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Metabolomic signatures of coral bleaching history

Abstract

Coral bleaching has a profound impact on the health and function of reef ecosystems, but the metabolomic effects of coral bleaching are largely uncharacterized. Here, untargeted metabolomics was used to analyse pairs of adjacent Montipora capitata corals that had contrasting bleaching phenotypes during a severe bleaching event in 2015. When these same corals were sampled four years later while visually healthy, there was a strong metabolomic signature of bleaching history. This was primarily driven by betaine lipids from the symbiont, where corals that did not bleach were enriched in saturated lyso-betaine lipids. Immune modulator molecules were also altered by bleaching history in both the coral host and the algal symbiont, suggesting a shared role in partner choice and bleaching response. Metabolomics from a separate set of validation corals was able to predict the bleaching phenotype with 100% accuracy. Experimental temperature stress induced phenotype-specific responses, which magnified differences between historical bleaching phenotypes. These findings indicate that natural bleaching susceptibility is manifested in the biochemistry of both the coral animal and its algal symbiont. This metabolome difference is stable through time and results in different physiological responses to temperature stress. This work provides insight into the biochemical mechanisms of coral bleaching and presents a valuable new tool for resilience-based reef restoration.

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Fig. 1: Metabolomes of coral reflect bleaching history.
Fig. 2: Betaine lipids drive bleaching history metabolomic signature.
Fig. 3: Bleaching history signature is found in both host and symbiont metabolomes.
Fig. 4: Heat stress further strengthens metabolomic bleaching history signature.
Fig. 5: Response of individual and metabolite families to temperature stress.

Data availability

Feature-based molecular networking is available at: https://gnps.ucsd.edu/ProteoSAFe/status.jsp?task=bb9b6126118c4ba1881f4483560012d3 and raw files are available at massive.ucsd.edu under MassIVE IDs MSV000085272 and MSV000085925. Ecological and metabolomic data and analysis scripts are available at https://github.com/druryc/mcap_metabolomics.

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Acknowledgements

We thank R. Gates for the inspiration to use molecular tools to investigate corals and develop real-world solutions to the global coral reef crisis. This work was funded by the Paul G. Allen Family Foundation. Lastly, we thank C. Cornell and K. Neugebauer for close reading and critique of the manuscript throughout the writing process. This is SOEST contribution number 11209 and HIMB contribution number 1838.

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T.N.F.R. and C.D. conceived the experiment. T.N.F.R., J.D., R.A.Q. and C.D. collected data. All authors analysed data, wrote the manuscript and approved the final version.

Corresponding authors

Correspondence to Robert A. Quinn or Crawford Drury.

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The authors declare no competing interests.

Additional information

Peer review information Nature Ecology & Evolution thanks Olivier Thomas, Simon Davy and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Kāneʻohe and coral bleaching history.

Corals were collected from Reef 13 in Kāneʻohe Bay, Oʻahu, Hawaiʻi (a). A representative pair of bleached and non-bleached corals at Reef 13 during the 2015 bleaching event (b). Overall sampling schematic (c). Abbreviations in panel C are as follows: NB=Non-Bleached and B=Bleached.

Extended Data Fig. 2 Metabolome diversity metrics.

Diversity metric for the metabolomes of bleached (B) and non-bleached (NB) corals including Shannon’s entropy (a), richness (b), and evenness (c). Boxplots are median with quartiles and whiskers extending 1.5 IQR beyond quartiles.

Extended Data Fig. 3 DGCC lipid MS/MS.

Extracted ion chromatogram and MS/MS spectra of betaine lipid DGCC 16:0/0:0 described in this manuscript in positive (a) and negative (b) modes. The proposed annotation of each selected fragment ion is highlighted by a red number.

Extended Data Fig. 4 DGCC lipid abundances and saturation index.

Box and whisker plots of (a) the most abundant fully saturated betaine lipid for the in situ validation corals and (b) the most important molecule for distinguishing between phenotypes from the random forests variable importance plot. Boxplots are median with quartiles and whiskers extending 1.5 IQR beyond quartiles. c, DGCC unsaturation index (calculated according to Rosette et al. 2019) from experimental bleached and non-bleached corals. d, Log total abundance of lyso-DGCC lipids from experimental corals. Boxplots are median with quartiles and whiskers extending 1.5 IQR beyond quartiles.

Extended Data Fig. 5 DGTS lipid abundances.

DGTS lipid abundances in corals based on HBP. These betaine lipids do not exhibit substantial differences between HBPs like the related DGCCs. Boxplots are median with quartiles and whiskers extending 1.5 IQR beyond quartiles. auc= area under curve.

Extended Data Fig. 6 Symbiont genotypes in corals from this study.

Relative symbiont abundance of genotypes in the study in 2019 (a) and for a larger set that includes validation samples from 2018 (b). Cladocopium vs Durursdinium dominance is stable over time.

Extended Data Fig. 7 Betaine lipids and algae abundances.

Linear regression of saturated (A,C) and unsaturated (B,D) betaine lipids versus Cladocopium (A,B) and Durisdinium (C,D) algal symbionts. Shaded areas represent 95% confidence intervals.

Extended Data Fig. 8 Known metabolite relationships with bleaching history.

a, PCA of lab corals using only known compounds. Points (n = 5 per genotype) represent individual samples colored by genotype (n = 10). Fill represents HBP (gray = non-bleached, white = bleached). b, PCA of field validation set using only known compounds. Points represent single samples from individual genotypes in the validation set which were not evaluated in panel A (n = 12). Fill represents HBP (gray = non-bleached, white = bleached). c, All known compounds ranked by descending variable importance for discriminating between HBPs. Colors represent molecular families assigned to individual molecules corresponding to Fig. 1. d, Relative variable importance of molecular families in all known compounds, arranged by ascending median rank (lower is more informative). Individual points correspond to ranked molecules in panel C, with horizontal bars showing first and third quartiles of each molecular family. Colors represent molecular families as in panel C.

Extended Data Fig. 9 Abundances of known compounds in bleached and non-bleached corals.

Box and whisker plots of biologically interesting known metabolites in the ‘lab corals’ (a-e) and the in situ ‘validation corals’ (f-j). Coral host-derived metabolites pantothenic acid (k) and tryptamine (l). Boxplots are median with quartiles and whiskers extending 1.5 IQR beyond quartiles. y-axis is the area under curve abundance.

Extended Data Fig. 10 Symbiont and bleached metabolome relationships with bleaching history and molecular family responses to heat stress.

PCA of all metabolites found in replicate symbiont pellets (a) and all metabolites found in replicate bleached host fragments (b). These samples were collected from colony 19 and 20, which are included in the larger lab dataset and represent a bleached and non-bleached colony, respectively. Fill represents HBP (gray = non-bleached, white = bleached). Multivariate response to heat stress for (c) Membrane Lipids and (d) Bioactive Molecules (e) Putative Microbial Products. Fill represents HBP (gray = non-bleached, white = bleached). Color represents initial and heat stress timepoints (black = initial, red = heat stress). Gray ellipses represent 95% confidence interval of phenotypes. Gray bars connect paired before-after samples.

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Roach, T.N.F., Dilworth, J., H., C.M. et al. Metabolomic signatures of coral bleaching history. Nat Ecol Evol 5, 495–503 (2021). https://doi.org/10.1038/s41559-020-01388-7

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