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

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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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References

  • Aeby GS, Williams GJ, Franklin EC, Kenyon J, Cox EF, Coles S, Work TM (2011a) Patterns of coral disease across the Hawaiian Archipelago: Relating disease to environment. PLoS One 6:e20370

  • Aeby GS, Williams GJ, Franklin EC, Haapkyla J, Harvell CD, Neale S, Page CA, Raymundo L, Vargas-Ángel B, Willis BL, Work TM, Davy SK (2011b) Growth anomalies on the coral genera Acropora and Porites are strongly associated with host density and human population size across the Indo-Pacific. PLoS One 6:e16887

  • Alonso A, Marsal S, Julià A (2015) Analytical methods in untargeted metabolomics: State of the art in 2015. Front Bioeng Biotechnol 3:23

  • Amelio I, Cutruzzolá F, Antonov A, Agostini M, Melino G (2014) Serine and glycine metabolism in cancer. Trends Biochem Sci 39:191–198

  • Andersson ER, Day RD, Loewenstein JM, Woodley CM, Schock TB (2019) Evaluation of sample preparation methods for the analysis of reef-building corals using 1H-NMR-based metabolomics. Metabolites 9:32

  • Andersson ER, Stewart JA, Work TM, Woodley CM, Schock TB, Day RD (2020) Morphological, elemental, and boron isotopic insights into pathophysiology of diseased coral growth anomalies. Sci Rep 10:8252

  • Aronson RB, Precht WF (2001) White-band disease and the changing face of Caribbean coral reefs. Hydrobiologia 460:25–38

  • Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216

  • Bahr KD, Jokiel PL, Toonen RJ (2015) The unnatural history of Kāne’ohe bay: Coral reef resilience in the face of centuries of anthropogenic impacts. PeerJ 3:e950

  • Benjamini Y, Hochberg Y (1995) Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. J R Stat Soc Ser B 57:289–300

  • Bijlsma S, Bobeldijk I, Verheij ER, Ramaker R, Kochhar S, Macdonald IA, Van Ommen B, Smilde AK (2006) Large-scale human metabolomics studies: A strategy for data (pre-) processing and validation. Anal Chem 78:567–574

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J of Biochem Physiol 37:911–917

  • Bruckner AW (2016) History of coral disease research. In: Diseases of coral. John Wiley and Sons Inc, pp 52–84

  • Bundy JG, Davey MP, Viant MR (2009) Environmental metabolomics: A critical review and future perspectives. Metabolomics 5:3–21

  • Burge CA, Mark Eakin C, Friedman CS, Froelich B, Hershberger PK, Hofmann EE, Petes LE, Prager KC, Weil E, Willis BL, Ford SE, Harvell CD (2014) Climate Change Influences on Marine Infectious Diseases: Implications for Management and Society. Ann Rev Mar Sci 6:249–277

  • Burns JHR, Takabayashi M (2011) Histopathology of growth anomaly affecting the coral, Montipora capitata: Implications on biological functions and population viability. PLoS One 6:e28854

  • Burriesci MS, Raab TK, Pringle JR (2012) Evidence that glucose is the major transferred metabolite in dinoflagellate-cnidarian symbiosis. J Exp Biol 215:3467–3477

  • Cappello T, Mauceri A, Corsaro C, Maisano M, Parrino V, Lo Paro G, Messina G, Fasulo S (2013) Impact of environmental pollution on caged mussels Mytilus galloprovincialis using NMR-based metabolomics. Mar Pollut Bull 77:132–139

  • Coles SL, Seapy DG (1998) Ultra-violet absorbing compounds and tumorous growths on acroporid corals from Bandar Khayran, Gulf of Oman, Indian Ocean. Coral Reefs 17:195–198

  • Cui G, Liew YJ, Li Y, Kharbatia N, Zahran NI, Emwas A-H, Eguiluz VM, Aranda M (2019) Host-dependent nitrogen recycling as a mechanism of symbiont control in Aiptasia. PLOS Genet 15:e1008189

  • De Meyer T, Sinnaeve D, Van Gasse B, Tsiporkova E, Rietzschel ER, De Buyzere ML, Gillebert TC, Bekaert S, Martins JC, Van Criekinge W (2008) NMR-based characterization of metabolic alterations in hypertension using an adaptive, intelligent binning algorithm. Anal Chem 80:3783–3790

  • Domart-Coulon IJ, Traylor-Knowles N, Peters E, Elbert D, Downs CA, Price K, Stubbs J, McLaughlin S, Cox E, Aeby G, Brown PR, Ostrander GK (2006) Comprehensive characterization of skeletal tissue growth anomalies of the finger coral Porites compressa. Coral Reefs 25:531–543

  • Frazier M, Helmkampf M, Bellinger MR, Geib SM, Takabayashi M (2017) De novo metatranscriptome assembly and coral gene expression profile of Montipora capitata with growth anomaly. BMC Genomics 18:710

  • Goodacre R (2007) Metabolomics of a Superorganism. J Nutr 137:259S–266S

  • Gordon B.R, Laggat W, Motti CA (2013) Extraction protocol for nontargeted NMR and LC-MS metabolomics-based analysis of hard coral and their algal symbionts. In: Metabolomics tools for natural product discovery: methods and protocols. Humana Press, pp 129–147

  • Green EP, Bruckner AW (2000) The significance of coral disease epizootiology for coral reef conservation. Biol Conserv 96:347–361

  • Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189

  • Hadaidi G, Gegner HM, Ziegler M, Voolstra CR (2019) Carbohydrate composition of mucus from scleractinian corals from the central Red Sea. Coral Reefs 38:21–27

  • Hagedorn M, Carter V, Zuchowicz N, Phillips M, Penfield C, Shamenek B, Vallen EA, Kleinhans FW, Peterson K, White M, Yancey PH (2015) Trehalose is a chemical attractant in the establishment of coral symbiosis. PLoS One 10: e0117087

  • Hartmann AC, Petras D, Quinn RA, Protsyuk I, Archer FI, Ransome E, Williams GJ, Bailey BA, Vermeij MJA, Alexandrov T, Dorrestein PC, Rohwer FL (2017) Meta-mass shift chemical profiling of metabolomes from coral reefs. Proc Natl Acad Sci USA 114:11685–11690

  • Hillyer KE, Dias D, Lutz A, Roessner U, Davy SK (2018) 13C metabolomics reveals widespread change in carbon fate during coral bleaching. Metabolomics 14:12

  • Hillyer KE, Dias DA, Lutz A, Wilkinson SP, Roessner U, Davy SK (2017) Metabolite profiling of symbiont and host during thermal stress and bleaching in the coral Acropora aspera. Coral Reefs 36:105–118

  • Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742

  • Hughes TP, Barnes ML, Bellwood DR, Cinner JE, Cumming GS, Jackson JBC, Kleypas J, Van De Leemput IA, Lough JM, Morrison TH, Palumbi SR, Van Nes EH, Scheffer M (2017) Coral reefs in the Anthropocene. Nature 546:82–90

  • Jacob D, Deborde C, Lefebvre M, Maucourt M, Moing A (2017) NMRProcFlow: a graphical and interactive tool dedicated to 1D spectra processing for NMR-based metabolomics. Metabolomics 13:36

  • Joyce AR, Palsson B (2006) The model organism as a system: Integrating “omics” data sets. Nat Rev Mol Cell Biol 7:198–210

  • Kaczmarsky L, Richardson LL (2007) Transmission of growth anomalies between Indo-Pacific Porites corals. J Invertebr Pathol 94:218–221

  • Kell DB, Oliver SG (2004) Here is the evidence, now what is the hypothesis? The complementary roles of inductive and hypothesis-driven science in the post-genomic era. BioEssays 26:99–105

  • Kelly LA, Heintz T, Lamb JB, Ainsworth TD, Willis BL (2016) Ecology and pathology of novel plaque-like growth anomalies affecting a reef-building coral on the great barrier reef. Front Mar Sci 3:151

  • Knowlton N (2001) The future of coral reefs. Proc Natl Acad Sci USA 98:5419–5425

  • Lesser MP, Bythell JC, Gates RD, Johnstone RW, Hoegh-Guldberg O (2007) Are infectious diseases really killing corals? Alternative interpretations of the experimental and ecological data. J Exp Mar Bio Ecol 346:36–44

  • Liu X, Zhang L, You L, Yu J, Cong M, Wang Q, Li F, Li L, Zhao J, Li C, Wu H (2011) Assessment of clam Ruditapes philippinarum as heavy metal bioindicators using NMR-based metabolomics. Clean - Soil, Air, Water 39:759–766

  • Lohr KE, Camp EF, Kuzhiumparambil U, Lutz A, Leggat W, Patterson JT, Suggett DJ (2019a) Resolving coral photoacclimation dynamics through coupled photophysiological and metabolomic profiling. J Exp Biol 222:jeb195982

  • Lohr KE, Khattri RB, Guingab-Cagmat J, Camp EF, Merritt ME, Garrett TJ, Patterson JT (2019b) Metabolomic profiles differ among unique genotypes of a threatened Caribbean coral. Sci Rep 9:6067

  • Madsen EL (2005) Identifying microorganisms responsible for ecologically significant biogeochemical processes. Nat Rev Microbiol 3:439–446

  • Markley JL, Brüschweiler R, Edison AS, Eghbalnia HR, Powers R, Raftery D, Wishart DS (2017) The future of NMR-based metabolomics. Curr Opin Biotechnol 43:34–40

  • Matthews JL, Cunning R, Ritson-Williams R, Oakley CA, Lutz A, Roessner U, Grossman AR, Weis VM, Gates RD, Davy SK (2020) Metabolite pools of the reef building coral Montipora capitata are unaffected by Symbiodiniaceae community composition. Coral Reefs 39:1727–1737

  • Moberg F, Folke C (1999) Ecological goods and services of coral reef ecosystems. Ecol Econ 29:215–233

  • Nakae D, Yoshiji H, Mizumoto Y, Horiguchi K, Shiraiwa K, Tamura K, Denda A, Konishi Y (1992) High Incidence of Hepatocellular Carcinomas Induced by a Choline Deficient L-Amino Acid Defined Diet in Rats. Cancer Res 52:5042–5045

  • Niculescu MD, Zeisel SH (2002) Diet, methyl donors and DNA methylation: interactions between dietary folate, methionine and choline. J Nutr 132:2333S–2335S

  • Ochsenkühn MA, Röthig T, D’Angelo C, Wiedenmann J, Voolstra CR (2017) The role of floridoside in osmoadaptation of coral-associated algal endosymbionts to high-salinity conditions. Sci Adv 3:e1602047

  • Odum HT, Odum EP (1955) Trophic structure and productivity of a windward coral reef community on Eniwetok Atoll. Ecol Monogr 25:291–320

  • Palmer CV, Baird AH (2018) Coral tumor-like growth anomalies induce an immune response and reduce fecundity. Dis Aquat Organ 130:77–81

  • Parkinson JE, Baums IB (2014) The extended phenotypes of marine symbioses: Ecological and evolutionary consequences of intraspecific genetic diversity in coral-algal associations. Front Microbiol 5:445

  • Pollock FJ, Morris PJ, Willis BL, Bourne DG (2011) The urgent need for robust coral disease diagnostics. PLoS Pathog 7:e1002183

  • Preston S, Richards Z (2021) Biological consequences of an outbreak of growth anomalies on Isopora palifera at the Cocos (Keeling) Islands. Coral Reefs 40:97–109

  • Putnam HM, Davidson JM, Gates RD (2016) Ocean acidification influences host DNA methylation and phenotypic plasticity in environmentally susceptible corals. Evol Appl 9:1165–1178

  • Puverel S, Tambutté E, Pereira-Mouriès L, Zoccola D, Allemand D, Tambutté S (2005) Soluble organic matrix of two Scleractinian corals: Partial and comparative analysis. Comp Biochem Physiol - B Biochem Mol Biol 141:480–487

  • Quinn RA, Vermeij MJA, Hartmann AC, d’Auriac IG, Benler S, Haas A, Quistad SD, Lim YW, Little M, Sandin S, Smith JE, Dorrestein PC, Rohwer F (2016) Metabolomics of reef benthic interactions reveals a bioactive lipid involved in coral defence. Proc R Soc B Biol Sci 283:20160469

  • Roach TNF, Little M, Arts MGI, Huckeba J, Haas AF, George EE, Quinn RA, Cobián-Güemes AG, Naliboff DS, Silveira CB, Vermeij MJA, Kelly LW, Dorrestein PC, Rohwer F (2020) A multiomic analysis of in situ coral-turf algal interactions. Proc Natl Acad Sci USA 117:13588–13595

  • Roach TNF, Dilworth J, Christian Martin H, Jones AD, Quinn RA, Drury C (2021) Metabolomic signatures of coral bleaching history. Nat Ecol Evol

  • Roberts LD, Souca AL, Gerszten RE, Clish CB (2012) Targeted metabolomics. In: Current protocols in molecular biology. John Wiley and Sons Inc, 98:30.2:30.2.1–30.2.24

  • Ross A, Schlotterbeck G, Dieterle F, Senn H (2007) NMR spectroscopy techniques for application to metabolomics. In: The handbook of metabonomics and metabolomics. Elsevier, pp 55–108

  • Sale TL, Hunter CL, Hong C, Moran AL (2019) Morphology, lipid composition, and reproduction in growth anomalies of the reef-building coral Porites evermanni and Porites lobata. Coral Reefs 38:881–893

  • Sogin EM, Putnam HM, Anderson PE, Gates RD (2016) Metabolomic signatures of increases in temperature and ocean acidification from the reef-building coral, Pocillopora damicornis. Metabolomics 12:71

  • Sogin EM, Anderson P, Williams P, Chen CS, Gates RD (2014) Application of 1H-NMR metabolomic profiling for reef-building corals. PLoS One 9:e111274

  • Sogin EM, Putnam HM, Nelson CE, Anderson P, Gates RD (2017) Correspondence of coral holobiont metabolome with symbiotic bacteria, archaea and Symbiodinium communities. Environ Microbiol Rep 9:310–315

  • Southam AD, Easton JM, Stentiford GD, Ludwig C, Arvanitis TN, Viant MR (2008) Metabolic changes in flatfish hepatic tumours revealed by NMR-based metabolomics and metabolic correlation networks. J Proteome Res 7:5277–5285

  • Spies NP, Takabayashi M (2013) Expression of galaxin and oncogene homologs in growth anomaly in the coral Montipora capitata. Dis Aquat Organ 104:249–256

  • Stien D, Suzuki M, Rodrigues AMS, Yvin M, Clergeaud F, Thorel E, Lebaron P (2020) A unique approach to monitor stress in coral exposed to emerging pollutants. Sci Rep 10:9601

  • Stien D, Clergeaud F, Rodrigues AMS, Lebaron K, Pillot R, Romans P, Fagervold S, Lebaron P (2019) Metabolomics reveal that octocrylene accumulates in Pocillopora damicornis tissues as fatty acid conjugates and triggers coral cell mitochondrial dysfunction. Anal Chem 91:990–995

  • Stimson J (2011) Ecological characterization of coral growth anomalies on Porites compressa in Hawai’i. Coral Reefs 30:133–142

  • Sumner LW, Amberg A, Barrett D, Beale MH, Beger R, Daykin CA, Fan TWM, Fiehn O, Goodacre R, Griffin JL, Hankemeier T, Hardy N, Harnly J, Higashi R, Kopka J, Lane AN, Lindon JC, Marriott P, Nicholls AW, Reily MD, Thaden JJ, Viant MR (2007) Proposed minimum reporting standards for chemical analysis: Chemical Analysis Working Group (CAWG) Metabolomics Standards Initiative (MSI). Metabolomics 3:211–221

  • Szymańska E, Saccenti E, Smilde AK, Westerhuis JA (2012) Double-check: validation of diagnostic statistics for PLS-DA models in metabolomics studies. Metabolomics 8:3–16

  • Ulrich EL, Akutsu H, Doreleijers JF, Harano Y, Ioannidis YE, Lin J, Livny M, Mading S, Maziuk D, Miller Z, Nakatani E, Schulte CF, Tolmie DE, Kent Wenger R, Yao H, Markley JL (2008) BioMagResBank. Nucleic Acids Res 36:D402–D408

  • van Dam J. W., Negri A. P., Uthicke S., and Mueller J. F. (2011) Chemical pollution of coral reefs: exposure and ecological effects. In: Ecological impacts of toxic chemicals. Bentham Science Publisher Ltd, pp 187–211

  • van den Berg RA, Hoefsloot HCJ, Westerhuis JA, Smilde AK, van der Werf MJ (2006) Centering, scaling, and transformations: Improving the biological information content of metabolomics data. BMC Genomics 7:142

  • Viant MR (2008) Recent developments in environmental metabolomics. Mol Biosyst 4:980–986

  • Vohsen SA, Fisher CR, Baums IB (2019) Metabolomic richness and fingerprints of deep-sea coral species and populations. Metabolomics 15:34

  • Williams A, Chiles EN, Conetta D, Pathmanathan JS, Cleves PA, Putnam HM, Su X, Bhattacharya D (2021) Metabolomic shifts associated with heat stress in coral holobionts. Sci Adv 7:eabd4210

  • Wishart DS, Tzur D, Knox C, Eisner R, Guo AC, Young N, Cheng D, Jewell K, Arndt D, Sawhney S, Fung C, Nikolai L, Lewis M, Coutouly MA, Forsythe I, Tang P, Shrivastava S, Jeroncic K, Stothard P, Amegbey G, Block D, Hau DD, Wagner J, Miniaci J, Clements M, Gebremedhin M, Guo N, Zhang Y, Duggan GE, MacInnis GD, Weljie AM, Dowlatabadi R, Bamforth F, Clive D, Greiner R, Li L, Marrie T, Sykes BD, Vogel HJ, Querengesser L (2007) HMDB: The human metabolome database. Nucleic Acids Res 35:D521–D526

  • Work TM, Aeby GS (2006) Systematically describing gross lesions in corals. Dis Aquat Organ 70:155–160

  • Work TM, Kaczmarsky LT, Peters EC (2016) Skeletal growth anomalies in corals. In: Diseases of coral. John Wiley and Sons Inc, pp 291–299

  • Wu H, Southam AD, Hines A, Viant MR (2008) High-throughput tissue extraction protocol for NMR- and MS-based metabolomics. Anal Biochem 372:204–212

  • Xia J, Wishart DS (2016) Using metaboanalyst 3.0 for comprehensive metabolomics data analysis. Curr Protoc Bioinform 55:14.10.1–14.10.91

  • Yasuda N, Hidaka M (2012) Cellular kinetics in growth anomalies of the scleractinian corals Porites australiensis and Montipora informis. Dis Aquat Organ 102: 1–11

  • Zhang Y, Sun J, Mu H, Lun JCY, Qiu JW (2017) Molecular pathology of skeletal growth anomalies in the brain coral Platygyra carnosa: A meta-transcriptomic analysis. Mar Pollut Bull 124:660–667

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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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  1. Rusty D. Day

    Present address: Marine Science and Nautical Training Academy (MANTA), 417 Planters Trace Dr, Charleston, SC, 29412, USA

Authors and Affiliations

  1. Grice Marine Laboratory, Department of Biology, College of Charleston, 205 Fort Johnson Rd., Charleston, SC, 29412, USA

    Erik R. Andersson & Rusty D. Day

  2. Chemical Sciences Division, National Institute of Standards and Technology, Hollings Marine Laboratory, Charleston, SC, 29412, USA

    Erik R. Andersson, Rusty D. Day & Tracey B. Schock

  3. U.S. Geological Survey National Wildlife Health Center, Honolulu Field Station, Honolulu, HI, 96850, USA

    Thierry M. Work

  4. Department of Computer Science and Software Engineering, California Polytechnic State University, San Luis Obispo, CA, 93407, USA

    Paul E. Anderson

  5. National Oceanic and Atmospheric Administration, National Ocean Service, National Centers for Coastal Ocean Sciences, Hollings Marine Laboratory, Charleston, SC, 29412, USA

    Cheryl M. Woodley

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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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