Eighteen Coral Genomes Reveal the Evolutionary Origin of Acropora Strategies to Accommodate Environmental Changes
The genus Acropora comprises the most diverse and abundant scleractinian corals (Anthozoa, Cnidaria) in coral reefs, the most diverse marine ecosystems on Earth. However, the genetic basis for the success and wide distribution of Acropora are unknown. Here, we sequenced complete genomes of 15 Acropo...
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Published in | Molecular biology and evolution Vol. 38; no. 1; pp. 16 - 30 |
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Main Authors | , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
Oxford University Press
01.01.2021
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Abstract | The genus Acropora comprises the most diverse and abundant scleractinian corals (Anthozoa, Cnidaria) in coral reefs, the most diverse marine ecosystems on Earth. However, the genetic basis for the success and wide distribution of Acropora are unknown. Here, we sequenced complete genomes of 15 Acropora species and 3 other acroporid taxa belonging to the genera Montipora and Astreopora to examine genomic novelties that explain their evolutionary success. We successfully obtained reasonable draft genomes of all 18 species. Molecular dating indicates that the Acropora ancestor survived warm periods without sea ice from the mid or late Cretaceous to the Early Eocene and that diversification of Acropora may have been enhanced by subsequent cooling periods. In general, the scleractinian gene repertoire is highly conserved; however, coral- or cnidarian-specific possible stress response genes are tandemly duplicated in Acropora. Enzymes that cleave dimethlysulfonioproprionate into dimethyl sulfide, which promotes cloud formation and combats greenhouse gasses, are the most duplicated genes in the Acropora ancestor. These may have been acquired by horizontal gene transfer from algal symbionts belonging to the family Symbiodiniaceae, or from coccolithophores, suggesting that although functions of this enzyme in Acropora are unclear, Acropora may have survived warmer marine environments in the past by enhancing cloud formation. In addition, possible antimicrobial peptides and symbiosis-related genes are under positive selection in Acropora, perhaps enabling adaptation to diverse environments. Our results suggest unique Acropora adaptations to ancient, warm marine environments and provide insights into its capacity to adjust to rising seawater temperatures. |
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AbstractList | The genus Acropora comprises the most diverse and abundant scleractinian corals (Anthozoa, Cnidaria) in coral reefs, the most diverse marine ecosystems on Earth. However, the genetic basis for the success and wide distribution of Acropora are unknown. Here, we sequenced complete genomes of 15 Acropora species and 3 other acroporid taxa belonging to the genera Montipora and Astreopora to examine genomic novelties that explain their evolutionary success. We successfully obtained reasonable draft genomes of all 18 species. Molecular dating indicates that the Acropora ancestor survived warm periods without sea ice from the mid or late Cretaceous to the Early Eocene and that diversification of Acropora may have been enhanced by subsequent cooling periods. In general, the scleractinian gene repertoire is highly conserved; however, coral- or cnidarian-specific possible stress response genes are tandemly duplicated in Acropora. Enzymes that cleave dimethlysulfonioproprionate into dimethyl sulfide, which promotes cloud formation and combats greenhouse gasses, are the most duplicated genes in the Acropora ancestor. These may have been acquired by horizontal gene transfer from algal symbionts belonging to the family Symbiodiniaceae, or from coccolithophores, suggesting that although functions of this enzyme in Acropora are unclear, Acropora may have survived warmer marine environments in the past by enhancing cloud formation. In addition, possible antimicrobial peptides and symbiosis-related genes are under positive selection in Acropora, perhaps enabling adaptation to diverse environments. Our results suggest unique Acropora adaptations to ancient, warm marine environments and provide insights into its capacity to adjust to rising seawater temperatures.The genus Acropora comprises the most diverse and abundant scleractinian corals (Anthozoa, Cnidaria) in coral reefs, the most diverse marine ecosystems on Earth. However, the genetic basis for the success and wide distribution of Acropora are unknown. Here, we sequenced complete genomes of 15 Acropora species and 3 other acroporid taxa belonging to the genera Montipora and Astreopora to examine genomic novelties that explain their evolutionary success. We successfully obtained reasonable draft genomes of all 18 species. Molecular dating indicates that the Acropora ancestor survived warm periods without sea ice from the mid or late Cretaceous to the Early Eocene and that diversification of Acropora may have been enhanced by subsequent cooling periods. In general, the scleractinian gene repertoire is highly conserved; however, coral- or cnidarian-specific possible stress response genes are tandemly duplicated in Acropora. Enzymes that cleave dimethlysulfonioproprionate into dimethyl sulfide, which promotes cloud formation and combats greenhouse gasses, are the most duplicated genes in the Acropora ancestor. These may have been acquired by horizontal gene transfer from algal symbionts belonging to the family Symbiodiniaceae, or from coccolithophores, suggesting that although functions of this enzyme in Acropora are unclear, Acropora may have survived warmer marine environments in the past by enhancing cloud formation. In addition, possible antimicrobial peptides and symbiosis-related genes are under positive selection in Acropora, perhaps enabling adaptation to diverse environments. Our results suggest unique Acropora adaptations to ancient, warm marine environments and provide insights into its capacity to adjust to rising seawater temperatures. The genus Acropora comprises the most diverse and abundant scleractinian corals (Anthozoa, Cnidaria) in coral reefs, the most diverse marine ecosystems on Earth. However, the genetic basis for the success and wide distribution of Acropora are unknown. Here, we sequenced complete genomes of 15 Acropora species and 3 other acroporid taxa belonging to the genera Montipora and Astreopora to examine genomic novelties that explain their evolutionary success. We successfully obtained reasonable draft genomes of all 18 species. Molecular dating indicates that the Acropora ancestor survived warm periods without sea ice from the mid or late Cretaceous to the Early Eocene and that diversification of Acropora may have been enhanced by subsequent cooling periods. In general, the scleractinian gene repertoire is highly conserved; however, coral- or cnidarian-specific possible stress response genes are tandemly duplicated in Acropora. Enzymes that cleave dimethlysulfonioproprionate into dimethyl sulfide, which promotes cloud formation and combats greenhouse gasses, are the most duplicated genes in the Acropora ancestor. These may have been acquired by horizontal gene transfer from algal symbionts belonging to the family Symbiodiniaceae, or from coccolithophores, suggesting that although functions of this enzyme in Acropora are unclear, Acropora may have survived warmer marine environments in the past by enhancing cloud formation. In addition, possible antimicrobial peptides and symbiosis-related genes are under positive selection in Acropora, perhaps enabling adaptation to diverse environments. Our results suggest unique Acropora adaptations to ancient, warm marine environments and provide insights into its capacity to adjust to rising seawater temperatures. The genus Acropora comprises the most diverse and abundant scleractinian corals (Anthozoa, Cnidaria) in coral reefs, the most diverse marine ecosystems on Earth. However, the genetic basis for the success and wide distribution of Acropora are unknown. Here, we sequenced complete genomes of 15 Acropora species and 3 other acroporid taxa belonging to the genera Montipora and Astreopora to examine genomic novelties that explain their evolutionary success. We successfully obtained reasonable draft genomes of all 18 species. Molecular dating indicates that the Acropora ancestor survived warm periods without sea ice from the mid or late Cretaceous to the Early Eocene and that diversification of Acropora may have been enhanced by subsequent cooling periods. In general, the scleractinian gene repertoire is highly conserved; however, coral- or cnidarian-specific possible stress response genes are tandemly duplicated in Acropora . Enzymes that cleave dimethlysulfonioproprionate into dimethyl sulfide, which promotes cloud formation and combats greenhouse gasses, are the most duplicated genes in the Acropora ancestor. These may have been acquired by horizontal gene transfer from algal symbionts belonging to the family Symbiodiniaceae, or from coccolithophores, suggesting that although functions of this enzyme in Acropora are unclear, Acropora may have survived warmer marine environments in the past by enhancing cloud formation. In addition, possible antimicrobial peptides and symbiosis-related genes are under positive selection in Acropora , perhaps enabling adaptation to diverse environments. Our results suggest unique Acropora adaptations to ancient, warm marine environments and provide insights into its capacity to adjust to rising seawater temperatures. The genus Acropora comprises the most diverse and abundant scleractinian corals (Anthozoa, Cnidaria) in coral reefs, the most diverse marine ecosystems on Earth. However, the genetic basis for the success and wide distribution of Acropora are unknown. Here, we sequenced complete genomes of 15 Acropora species and 3 other acroporid taxa belonging to the genera Montipora and Astreopora to examine genomic novelties that explain their evolutionary success. We successfully obtained reasonable draft genomes of all 18 species. Molecular dating indicates that the Acropora ancestor survived warm periods without sea ice from the mid or late Cretaceous to the Early Eocene and that diversification of Acropora may have been enhanced by subsequent cooling periods. In general, the scleractinian gene repertoire is highly conserved; however, coral- or cnidarian-specific possible stress response genes are tandemly duplicated in Acropora. Enzymes that cleave dimethlysulfonioproprionate into dimethyl sulfide, which promotes cloud formation and combats greenhouse gasses, are the most duplicated genes in the Acropora ancestor. These may have been acquired by horizontal gene transfer from algal symbionts belonging to the family Symbiodiniaceae, or from coccolithophores, suggesting that although functions of this enzyme in Acropora are unclear, Acropora may have survived warmer marine environments in the past by enhancing cloud formation. In addition, possible antimicrobial peptides and symbiosis- related genes are under positive selection in Acropora, perhaps enabling adaptation to diverse environments. Our results suggest unique Acropora adaptations to ancient, warm marine environments and provide insights into its capacity to adjust to rising seawater temperatures. Key words: genome sequencing, gene duplicatoin, scleractinian corals, environment. |
Audience | Academic |
Author | Khalturin, Konstantin Satoh, Noriyuki Kawamitsu, Mayumi Suzuki, Go Zayasu, Yuna Kanda, Miyuki Shinzato, Chuya Inoue, Jun Yoshioka, Yuki Yamashita, Hiroshi |
AuthorAffiliation | 5 Research Center for Subtropical Fisheries, Seikai National Fisheries Research Institute, Japan Fisheries Research and Education Agency , Okinawa, Japan 2 Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University , Okinawa, Japan 3 DNA Sequence Section (SQC), Okinawa Institute of Science and Technology Graduate University , Onna, Okinawa, Japan 1 Atmosphere and Ocean Research Institute, The University of Tokyo , Chiba, Japan 4 Graduate School of Frontier Sciences, The University of Tokyo , Kashiwa, Chiba, Japan |
AuthorAffiliation_xml | – name: 2 Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University , Okinawa, Japan – name: 1 Atmosphere and Ocean Research Institute, The University of Tokyo , Chiba, Japan – name: 3 DNA Sequence Section (SQC), Okinawa Institute of Science and Technology Graduate University , Onna, Okinawa, Japan – name: 5 Research Center for Subtropical Fisheries, Seikai National Fisheries Research Institute, Japan Fisheries Research and Education Agency , Okinawa, Japan – name: 4 Graduate School of Frontier Sciences, The University of Tokyo , Kashiwa, Chiba, Japan |
Author_xml | – sequence: 1 givenname: Chuya orcidid: 0000-0003-4954-6373 surname: Shinzato fullname: Shinzato, Chuya email: c.shinzato@aori.u-tokyo.ac.jp organization: Atmosphere and Ocean Research Institute, The University of Tokyo, Chiba, Japan – sequence: 2 givenname: Konstantin surname: Khalturin fullname: Khalturin, Konstantin organization: Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University, Okinawa, Japan – sequence: 3 givenname: Jun surname: Inoue fullname: Inoue, Jun organization: Atmosphere and Ocean Research Institute, The University of Tokyo, Chiba, Japan – sequence: 4 givenname: Yuna surname: Zayasu fullname: Zayasu, Yuna organization: Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University, Okinawa, Japan – sequence: 5 givenname: Miyuki surname: Kanda fullname: Kanda, Miyuki organization: DNA Sequence Section (SQC), Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa, Japan – sequence: 6 givenname: Mayumi surname: Kawamitsu fullname: Kawamitsu, Mayumi organization: DNA Sequence Section (SQC), Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa, Japan – sequence: 7 givenname: Yuki orcidid: 0000-0001-6348-4629 surname: Yoshioka fullname: Yoshioka, Yuki organization: Atmosphere and Ocean Research Institute, The University of Tokyo, Chiba, Japan – sequence: 8 givenname: Hiroshi surname: Yamashita fullname: Yamashita, Hiroshi organization: Research Center for Subtropical Fisheries, Seikai National Fisheries Research Institute, Japan Fisheries Research and Education Agency, Okinawa, Japan – sequence: 9 givenname: Go surname: Suzuki fullname: Suzuki, Go organization: Research Center for Subtropical Fisheries, Seikai National Fisheries Research Institute, Japan Fisheries Research and Education Agency, Okinawa, Japan – sequence: 10 givenname: Noriyuki surname: Satoh fullname: Satoh, Noriyuki organization: Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University, Okinawa, Japan |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32877528$$D View this record in MEDLINE/PubMed |
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Copyright | The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. 2020 The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. COPYRIGHT 2021 Oxford University Press The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This work is published under http://creativecommons.org/licenses/by-nc/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. |
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Keywords | genome sequencing environment gene duplicatoin scleractinian corals |
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Snippet | The genus Acropora comprises the most diverse and abundant scleractinian corals (Anthozoa, Cnidaria) in coral reefs, the most diverse marine ecosystems on... The genus Acropora comprises the most diverse and abundant scleractinian corals (Anthozoa, Cnidaria) in coral reefs, the most diverse marine ecosystems on... |
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SubjectTerms | Acropora Adaptation, Biological Air pollution Algae Animals Anthozoa - genetics Antimicrobial peptides Biological Evolution Climate Change Coccoliths Coral reefs Coral reefs and islands Corals Cretaceous Dimethyl sulfide Discoveries Environmental changes Enzymes Eocene Evolution Fossils Gene duplication Gene transfer Genes Genetic aspects Genome Genomes Genomics Greenhouse gases Horizontal transfer Marine ecosystems Marine environment Peptides Positive selection Sea ice Sea-water Seawater Symbionts Symbiosis Water temperature Whole genome sequencing |
Title | Eighteen Coral Genomes Reveal the Evolutionary Origin of Acropora Strategies to Accommodate Environmental Changes |
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