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

Overview

Journal iScience

Publisher Cell Press

Date 2020 May 22

PMID 32438323

Citations 15

Authors

David K Ngugi

Maren Ziegler

Carlos M Duarte

Christian R Voolstra

Affiliations

Soon will be listed here.

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 10-10 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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References

Kageyama H, Tanaka Y, Takabe T . Biosynthetic pathways of glycinebetaine in Thalassiosira pseudonana; functional characterization of enzyme catalyzing three-step methylation of glycine. Plant Physiol Biochem. 2018; 127:248-255. DOI: 10.1016/j.plaphy.2018.03.032. View

Oren A . Bioenergetic aspects of halophilism. Microbiol Mol Biol Rev. 1999; 63(2):334-48. PMC: 98969. DOI: 10.1128/MMBR.63.2.334-348.1999. View

Yancey P, Heppenstall M, Ly S, Andrell R, Gates R, Carter V . Betaines and dimethylsulfoniopropionate as major osmolytes in cnidaria with endosymbiotic dinoflagellates. Physiol Biochem Zool. 2009; 83(1):167-73. DOI: 10.1086/644625. View

Peter H, Burkovski A, Kramer R . Isolation, characterization, and expression of the Corynebacterium glutamicum betP gene, encoding the transport system for the compatible solute glycine betaine. J Bacteriol. 1996; 178(17):5229-34. PMC: 178321. DOI: 10.1128/jb.178.17.5229-5234.1996. View

Kirch H, Bartels D, Wei Y, Schnable P, Wood A . The ALDH gene superfamily of Arabidopsis. Trends Plant Sci. 2004; 9(8):371-7. DOI: 10.1016/j.tplants.2004.06.004. View

Holm P, Hustad S, Ueland P, Vollset S, Grotmol T, Schneede J . Modulation of the homocysteine-betaine relationship by methylenetetrahydrofolate reductase 677 C->t genotypes and B-vitamin status in a large-scale epidemiological study. J Clin Endocrinol Metab. 2007; 92(4):1535-41. DOI: 10.1210/jc.2006-1471. View

Sanudo-Wilhelmy S, Gomez-Consarnau L, Suffridge C, Webb E . The role of B vitamins in marine biogeochemistry. Ann Rev Mar Sci. 2013; 6:339-67. DOI: 10.1146/annurev-marine-120710-100912. View

Hagedorn M, Carter V, Ly S, Andrell R, Yancey P, Leong J . Analysis of internal osmolality in developing coral larvae, Fungia scutaria. Physiol Biochem Zool. 2009; 83(1):157-66. DOI: 10.1086/648484. View

Courtenay E, Capp M, Anderson C, Record Jr M . Vapor pressure osmometry studies of osmolyte-protein interactions: implications for the action of osmoprotectants in vivo and for the interpretation of "osmotic stress" experiments in vitro. Biochemistry. 2000; 39(15):4455-71. DOI: 10.1021/bi992887l. View

10.

Klemetsen T, Raknes I, Fu J, Agafonov A, Balasundaram S, Tartari G . The MAR databases: development and implementation of databases specific for marine metagenomics. Nucleic Acids Res. 2017; 46(D1):D692-D699. PMC: 5753341. DOI: 10.1093/nar/gkx1036. View

11.

Burg M, Ferraris J . Intracellular organic osmolytes: function and regulation. J Biol Chem. 2008; 283(12):7309-13. PMC: 2276334. DOI: 10.1074/jbc.R700042200. View

12.

Spielmeyer A, Pohnert G . Influence of temperature and elevated carbon dioxide on the production of dimethylsulfoniopropionate and glycine betaine by marine phytoplankton. Mar Environ Res. 2011; 73:62-9. DOI: 10.1016/j.marenvres.2011.11.002. View

13.

Bashir A, Hoffmann T, Smits S, Bremer E . Dimethylglycine provides salt and temperature stress protection to Bacillus subtilis. Appl Environ Microbiol. 2014; 80(9):2773-85. PMC: 3993278. DOI: 10.1128/AEM.00078-14. View

14.

Whitman W, Coleman D, Wiebe W . Prokaryotes: the unseen majority. Proc Natl Acad Sci U S A. 1998; 95(12):6578-83. PMC: 33863. DOI: 10.1073/pnas.95.12.6578. View

15.

Curson A, Liu J, Bermejo Martinez A, Green R, Chan Y, Carrion O . Dimethylsulfoniopropionate biosynthesis in marine bacteria and identification of the key gene in this process. Nat Microbiol. 2017; 2:17009. DOI: 10.1038/nmicrobiol.2017.9. View

16.

LaJeunesse T, Parkinson J, Gabrielson P, Jeong H, Reimer J, Voolstra C . Systematic Revision of Symbiodiniaceae Highlights the Antiquity and Diversity of Coral Endosymbionts. Curr Biol. 2018; 28(16):2570-2580.e6. DOI: 10.1016/j.cub.2018.07.008. View

17.

Welsh D . Ecological significance of compatible solute accumulation by micro-organisms: from single cells to global climate. FEMS Microbiol Rev. 2000; 24(3):263-90. DOI: 10.1111/j.1574-6976.2000.tb00542.x. View

18.

Nyyssola A, Reinikainen T, Leisola M . Characterization of glycine sarcosine N-methyltransferase and sarcosine dimethylglycine N-methyltransferase. Appl Environ Microbiol. 2001; 67(5):2044-50. PMC: 92834. DOI: 10.1128/AEM.67.5.2044-2050.2001. View

19.

Beale R, Airs R . Quantification of glycine betaine, choline and trimethylamine N-oxide in seawater particulates: Minimisation of seawater associated ion suppression. Anal Chim Acta. 2016; 938:114-22. DOI: 10.1016/j.aca.2016.07.016. View

20.

Neave M, Rachmawati R, Xun L, Michell C, Bourne D, Apprill A . Differential specificity between closely related corals and abundant Endozoicomonas endosymbionts across global scales. ISME J. 2016; 11(1):186-200. PMC: 5335547. DOI: 10.1038/ismej.2016.95. View