Genomic Blueprint of Glycine Betaine Metabolism in Coral Metaorganisms and Their Contribution to Reef Nitrogen Budgets

David Ngugi; Maren Ziegler; Carlos M. Duarte; Christian R. Voolstra

doi:10.1016/j.isci.2020.101120

Genomic Blueprint of Glycine Betaine Metabolism in Coral Metaorganisms and Their Contribution to Reef Nitrogen Budgets

David Ngugi, Maren Ziegler, Carlos M. Duarte, Christian R. Voolstra

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

27 Scopus citations

Abstract

The osmolyte glycine betaine (GB) ranks among the few widespread biomolecules in all three domains of life. In corals, tissue concentrations of GB are substantially higher than in the ambient seawater. However, the synthetic routes remain unresolved, questioning whether intracellular GB originates from de novo synthesis or heterotrophic input. Here we show that the genomic blueprint of coral metaorganisms encode the biosynthetic and degradation machinery for GB. Member organisms also adopted the prokaryotic high-affinity carrier-mediated uptake of exogenous GB, rendering coral reefs potential sinks of marine dissolved GB. The machinery metabolizing GB is highly expressed in the coral model Aiptasia and its microalgal symbionts, signifying GB's role in the cnidarian-dinoflagellate symbiosis. We estimate that corals store between 106–109 grams of GB globally, representing about 16% of their nitrogen biomass. Our findings provide a framework for further mechanistic studies addressing GB's role in coral biology and reef ecosystem nitrogen cycling.

Original language	English (US)
Pages (from-to)	101120
Journal	iScience
Volume	23
Issue number	5
DOIs	https://doi.org/10.1016/j.isci.2020.101120
State	Published - Apr 30 2020

Bibliographical note

KAUST Repository Item: Exported on 2020-10-01
Acknowledgements: We thank Dorothee Huchon (Tel Aviv University) for kindly availing the myxosporian genomes and transcriptomes and Eric Pelletier (Genoscope) for assistance with the eukaryotic gene catalog data. Additionally, we are grateful to Craig Michell for assistance with metagenomic library construction and the technical personnel at KAUST's Bioscience Core Lab for sequencing. Furthermore, we thank the Coastal & Marine Resources core laboratory team for their help in undertaking the sampling and members of the Thurber lab (Rebecca Vega Thurber, Jerome Payet, and Ryan McMinds) at Oregon State University for sampling assistance. The metagenomic sequencing project was funded through the KAUST SEED funding scheme to C.R. Voolstra. D.K.N. conceived and designed the study and performed the bioinformatic analyses. M.Z. and C.R.V. determined and provided the metagenomic data. C.M.D. provided the bioinformatic resources for the analyses. D.K.N. wrote the manuscript with contributions from all authors. The authors declare no competing interests.

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This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1016/j.isci.2020.101120

https://repository.kaust.edu.sa/bitstream/10754/662927/1/Genomic%20Blueprints.pdf

Cite this

@article{99c110bd2b044198b4800e67ddc7ede6,

title = "Genomic Blueprint of Glycine Betaine Metabolism in Coral Metaorganisms and Their Contribution to Reef Nitrogen Budgets",

abstract = "The osmolyte glycine betaine (GB) ranks among the few widespread biomolecules in all three domains of life. In corals, tissue concentrations of GB are substantially higher than in the ambient seawater. However, the synthetic routes remain unresolved, questioning whether intracellular GB originates from de novo synthesis or heterotrophic input. Here we show that the genomic blueprint of coral metaorganisms encode the biosynthetic and degradation machinery for GB. Member organisms also adopted the prokaryotic high-affinity carrier-mediated uptake of exogenous GB, rendering coral reefs potential sinks of marine dissolved GB. The machinery metabolizing GB is highly expressed in the coral model Aiptasia and its microalgal symbionts, signifying GB's role in the cnidarian-dinoflagellate symbiosis. We estimate that corals store between 106–109 grams of GB globally, representing about 16% of their nitrogen biomass. Our findings provide a framework for further mechanistic studies addressing GB's role in coral biology and reef ecosystem nitrogen cycling.",

author = "David Ngugi and Maren Ziegler and Duarte, {Carlos M.} and Voolstra, {Christian R.}",

note = "KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: We thank Dorothee Huchon (Tel Aviv University) for kindly availing the myxosporian genomes and transcriptomes and Eric Pelletier (Genoscope) for assistance with the eukaryotic gene catalog data. Additionally, we are grateful to Craig Michell for assistance with metagenomic library construction and the technical personnel at KAUST's Bioscience Core Lab for sequencing. Furthermore, we thank the Coastal & Marine Resources core laboratory team for their help in undertaking the sampling and members of the Thurber lab (Rebecca Vega Thurber, Jerome Payet, and Ryan McMinds) at Oregon State University for sampling assistance. The metagenomic sequencing project was funded through the KAUST SEED funding scheme to C.R. Voolstra. D.K.N. conceived and designed the study and performed the bioinformatic analyses. M.Z. and C.R.V. determined and provided the metagenomic data. C.M.D. provided the bioinformatic resources for the analyses. D.K.N. wrote the manuscript with contributions from all authors. The authors declare no competing interests.",

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N1 - KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: We thank Dorothee Huchon (Tel Aviv University) for kindly availing the myxosporian genomes and transcriptomes and Eric Pelletier (Genoscope) for assistance with the eukaryotic gene catalog data. Additionally, we are grateful to Craig Michell for assistance with metagenomic library construction and the technical personnel at KAUST's Bioscience Core Lab for sequencing. Furthermore, we thank the Coastal & Marine Resources core laboratory team for their help in undertaking the sampling and members of the Thurber lab (Rebecca Vega Thurber, Jerome Payet, and Ryan McMinds) at Oregon State University for sampling assistance. The metagenomic sequencing project was funded through the KAUST SEED funding scheme to C.R. Voolstra. D.K.N. conceived and designed the study and performed the bioinformatic analyses. M.Z. and C.R.V. determined and provided the metagenomic data. C.M.D. provided the bioinformatic resources for the analyses. D.K.N. wrote the manuscript with contributions from all authors. The authors declare no competing interests.

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N2 - The osmolyte glycine betaine (GB) ranks among the few widespread biomolecules in all three domains of life. In corals, tissue concentrations of GB are substantially higher than in the ambient seawater. However, the synthetic routes remain unresolved, questioning whether intracellular GB originates from de novo synthesis or heterotrophic input. Here we show that the genomic blueprint of coral metaorganisms encode the biosynthetic and degradation machinery for GB. Member organisms also adopted the prokaryotic high-affinity carrier-mediated uptake of exogenous GB, rendering coral reefs potential sinks of marine dissolved GB. The machinery metabolizing GB is highly expressed in the coral model Aiptasia and its microalgal symbionts, signifying GB's role in the cnidarian-dinoflagellate symbiosis. We estimate that corals store between 106–109 grams of GB globally, representing about 16% of their nitrogen biomass. Our findings provide a framework for further mechanistic studies addressing GB's role in coral biology and reef ecosystem nitrogen cycling.

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Genomic Blueprint of Glycine Betaine Metabolism in Coral Metaorganisms and Their Contribution to Reef Nitrogen Budgets

Abstract

Bibliographical note

UN SDGs

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Red Sea coral metagenomes

Cite this

Genomic Blueprint of Glycine Betaine Metabolism in Coral Metaorganisms and Their Contribution to Reef Nitrogen Budgets

Abstract

Bibliographical note

UN SDGs

Access to Document

Other files and links

Fingerprint

Datasets

Red Sea coral metagenomes

Cite this