removal method (Thompson, 1986), that is removing particular components from an artificial diet. Parasitoid wasps can manipulate their hosts to produce a nutri- tionally favorable environment for parasitoid development, and there is considerable evidence that they do so through venoms and teratocytes injected by the mother into the host and via modifica- tions induced by feeding larvae (Nakamatsu and Tanaka, 2003; Nakamatsu and Tanaka, 2004; Pennacchio et al., 2014). For example, parasitoid venoms induce a higher concentration of lipids, which is confirmed by in vitro injection of venom into the host (Nakamatsu and Tanaka, 2003; Nakamatsu and Tanaka, 2004). Detailed transcriptomic and metabolomic analyses of venom injected hosts of Nasonia vitripennis reveal dramatic alterations in host gene expression (Martinson et al., 2014), sugar, chitin, and lipid metabolism, as well as elevation of free amino acid levels (Mrinalini et al., 2015). To meet the demands of the developing wasp larvae, nutritional com- ponents such as proteins, acylglycerols and free amino acids change in the hemolymph of the para- sitized pea aphid Acyrthosiphon pisum during development of parasitoid wasp Aphidius ervi larvae (Pennacchio et al., 1995; Rahbe ´ et al., 2002). Previous studies showed that at early stages, endo- parasitoid wasp larvae absorb nutrients from host hemolymph through thin exoskeletons and epider- mis, whereas they absorb nutrients mainly through gut epithelium at later stages (Giordana et al., 2003; Caccia et al., 2005; Grimaldi et al., 2006; Pennacchio et al., 2014). Although parasitoids develop on a nutritionally rich food resource and manipulate the nutritional qualities of the host, there have been very few studies on how this relationship impacts their genomic evolution. Although some studies have investigated lipid utilization and biosynthesis in parasitoids (Visser and Ellers, 2008; Visser et al., 2010; Visser et al., 2012; Lammers et al., 2019), there has been very little research on changes in amino acid biosynthetic pathways. To investigate the idea that parasitoids have lost essential amino acid synthesis genes due to their amino-acid-rich food resource, we first conducted genome sequencing of Cotesia chilonis and exam- ined its genomic repertoire for amino acid synthesis pathway genes. To place these results in an evo- lutionary context, we next examined the genomes of 38 hymenopteran species (3 sawflies, 17 aculeates and 18 parasitoids) for which well assembled and annotated genomes are available, and compared these to a set of 13 other holometabolous and hemimetabolous arthropods. We then returned to C. chilonis to conduct a set of experiments to investigate the amino acid requirements of their larvae, in light of the pathways predicted to be disrupted by the genomic analysis. To investi- gate the effects of parasitoid venom and feeding larvae on host amino acids, changes in these host nutrition components in host hemolymph were analyzed after parasitism by this wasp, using UPLC- MS/MS (ultra-performance liquid chromatography tandem mass spectrometry). Finally, the in vitro deletion method was used to determine which essential amino acids developing wasps require from its host. Here, we consider three kinds of losses relevant to amino acid metabolism: gene loss in amino acid pathways, pathway disruption due to gene loss, and loss of synthesis ability for different amino acids. It is noteworthy that pathway disruption for a particular amino acid does not always mean loss of the ability to synthesize that amino acid, because there are alternative pathways for synthesis of some amino acids. Our results indicate a disruption of 16 amino acid pathways at the base of the branch leading to holometabolous insects, which disrupted the synthetic capability for four amino acids (tryptophan, phenylalanine, tyrosine and histidine). Additional disruption of seven pathways
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