Gill Transcriptomic Responses to Toxin-producing Alga Prymnesium parvum in Rainbow Trout

Morag Clinton; Elżbieta Król; Dagoberto Sepúlveda; Nikolaj R. Andersen; Andrew S. Brierley; David E. K. Ferrier; Per Juel Hansen; Niels Lorenzen; Samuel A. M. Martin

doi:10.3389/fimmu.2021.794593

Gill Transcriptomic Responses to Toxin-producing Alga Prymnesium parvum in Rainbow Trout

Morag Clinton, Elżbieta Król, Dagoberto Sepúlveda, Nikolaj R. Andersen, Andrew S. Brierley, David E. K. Ferrier, Per Juel Hansen, Niels Lorenzen, Samuel A. M. Martin^* (Corresponding Author)

^*Corresponding author for this work

Aberdeen Centre For Environmental Sustainability

Research output: Contribution to journal › Article › peer-review

2 Citations (Scopus)

8 Downloads (Pure)

Abstract

The gill of teleost fish is a multifunctional organ involved in many physiological processes, including protection of the mucosal gill surface against pathogens and other environmental antigens by the gill-associated lymphoid tissue (GIALT). Climate change associated phenomena, such as increasing frequency and magnitude of harmful algal blooms (HABs) put extra strain on gill function, contributing to enhanced fish mortality and fish kills. However, the molecular basis of the HAB-induced gill injury remains largely unknown due to the lack of high-throughput transcriptomic studies performed on teleost fish in laboratory conditions. We used juvenile rainbow trout (Oncorhynchus mykiss) to investigate the transcriptomic responses of the gill tissue to two (high and low) sublethal densities of the toxin-producing alga Prymnesium parvum, in relation to non-exposed control fish. The exposure time to P. parvum (4–5 h) was sufficient to identify three different phenotypic responses among the exposed fish, enabling us to focus on the common gill transcriptomic responses to P. parvum that were independent of dose and phenotype. The inspection of common differentially expressed genes (DEGs), canonical pathways, upstream regulators and downstream effects pointed towards P. parvum-induced inflammatory response and gill inflammation driven by alterations of Acute Phase Response Signalling, IL-6 Signalling, IL-10 Signalling, Role of PKR in Interferon Induction and Antiviral Response, IL-8 Signalling and IL-17 Signalling pathways. While we could not determine if the inferred gill inflammation was progressing or resolving, our study clearly suggests that P. parvum blooms may contribute to the serious gill disorders in fish. By providing insights into the gill transcriptomic responses to toxin-producing P. parvum in teleost fish, our research opens new avenues for investigating how to monitor and mitigate toxicity of HABs before they become lethal.

Original language	English
Article number	794593
Number of pages	17
Journal	Frontiers in Immunology
Volume	12
DOIs	https://doi.org/10.3389/fimmu.2021.794593
Publication status	Published - 8 Dec 2021

Bibliographical note

This work was supported by the BBSRC EastBio PhD studentship awarded to MC, the Danish Strategic Research Council grant No 060300449B HABFISH, and the European Maritime and Fisheries Fund and the Danish Fisheries Agency joint grant “Sundt Dambrug”. Molecular work at University of Aberdeen was funded by Scottish Aquaculture Innovation grant SL 2017 08. EK was supported by BBSRC grant BB/R018812/1.

Data Availability Statement

The datasets generated for this study are available in the ArrayExpress repository (http://www.ebi.ac.uk/arrayexpress/) under accession numbers A-MEXP-2315 (Trout_imm_v1 array design) and E-MTAB-10541 (microarray raw data).

Keywords

gill health
gill inflammation
microarray
cytokines
hypoxia
harmful algal bloom (HAB)
golden algal

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.3389/fimmu.2021.794593Licence: CC BY

Clinton_etal_fimmu_Alga_Prymnesium_parvum_VOR
Copyright © 2021 Clinton, Król, Sepúlveda, Andersen, Brierley, Ferrier, Hansen, Lorenzen and Martin. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. https://creativecommons.org/licenses/by/4.0/
Final published version, 2.66 MBLicence: CC BY

Gill Transcriptomic Responses to Toxin-producing Alga Prymnesium parvum in Rainbow Trout
Krol, E. (Creator), EMBL-EBI, 10 Nov 2021
https://www.ebi.ac.uk/arrayexpress/experiments/E-MTAB-10541/
Dataset
Rainbow trout 4 x 44 platform. Oligos based on TC seqences from TIGRE database, (40125 oligos) and a further 1287 immune genes to enrich the coverage of these genes develpoed during the EUFP7 project IMAQUANIM.
Martin, S. (Creator), EMBL-EBI, 8 Dec 2021
https://www.ebi.ac.uk/arrayexpress/arrays/A-MEXP-2315/
Dataset

Cite this

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AU - Andersen, Nikolaj R.

AU - Brierley, Andrew S.

AU - Ferrier, David E. K.

AU - Hansen, Per Juel

AU - Lorenzen, Niels

AU - Martin, Samuel A. M.

N1 - This work was supported by the BBSRC EastBio PhD studentship awarded to MC, the Danish Strategic Research Council grant No 060300449B HABFISH, and the European Maritime and Fisheries Fund and the Danish Fisheries Agency joint grant “Sundt Dambrug”. Molecular work at University of Aberdeen was funded by Scottish Aquaculture Innovation grant SL 2017 08. EK was supported by BBSRC grant BB/R018812/1.

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N2 - The gill of teleost fish is a multifunctional organ involved in many physiological processes, including protection of the mucosal gill surface against pathogens and other environmental antigens by the gill-associated lymphoid tissue (GIALT). Climate change associated phenomena, such as increasing frequency and magnitude of harmful algal blooms (HABs) put extra strain on gill function, contributing to enhanced fish mortality and fish kills. However, the molecular basis of the HAB-induced gill injury remains largely unknown due to the lack of high-throughput transcriptomic studies performed on teleost fish in laboratory conditions. We used juvenile rainbow trout (Oncorhynchus mykiss) to investigate the transcriptomic responses of the gill tissue to two (high and low) sublethal densities of the toxin-producing alga Prymnesium parvum, in relation to non-exposed control fish. The exposure time to P. parvum (4–5 h) was sufficient to identify three different phenotypic responses among the exposed fish, enabling us to focus on the common gill transcriptomic responses to P. parvum that were independent of dose and phenotype. The inspection of common differentially expressed genes (DEGs), canonical pathways, upstream regulators and downstream effects pointed towards P. parvum-induced inflammatory response and gill inflammation driven by alterations of Acute Phase Response Signalling, IL-6 Signalling, IL-10 Signalling, Role of PKR in Interferon Induction and Antiviral Response, IL-8 Signalling and IL-17 Signalling pathways. While we could not determine if the inferred gill inflammation was progressing or resolving, our study clearly suggests that P. parvum blooms may contribute to the serious gill disorders in fish. By providing insights into the gill transcriptomic responses to toxin-producing P. parvum in teleost fish, our research opens new avenues for investigating how to monitor and mitigate toxicity of HABs before they become lethal.

AB - The gill of teleost fish is a multifunctional organ involved in many physiological processes, including protection of the mucosal gill surface against pathogens and other environmental antigens by the gill-associated lymphoid tissue (GIALT). Climate change associated phenomena, such as increasing frequency and magnitude of harmful algal blooms (HABs) put extra strain on gill function, contributing to enhanced fish mortality and fish kills. However, the molecular basis of the HAB-induced gill injury remains largely unknown due to the lack of high-throughput transcriptomic studies performed on teleost fish in laboratory conditions. We used juvenile rainbow trout (Oncorhynchus mykiss) to investigate the transcriptomic responses of the gill tissue to two (high and low) sublethal densities of the toxin-producing alga Prymnesium parvum, in relation to non-exposed control fish. The exposure time to P. parvum (4–5 h) was sufficient to identify three different phenotypic responses among the exposed fish, enabling us to focus on the common gill transcriptomic responses to P. parvum that were independent of dose and phenotype. The inspection of common differentially expressed genes (DEGs), canonical pathways, upstream regulators and downstream effects pointed towards P. parvum-induced inflammatory response and gill inflammation driven by alterations of Acute Phase Response Signalling, IL-6 Signalling, IL-10 Signalling, Role of PKR in Interferon Induction and Antiviral Response, IL-8 Signalling and IL-17 Signalling pathways. While we could not determine if the inferred gill inflammation was progressing or resolving, our study clearly suggests that P. parvum blooms may contribute to the serious gill disorders in fish. By providing insights into the gill transcriptomic responses to toxin-producing P. parvum in teleost fish, our research opens new avenues for investigating how to monitor and mitigate toxicity of HABs before they become lethal.

KW - gill health

KW - gill inflammation

KW - microarray

KW - cytokines

KW - hypoxia

KW - harmful algal bloom (HAB)

KW - golden algal

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DO - 10.3389/fimmu.2021.794593

M3 - Article

SN - 1664-3224

VL - 12

JO - Frontiers in Immunology

JF - Frontiers in Immunology

M1 - 794593

ER -

Gill Transcriptomic Responses to Toxin-producing Alga Prymnesium parvum in Rainbow Trout

Abstract

Bibliographical note

Data Availability Statement

Keywords

UN SDGs

Access to Document

Fingerprint

Datasets

Gill Transcriptomic Responses to Toxin-producing Alga Prymnesium parvum in Rainbow Trout

Rainbow trout 4 x 44 platform. Oligos based on TC seqences from TIGRE database, (40125 oligos) and a further 1287 immune genes to enrich the coverage of these genes develpoed during the EUFP7 project IMAQUANIM.

Cite this