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Identifying metabolic alterations associated with coral growth anomalies using 1H NMR metabolomics

Abstract

Coral growth anomalies (GAs) are tumor-like protrusions that are detrimental to coral health, affecting both the coral skeleton and soft tissues. These lesions are increasingly found throughout the tropics and are commonly associated with high human population density, yet little is known about the molecular pathology of the disease. Here, we investigate the metabolic impacts of GAs through 1H nuclear magnetic resonance (NMR) metabolomics in Porites compressa tissues from a site of high disease prevalence (Coconut Island, Hawaii). We putatively identified 18 metabolites (8.1% of total annotated features) through complementary 1H and 1H–13C heteronuclear single quantum correlation NMR data that increase confidence in pathway analyses and may bolster future coral metabolite annotation efforts. Extract yield was elevated in both GA and unaffected (normal tissue from a diseased colony) compared to reference (normal tissue from GA-free colony) samples, potentially indicating elevated metabolic activity in GA-impacted colonies. Relatively high variation in metabolomic profiles among coral samples of the same treatment (i.e., inter-colony variation) confounded data interpretation, however, analyses of paired GA and unaffected samples identified 73 features that differed between these respective metabolome types. These features were largely annotated as unknowns, but 1-methylnicotinamide and trigonelline were found to be elevated in GA samples, while betaine, glycine, and histamine were lower in GA samples. Pathway analyses indicate decreased choline oxidation in GA samples, making this a pathway of interest for future targeted studies. Collectively, our results provide unique insights into GA pathophysiology by showing these lesions alter both the absolute and relative metabolism of affected colonies and by identifying features (metabolites and unknowns) and metabolic pathways of interest in GA pathophysiology going forward.

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Acknowledgements

We thank the Woodley lab staff at the National Oceanic and Atmospheric Administration coral culture facility for providing Orbicella faveolata specimens for use as control materials in this work. We also thank the National Institute of Standards and Technology Biorepository for storage of the coral samples, Ben Flanagan for his help with laboratory work, and Julie Loewenstein for her advice in preparing this manuscript. Diagrams used in Figs. 1a and 5 were created using BioRender scientific illustration tool (Biorender.com). P. compressa illustrations used in Fig. 1a are based on a photograph by David R. with modifications (https://www.inaturalist.org/observations/14939424). Observation © David R. 2018 (Creative Commons Attribution-NonCommercial license (CC BY-NC 4.0)).

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Correspondence to Erik R. Andersson.

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Andersson, E.R., Day, R.D., Work, T.M. et al. Identifying metabolic alterations associated with coral growth anomalies using 1H NMR metabolomics. Coral Reefs 40, 1195–1209 (2021). https://doi.org/10.1007/s00338-021-02125-7

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Keywords

  • Coral disease
  • Growth anomalies
  • Metabolomics
  • NMR spectroscopy
  • Porites compressa