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Multi-omics analysis reveals the molecular response to heat stress in a “red tide” dinoflagellate
BACKGROUND: “Red tides” are harmful algal blooms caused by dinoflagellate microalgae that accumulate toxins lethal to other organisms, including humans via consumption of contaminated seafood. These algal blooms are driven by a combination of environmental factors including nutrient enrichment, part...
Autores principales: | , , , , , , , , , , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10666404/ https://www.ncbi.nlm.nih.gov/pubmed/37996937 http://dx.doi.org/10.1186/s13059-023-03107-4 |
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author | Dougan, Katherine E. Deng, Zhi-Luo Wöhlbrand, Lars Reuse, Carsten Bunk, Boyke Chen, Yibi Hartlich, Juliane Hiller, Karsten John, Uwe Kalvelage, Jana Mansky, Johannes Neumann-Schaal, Meina Overmann, Jörg Petersen, Jörn Sanchez-Garcia, Selene Schmidt-Hohagen, Kerstin Shah, Sarah Spröer, Cathrin Sztajer, Helena Wang, Hui Bhattacharya, Debashish Rabus, Ralf Jahn, Dieter Chan, Cheong Xin Wagner-Döbler, Irene |
author_facet | Dougan, Katherine E. Deng, Zhi-Luo Wöhlbrand, Lars Reuse, Carsten Bunk, Boyke Chen, Yibi Hartlich, Juliane Hiller, Karsten John, Uwe Kalvelage, Jana Mansky, Johannes Neumann-Schaal, Meina Overmann, Jörg Petersen, Jörn Sanchez-Garcia, Selene Schmidt-Hohagen, Kerstin Shah, Sarah Spröer, Cathrin Sztajer, Helena Wang, Hui Bhattacharya, Debashish Rabus, Ralf Jahn, Dieter Chan, Cheong Xin Wagner-Döbler, Irene |
author_sort | Dougan, Katherine E. |
collection | PubMed |
description | BACKGROUND: “Red tides” are harmful algal blooms caused by dinoflagellate microalgae that accumulate toxins lethal to other organisms, including humans via consumption of contaminated seafood. These algal blooms are driven by a combination of environmental factors including nutrient enrichment, particularly in warm waters, and are increasingly frequent. The molecular, regulatory, and evolutionary mechanisms that underlie the heat stress response in these harmful bloom-forming algal species remain little understood, due in part to the limited genomic resources from dinoflagellates, complicated by the large sizes of genomes, exhibiting features atypical of eukaryotes. RESULTS: We present the de novo assembled genome (~ 4.75 Gbp with 85,849 protein-coding genes), transcriptome, proteome, and metabolome from Prorocentrum cordatum, a globally abundant, bloom-forming dinoflagellate. Using axenic algal cultures, we study the molecular mechanisms that underpin the algal response to heat stress, which is relevant to current ocean warming trends. We present the first evidence of a complementary interplay between RNA editing and exon usage that regulates the expression and functional diversity of biomolecules, reflected by reduction in photosynthesis, central metabolism, and protein synthesis. These results reveal genomic signatures and post-transcriptional regulation for the first time in a pelagic dinoflagellate. CONCLUSIONS: Our multi-omics analyses uncover the molecular response to heat stress in an important bloom-forming algal species, which is driven by complex gene structures in a large, high-G+C genome, combined with multi-level transcriptional regulation. The dynamics and interplay of molecular regulatory mechanisms may explain in part how dinoflagellates diversified to become some of the most ecologically successful organisms on Earth. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13059-023-03107-4. |
format | Online Article Text |
id | pubmed-10666404 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-106664042023-11-23 Multi-omics analysis reveals the molecular response to heat stress in a “red tide” dinoflagellate Dougan, Katherine E. Deng, Zhi-Luo Wöhlbrand, Lars Reuse, Carsten Bunk, Boyke Chen, Yibi Hartlich, Juliane Hiller, Karsten John, Uwe Kalvelage, Jana Mansky, Johannes Neumann-Schaal, Meina Overmann, Jörg Petersen, Jörn Sanchez-Garcia, Selene Schmidt-Hohagen, Kerstin Shah, Sarah Spröer, Cathrin Sztajer, Helena Wang, Hui Bhattacharya, Debashish Rabus, Ralf Jahn, Dieter Chan, Cheong Xin Wagner-Döbler, Irene Genome Biol Research BACKGROUND: “Red tides” are harmful algal blooms caused by dinoflagellate microalgae that accumulate toxins lethal to other organisms, including humans via consumption of contaminated seafood. These algal blooms are driven by a combination of environmental factors including nutrient enrichment, particularly in warm waters, and are increasingly frequent. The molecular, regulatory, and evolutionary mechanisms that underlie the heat stress response in these harmful bloom-forming algal species remain little understood, due in part to the limited genomic resources from dinoflagellates, complicated by the large sizes of genomes, exhibiting features atypical of eukaryotes. RESULTS: We present the de novo assembled genome (~ 4.75 Gbp with 85,849 protein-coding genes), transcriptome, proteome, and metabolome from Prorocentrum cordatum, a globally abundant, bloom-forming dinoflagellate. Using axenic algal cultures, we study the molecular mechanisms that underpin the algal response to heat stress, which is relevant to current ocean warming trends. We present the first evidence of a complementary interplay between RNA editing and exon usage that regulates the expression and functional diversity of biomolecules, reflected by reduction in photosynthesis, central metabolism, and protein synthesis. These results reveal genomic signatures and post-transcriptional regulation for the first time in a pelagic dinoflagellate. CONCLUSIONS: Our multi-omics analyses uncover the molecular response to heat stress in an important bloom-forming algal species, which is driven by complex gene structures in a large, high-G+C genome, combined with multi-level transcriptional regulation. The dynamics and interplay of molecular regulatory mechanisms may explain in part how dinoflagellates diversified to become some of the most ecologically successful organisms on Earth. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13059-023-03107-4. BioMed Central 2023-11-23 /pmc/articles/PMC10666404/ /pubmed/37996937 http://dx.doi.org/10.1186/s13059-023-03107-4 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data. |
spellingShingle | Research Dougan, Katherine E. Deng, Zhi-Luo Wöhlbrand, Lars Reuse, Carsten Bunk, Boyke Chen, Yibi Hartlich, Juliane Hiller, Karsten John, Uwe Kalvelage, Jana Mansky, Johannes Neumann-Schaal, Meina Overmann, Jörg Petersen, Jörn Sanchez-Garcia, Selene Schmidt-Hohagen, Kerstin Shah, Sarah Spröer, Cathrin Sztajer, Helena Wang, Hui Bhattacharya, Debashish Rabus, Ralf Jahn, Dieter Chan, Cheong Xin Wagner-Döbler, Irene Multi-omics analysis reveals the molecular response to heat stress in a “red tide” dinoflagellate |
title | Multi-omics analysis reveals the molecular response to heat stress in a “red tide” dinoflagellate |
title_full | Multi-omics analysis reveals the molecular response to heat stress in a “red tide” dinoflagellate |
title_fullStr | Multi-omics analysis reveals the molecular response to heat stress in a “red tide” dinoflagellate |
title_full_unstemmed | Multi-omics analysis reveals the molecular response to heat stress in a “red tide” dinoflagellate |
title_short | Multi-omics analysis reveals the molecular response to heat stress in a “red tide” dinoflagellate |
title_sort | multi-omics analysis reveals the molecular response to heat stress in a “red tide” dinoflagellate |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10666404/ https://www.ncbi.nlm.nih.gov/pubmed/37996937 http://dx.doi.org/10.1186/s13059-023-03107-4 |
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