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The diarrhetic shellfish-poisoning toxin, okadaic acid, provokes gastropathy, dysbiosis and susceptibility to bacterial infection in a non-rodent bioassay, Galleria mellonella

Helena Emery Orcid Logo, William Traves, Andrew Rowley, Christopher Coates

Archives of Toxicology, Volume: 95, Issue: 10, Pages: 3361 - 3376

Swansea University Authors: Helena Emery Orcid Logo, Andrew Rowley, Christopher Coates

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DOI (Published version): 10.1007/s00204-021-03132-x

Abstract

Diarrhetic shellfish-poisoning (DSP) toxins such as okadaic acid and dinophysistoxins harm the human gastrointestinal tract, and therefore, their levels are regulated to an upper limit of 160 μg per kg tissue to protect consumers. Rodents are used routinely for risk assessment and studies concerning...

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Published in: Archives of Toxicology
ISSN: 0340-5761 1432-0738
Published: Springer Science and Business Media LLC 2021
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URI: https://cronfa.swan.ac.uk/Record/cronfa57518
first_indexed 2021-08-04T13:19:43Z
last_indexed 2021-11-04T04:23:11Z
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Rodents are used routinely for risk assessment and studies concerning mechanisms of toxicity, but there is a general move toward reducing and replacing vertebrates for these bioassays. We have adopted insect larvae of the wax moth Galleria mellonella as a surrogate toxicology model. We treated larvae with environmentally relevant doses of okadaic acid (80&#x2013;400 &#x3BC;g/kg) via intrahaemocoelic injection or gavage to determine marine toxin-related health decline: (1) whether pre-exposure to a sub-lethal dose of toxin (80 &#x3BC;g/kg) enhances susceptibility to bacterial infection, or (2) alters tissue pathology and bacterial community (microbiome) composition of the midgut. A sub-lethal dose of okadaic acid (80 &#x3BC;g/kg) followed 24 h later by bacterial inoculation (2&#x2009;&#xD7;&#x2009;105 Escherichia coli) reduced larval survival levels to 47%, when compared to toxin (90%) or microbial challenge (73%) alone. Histological analysis of the midgut depicted varying levels of tissue disruption, including nuclear aberrations associated with cell death (karyorrhexis, pyknosis), loss of organ architecture, and gross epithelial displacement into the lumen. Moreover, okadaic acid presence in the midgut coincided with a shift in the resident bacterial population over time in that substantial reductions in diversity (Shannon) and richness (Chao-1) indices were observed at 240 &#x3BC;g toxin per kg. 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spelling 2021-11-03T12:52:44.6410208 v2 57518 2021-08-04 The diarrhetic shellfish-poisoning toxin, okadaic acid, provokes gastropathy, dysbiosis and susceptibility to bacterial infection in a non-rodent bioassay, Galleria mellonella ddcdeaa3de5b3256ab5832a9a7377f1b 0000-0003-1890-4254 Helena Emery Helena Emery true false e98124f6e62b9592786899d7059e3a79 Andrew Rowley Andrew Rowley true false af160934b75bea5b8ba83d68b3d1a003 Christopher Coates Christopher Coates true false 2021-08-04 MEDS Diarrhetic shellfish-poisoning (DSP) toxins such as okadaic acid and dinophysistoxins harm the human gastrointestinal tract, and therefore, their levels are regulated to an upper limit of 160 μg per kg tissue to protect consumers. Rodents are used routinely for risk assessment and studies concerning mechanisms of toxicity, but there is a general move toward reducing and replacing vertebrates for these bioassays. We have adopted insect larvae of the wax moth Galleria mellonella as a surrogate toxicology model. We treated larvae with environmentally relevant doses of okadaic acid (80–400 μg/kg) via intrahaemocoelic injection or gavage to determine marine toxin-related health decline: (1) whether pre-exposure to a sub-lethal dose of toxin (80 μg/kg) enhances susceptibility to bacterial infection, or (2) alters tissue pathology and bacterial community (microbiome) composition of the midgut. A sub-lethal dose of okadaic acid (80 μg/kg) followed 24 h later by bacterial inoculation (2 × 105 Escherichia coli) reduced larval survival levels to 47%, when compared to toxin (90%) or microbial challenge (73%) alone. Histological analysis of the midgut depicted varying levels of tissue disruption, including nuclear aberrations associated with cell death (karyorrhexis, pyknosis), loss of organ architecture, and gross epithelial displacement into the lumen. Moreover, okadaic acid presence in the midgut coincided with a shift in the resident bacterial population over time in that substantial reductions in diversity (Shannon) and richness (Chao-1) indices were observed at 240 μg toxin per kg. Okadaic acid-induced deterioration of the insect alimentary canal resembles those changes reported for rodent bioassays. Journal Article Archives of Toxicology 95 10 3361 3376 Springer Science and Business Media LLC 0340-5761 1432-0738 Histopathology; 16S (V3–V4) rRNA microbiome; Immune-compromised; In vivo model; Food poisoning; Marine toxins 1 10 2021 2021-10-01 10.1007/s00204-021-03132-x COLLEGE NANME Medical School COLLEGE CODE MEDS Swansea University SU Library paid the OA fee (TA Institutional Deal) Interreg; KESS2 2021-11-03T12:52:44.6410208 2021-08-04T14:17:55.3175743 Faculty of Science and Engineering School of Biosciences, Geography and Physics - Biosciences Helena Emery 0000-0003-1890-4254 1 William Traves 2 Andrew Rowley 3 Christopher Coates 4 57518__20818__c531da6a4efa403bb647bb879c054404.pdf 57518.pdf 2021-09-10T14:14:06.4496088 Output 5015719 application/pdf Version of Record true © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License true eng http://creativecommons.org/licenses/by/4.0/
title The diarrhetic shellfish-poisoning toxin, okadaic acid, provokes gastropathy, dysbiosis and susceptibility to bacterial infection in a non-rodent bioassay, Galleria mellonella
spellingShingle The diarrhetic shellfish-poisoning toxin, okadaic acid, provokes gastropathy, dysbiosis and susceptibility to bacterial infection in a non-rodent bioassay, Galleria mellonella
Helena Emery
Andrew Rowley
Christopher Coates
title_short The diarrhetic shellfish-poisoning toxin, okadaic acid, provokes gastropathy, dysbiosis and susceptibility to bacterial infection in a non-rodent bioassay, Galleria mellonella
title_full The diarrhetic shellfish-poisoning toxin, okadaic acid, provokes gastropathy, dysbiosis and susceptibility to bacterial infection in a non-rodent bioassay, Galleria mellonella
title_fullStr The diarrhetic shellfish-poisoning toxin, okadaic acid, provokes gastropathy, dysbiosis and susceptibility to bacterial infection in a non-rodent bioassay, Galleria mellonella
title_full_unstemmed The diarrhetic shellfish-poisoning toxin, okadaic acid, provokes gastropathy, dysbiosis and susceptibility to bacterial infection in a non-rodent bioassay, Galleria mellonella
title_sort The diarrhetic shellfish-poisoning toxin, okadaic acid, provokes gastropathy, dysbiosis and susceptibility to bacterial infection in a non-rodent bioassay, Galleria mellonella
author_id_str_mv ddcdeaa3de5b3256ab5832a9a7377f1b
e98124f6e62b9592786899d7059e3a79
af160934b75bea5b8ba83d68b3d1a003
author_id_fullname_str_mv ddcdeaa3de5b3256ab5832a9a7377f1b_***_Helena Emery
e98124f6e62b9592786899d7059e3a79_***_Andrew Rowley
af160934b75bea5b8ba83d68b3d1a003_***_Christopher Coates
author Helena Emery
Andrew Rowley
Christopher Coates
author2 Helena Emery
William Traves
Andrew Rowley
Christopher Coates
format Journal article
container_title Archives of Toxicology
container_volume 95
container_issue 10
container_start_page 3361
publishDate 2021
institution Swansea University
issn 0340-5761
1432-0738
doi_str_mv 10.1007/s00204-021-03132-x
publisher Springer Science and Business Media LLC
college_str Faculty of Science and Engineering
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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 Diarrhetic shellfish-poisoning (DSP) toxins such as okadaic acid and dinophysistoxins harm the human gastrointestinal tract, and therefore, their levels are regulated to an upper limit of 160 μg per kg tissue to protect consumers. Rodents are used routinely for risk assessment and studies concerning mechanisms of toxicity, but there is a general move toward reducing and replacing vertebrates for these bioassays. We have adopted insect larvae of the wax moth Galleria mellonella as a surrogate toxicology model. We treated larvae with environmentally relevant doses of okadaic acid (80–400 μg/kg) via intrahaemocoelic injection or gavage to determine marine toxin-related health decline: (1) whether pre-exposure to a sub-lethal dose of toxin (80 μg/kg) enhances susceptibility to bacterial infection, or (2) alters tissue pathology and bacterial community (microbiome) composition of the midgut. A sub-lethal dose of okadaic acid (80 μg/kg) followed 24 h later by bacterial inoculation (2 × 105 Escherichia coli) reduced larval survival levels to 47%, when compared to toxin (90%) or microbial challenge (73%) alone. Histological analysis of the midgut depicted varying levels of tissue disruption, including nuclear aberrations associated with cell death (karyorrhexis, pyknosis), loss of organ architecture, and gross epithelial displacement into the lumen. Moreover, okadaic acid presence in the midgut coincided with a shift in the resident bacterial population over time in that substantial reductions in diversity (Shannon) and richness (Chao-1) indices were observed at 240 μg toxin per kg. Okadaic acid-induced deterioration of the insect alimentary canal resembles those changes reported for rodent bioassays.
published_date 2021-10-01T20:16:29Z
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