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(Seps) of the Branchiuran Ectoparasite Argulus Foliaceus (Linnaeus, 1758) Reveals Unique Secreted Proteins Amongst Haematophagous Ecdysozoa Aisha Ambuali1,2* , Sean J

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(Seps) of the Branchiuran Ectoparasite Argulus Foliaceus (Linnaeus, 1758) Reveals Unique Secreted Proteins Amongst Haematophagous Ecdysozoa Aisha Ambuali1,2* , Sean J AmbuAli et al. Parasites Vectors (2020) 13:88 https://doi.org/10.1186/s13071-020-3964-z Parasites & Vectors RESEARCH Open Access Identifcation of proteins from the secretory/ excretory products (SEPs) of the branchiuran ectoparasite Argulus foliaceus (Linnaeus, 1758) reveals unique secreted proteins amongst haematophagous ecdysozoa Aisha AmbuAli1,2* , Sean J. Monaghan1, Kevin McLean3, Neil F. Inglis3, Michaël Bekaert1, Stefanie Wehner1,4 and James E. Bron1 Abstract Background: It is hypothesised that being a blood-feeding ectoparasite, Argulus foliaceus (Linnaeus, 1758), uses similar mechanisms for digestion and host immune evasion to those used by other haematophagous ecdysozoa, including caligid copepods (e.g. sea louse). We recently described and characterised glands associated with the feeding appendages of A. foliaceus using histological techniques. The work described in the present study is the frst undertaken with the objective of identifying and partially characterising the components secreted from these glands using a proteomic approach. Methods: Argulus foliaceus parasites were sampled from the skin of rainbow trout (Oncorhynchus mykiss), from Loch Fad on the Isle of Bute, Scotland, UK. The proteins from A. foliaceus secretory/excretory products (SEPs) were collected from the supernatant of artifcial freshwater conditioned with active adult parasites (n 5–9 per ml; n 560 total). Pro- teins within the SEPs were identifed and characterised using LC-ESI-MS/MS analysis. Data= are available= via ProteomeX- change with identifer PXD016226. Results: Data mining of a protein database translated from an A. foliaceus dataset using ProteinScape allowed identi- fcation of 27 predicted protein sequences from the A. foliaceus SEPs, each protein matching the criteria of 2 peptides with at least 4 contiguous amino acids. Nine proteins had no matching sequence through OmicsBox (Blast2GO) analysis searches suggesting that Argulus spp. may additionally have unique proteins present in their SEPs. SignalP 5.0 software, identifed 13 proteins with a signal sequence suggestive of signal peptides and supportive of secreted proteins being identifed. Notably, the functional characteristics of identifed A. foliaceus proteins/domains have also been described from the salivary glands and saliva of other blood-feeding arthropods such as ticks. Identifed proteins included: transporters, peroxidases, metalloproteases, proteases and serine protease inhibitors which are known to play roles in parasite immune evasion/induction (e.g. astacin), immunomodulation (e.g. serpin) and digestion (e.g. trypsin). *Correspondence: [email protected] 1 Institute of Aquaculture, School of Natural Sciences, University of Stirling, Stirling FK9 4LA, UK Full list of author information is available at the end of the article © The Author(s) 2020. 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. AmbuAli et al. Parasites Vectors (2020) 13:88 Page 2 of 13 Conclusions: To our knowledge, the present study represents the frst proteomic analysis undertaken for SEPs from any branchiuran fsh louse. Here we reveal possible functional roles of A. foliaceus SEPs in digestion and immunomod- ulation, with a number of protein families shared with other haematophagous ectoparasites. A number of apparently unique secreted proteins were identifed compared to other haematophagous ecdysozoa. Keywords: Secretions, Immunomodulation, Fish lice, Argulus, Branchiura Background data relating to the functional roles of these proteins, and Argulus foliaceus (Linnaeus, 1758) is a member of the have facilitated their molecular and biological characteri- branchiuran family Argulidae and has a worldwide distri- sation [21]. Recent transcriptomic and proteomic stud- bution [1–3]. In the UK, this parasitic arthropod causes ies of salivary glands from diferent species of ticks have the condition argulosis, which has economic impacts for similarly identifed a diverse range of active molecules/ both aquaculture and sports fshing industries [4] and proteins that modify the hosts’ physiology [29–31]. Given afects wild and cultured fsh populations [5, 6]. the success of these studies in identifying active compo- Argulus spp. attach to their hosts for extended peri- nents of the saliva of other haematophagous arthropods, ods using the frst maxillae, which form hooks as larvae a proteomics approach may prove similarly productive to but are modifed into suction discs as adults. It has been decipher the composition and role of A. foliaceus SEPs. hypothesised that to enable long term host contact and In two earlier studies, western blots of whole body feeding, Argulus spp., like other ectoparasitic arthropods extracts of A. siamensis (Wilson, 1926) [32] and A. folia- such as ticks and salmon lice (Lepeophtheirus salmonis ceus [33] revealed the presence of a number of immuno- (Krøyer, 1837)), must secrete a range of pharmacologi- dominant polypeptides recognised by immune rainbow cally active components. Tese components have been trout (Oncorhynchus mykiss (Walbaum, 1792)) and rab- suggested to be produced in the parasite’s spinal, probos- bit serum. Notably, and despite phylogenetic distance, cis and labial glands and to be delivered through the pre- antigenic cross-reactivity between A. foliaceus and para- oral spine and the mouth tube to facilitate blood-feeding sitic caligid copepod (L. salmonis and Caligus elongatus [7, 8]. Argulus spp. have been reported to feed on blood (von Nordmann, 1832)) antigens was demonstrated using [9–11], mucus [12] and host skin [13] and thus have serum antibodies raised against A. foliaceus in rainbow a presumed requirement to modulate host immunity. trout [20]. Both caligid sea lice and branchiuran fresh- Pharmacologically active substances delivered in para- water lice feed on the fsh epithelium, mucus and blood site secretions aid in modulating such defence mecha- to some degree. To allow this, sea lice SEPs comprise a nisms including those associated with pain, haemostasis, number of immunomodulatory proteins [34, 35] includ- infammation, complement activation and tissue repair ing metallopeptidases, serine proteinases and cysteine [14–19]. However, to date there are limited genomic proteinases; previously identifed in tick saliva [36]. Sea resources available for detailed investigation of this para- lice SEPs also contain anti-oxidant proteins identifed in site. Furthermore, little formal data have been collected helminths [37], and serine endopeptidases, e.g. trypsins, on either the composition or function of Argulus spp. identifed in fies [38]. Whether the mechanisms involved secreted proteins or other active components [20]. in parasitism are similar between sea lice and other During blood-feeding, other haematophagous arthro- arthropods parasitising fsh has yet to be established. pods inject the host with salivary products rich in diges- From the foregoing, the aim of the present study was tive enzymes and other pharmacologically active proteins to identify and characterise protein components of the that have anti-haemostatic, anti-infammatory and SEPs produced by A. foliaceus. Characterisation of these immunomodulatory properties. Tese salivary products proteins is key to establishing the biological function of help in counteracting the host immune response and branchiuran/A. foliaceus SEPs and can assist in identify- wound recovery and hence facilitate feeding [21–28]. ing potential vaccine candidates or drug targets for the Recently, proteomics-based studies have contributed future development of more sustainable argulosis con- considerably to the identifcation of proteins from the trol strategies. To this end, proteomic data generated by salivary glands of a number of haematophagous insects LC-ESI-MS/MS were searched against a bespoke protein including diferent species of mosquitoes i.e. Anoph- database assembled using proteins translated from an A. eles stephensi Liston, 1901, A. campestris-like, Aedes foliaceus transcriptomic dataset (submitted to the EBI aegypti (Linnaeus in Hasselquist, 1762) and Culex pipiens with a project number PRJEB34947) and likely biological quinquefasciatus Say, 1823. Tese studies have provided roles for discovered proteins ascribed. AmbuAli et al. Parasites Vectors (2020) 13:88 Page 3 of 13 Methods a silver staining kit (ProteoSilver ™-PROTSIL1-1KT, St. Sample collection and incubation in artifcial freshwater Louis, USA). Te gel was scanned using a benchtop scan- Adult argulids were collected directly from fsh hosts, ner (EPSON expression 1680
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