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Hematodinium sp. infection does not drive collateral disease contraction in a crustacean host

Charlotte Davies Orcid Logo, Jessica E Thomas, Sophie Malkin, Frederico Batista, Andrew Rowley, Christopher Coates, Jess Bevan

eLife, Volume: 11

Swansea University Authors: Charlotte Davies Orcid Logo, Sophie Malkin, Frederico Batista, Andrew Rowley, Christopher Coates, Jess Bevan

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DOI (Published version): 10.7554/elife.70356

Abstract

Host, pathogen, and environment are determinants of the disease triangle, the latter being a key driver of disease outcomes and persistence within a community. The dinoflagellate genus Hematodinium is detrimental to crustaceans globally – considered to suppress the innate defences of hosts, making t...

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ISSN: 2050-084X
Published: eLife Sciences Publications, Ltd 2022
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URI: https://cronfa.swan.ac.uk/Record/cronfa59336
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The dinoflagellate genus Hematodinium is detrimental to crustaceans globally &#x2013; considered to suppress the innate defences of hosts, making them more susceptible to co-infections. Evidence supporting immune suppression is largely anecdotal and sourced from diffuse accounts of compromised decapods. We used a population of shore crabs (Carcinus maenas), where Hematodinium sp. is endemic, to determine the extent of collateral infections across two distinct environments (open-water, semi-closed dock). Using a multi-resource approach (PCR, histology, haematology, population genetics, eDNA), we identified 162 Hematodinium-positive crabs and size/sex-matched these to 162 Hematodinium-free crabs out of 1191 analysed. Crabs were interrogated for known additional disease-causing agents; haplosporidians, microsporidians, mikrocytids, Vibrio spp., fungi, Sacculina, trematodes, and haemolymph bacterial loads. We found no significant differences in occurrence, severity, or composition of collateral infections between Hematodinium-positive and Hematodinium-free crabs at either site, but crucially, we recorded site-restricted blends of pathogens. We found no gross signs of host cell immune reactivity towards Hematodinium in the presence or absence of other pathogens. We contend Hematodinium sp. is not the proximal driver of co-infections in shore crabs, which suggests an evolutionary drive towards latency in this environmentally plastic host.</abstract><type>Journal Article</type><journal>eLife</journal><volume>11</volume><journalNumber/><paginationStart/><paginationEnd/><publisher>eLife Sciences Publications, Ltd</publisher><placeOfPublication/><isbnPrint/><isbnElectronic/><issnPrint/><issnElectronic>2050-084X</issnElectronic><keywords>aquatic vectors; carcinas maenas; carcinus maenas; disease connectivity; eDNA; ecology; endoparasites; immunology; immunopathology; inflammation; marine epizootiology; shore crabs</keywords><publishedDay>18</publishedDay><publishedMonth>2</publishedMonth><publishedYear>2022</publishedYear><publishedDate>2022-02-18</publishedDate><doi>10.7554/elife.70356</doi><url/><notes/><college>COLLEGE NANME</college><department>Biosciences</department><CollegeCode>COLLEGE CODE</CollegeCode><DepartmentCode>SBI</DepartmentCode><institution>Swansea University</institution><apcterm>External research funder(s) paid the OA fee (includes OA grants disbursed by the Library)</apcterm><funders>This study was part-funded by the European Regional Development fund through the Ireland Wales Cooperation Programme, BLUEFISH, awarded to CJC and AFR. 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spelling 2022-08-16T14:40:55.3117172 v2 59336 2022-02-09 Hematodinium sp. infection does not drive collateral disease contraction in a crustacean host a0febe211e502356dad1dab51a43761c 0000-0002-5853-1934 Charlotte Davies Charlotte Davies true false 17ff4136248e9382802ced1bc1d680e4 Sophie Malkin Sophie Malkin true false 77657489849b520529e56265f39a5724 Frederico Batista Frederico Batista true false e98124f6e62b9592786899d7059e3a79 Andrew Rowley Andrew Rowley true false af160934b75bea5b8ba83d68b3d1a003 Christopher Coates Christopher Coates true false 11f13b14aed072e93e611759d9aa090f Jess Bevan Jess Bevan true false 2022-02-09 SBI Host, pathogen, and environment are determinants of the disease triangle, the latter being a key driver of disease outcomes and persistence within a community. The dinoflagellate genus Hematodinium is detrimental to crustaceans globally – considered to suppress the innate defences of hosts, making them more susceptible to co-infections. Evidence supporting immune suppression is largely anecdotal and sourced from diffuse accounts of compromised decapods. We used a population of shore crabs (Carcinus maenas), where Hematodinium sp. is endemic, to determine the extent of collateral infections across two distinct environments (open-water, semi-closed dock). Using a multi-resource approach (PCR, histology, haematology, population genetics, eDNA), we identified 162 Hematodinium-positive crabs and size/sex-matched these to 162 Hematodinium-free crabs out of 1191 analysed. Crabs were interrogated for known additional disease-causing agents; haplosporidians, microsporidians, mikrocytids, Vibrio spp., fungi, Sacculina, trematodes, and haemolymph bacterial loads. We found no significant differences in occurrence, severity, or composition of collateral infections between Hematodinium-positive and Hematodinium-free crabs at either site, but crucially, we recorded site-restricted blends of pathogens. We found no gross signs of host cell immune reactivity towards Hematodinium in the presence or absence of other pathogens. We contend Hematodinium sp. is not the proximal driver of co-infections in shore crabs, which suggests an evolutionary drive towards latency in this environmentally plastic host. Journal Article eLife 11 eLife Sciences Publications, Ltd 2050-084X aquatic vectors; carcinas maenas; carcinus maenas; disease connectivity; eDNA; ecology; endoparasites; immunology; immunopathology; inflammation; marine epizootiology; shore crabs 18 2 2022 2022-02-18 10.7554/elife.70356 COLLEGE NANME Biosciences COLLEGE CODE SBI Swansea University External research funder(s) paid the OA fee (includes OA grants disbursed by the Library) This study was part-funded by the European Regional Development fund through the Ireland Wales Cooperation Programme, BLUEFISH, awarded to CJC and AFR. AFR was also part-funded by the BBSRC/NERC ARCH UK Aquaculture Initiative (BB/P017215/1), and start-up funds from Swansea University assigned to CJC were used to supplement this study. 2022-08-16T14:40:55.3117172 2022-02-09T11:22:56.8472378 Faculty of Science and Engineering School of Biosciences, Geography and Physics - Biosciences Charlotte Davies 0000-0002-5853-1934 1 Jessica E Thomas 2 Sophie Malkin 3 Frederico Batista 4 Andrew Rowley 5 Christopher Coates 6 Jess Bevan 7 59336__22416__4cf1318a9242427a9171cb476331f3c8.pdf 59336.pdf 2022-02-21T18:24:32.8346984 Output 11025200 application/pdf Version of Record true Copyright Davies et al. This article is distributed under the terms of the Creative Commons Attribution License true eng http://creativecommons.org/licenses/by/4.0/
title Hematodinium sp. infection does not drive collateral disease contraction in a crustacean host
spellingShingle Hematodinium sp. infection does not drive collateral disease contraction in a crustacean host
Charlotte Davies
Sophie Malkin
Frederico Batista
Andrew Rowley
Christopher Coates
Jess Bevan
title_short Hematodinium sp. infection does not drive collateral disease contraction in a crustacean host
title_full Hematodinium sp. infection does not drive collateral disease contraction in a crustacean host
title_fullStr Hematodinium sp. infection does not drive collateral disease contraction in a crustacean host
title_full_unstemmed Hematodinium sp. infection does not drive collateral disease contraction in a crustacean host
title_sort Hematodinium sp. infection does not drive collateral disease contraction in a crustacean host
author_id_str_mv a0febe211e502356dad1dab51a43761c
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author_id_fullname_str_mv a0febe211e502356dad1dab51a43761c_***_Charlotte Davies
17ff4136248e9382802ced1bc1d680e4_***_Sophie Malkin
77657489849b520529e56265f39a5724_***_Frederico Batista
e98124f6e62b9592786899d7059e3a79_***_Andrew Rowley
af160934b75bea5b8ba83d68b3d1a003_***_Christopher Coates
11f13b14aed072e93e611759d9aa090f_***_Jess Bevan
author Charlotte Davies
Sophie Malkin
Frederico Batista
Andrew Rowley
Christopher Coates
Jess Bevan
author2 Charlotte Davies
Jessica E Thomas
Sophie Malkin
Frederico Batista
Andrew Rowley
Christopher Coates
Jess Bevan
format Journal article
container_title eLife
container_volume 11
publishDate 2022
institution Swansea University
issn 2050-084X
doi_str_mv 10.7554/elife.70356
publisher eLife Sciences Publications, Ltd
college_str Faculty of Science and Engineering
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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
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description Host, pathogen, and environment are determinants of the disease triangle, the latter being a key driver of disease outcomes and persistence within a community. The dinoflagellate genus Hematodinium is detrimental to crustaceans globally – considered to suppress the innate defences of hosts, making them more susceptible to co-infections. Evidence supporting immune suppression is largely anecdotal and sourced from diffuse accounts of compromised decapods. We used a population of shore crabs (Carcinus maenas), where Hematodinium sp. is endemic, to determine the extent of collateral infections across two distinct environments (open-water, semi-closed dock). Using a multi-resource approach (PCR, histology, haematology, population genetics, eDNA), we identified 162 Hematodinium-positive crabs and size/sex-matched these to 162 Hematodinium-free crabs out of 1191 analysed. Crabs were interrogated for known additional disease-causing agents; haplosporidians, microsporidians, mikrocytids, Vibrio spp., fungi, Sacculina, trematodes, and haemolymph bacterial loads. We found no significant differences in occurrence, severity, or composition of collateral infections between Hematodinium-positive and Hematodinium-free crabs at either site, but crucially, we recorded site-restricted blends of pathogens. We found no gross signs of host cell immune reactivity towards Hematodinium in the presence or absence of other pathogens. We contend Hematodinium sp. is not the proximal driver of co-infections in shore crabs, which suggests an evolutionary drive towards latency in this environmentally plastic host.
published_date 2022-02-18T04:16:34Z
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