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Roles of Three Putative Salmon Louse (Lepeophtheirus Salmonis)

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Roles of Three Putative Salmon Louse (Lepeophtheirus Salmonis) Dalvin et al. Parasites Vectors (2021) 14:206 https://doi.org/10.1186/s13071-021-04690-w Parasites & Vectors RESEARCH Open Access Roles of three putative salmon louse (Lepeophtheirus salmonis) prostaglandin E2 synthases in physiology and host–parasite interactions Sussie Dalvin1, Christiane Eichner2, Michael Dondrup3 and Aina‑Cathrine Øvergård2* Abstract Background: The salmon louse (Lepeophtheirus salmonis) is a parasite of salmonid fsh. Atlantic salmon (Salmo salar) exhibit only a limited and inefective immune response when infested with this parasite. Prostaglandins (PGs) have many biological functions in both invertebrates and vertebrates, one of which is the regulation of immune responses. This has led to the suggestion that prostaglandin E2 (PGE2) is important in the salmon louse host–parasite interaction, although studies of a salmon louse prostaglandin E2 synthase (PGES) 2 gene have not enabled conformation of this hypothesis. The aim of the present study was, therefore, to characterize two additional PGES‑like genes. Methods: Lepeophtheirus salmonis microsomal glutathione S‑transferase 1 like (LsMGST1L) and LsPGES3L were inves‑ tigated by sequencing, phylogenetics, transcript localization and expression studies. Moreover, the function of these putative PGES genes in addition to the previously identifed LsPGES2 gene was analyzed in double stranded (ds) RNA‑ mediated knockdown (KD) salmon louse. Results: Analysis of the three putative LsPGES genes showed a rather constitutive transcript level throughout development from nauplius to the adult stages, and in a range of tissues, with the highest levels in the ovaries or gut. DsRNA‑mediated KD of these transcripts did not produce any characteristic changes in phenotype, and KD animals displayed a normal reproductive output. The ability of the parasite to infect or modulate the immune response of the host fsh was also not afected by KD. Conclusions: Salmon louse prostaglandins may play endogenous roles in the management of reproduction and oxidative stress and may be a product of salmon louse blood digestions. Keywords: Invertebrate, Arthropod, Copepod, Blood‑feeding, RNA interference, ROS, Immune response Background stages: nauplius 1, nauplius 2 and the infective copepodid Te salmon louse (Lepeophtheirus salmonis) is a marine stage. All further development takes place on the fsh and ectoparasite of salmonid fsh, feeding on fsh mucus, skin consists of two chalimi, two preadult stages and the adult and blood [1, 2]. Salmon lice have a life-cycle consist- stage [3, 4]. Heavy infestations can cause severe problems ing of eight stages, starting with three planktonic larval to the host, including wounding, secondary infections and osmotic disturbances [5, 6]. Infestations of farmed *Correspondence: aina‑[email protected] fsh have been difcult to manage due to the develop- 2 Department of Biological Sciences, SLCR‑Sea Lice Research Centre, ment of resistance against parasiticides [7], and the nega- University of Bergen, P. box 7803, 5020 Bergen, Norway tive impact on wild salmonid fsh through transmission Full list of author information is available at the end of the article © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Dalvin et al. Parasites Vectors (2021) 14:206 Page 2 of 17 of lice from farmed to wild fsh stocks is a cause of envi- Atlantic salmon (Salmo salar) display a limited and ronmental concern [8–10]. mainly local immune response to salmon louse, which Prostaglandin E2 (PGE2) is an eicosanoid component does not eliminate the infection [32–35]. Tis has led to with hormone-like functions, derived from arachidonic eforts to understand how the salmon louse modulates its acid (AA) through three sequential enzymatic reactions host, and PGE2 has been put forward as a putative can- [11]. Generally, phospholipase A 2 releases AA from cell didate for immune modulation. PGE2 has been detected membranes, a cyclooxygenase (COX) converts AA to in excretory/secretory products from dopamine-treated PGG2 and further to PGH 2, which can be metabolized to salmon louse, and it was demonstrated that the level of PGE2 by PGE 2 synthases (PGESs). Te action of PGE 2 is PGE2 quickly dropped after lice were removed from the dependent on the binding of prostanoid EP receptor sub- host fsh [36, 37]. Moreover, Atlantic salmon immune tis- types (EP1–4), and PGE2 has diverse roles in physiologi- sue express the EP4 prostaglandin E receptors [38], and cal processes, such as infammation, reproduction and PGE2 treatment has been shown to down-modulate the embryonic development, depending on cell type and EP expression of MHC class I proteins and interleukin-1β receptor subtype [12–16]. in a salmon macrophage-like cell line [37]. However, in a PGESs are found in a large range of organisms where more recent study in which excretory/secretory products they play diverse physiological roles [17]. In mammals, were obtained by agitating lice in sea water, PGE 2 was not three isotypes of PGES exist, two of which are mem- identifed [39]. Moreover, studies of a putative salmon brane bound (PGES1 and -2) and one cytosolic (PGES3). louse gene, PGES2 (LsPGES2) were unable to reveal any Tese isotypes typically display diferent enzymatic involvement of LsPGES2 in the host–parasite interaction properties, expression patterns, cellular localizations [40]. Instead, expression of LsPGES2 indicated a function and functions. PGESs have also been described in many in reproductive organs, although no visible alteration in arthropods, including crustacean species, and similar to reproductive phenotype was observed in knockdown mammals, three genes encoding PGESs have been found (KD) animals. in penaeid shrimp [18]. Te functional property of a few In the present study, we hypothesized that this lack of invertebrate synthases has also been confrmed, where phenotypic alterations is due to the action of additional the conversion of PGH2 to PGE2 by recombinant Gam- salmon lice PGES genes beyond the already described marus and Caprella sp. PGES2 has been demonstrated LsPGES2 and that these may be involved in the host– [19]. PGESs and their product PGE2 are involved in parasite interaction in addition to endogenous processes. reproduction, including maturation of ovaries and vitel- Two additional genes with putative PGES activity were logenesis in prawn and crabs [18, 20–22]. PGES has also identifed and their functional role analyzed by double- been detected in blood cells of crab, indicative of a role stranded (ds) RNA-mediated KD and studies of host– in immunity [23], and PGE2 has been detected in both parasite interactions, reproduction, oxidative stress and tapeworms and crab nervous tissue where it is likely to be blood digestion. important for development and function [20, 24]. Parasites with a long-term interaction with their host need mechanisms to evade potential host immune reac- Methods tion, and prostaglandins (PGs) such as PGE 2 have been Culture of salmon lice and source of tissue found to play important roles in many host–parasite Laboratory strains of the Atlantic salmon lice subspecies protozoan and metazoan interactions [25, 26]. How- Lepeophtheirus salmonis salmonis [41] were maintained ever, uncovering the role of PGs is complicated by their on farmed Atlantic salmon (Salmo salar) according to diverse roles and the fact that these compounds are pro- Hamre et al. [42]. Te salmon were hand fed a commer- duced by both the host and the parasite [27]. In blood- cial diet and reared in sea water with a salinity of 34.5 g/ feeding arthropods such as ticks, PGs are suggested to be kg and a temperature of 10 °C. Eggs, nauplii and copepo- involved in vasodilation and immune modulation in the dids were kept in seawater from the same source. Nauplii host, as high concentrations of PGE 2 are found in tick were obtained from hatching eggs and kept in a fow- saliva [28–30]. Both PGE2 and PGD2 have been detected through single-well system [42]. in gland secretions from the fsh tapeworm Diphylloboth- For ontogenetic expression analysis of the two PGES- rium dendriticum when incubated in serum from a host like genes, LsMGST1L and LsPGES3L, we collected a fsh [24], and in vitro studies have suggested that PGE2 time-series of all lice stages from egg to adult lice, in pen- derived from the tapeworm Schistocephalus solidus have taplicate samples, as follows: (i) eggs: 1 egg sac (string) the potential to modulate host leukocyte viability and (containing approximately 200 eggs; (ii) nauplius 1, nau- reactive oxygen species production [31]. plius 2 and copepodids (free-living) (approximately 100 larvae); copepodids, 2 days post-infestation (dpi) and 4 Dalvin et al. Parasites Vectors (2021) 14:206 Page 3 of 17 dpi (60 larvae); (iv) chalimus: chalimus 1 (30 animals) and amplifcation kit (Clontech Laboratories, Inc. Mountain chalimus 2 (20 animals); (v) preadult and adult stages: View, CA, USA) using 1 μg total RNA from adult female single animals (adult females were defned as young lice.
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