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Multi-omics analysis reveals the molecular response to heat stress in a “red tide” dinoflagellate

Katherine E. Dougan, Zhi-Luo Deng, Lars Wöhlbrand, Carsten Reuse, Boyke Bunk, Yibi Chen, Juliane Hartlich, Karsten Hiller, View ORCID ProfileUwe John, Jana Kalvelage, Johannes Mansky, Meina Neumann-Schaal, Jörg Overmann, Jörn Petersen, Selene Sanchez-Garcia, Kerstin Schmidt-Hohagen, Sarah Shah, Cathrin Spröer, Helena Sztajer, Hui Wang, Debashish Bhattacharya, Ralf Rabus, Dieter Jahn, View ORCID ProfileCheong Xin Chan, View ORCID ProfileIrene Wagner-Döbler
doi: https://doi.org/10.1101/2022.07.25.501386
Katherine E. Dougan
1The University of Queensland, School of Chemistry and Molecular Biosciences, Australian Centre for Ecogenomics, Brisbane, QLD 4072, Australia
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Zhi-Luo Deng
2Helmholtz-Center for Infection Research (HZI), Inhoffenstr. 7, 38124 Braunschweig, Germany
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Lars Wöhlbrand
3Institute for Chemistry and Biology of the Marine Environment (ICBM), Carl von Ossietzky University of Oldenburg, 26129 Oldenburg, Germany
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Carsten Reuse
4Braunschweig Center for Systems Biology (BRICS), Technische Universität Braunschweig, Rebenring 56, 38106 Braunschweig, Germany
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Boyke Bunk
5German Culture Collection for Microorganisms and Cell Cultures (DSMZ), Inhoffenstraße 7B, 38124 Braunschweig, Germany
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Yibi Chen
1The University of Queensland, School of Chemistry and Molecular Biosciences, Australian Centre for Ecogenomics, Brisbane, QLD 4072, Australia
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Juliane Hartlich
4Braunschweig Center for Systems Biology (BRICS), Technische Universität Braunschweig, Rebenring 56, 38106 Braunschweig, Germany
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Karsten Hiller
4Braunschweig Center for Systems Biology (BRICS), Technische Universität Braunschweig, Rebenring 56, 38106 Braunschweig, Germany
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Uwe John
6Alfred Wegener Institute, Helmholtz Centre for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, Germany
7Helmholtz Institute for Functional Marine Biodiversity at the University of Oldenburg (HIFMB), Ammerländer Heersstraße 231, 26129 Oldenburg, Germany
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Jana Kalvelage
3Institute for Chemistry and Biology of the Marine Environment (ICBM), Carl von Ossietzky University of Oldenburg, 26129 Oldenburg, Germany
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Johannes Mansky
4Braunschweig Center for Systems Biology (BRICS), Technische Universität Braunschweig, Rebenring 56, 38106 Braunschweig, Germany
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Meina Neumann-Schaal
5German Culture Collection for Microorganisms and Cell Cultures (DSMZ), Inhoffenstraße 7B, 38124 Braunschweig, Germany
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Jörg Overmann
5German Culture Collection for Microorganisms and Cell Cultures (DSMZ), Inhoffenstraße 7B, 38124 Braunschweig, Germany
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Jörn Petersen
5German Culture Collection for Microorganisms and Cell Cultures (DSMZ), Inhoffenstraße 7B, 38124 Braunschweig, Germany
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Selene Sanchez-Garcia
4Braunschweig Center for Systems Biology (BRICS), Technische Universität Braunschweig, Rebenring 56, 38106 Braunschweig, Germany
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Kerstin Schmidt-Hohagen
4Braunschweig Center for Systems Biology (BRICS), Technische Universität Braunschweig, Rebenring 56, 38106 Braunschweig, Germany
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Sarah Shah
1The University of Queensland, School of Chemistry and Molecular Biosciences, Australian Centre for Ecogenomics, Brisbane, QLD 4072, Australia
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Cathrin Spröer
5German Culture Collection for Microorganisms and Cell Cultures (DSMZ), Inhoffenstraße 7B, 38124 Braunschweig, Germany
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Helena Sztajer
4Braunschweig Center for Systems Biology (BRICS), Technische Universität Braunschweig, Rebenring 56, 38106 Braunschweig, Germany
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Hui Wang
4Braunschweig Center for Systems Biology (BRICS), Technische Universität Braunschweig, Rebenring 56, 38106 Braunschweig, Germany
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Debashish Bhattacharya
8Rutgers University, Department of Biochemistry and Microbiology, New Brunswick, NJ 08901, USA
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Ralf Rabus
3Institute for Chemistry and Biology of the Marine Environment (ICBM), Carl von Ossietzky University of Oldenburg, 26129 Oldenburg, Germany
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Dieter Jahn
4Braunschweig Center for Systems Biology (BRICS), Technische Universität Braunschweig, Rebenring 56, 38106 Braunschweig, Germany
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Cheong Xin Chan
1The University of Queensland, School of Chemistry and Molecular Biosciences, Australian Centre for Ecogenomics, Brisbane, QLD 4072, Australia
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  • For correspondence: c.chan1@uq.edu.au i.wagner-doebler@tu-braunschweig.de
Irene Wagner-Döbler
4Braunschweig Center for Systems Biology (BRICS), Technische Universität Braunschweig, Rebenring 56, 38106 Braunschweig, Germany
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  • For correspondence: c.chan1@uq.edu.au i.wagner-doebler@tu-braunschweig.de
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Abstract

“Red tides” are harmful algal blooms (HABs) caused by dinoflagellate microalgae that accumulate toxins lethal to other organisms, including humans via consumption of contaminated seafood. Increasingly frequent, HABs are driven by a combination of environmental factors including nutrient enrichment, particularly in warm waters. Here, we present the de novo assembled genome (~4.75 Gbp), transcriptome, proteome, and metabolome from Prorocentrum cordatum, a globally abundant, bloom-forming dinoflagellate. Using axenic algal cultures, we studied the molecular mechanisms that underpin response to temperature stress, which is relevant to current ocean warming trends. We discovered 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. Our multi-omics analyses uncover the molecular response to heat stress in an important HAB species, which is driven by complex gene structures in a large, high-G+C genome, combined with multi-level transcriptional regulation.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • The manuscript has a new title that reflects the main focus of the study: Multi-omics analysis reveals the molecular response to heat stress in a red tide dinoflagellate. The text was streamlined and an analysis of dino-SL was added.

  • https://cloudstor.aarnet.edu.au/plus/s/nxC7atJTpJuyr8h

  • https://fairdomhub.org/sops/551?code=RrSjntdGsUnt2zRDdFKIKnfmJviLFvw3O7BzG9Lv

  • https://fairdomhub.org/sops/549?code=TKCZcudIA05oY%2FSnAFW67R2IwE91d1x%2F9eQp6dnH

  • https://fairdomhub.org/data_files/6075?code=kyxQ9ljLVTxjU54Wrk5HS62bQj6Z9niiJtT30GSc

  • https://fairdomhub.org/data_files/6059?code=GhhJoFC9oBKYd7fWRlE9kZ%2BpMGnGRMD2Cvtf8sLE

  • https://fairdomhub.org/data_files/6058?code=QwaeOVVnEvuCXftZqObFSFD82emv0qEqhs9oiHV1

  • https://fairdomhub.org/data_files/6057?code=4PPrRrP6qwTuD1iekFWzxzRijAyGkbeaySaybJjI

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted November 22, 2022.
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Multi-omics analysis reveals the molecular response to heat stress in a “red tide” dinoflagellate
Katherine E. Dougan, Zhi-Luo Deng, Lars Wöhlbrand, Carsten Reuse, Boyke Bunk, Yibi Chen, Juliane Hartlich, Karsten Hiller, Uwe John, Jana Kalvelage, Johannes Mansky, Meina Neumann-Schaal, Jörg Overmann, Jörn Petersen, Selene Sanchez-Garcia, Kerstin Schmidt-Hohagen, Sarah Shah, Cathrin Spröer, Helena Sztajer, Hui Wang, Debashish Bhattacharya, Ralf Rabus, Dieter Jahn, Cheong Xin Chan, Irene Wagner-Döbler
bioRxiv 2022.07.25.501386; doi: https://doi.org/10.1101/2022.07.25.501386
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Multi-omics analysis reveals the molecular response to heat stress in a “red tide” dinoflagellate
Katherine E. Dougan, Zhi-Luo Deng, Lars Wöhlbrand, Carsten Reuse, Boyke Bunk, Yibi Chen, Juliane Hartlich, Karsten Hiller, Uwe John, Jana Kalvelage, Johannes Mansky, Meina Neumann-Schaal, Jörg Overmann, Jörn Petersen, Selene Sanchez-Garcia, Kerstin Schmidt-Hohagen, Sarah Shah, Cathrin Spröer, Helena Sztajer, Hui Wang, Debashish Bhattacharya, Ralf Rabus, Dieter Jahn, Cheong Xin Chan, Irene Wagner-Döbler
bioRxiv 2022.07.25.501386; doi: https://doi.org/10.1101/2022.07.25.501386

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