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      Fast and pervasive transcriptomic resilience and acclimation of extremely heat-tolerant coral holobionts from the northern Red Sea

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          Significance

          Coral reefs are in catastrophic decline worldwide, in part due to increasingly warm surface waters that cause mass coral bleaching and mortality. However, corals in the northern Red Sea and Gulf of Aqaba have shown no sign of bleaching, despite local seawater temperature rising faster than the global average. We show that the exceptional heat tolerance of the common symbiotic reef-building coral Stylophora pistillata from the Gulf of Aqaba is based on a rapid gene expression response and recovery pattern when exposed to heat stress up to 32 °C. Such temperatures are not anticipated to occur in the region within this century, giving real hope for the preservation of at least one major coral reef ecosystem for future generations.

          Abstract

          Corals from the northern Red Sea and Gulf of Aqaba exhibit extreme thermal tolerance. To examine the underlying gene expression dynamics, we exposed Stylophora pistillata from the Gulf of Aqaba to short-term (hours) and long-term (weeks) heat stress with peak seawater temperatures ranging from their maximum monthly mean of 27 °C (baseline) to 29.5 °C, 32 °C, and 34.5 °C. Corals were sampled at the end of the heat stress as well as after a recovery period at baseline temperature. Changes in coral host and symbiotic algal gene expression were determined via RNA-sequencing (RNA-Seq). Shifts in coral microbiome composition were detected by complementary DNA (cDNA)-based 16S ribosomal RNA (rRNA) gene sequencing. In all experiments up to 32 °C, RNA-Seq revealed fast and pervasive changes in gene expression, primarily in the coral host, followed by a return to baseline gene expression for the majority of coral (>94%) and algal (>71%) genes during recovery. At 34.5 °C, large differences in gene expression were observed with minimal recovery, high coral mortality, and a microbiome dominated by opportunistic bacteria (including Vibrio species), indicating that a lethal temperature threshold had been crossed. Our results show that the S. pistillata holobiont can mount a rapid and pervasive gene expression response contingent on the amplitude and duration of the thermal stress. We propose that the transcriptomic resilience and transcriptomic acclimation observed are key to the extraordinary thermal tolerance of this holobiont and, by inference, of other northern Red Sea coral holobionts, up to seawater temperatures of at least 32 °C, that is, 5 °C above their current maximum monthly mean.

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          Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2

          In comparative high-throughput sequencing assays, a fundamental task is the analysis of count data, such as read counts per gene in RNA-seq, for evidence of systematic changes across experimental conditions. Small replicate numbers, discreteness, large dynamic range and the presence of outliers require a suitable statistical approach. We present DESeq2, a method for differential analysis of count data, using shrinkage estimation for dispersions and fold changes to improve stability and interpretability of estimates. This enables a more quantitative analysis focused on the strength rather than the mere presence of differential expression. The DESeq2 package is available at http://www.bioconductor.org/packages/release/bioc/html/DESeq2.html. Electronic supplementary material The online version of this article (doi:10.1186/s13059-014-0550-8) contains supplementary material, which is available to authorized users.
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            Trimmomatic: a flexible trimmer for Illumina sequence data

            Motivation: Although many next-generation sequencing (NGS) read preprocessing tools already existed, we could not find any tool or combination of tools that met our requirements in terms of flexibility, correct handling of paired-end data and high performance. We have developed Trimmomatic as a more flexible and efficient preprocessing tool, which could correctly handle paired-end data. Results: The value of NGS read preprocessing is demonstrated for both reference-based and reference-free tasks. Trimmomatic is shown to produce output that is at least competitive with, and in many cases superior to, that produced by other tools, in all scenarios tested. Availability and implementation: Trimmomatic is licensed under GPL V3. It is cross-platform (Java 1.5+ required) and available at http://www.usadellab.org/cms/index.php?page=trimmomatic Contact: usadel@bio1.rwth-aachen.de Supplementary information: Supplementary data are available at Bioinformatics online.
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              The Sequence Alignment/Map format and SAMtools

              Summary: The Sequence Alignment/Map (SAM) format is a generic alignment format for storing read alignments against reference sequences, supporting short and long reads (up to 128 Mbp) produced by different sequencing platforms. It is flexible in style, compact in size, efficient in random access and is the format in which alignments from the 1000 Genomes Project are released. SAMtools implements various utilities for post-processing alignments in the SAM format, such as indexing, variant caller and alignment viewer, and thus provides universal tools for processing read alignments. Availability: http://samtools.sourceforge.net Contact: rd@sanger.ac.uk
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc Natl Acad Sci U S A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                11 May 2021
                03 May 2021
                03 May 2021
                : 118
                : 19
                : e2023298118
                Affiliations
                [1] aLaboratory for Biological Geochemistry, School of Architecture, Civil and Environmental Engineering, Ecole Polytechnique Fédérale de Lausanne (EPFL), 1015 Lausanne, Switzerland;
                [2] bDepartment of Biological Sciences, Old Dominion University , Norfolk, VA 23529;
                [3] cDepartment of Biology, University of Konstanz , 78457 Konstanz, Germany;
                [4] dThe Goodman Faculty of Life Sciences, Bar-Ilan University , 52900 Ramat-Gan, Israel;
                [5] eLaboratory for Coral Reef Ecology, Interuniversity Institute for Marine Sciences , 88103 Eilat, Israel;
                [6] fCenter for Advanced Surface Analysis, Institute of Earth Sciences, University of Lausanne , CH-1015 Lausanne, Switzerland
                Author notes
                1To whom correspondence may be addressed. Email: r.savary@ 123456epfl.ch .

                Edited by Nancy Knowlton, Smithsonian Institution, Washington, DC, and approved March 17, 2021 (received for review November 11, 2020)

                Author contributions: R.S., D.J.B., C.R.V., N.R.E., M.F., and A.M. designed research; R.S., D.J.B., A.C., N.R.E., and G.B.-P. performed research; R.S. and A.C. analyzed data; and R.S., D.J.B., C.R.V., and A.M. wrote the paper.

                Author information
                https://orcid.org/0000-0002-6338-6807
                https://orcid.org/0000-0003-1510-8375
                https://orcid.org/0000-0003-4555-3795
                https://orcid.org/0000-0002-4080-9010
                https://orcid.org/0000-0003-3318-5593
                https://orcid.org/0000-0003-0656-6649
                https://orcid.org/0000-0003-4911-4562
                https://orcid.org/0000-0002-4542-2819
                Article
                202023298
                10.1073/pnas.2023298118
                8126839
                33941698
                2529caaa-86fd-4509-878f-389d3f575547
                Copyright © 2021 the Author(s). Published by PNAS.

                This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

                History
                Page count
                Pages: 9
                Funding
                Funded by: AXA Research Fund (AXA) 501100001961
                Award ID: Ocean
                Award ID: marine biodiversity and conflict prevention
                Award Recipient : Romain Savary
                Funded by: United States - Israel Binational Science Foundation (BSF) 100006221
                Award ID: 2016403
                Award Recipient : Daniel J Barshis Award Recipient : Maoz Fine
                Funded by: United States - Israel Binational Science Foundation (BSF) 100006221
                Award ID: 2016403
                Award Recipient : Daniel J Barshis Award Recipient : Maoz Fine
                Funded by: Deutsche Forschungsgemeinschaft (DFG) 501100001659
                Award ID: 433042944
                Award Recipient : Christian R. Voolstra
                Funded by: National Science Foundation (NSF) 100000001
                Award ID: 1833201
                Award Recipient : Daniel J Barshis
                Funded by: Swiss National Science Foundation
                Award ID: 200021_179092
                Award Recipient : Anders Meibom
                Categories
                414
                Biological Sciences
                Ecology
                From the Cover

                coral bleaching,microbiome,heat stress,gene expression profiling,metaorganism

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