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Extracellular vesicle signatures and protein citrullination are modified in shore crabs (Carcinus maenas) infected with Hematodinium sp

Christopher Coates, Igor Kraev Orcid Logo, Andrew Rowley, Sigrun Lange Orcid Logo

Virulence, Volume: 14, Issue: 1

Swansea University Authors: Christopher Coates, Andrew Rowley

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DOI (Published version): 10.1080/21505594.2023.2180932

Abstract

Epizootiologists recurrently encounter symbionts and pathobionts in the haemolymph (blood equivalent) of shellfish. One such group is the dinoflagellate genus Hematodinium, which contains several species that cause debilitating disease in decapod crustaceans. The shore crab Carcinus maenas acts as a...

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Published in: Virulence
ISSN: 2150-5594 2150-5608
Published: Informa UK Limited 2023
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URI: https://cronfa.swan.ac.uk/Record/cronfa62681
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spelling 2023-03-08T19:12:16.0704910 v2 62681 2023-02-17 Extracellular vesicle signatures and protein citrullination are modified in shore crabs (Carcinus maenas) infected with Hematodinium sp c62fa509397c2af92b316cda4987ff8e Christopher Coates Christopher Coates true false e98124f6e62b9592786899d7059e3a79 Andrew Rowley Andrew Rowley true false 2023-02-17 Epizootiologists recurrently encounter symbionts and pathobionts in the haemolymph (blood equivalent) of shellfish. One such group is the dinoflagellate genus Hematodinium, which contains several species that cause debilitating disease in decapod crustaceans. The shore crab Carcinus maenas acts as a mobile reservoir of microparasites, including Hematodinium sp., thereby posing a risk to other co-located commercially important species, e.g. velvet crabs (Necora puber). Despite the widespread prevalence and documented seasonality of Hematodinium infection dynamics, there is a knowledge gap regarding host-pathogen antibiosis, namely, how Hematodinium avoids the host’s immune defences. Herein, we interrogated the haemolymph of Hematodinium-positive and Hematodinium-negative crabs for extracellular vesicle (EV) profiles (a proxy for cellular communication), alongside proteomic signatures for post-translational citrullination/deimination performed by arginine deiminases, which can infer a pathologic state. Circulating EV numbers in parasitized crab haemolymph were reduced significantly, accompanied by smaller EV modal size profiles (albeit non-significantly) when compared to Hematodinium-negative controls. Differences were observed for citrullinated/deiminated target proteins in the haemolymph between the parasitized and control crabs, with fewer hits identified overall in the former. Three deiminated proteins specific to parasitized crab haemolymph were actin, Down syndrome cell adhesion molecule (DSCAM), and nitric oxide synthase – factors that contribute to innate immunity. We report, for the first time, Hematodinium sp. could interfere with EV biogenesis, and that protein deimination is a putative mechanism of immune-modulation in crustacean-Hematodinium interactions. Journal Article Virulence 14 1 Informa UK Limited 2150-5594 2150-5608 Peptidylarginine deiminase (PAD); arginine deiminase (ADI); innate immunity; haemocytes; cell-cell communication; marine disease 2 3 2023 2023-03-02 10.1080/21505594.2023.2180932 COLLEGE NANME COLLEGE CODE Swansea University External research funder(s) paid the OA fee (includes OA grants disbursed by the Library) ARCH UK; BB/P017215/1 2023-03-08T19:12:16.0704910 2023-02-17T14:02:28.1043363 Faculty of Science and Engineering School of Biosciences, Geography and Physics - Biosciences Christopher Coates 1 Igor Kraev 0000-0003-1822-278x 2 Andrew Rowley 3 Sigrun Lange 0000-0002-7193-3102 4 62681__26785__506f8e7f88ee4a41b354731b2f002d00.pdf 62681_VoR.pdf 2023-03-08T19:10:16.5030063 Output 2495233 application/pdf Version of Record true © 2023 The Author(s). This is an Open Access article distributed under the terms of the Creative Commons Attribution License true eng http://creativecommons.org/licenses/by/4.0/
title Extracellular vesicle signatures and protein citrullination are modified in shore crabs (Carcinus maenas) infected with Hematodinium sp
spellingShingle Extracellular vesicle signatures and protein citrullination are modified in shore crabs (Carcinus maenas) infected with Hematodinium sp
Christopher Coates
Andrew Rowley
title_short Extracellular vesicle signatures and protein citrullination are modified in shore crabs (Carcinus maenas) infected with Hematodinium sp
title_full Extracellular vesicle signatures and protein citrullination are modified in shore crabs (Carcinus maenas) infected with Hematodinium sp
title_fullStr Extracellular vesicle signatures and protein citrullination are modified in shore crabs (Carcinus maenas) infected with Hematodinium sp
title_full_unstemmed Extracellular vesicle signatures and protein citrullination are modified in shore crabs (Carcinus maenas) infected with Hematodinium sp
title_sort Extracellular vesicle signatures and protein citrullination are modified in shore crabs (Carcinus maenas) infected with Hematodinium sp
author_id_str_mv c62fa509397c2af92b316cda4987ff8e
e98124f6e62b9592786899d7059e3a79
author_id_fullname_str_mv c62fa509397c2af92b316cda4987ff8e_***_Christopher Coates
e98124f6e62b9592786899d7059e3a79_***_Andrew Rowley
author Christopher Coates
Andrew Rowley
author2 Christopher Coates
Igor Kraev
Andrew Rowley
Sigrun Lange
format Journal article
container_title Virulence
container_volume 14
container_issue 1
publishDate 2023
institution Swansea University
issn 2150-5594
2150-5608
doi_str_mv 10.1080/21505594.2023.2180932
publisher Informa UK Limited
college_str Faculty of Science and Engineering
hierarchytype
hierarchy_top_id facultyofscienceandengineering
hierarchy_top_title Faculty of Science and Engineering
hierarchy_parent_id facultyofscienceandengineering
hierarchy_parent_title Faculty of Science and Engineering
department_str School of Biosciences, Geography and Physics - Biosciences{{{_:::_}}}Faculty of Science and Engineering{{{_:::_}}}School of Biosciences, Geography and Physics - Biosciences
document_store_str 1
active_str 0
description Epizootiologists recurrently encounter symbionts and pathobionts in the haemolymph (blood equivalent) of shellfish. One such group is the dinoflagellate genus Hematodinium, which contains several species that cause debilitating disease in decapod crustaceans. The shore crab Carcinus maenas acts as a mobile reservoir of microparasites, including Hematodinium sp., thereby posing a risk to other co-located commercially important species, e.g. velvet crabs (Necora puber). Despite the widespread prevalence and documented seasonality of Hematodinium infection dynamics, there is a knowledge gap regarding host-pathogen antibiosis, namely, how Hematodinium avoids the host’s immune defences. Herein, we interrogated the haemolymph of Hematodinium-positive and Hematodinium-negative crabs for extracellular vesicle (EV) profiles (a proxy for cellular communication), alongside proteomic signatures for post-translational citrullination/deimination performed by arginine deiminases, which can infer a pathologic state. Circulating EV numbers in parasitized crab haemolymph were reduced significantly, accompanied by smaller EV modal size profiles (albeit non-significantly) when compared to Hematodinium-negative controls. Differences were observed for citrullinated/deiminated target proteins in the haemolymph between the parasitized and control crabs, with fewer hits identified overall in the former. Three deiminated proteins specific to parasitized crab haemolymph were actin, Down syndrome cell adhesion molecule (DSCAM), and nitric oxide synthase – factors that contribute to innate immunity. We report, for the first time, Hematodinium sp. could interfere with EV biogenesis, and that protein deimination is a putative mechanism of immune-modulation in crustacean-Hematodinium interactions.
published_date 2023-03-02T04:22:29Z
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