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pmid:32070416

Identification of proteins from the secretory/excretory products (SEPs) of the branchiuran ectoparasite Argulus foliaceus (Linnaeus, 1758) reveals unique secreted proteins amongst haematophagous ecdysozoa.

Aisha AmbuAli · Sean J Monaghan · Kevin McLean · Neil F Inglis · Michaël Bekaert · Stefanie Wehner · James E Bron

Parasites & vectors · 2020 doi:10.1186/s13071-020-3964-z

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Experiment

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Data

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pmid:32070416
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title
Identification of proteins from the secretory/excretory products (SEPs) of the branchiuran ectoparasite Argulus foliaceus (Linnaeus, 1758) reveals unique secreted proteins amongst haematophagous ecdysozoa.
doi
10.1186/s13071-020-3964-z
pmid
32070416
authors array · 7 items
[0]
Aisha AmbuAli
[1]
Sean J Monaghan
[2]
Kevin McLean
[3]
Neil F Inglis
[4]
Michaël Bekaert
[5]
Stefanie Wehner
[6]
James E Bron
journal
Parasites & vectors
year
2020
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 first 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 artificial freshwater conditioned with active adult parasites (n = 5-9 per ml; n = 560 total). Proteins within the SEPs were identified and characterised using LC-ESI-MS/MS analysis. Data are available via ProteomeXchange with identifier PXD016226. RESULTS: Data mining of a protein database translated from an A. foliaceus dataset using ProteinScape allowed identification 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, identified 13 proteins with a signal sequence suggestive of signal peptides and supportive of secreted proteins being identified. Notably, the functional characteristics of identified A. foliaceus proteins/domains have also been described from the salivary glands and saliva of other blood-feeding arthropods such as ticks. Identified 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). CONCLUSIONS: To our knowledge, the present study represents the first proteomic analysis undertaken for SEPs from any branchiuran fish louse. Here we reveal possible functional roles of A. foliaceus SEPs in digestion and immunomodulation, with a number of protein families shared with other haematophagous ectoparasites. A number of apparently unique secreted proteins were identified compared to other haematophagous ecdysozoa.
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The datasets which support the conclusions are included within the article. The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium via the PRIDE [110] partner repository with the dataset identifier PXD016226 [111, 112].
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The datasets which support the conclusions are included within the article. The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium via the PRIDE [110] partner repository with the dataset identifier PXD016226 [111, 112].
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Identification of proteins from the secretory / excretory products (SEPs) of the branchiuran ectoparasite Argulus foliaceus
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List of proteins identified by GeLC-MS/MS analysis of A. foliaceus secretory/excretory products showing hits with OmicsBOx (Blast2Go) database
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List of proteins identified by GeLC-MS/MS analysis of A. foliaceus secretory/excretory products showing hits with OmicsBOx (Blast2Go) database
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[1]
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[2]
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[3]
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[4]
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SC (%)
[6]
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SignalP
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NCBI ID
[1] array · 12 items
[0]
Vitellogenin_N
[1]
afol_3429.1p
[2]
Von Willebrand factor type D domain protein
[3]
172.5
[4]
55
[5]
39.4
[6]
1499
[7]
8.39E−11
[8]
Yes
[9]
Ixodes scapularis
[10]
Transporters, osmolality, immunity and clotting [25, 51–53]
[11]
XP_029822532.1
[2] array · 10 items
[0]
afol_51180.1p
[1]
Vitellogenin-like isoform X1
[2]
183.8
[3]
44
[4]
30.1
[5]
1582
[6]
1.26E−11
[7]
No
[8]
Ixodes scapularis
[9]
XP_029826448.1
[3] array · 12 items
[0]
Hemocyanin
[1]
afol_43548.1p
[2]
Hemocyanin subunit type 1 precursor
[3]
81.2
[4]
18
[5]
26.3
[6]
697
[7]
0
[8]
Yes
[9]
Argulus foliaceus
[10]
Respiratory, protein storage [54]
[11]
CUH82791.1
[4] array · 10 items
[0]
afol_52001.1p
[1]
Hemocyanin A chain
[2]
36.2
[3]
8
[4]
30.6
[5]
314
[6]
0
[7]
No
[8]
Argulus foliaceus
[9]
CUH82792.1
[5] array · 12 items
[0]
Astacin
[1]
afol_16671.1p
[2]
Protein SpAN-like
[3]
72.6
[4]
11
[5]
21.2
[6]
660
[7]
1.49E−55
[8]
Yes
[9]
Saccoglossus kowalevskii
[10]
Immunity; antifungal activity [55], food digestion, host penetration, immune evasion or activation [56–58]
[11]
XP_002739691.1
[6] array · 10 items
[0]
afol_52344.2p
[1]
Protein SpAN-like
[2]
76.4
[3]
12
[4]
17.6
[5]
687
[6]
2.85E−50
[7]
No
[8]
Penaeus vannamei
[9]
XP_027221531.1
[7] array · 10 items
[0]
afol_18725.8p
[1]
Blastula protease 10-like
[2]
50.7
[3]
8
[4]
18.4
[5]
462
[6]
1.44E−17
[7]
No
[8]
Penaeus vannamei
[9]
XP_027219989.1
[8] array · 12 items
[0]
Serpin
[1]
afol_27409.2p
[2]
Serpin B6-like
[3]
51.4
[4]
7
[5]
20.0
[6]
461
[7]
6.15E−66
[8]
No
[9]
Rhipicephalus microplus
[10]
Anticoagulation activity, modulate host immune response, regulation of host inflammation, antihaemostatic effects, and platelet aggregation [59–64]
[11]
AHC98669.1
[9] array · 10 items
[0]
afol_25414.2p
[1]
Leukocyte elastase inhibitor-like
[2]
11.2
[3]
4
[4]
35.1
[5]
94
[6]
1.05E−16
[7]
No
[8]
Ixodes scapularis
[9]
EEC05896.1
[10] array · 12 items
[0]
Fasciclin
[1]
afol_20127.1p
[2]
Beta-ig-h3 fasciclin
[3]
37.1
[4]
5
[5]
23.1
[6]
333
[7]
1.64E−22
[8]
Yes
[9]
Culex quinquefasciatus
[10]
Mediate cell adhesion [65, 66]
[11]
XP_001847648.1
[11] array · 12 items
[0]
Trypsin
[1]
afol_3246.7p
[2]
Transmembrane protease serine 9
[3]
28.1
[4]
5
[5]
21.4
[6]
262
[7]
2.81E−12
[8]
No
[9]
Penaeus vannamei
[10]
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[11]
XP_027224040.1
[12] array · 10 items
[0]
afol_16878.20p
[1]
Trypsin-1
[2]
32.0
[3]
9
[4]
34.5
[5]
293
[6]
6.81E−61
[7]
Yes
[8]
Ceratitis capitata
[9]
XP_004520346.1
[13] array · 10 items
[0]
afol_19181.1p
[1]
Serine protease 29
[2]
47.0
[3]
7
[4]
24.5
[5]
466
[6]
8.72E−87
[7]
Yes
[8]
Bombus terrestris
[9]
XP_020722765.1
[14] array · 10 items
[0]
afol_18345.1p
[1]
Transmembrane protease serine 9-like
[2]
18.3
[3]
4
[4]
25.6
[5]
164
[6]
1.38E−17
[7]
No
[8]
Drosophila navojoa
[9]
XP_030246706.1
[15] array · 10 items
[0]
afol_51127.2p
[1]
Trypsin
[2]
25.1
[3]
3
[4]
15.7
[5]
236
[6]
2.13E−57
[7]
No
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Penaeus vannamei
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ROT79324.1
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afol_56688.3p
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Serine protease1/2
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29.1
[3]
2
[4]
6.1
[5]
262
[6]
3.42E−39
[7]
Yes
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Ixodes scapularis
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XP_029851465.1
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[0]
Peptidase_M14
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afol_12392.3p
[2]
Mast cell carboxypeptidase A
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48.3
[4]
5
[5]
16.7
[6]
424
[7]
4.21E−88
[8]
No
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Penaeus vannamei
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Proteolytic-enzyme [68])
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XP_027226524.1
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[0]
VIT
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afol_32337.1p
[2]
Inter-alpha-trypsin inhibitor heavy chain H4-like isoform X2
[3]
98.2
[4]
4
[5]
7.4
[6]
883
[7]
2.31E−151
[8]
Yes
[9]
Lingula anatina
[10]
Proteinase inhibitor [36]
[11]
XP_013407760.1
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Proteins identified from A. foliaceus secretory/excretory products by mass spectrometric analysis that showed no hits in OmicsBox/Blast2GO and were blasted against Metazoa in NCBI BLASTP, signal P
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Proteins identified from A. foliaceus secretory/excretory products by mass spectrometric analysis that showed no hits in OmicsBox/Blast2GO and were blasted against Metazoa in NCBI BLASTP, signal P
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[0] array · 7 items
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NCBI ID
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[0]
afol_3444.2p
[1]
192
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20.7
[3]
40.1
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afol_55421.1p
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140
[2]
14.9
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42.1
[4]
0.57
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XP_008192422.1
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afol_9654.1p
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408
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afol_25364.1p
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XP_029189514.1
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afol_15401.2p
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13
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afol_2470.1p
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111
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17.1
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0.006
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XP_017135474.1
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afol_50565.1p
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388
[2]
43.8
[3]
10.6
[4]
[5]
[6]
Yes
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afol_52850.1p
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399
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43.7
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6
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0.083
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XP_023212714.1
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Yes
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afol_45298.1p
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189
[2]
21.5
[3]
25.4
[4]
0.49
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EEC08850.1
[6]
Yes
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Complete file
{"sci_version": "1.0", "schema": "https://corpus.bntrg.co.uk/sci/1.0/sci.schema.json", "id": "pmid:32070416", "kind": "science-record", "revision": 3, "content_hash": "sha256:edb12693c78c308ee793875d71237969ec972a57f26f19154c3ffc1e906066cb", "created_at": "2026-11-01T15:40:56Z", "updated_at": "2026-11-01T18:51:58Z", "generator": {"name": "corpus-assay-engine", "run_id": "reading-sci-2026-11-01"}, "paper": {"state": "complete", "title": "Identification of proteins from the secretory/excretory products (SEPs) of the branchiuran ectoparasite Argulus foliaceus (Linnaeus, 1758) reveals unique secreted proteins amongst haematophagous ecdysozoa.", "doi": "10.1186/s13071-020-3964-z", "pmid": "32070416", "authors": ["Aisha AmbuAli", "Sean J Monaghan", "Kevin McLean", "Neil F Inglis", "Michaël Bekaert", "Stefanie Wehner", "James E Bron"], "journal": "Parasites & vectors", "year": 2020, "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 first undertaken with the objective of identifying and partially characterising the components secreted from these glands using a proteomic approach.\nMETHODS: 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 artificial freshwater conditioned with active adult parasites (n = 5-9 per ml; n = 560 total). Proteins within the SEPs were identified and characterised using LC-ESI-MS/MS analysis. Data are available via ProteomeXchange with identifier PXD016226.\nRESULTS: Data mining of a protein database translated from an A. foliaceus dataset using ProteinScape allowed identification 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, identified 13 proteins with a signal sequence suggestive of signal peptides and supportive of secreted proteins being identified. Notably, the functional characteristics of identified A. foliaceus proteins/domains have also been described from the salivary glands and saliva of other blood-feeding arthropods such as ticks. Identified 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).\nCONCLUSIONS: To our knowledge, the present study represents the first proteomic analysis undertaken for SEPs from any branchiuran fish louse. Here we reveal possible functional roles of A. foliaceus SEPs in digestion and immunomodulation, with a number of protein families shared with other haematophagous ectoparasites. A number of apparently unique secreted proteins were identified compared to other haematophagous ecdysozoa.", "claims": [{"id": "claim-data-access", "statement": "The datasets which support the conclusions are included within the article. 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This lane did not download the dataset or read its licence.", "duration_hours": null, "parameters": {}, "inputs": ["data:geo:PXD016226"], "outputs": ["the source data with its repository provenance"], "instruments": [], "reagents": []}, {"id": "run_analysis", "order": 3, "name": "Run the published analysis", "kind": "analysis", "state": "complete", "blocked_on": null, "description": "Apply the paper's statistical method to the resolved series and compare the result with the published target.", "duration_hours": null, "parameters": {}, "inputs": ["data:geo:PXD016226"], "outputs": ["the replicated result and its comparison"], "instruments": [], "reagents": []}], "materials": [], "instruments": [], "reagents": [], "conditions": {}, "gaps": []}, "data": {"state": "partial", "assets": [{"id": "source:pmid:32070416", "role": "manuscript", "format": "xml", "media_type": "application/xml", "uri": "https://doi.org/10.1186/s13071-020-3964-z", "sha256": "sha256:49c041b40c351ff20d0c7a8119d6f998b85b3da2bb94dcd6bec5341a7116df28", "bytes": 44643, "access": "open", "state": "resolved", "reader": null, "reader_status": "reader_required", "identifier": "10.1186/s13071-020-3964-z", "version": null, "note": "Full article fetched from PMC; the checksum covers the rendered section body, not the original XML bytes.", "structure": {"pmcid": "PMC7029603", "source": "europe_pmc_fulltext", "coverage": "whole_body_without_references", "text_hash_scope": "rendered_section_body"}}, {"id": "data:geo:PXD016226", "role": "raw", "format": "geo-series", "media_type": "application/vnd.ncbi.geo-series+json", "uri": "https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=PXD016226", "sha256": null, "bytes": null, "access": "open", "state": "resolved", "reader": null, "reader_status": "reader_required", "identifier": "PXD016226", "version": null, "note": "The datasets which support the conclusions are included within the article. 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