Comparative genomics explains the evolutionary success of reef-forming corals

Debashish Bhattacharya; Shobhit Agrawal; Manuel Aranda; Sebastian Baumgarten; Mahdi Belcaid; Jeana L Drake; Douglas Erwin; Sylvian Foret; Ruth D Gates; David F Gruber; Bishoy Kamel; Michael P Lesser; Oren Levy; Yi Jin Liew; Matthew MacManes; Tali Mass; Monica Medina; Shaadi Mehr; Eli Meyer; Dana C Price; Hollie M Putnam; Huan Qiu; Chuya Shinzato; Eiichi Shoguchi; Alexander J Stokes; Sylvie Tambutté; Dan Tchernov; Christian R. Voolstra; Nicole Wagner; Charles W Walker; Andreas PM Weber; Virginia Weis; Ehud Zelzion; Didier Zoccola; Paul G Falkowski

doi:10.7554/eLife.13288

Comparative genomics explains the evolutionary success of reef-forming corals

Debashish Bhattacharya, Shobhit Agrawal, Manuel Aranda, Sebastian Baumgarten, Mahdi Belcaid, Jeana L Drake, Douglas Erwin, Sylvian Foret, Ruth D Gates, David F Gruber, Bishoy Kamel, Michael P Lesser, Oren Levy, Yi Jin Liew, Matthew MacManes, Tali Mass, Monica Medina, Shaadi Mehr, Eli Meyer, Dana C PriceHollie M Putnam, Huan Qiu, Chuya Shinzato, Eiichi Shoguchi, Alexander J Stokes, Sylvie Tambutté, Dan Tchernov, Christian R. Voolstra, Nicole Wagner, Charles W Walker, Andreas PM Weber, Virginia Weis, Ehud Zelzion, Didier Zoccola, Paul G Falkowski

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152 Scopus citations

Abstract

Transcriptome and genome data from twenty stony coral species and a selection of reference bilaterians were studied to elucidate coral evolutionary history. We identified genes that encode the proteins responsible for the precipitation and aggregation of the aragonite skeleton on which the organisms live, and revealed a network of environmental sensors that coordinate responses of the host animals to temperature, light, and pH. Furthermore, we describe a variety of stress-related pathways, including apoptotic pathways that allow the host animals to detoxify reactive oxygen and nitrogen species that are generated by their intracellular photosynthetic symbionts, and determine the fate of corals under environmental stress. Some of these genes arose through horizontal gene transfer and comprise at least 0.2% of the animal gene inventory. Our analysis elucidates the evolutionary strategies that have allowed symbiotic corals to adapt and thrive for hundreds of millions of years.

Original language	English (US)
Journal	eLife
Volume	5
Issue number	MAY2016
DOIs	https://doi.org/10.7554/eLife.13288
State	Published - May 24 2016

Bibliographical note

KAUST Repository Item: Exported on 2020-10-01
Acknowledgements: This work was made possible by grants from the National Science Foundation, especially EF-1408097, to PGF, DB, RDG, HMP and TM, which sponsored the workshop. Additional funding was provided by the National Science Foundation through grants EF-1041143/RU 432635 and EF-1416785 awarded to PGF, DB, and TM, respectively. RDG, HMP, and AJS were supported by grants from the National Institutes of Health, NIMHD P20MD006084, the Hawaii Community Foundation, Leahi Fund 13ADVC-60228 and NSF OCE PRF 1323822 and National Science Foundation Experimental Program to Stimulate Competitive Research Hawaii: EPS-0903833. CRV and MA acknowledge funding by the King Abdullah University of Science and Technology (KAUST).

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https://repository.kaust.edu.sa/bitstream/10754/613035/1/e13288-download.pdf

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Bhattacharya, D., Agrawal, S., Aranda, M., Baumgarten, S., Belcaid, M., Drake, J. L., Erwin, D., Foret, S., Gates, R. D., Gruber, D. F., Kamel, B., Lesser, M. P., Levy, O., Liew, Y. J., MacManes, M., Mass, T., Medina, M., Mehr, S., Meyer, E., ... Falkowski, P. G. (2016). Comparative genomics explains the evolutionary success of reef-forming corals. eLife, 5(MAY2016). https://doi.org/10.7554/eLife.13288

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title = "Comparative genomics explains the evolutionary success of reef-forming corals",

abstract = "Transcriptome and genome data from twenty stony coral species and a selection of reference bilaterians were studied to elucidate coral evolutionary history. We identified genes that encode the proteins responsible for the precipitation and aggregation of the aragonite skeleton on which the organisms live, and revealed a network of environmental sensors that coordinate responses of the host animals to temperature, light, and pH. Furthermore, we describe a variety of stress-related pathways, including apoptotic pathways that allow the host animals to detoxify reactive oxygen and nitrogen species that are generated by their intracellular photosynthetic symbionts, and determine the fate of corals under environmental stress. Some of these genes arose through horizontal gene transfer and comprise at least 0.2% of the animal gene inventory. Our analysis elucidates the evolutionary strategies that have allowed symbiotic corals to adapt and thrive for hundreds of millions of years.",

author = "Debashish Bhattacharya and Shobhit Agrawal and Manuel Aranda and Sebastian Baumgarten and Mahdi Belcaid and Drake, {Jeana L} and Douglas Erwin and Sylvian Foret and Gates, {Ruth D} and Gruber, {David F} and Bishoy Kamel and Lesser, {Michael P} and Oren Levy and Liew, {Yi Jin} and Matthew MacManes and Tali Mass and Monica Medina and Shaadi Mehr and Eli Meyer and Price, {Dana C} and Putnam, {Hollie M} and Huan Qiu and Chuya Shinzato and Eiichi Shoguchi and Stokes, {Alexander J} and Sylvie Tambutt{\'e} and Dan Tchernov and Voolstra, {Christian R.} and Nicole Wagner and Walker, {Charles W} and Weber, {Andreas PM} and Virginia Weis and Ehud Zelzion and Didier Zoccola and Falkowski, {Paul G}",

note = "KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: This work was made possible by grants from the National Science Foundation, especially EF-1408097, to PGF, DB, RDG, HMP and TM, which sponsored the workshop. Additional funding was provided by the National Science Foundation through grants EF-1041143/RU 432635 and EF-1416785 awarded to PGF, DB, and TM, respectively. RDG, HMP, and AJS were supported by grants from the National Institutes of Health, NIMHD P20MD006084, the Hawaii Community Foundation, Leahi Fund 13ADVC-60228 and NSF OCE PRF 1323822 and National Science Foundation Experimental Program to Stimulate Competitive Research Hawaii: EPS-0903833. CRV and MA acknowledge funding by the King Abdullah University of Science and Technology (KAUST).",

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Bhattacharya, D, Agrawal, S, Aranda, M, Baumgarten, S, Belcaid, M, Drake, JL, Erwin, D, Foret, S, Gates, RD, Gruber, DF, Kamel, B, Lesser, MP, Levy, O, Liew, YJ, MacManes, M, Mass, T, Medina, M, Mehr, S, Meyer, E, Price, DC, Putnam, HM, Qiu, H, Shinzato, C, Shoguchi, E, Stokes, AJ, Tambutté, S, Tchernov, D, Voolstra, CR, Wagner, N, Walker, CW, Weber, APM, Weis, V, Zelzion, E, Zoccola, D & Falkowski, PG 2016, 'Comparative genomics explains the evolutionary success of reef-forming corals', eLife, vol. 5, no. MAY2016. https://doi.org/10.7554/eLife.13288

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T1 - Comparative genomics explains the evolutionary success of reef-forming corals

AU - Bhattacharya, Debashish

AU - Agrawal, Shobhit

AU - Aranda, Manuel

AU - Baumgarten, Sebastian

AU - Belcaid, Mahdi

AU - Drake, Jeana L

AU - Erwin, Douglas

AU - Foret, Sylvian

AU - Gates, Ruth D

AU - Gruber, David F

AU - Kamel, Bishoy

AU - Lesser, Michael P

AU - Levy, Oren

AU - Liew, Yi Jin

AU - MacManes, Matthew

AU - Mass, Tali

AU - Medina, Monica

AU - Mehr, Shaadi

AU - Meyer, Eli

AU - Price, Dana C

AU - Putnam, Hollie M

AU - Qiu, Huan

AU - Shinzato, Chuya

AU - Shoguchi, Eiichi

AU - Stokes, Alexander J

AU - Tambutté, Sylvie

AU - Tchernov, Dan

AU - Voolstra, Christian R.

AU - Wagner, Nicole

AU - Walker, Charles W

AU - Weber, Andreas PM

AU - Weis, Virginia

AU - Zelzion, Ehud

AU - Zoccola, Didier

AU - Falkowski, Paul G

N1 - KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: This work was made possible by grants from the National Science Foundation, especially EF-1408097, to PGF, DB, RDG, HMP and TM, which sponsored the workshop. Additional funding was provided by the National Science Foundation through grants EF-1041143/RU 432635 and EF-1416785 awarded to PGF, DB, and TM, respectively. RDG, HMP, and AJS were supported by grants from the National Institutes of Health, NIMHD P20MD006084, the Hawaii Community Foundation, Leahi Fund 13ADVC-60228 and NSF OCE PRF 1323822 and National Science Foundation Experimental Program to Stimulate Competitive Research Hawaii: EPS-0903833. CRV and MA acknowledge funding by the King Abdullah University of Science and Technology (KAUST).

PY - 2016/5/24

Y1 - 2016/5/24

N2 - Transcriptome and genome data from twenty stony coral species and a selection of reference bilaterians were studied to elucidate coral evolutionary history. We identified genes that encode the proteins responsible for the precipitation and aggregation of the aragonite skeleton on which the organisms live, and revealed a network of environmental sensors that coordinate responses of the host animals to temperature, light, and pH. Furthermore, we describe a variety of stress-related pathways, including apoptotic pathways that allow the host animals to detoxify reactive oxygen and nitrogen species that are generated by their intracellular photosynthetic symbionts, and determine the fate of corals under environmental stress. Some of these genes arose through horizontal gene transfer and comprise at least 0.2% of the animal gene inventory. Our analysis elucidates the evolutionary strategies that have allowed symbiotic corals to adapt and thrive for hundreds of millions of years.

AB - Transcriptome and genome data from twenty stony coral species and a selection of reference bilaterians were studied to elucidate coral evolutionary history. We identified genes that encode the proteins responsible for the precipitation and aggregation of the aragonite skeleton on which the organisms live, and revealed a network of environmental sensors that coordinate responses of the host animals to temperature, light, and pH. Furthermore, we describe a variety of stress-related pathways, including apoptotic pathways that allow the host animals to detoxify reactive oxygen and nitrogen species that are generated by their intracellular photosynthetic symbionts, and determine the fate of corals under environmental stress. Some of these genes arose through horizontal gene transfer and comprise at least 0.2% of the animal gene inventory. Our analysis elucidates the evolutionary strategies that have allowed symbiotic corals to adapt and thrive for hundreds of millions of years.

UR - http://hdl.handle.net/10754/613035

UR - http://elifesciences.org/lookup/doi/10.7554/eLife.13288

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DO - 10.7554/eLife.13288

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C2 - 27218454

SN - 2050-084X

VL - 5

JO - eLife

JF - eLife

IS - MAY2016

ER -

Comparative genomics explains the evolutionary success of reef-forming corals

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