Millennia-old coral holobiont DNA provides insight into future adaptive trajectories

Carly B. Scott; Anny Cárdenas; Matthew Mah; Vagheesh M. Narasimhan; Nadin Rohland; Lauren T. Toth; Christian R. Voolstra; David Reich; Mikhail V. Matz

doi:10.1111/mec.16642

Millennia-old coral holobiont DNA provides insight into future adaptive trajectories

Carly B. Scott, Anny Cárdenas, Matthew Mah, Vagheesh M. Narasimhan, Nadin Rohland, Lauren T. Toth, Christian R. Voolstra, David Reich, Mikhail V. Matz

Research output: Contribution to journal › Article › peer-review

8 Scopus citations

Abstract

Ancient DNA (aDNA) has been applied to evolutionary questions across a wide variety of taxa. Here, for the first time, we leverage aDNA from millennia-old fossil coral fragments to gain new insights into a rapidly declining western Atlantic reef ecosystem. We sampled four Acropora palmata fragments (dated 4215 BCE - 1099 CE) obtained from two Florida Keys reef cores. From these samples, we established that it is possible both to sequence ancient DNA from reef cores and place the data in the context of modern-day genetic variation. We recovered varying amounts of nuclear DNA exhibiting the characteristic signatures of aDNA from the A. palmata fragments. To describe the holobiont sensu lato, which plays a crucial role in reef health, we utilized metagenome-assembled genomes as a reference to identify a large additional proportion of ancient microbial DNA from the samples. The samples shared many common microbes with modern-day coral holobionts from the same region, suggesting remarkable holobiont stability over time. Despite efforts, we were unable to recover ancient Symbiodiniaceae reads from the samples. Comparing the ancient A. palmata data to whole-genome sequencing data from living acroporids, we found that while slightly distinct, ancient samples were most closely related to individuals of their own species. Together, these results provide a proof-of-principle showing that it is possible to carry out direct analysis of coral holobiont change over time, which lays a foundation for studying the impacts of environmental stress and evolutionary constraints.

Original language	English (US)
Journal	Molecular Ecology
DOIs	https://doi.org/10.1111/mec.16642
State	Published - Aug 9 2022
Externally published	Yes

Bibliographical note

KAUST Repository Item: Exported on 2022-09-14
Acknowledged KAUST grant number(s): URF/1/3400-01-01
Acknowledgements: The project was supported by the National Science Foundation grant O C E-1737312 to M.V.M, and the KAUST competitive research grant URF/1/3400-01-01 to AC and CRV. The bioinformatics analysis was accomplished using computational resources provided by the Texas Advanced Computing Center. The Durisdinium sp. genome used was provided pre-publication by Katherine Dougan, Anthony Bellantuono, Camila Granados-Cifuentes, and Mauricio Rodriguez-Lanetty. The reef core collections are supported by the U.S. Geological Survey Coastal/Marine Hazards and Resources Program. We thank Fatma Zalzala and Kristen Stewardson for sample preparation, DNA extraction and library preparation and Matthew Mah for initial bioinformatics processing. D.R. is an Investigator of the Howard Hughes Medical Institute. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.
This publication acknowledges KAUST support, but has no KAUST affiliated authors.

ASJC Scopus subject areas

Ecology, Evolution, Behavior and Systematics
Genetics

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10.1111/mec.16642

Cite this

@article{d4c409234c4047979af6eff722c71877,

title = "Millennia-old coral holobiont DNA provides insight into future adaptive trajectories",

abstract = "Ancient DNA (aDNA) has been applied to evolutionary questions across a wide variety of taxa. Here, for the first time, we leverage aDNA from millennia-old fossil coral fragments to gain new insights into a rapidly declining western Atlantic reef ecosystem. We sampled four Acropora palmata fragments (dated 4215 BCE - 1099 CE) obtained from two Florida Keys reef cores. From these samples, we established that it is possible both to sequence ancient DNA from reef cores and place the data in the context of modern-day genetic variation. We recovered varying amounts of nuclear DNA exhibiting the characteristic signatures of aDNA from the A. palmata fragments. To describe the holobiont sensu lato, which plays a crucial role in reef health, we utilized metagenome-assembled genomes as a reference to identify a large additional proportion of ancient microbial DNA from the samples. The samples shared many common microbes with modern-day coral holobionts from the same region, suggesting remarkable holobiont stability over time. Despite efforts, we were unable to recover ancient Symbiodiniaceae reads from the samples. Comparing the ancient A. palmata data to whole-genome sequencing data from living acroporids, we found that while slightly distinct, ancient samples were most closely related to individuals of their own species. Together, these results provide a proof-of-principle showing that it is possible to carry out direct analysis of coral holobiont change over time, which lays a foundation for studying the impacts of environmental stress and evolutionary constraints.",

author = "Scott, {Carly B.} and Anny C{\'a}rdenas and Matthew Mah and Narasimhan, {Vagheesh M.} and Nadin Rohland and Toth, {Lauren T.} and Voolstra, {Christian R.} and David Reich and Matz, {Mikhail V.}",

note = "KAUST Repository Item: Exported on 2022-09-14 Acknowledged KAUST grant number(s): URF/1/3400-01-01 Acknowledgements: The project was supported by the National Science Foundation grant O C E-1737312 to M.V.M, and the KAUST competitive research grant URF/1/3400-01-01 to AC and CRV. The bioinformatics analysis was accomplished using computational resources provided by the Texas Advanced Computing Center. The Durisdinium sp. genome used was provided pre-publication by Katherine Dougan, Anthony Bellantuono, Camila Granados-Cifuentes, and Mauricio Rodriguez-Lanetty. The reef core collections are supported by the U.S. Geological Survey Coastal/Marine Hazards and Resources Program. We thank Fatma Zalzala and Kristen Stewardson for sample preparation, DNA extraction and library preparation and Matthew Mah for initial bioinformatics processing. D.R. is an Investigator of the Howard Hughes Medical Institute. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government. This publication acknowledges KAUST support, but has no KAUST affiliated authors.",

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month = aug,

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doi = "10.1111/mec.16642",

language = "English (US)",

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AU - Scott, Carly B.

AU - Cárdenas, Anny

AU - Mah, Matthew

AU - Narasimhan, Vagheesh M.

AU - Rohland, Nadin

AU - Toth, Lauren T.

AU - Voolstra, Christian R.

AU - Reich, David

AU - Matz, Mikhail V.

N1 - KAUST Repository Item: Exported on 2022-09-14 Acknowledged KAUST grant number(s): URF/1/3400-01-01 Acknowledgements: The project was supported by the National Science Foundation grant O C E-1737312 to M.V.M, and the KAUST competitive research grant URF/1/3400-01-01 to AC and CRV. The bioinformatics analysis was accomplished using computational resources provided by the Texas Advanced Computing Center. The Durisdinium sp. genome used was provided pre-publication by Katherine Dougan, Anthony Bellantuono, Camila Granados-Cifuentes, and Mauricio Rodriguez-Lanetty. The reef core collections are supported by the U.S. Geological Survey Coastal/Marine Hazards and Resources Program. We thank Fatma Zalzala and Kristen Stewardson for sample preparation, DNA extraction and library preparation and Matthew Mah for initial bioinformatics processing. D.R. is an Investigator of the Howard Hughes Medical Institute. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government. This publication acknowledges KAUST support, but has no KAUST affiliated authors.

PY - 2022/8/9

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N2 - Ancient DNA (aDNA) has been applied to evolutionary questions across a wide variety of taxa. Here, for the first time, we leverage aDNA from millennia-old fossil coral fragments to gain new insights into a rapidly declining western Atlantic reef ecosystem. We sampled four Acropora palmata fragments (dated 4215 BCE - 1099 CE) obtained from two Florida Keys reef cores. From these samples, we established that it is possible both to sequence ancient DNA from reef cores and place the data in the context of modern-day genetic variation. We recovered varying amounts of nuclear DNA exhibiting the characteristic signatures of aDNA from the A. palmata fragments. To describe the holobiont sensu lato, which plays a crucial role in reef health, we utilized metagenome-assembled genomes as a reference to identify a large additional proportion of ancient microbial DNA from the samples. The samples shared many common microbes with modern-day coral holobionts from the same region, suggesting remarkable holobiont stability over time. Despite efforts, we were unable to recover ancient Symbiodiniaceae reads from the samples. Comparing the ancient A. palmata data to whole-genome sequencing data from living acroporids, we found that while slightly distinct, ancient samples were most closely related to individuals of their own species. Together, these results provide a proof-of-principle showing that it is possible to carry out direct analysis of coral holobiont change over time, which lays a foundation for studying the impacts of environmental stress and evolutionary constraints.

AB - Ancient DNA (aDNA) has been applied to evolutionary questions across a wide variety of taxa. Here, for the first time, we leverage aDNA from millennia-old fossil coral fragments to gain new insights into a rapidly declining western Atlantic reef ecosystem. We sampled four Acropora palmata fragments (dated 4215 BCE - 1099 CE) obtained from two Florida Keys reef cores. From these samples, we established that it is possible both to sequence ancient DNA from reef cores and place the data in the context of modern-day genetic variation. We recovered varying amounts of nuclear DNA exhibiting the characteristic signatures of aDNA from the A. palmata fragments. To describe the holobiont sensu lato, which plays a crucial role in reef health, we utilized metagenome-assembled genomes as a reference to identify a large additional proportion of ancient microbial DNA from the samples. The samples shared many common microbes with modern-day coral holobionts from the same region, suggesting remarkable holobiont stability over time. Despite efforts, we were unable to recover ancient Symbiodiniaceae reads from the samples. Comparing the ancient A. palmata data to whole-genome sequencing data from living acroporids, we found that while slightly distinct, ancient samples were most closely related to individuals of their own species. Together, these results provide a proof-of-principle showing that it is possible to carry out direct analysis of coral holobiont change over time, which lays a foundation for studying the impacts of environmental stress and evolutionary constraints.

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UR - https://onlinelibrary.wiley.com/doi/10.1111/mec.16642

U2 - 10.1111/mec.16642

DO - 10.1111/mec.16642

M3 - Article

C2 - 35943423

SN - 0962-1083

JO - Molecular Ecology

JF - Molecular Ecology

ER -

Millennia-old coral holobiont DNA provides insight into future adaptive trajectories

Abstract

Bibliographical note

ASJC Scopus subject areas

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