Unbiased high-throughput characterization of mussel transcriptomic responses to sublethal concentrations of the biotoxin okadaic acid
Background. Harmful Algal Blooms (HABs) responsible for Diarrhetic Shellfish Poisoning (DSP) represent a major threat for human consumers of shellfish. The biotoxin Okadaic Acid (OA), a well-known phosphatase inhibitor and tumor promoter, is the primary cause of acute DSP intoxications. Although sev...
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PeerJ Inc.
2015-11-01
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record_format |
Article |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Victoria Suarez-Ulloa Juan Fernandez-Tajes Vanessa Aguiar-Pulido M. Veronica Prego-Faraldo Fernanda Florez-Barros Alexia Sexto-Iglesias Josefina Mendez Jose M. Eirin-Lopez |
spellingShingle |
Victoria Suarez-Ulloa Juan Fernandez-Tajes Vanessa Aguiar-Pulido M. Veronica Prego-Faraldo Fernanda Florez-Barros Alexia Sexto-Iglesias Josefina Mendez Jose M. Eirin-Lopez Unbiased high-throughput characterization of mussel transcriptomic responses to sublethal concentrations of the biotoxin okadaic acid PeerJ Okadaic acid Marine pollution Transcriptomics Diarrhetic shellfish poisoning Biomonitoring Harmful algal blooms |
author_facet |
Victoria Suarez-Ulloa Juan Fernandez-Tajes Vanessa Aguiar-Pulido M. Veronica Prego-Faraldo Fernanda Florez-Barros Alexia Sexto-Iglesias Josefina Mendez Jose M. Eirin-Lopez |
author_sort |
Victoria Suarez-Ulloa |
title |
Unbiased high-throughput characterization of mussel transcriptomic responses to sublethal concentrations of the biotoxin okadaic acid |
title_short |
Unbiased high-throughput characterization of mussel transcriptomic responses to sublethal concentrations of the biotoxin okadaic acid |
title_full |
Unbiased high-throughput characterization of mussel transcriptomic responses to sublethal concentrations of the biotoxin okadaic acid |
title_fullStr |
Unbiased high-throughput characterization of mussel transcriptomic responses to sublethal concentrations of the biotoxin okadaic acid |
title_full_unstemmed |
Unbiased high-throughput characterization of mussel transcriptomic responses to sublethal concentrations of the biotoxin okadaic acid |
title_sort |
unbiased high-throughput characterization of mussel transcriptomic responses to sublethal concentrations of the biotoxin okadaic acid |
publisher |
PeerJ Inc. |
series |
PeerJ |
issn |
2167-8359 |
publishDate |
2015-11-01 |
description |
Background. Harmful Algal Blooms (HABs) responsible for Diarrhetic Shellfish Poisoning (DSP) represent a major threat for human consumers of shellfish. The biotoxin Okadaic Acid (OA), a well-known phosphatase inhibitor and tumor promoter, is the primary cause of acute DSP intoxications. Although several studies have described the molecular effects of high OA concentrations on sentinel organisms (e.g., bivalve molluscs), the effect of prolonged exposures to low (sublethal) OA concentrations is still unknown. In order to fill this gap, this work combines Next-Generation sequencing and custom-made microarray technologies to develop an unbiased characterization of the transcriptomic response of mussels during early stages of a DSP bloom.Methods. Mussel specimens were exposed to a HAB episode simulating an early stage DSP bloom (200 cells/L of the dinoflagellate Prorocentrum lima for 24 h). The unbiased characterization of the transcriptomic responses triggered by OA was carried out using two complementary methods of cDNA library preparation: normalized and Suppression Subtractive Hybridization (SSH). Libraries were sequenced and read datasets were mapped to Gene Ontology and KEGG databases. A custom-made oligonucleotide microarray was developed based on these data, completing the expression analysis of digestive gland and gill tissues.Results. Our findings show that exposure to sublethal concentrations of OA is enough to induce gene expression modifications in the mussel Mytilus. Transcriptomic analyses revealed an increase in proteasomal activity, molecular transport, cell cycle regulation, energy production and immune activity in mussels. Oppositely, a number of transcripts hypothesized to be responsive to OA (notably the Serine/Threonine phosphatases PP1 and PP2A) failed to show substantial modifications. Both digestive gland and gill tissues responded similarly to OA, although expression modifications were more dramatic in the former, supporting the choice of this tissue for future biomonitoring studies.Discussion. Exposure to OA concentrations within legal limits for safe consumption of shellfish is enough to disrupt important cellular processes in mussels, eliciting sharp transcriptional changes as a result. By combining the study of cDNA libraries and a custom-made OA-specific microarray, our work provides a comprehensive characterization of the OA-specific transcriptome, improving the accuracy of the analysis of expresion profiles compared to single-replicated RNA-seq methods. The combination of our data with related studies helps understanding the molecular mechanisms underlying molecular responses to DSP episodes in marine organisms, providing useful information to develop a new generation of tools for the monitoring of OA pollution. |
topic |
Okadaic acid Marine pollution Transcriptomics Diarrhetic shellfish poisoning Biomonitoring Harmful algal blooms |
url |
https://peerj.com/articles/1429.pdf |
work_keys_str_mv |
AT victoriasuarezulloa unbiasedhighthroughputcharacterizationofmusseltranscriptomicresponsestosublethalconcentrationsofthebiotoxinokadaicacid AT juanfernandeztajes unbiasedhighthroughputcharacterizationofmusseltranscriptomicresponsestosublethalconcentrationsofthebiotoxinokadaicacid AT vanessaaguiarpulido unbiasedhighthroughputcharacterizationofmusseltranscriptomicresponsestosublethalconcentrationsofthebiotoxinokadaicacid AT mveronicapregofaraldo unbiasedhighthroughputcharacterizationofmusseltranscriptomicresponsestosublethalconcentrationsofthebiotoxinokadaicacid AT fernandaflorezbarros unbiasedhighthroughputcharacterizationofmusseltranscriptomicresponsestosublethalconcentrationsofthebiotoxinokadaicacid AT alexiasextoiglesias unbiasedhighthroughputcharacterizationofmusseltranscriptomicresponsestosublethalconcentrationsofthebiotoxinokadaicacid AT josefinamendez unbiasedhighthroughputcharacterizationofmusseltranscriptomicresponsestosublethalconcentrationsofthebiotoxinokadaicacid AT josemeirinlopez unbiasedhighthroughputcharacterizationofmusseltranscriptomicresponsestosublethalconcentrationsofthebiotoxinokadaicacid |
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doaj-70437fa5005a4ed4afa5cf85f18b522e2020-11-25T00:37:32ZengPeerJ Inc.PeerJ2167-83592015-11-013e142910.7717/peerj.1429Unbiased high-throughput characterization of mussel transcriptomic responses to sublethal concentrations of the biotoxin okadaic acidVictoria Suarez-Ulloa0Juan Fernandez-Tajes1Vanessa Aguiar-Pulido2M. Veronica Prego-Faraldo3Fernanda Florez-Barros4Alexia Sexto-Iglesias5Josefina Mendez6Jose M. Eirin-Lopez7Chromatin Structure and Evolution Group (Chromevol), Department of Biological Sciences, Florida International University, Miami, FL, United States of AmericaMcCarthy Group, Wellcome Trust Center for Human Genetics, University of Oxford, Oxford, United KingdomBioinformatics Research Group (BioRG), School of Computing & Information Sciences, Florida International University, Miami, FL, United States of AmericaChromatin Structure and Evolution Group (Chromevol), Department of Biological Sciences, Florida International University, Miami, FL, United States of AmericaCentre for Nephrology, Royal Free Hospital, University College London, London, United KingdomXenomar Group, Department of Cellular and Molecular Biology, University of A Coruña, A Coruña, SpainXenomar Group, Department of Cellular and Molecular Biology, University of A Coruña, A Coruña, SpainChromatin Structure and Evolution Group (Chromevol), Department of Biological Sciences, Florida International University, Miami, FL, United States of AmericaBackground. Harmful Algal Blooms (HABs) responsible for Diarrhetic Shellfish Poisoning (DSP) represent a major threat for human consumers of shellfish. The biotoxin Okadaic Acid (OA), a well-known phosphatase inhibitor and tumor promoter, is the primary cause of acute DSP intoxications. Although several studies have described the molecular effects of high OA concentrations on sentinel organisms (e.g., bivalve molluscs), the effect of prolonged exposures to low (sublethal) OA concentrations is still unknown. In order to fill this gap, this work combines Next-Generation sequencing and custom-made microarray technologies to develop an unbiased characterization of the transcriptomic response of mussels during early stages of a DSP bloom.Methods. Mussel specimens were exposed to a HAB episode simulating an early stage DSP bloom (200 cells/L of the dinoflagellate Prorocentrum lima for 24 h). The unbiased characterization of the transcriptomic responses triggered by OA was carried out using two complementary methods of cDNA library preparation: normalized and Suppression Subtractive Hybridization (SSH). Libraries were sequenced and read datasets were mapped to Gene Ontology and KEGG databases. A custom-made oligonucleotide microarray was developed based on these data, completing the expression analysis of digestive gland and gill tissues.Results. Our findings show that exposure to sublethal concentrations of OA is enough to induce gene expression modifications in the mussel Mytilus. Transcriptomic analyses revealed an increase in proteasomal activity, molecular transport, cell cycle regulation, energy production and immune activity in mussels. Oppositely, a number of transcripts hypothesized to be responsive to OA (notably the Serine/Threonine phosphatases PP1 and PP2A) failed to show substantial modifications. Both digestive gland and gill tissues responded similarly to OA, although expression modifications were more dramatic in the former, supporting the choice of this tissue for future biomonitoring studies.Discussion. Exposure to OA concentrations within legal limits for safe consumption of shellfish is enough to disrupt important cellular processes in mussels, eliciting sharp transcriptional changes as a result. By combining the study of cDNA libraries and a custom-made OA-specific microarray, our work provides a comprehensive characterization of the OA-specific transcriptome, improving the accuracy of the analysis of expresion profiles compared to single-replicated RNA-seq methods. The combination of our data with related studies helps understanding the molecular mechanisms underlying molecular responses to DSP episodes in marine organisms, providing useful information to develop a new generation of tools for the monitoring of OA pollution.https://peerj.com/articles/1429.pdfOkadaic acidMarine pollutionTranscriptomicsDiarrhetic shellfish poisoningBiomonitoringHarmful algal blooms |