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 inMolecular biology and evolution Vol. 38; no. 1; pp. 16 - 30
Main Authors Shinzato, Chuya, Khalturin, Konstantin, Inoue, Jun, Zayasu, Yuna, Kanda, Miyuki, Kawamitsu, Mayumi, Yoshioka, Yuki, Yamashita, Hiroshi, Suzuki, Go, Satoh, Noriyuki
Format Journal Article
LanguageEnglish
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.
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
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– 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
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  surname: Shinzato
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  organization: Atmosphere and Ocean Research Institute, The University of Tokyo, Chiba, Japan
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  fullname: Khalturin, Konstantin
  organization: Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University, Okinawa, Japan
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  fullname: Inoue, Jun
  organization: Atmosphere and Ocean Research Institute, The University of Tokyo, Chiba, Japan
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  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
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  givenname: Mayumi
  surname: Kawamitsu
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  organization: DNA Sequence Section (SQC), Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa, Japan
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  orcidid: 0000-0001-6348-4629
  surname: Yoshioka
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  organization: Atmosphere and Ocean Research Institute, The University of Tokyo, Chiba, Japan
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  givenname: Hiroshi
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  fullname: Yamashita, Hiroshi
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– 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
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/32877528$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
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.
Copyright_xml – notice: The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. 2020
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– notice: COPYRIGHT 2021 Oxford University Press
– notice: 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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DOI 10.1093/molbev/msaa216
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Issue 1
Keywords genome sequencing
environment
gene duplicatoin
scleractinian corals
Language English
License This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
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The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
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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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pubmed
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SourceType Open Access Repository
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StartPage 16
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
URI https://www.ncbi.nlm.nih.gov/pubmed/32877528
https://www.proquest.com/docview/3171299434
https://www.proquest.com/docview/2439975474
https://pubmed.ncbi.nlm.nih.gov/PMC7783167
Volume 38
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