Skip to main content

Advertisement

SpringerLink
Log in

Mass spectrometry–based metabolomic signatures of coral bleaching under thermal stress

  • Research Paper
  • Published:
Analytical and Bioanalytical Chemistry Aims and scope Submit manuscript

Abstract

Coral bleaching caused by climate change has resulted in large-scale coral reef decline worldwide. However, the knowledge of physiological response mechanisms of scleractinian corals under high-temperature stress is still challenging. Here, untargeted mass spectrometry–based metabolomics combining with Global Natural Product Social Molecular Networking (GNPS) was utilized to investigate the physiological response of the coral species Pavona decussata under thermal stress. A wide variety of metabolites (including lipids, fatty acids, amino acids, peptides, osmolytes) were identified as the potential biomarkers and subjected to metabolic pathway enrichment analysis. We discovered that, in the thermal-stressed P. decussata coral holobiont, (1) numerous metabolites in classes of lipids and amino acids significantly decreased, indicating an enhanced lipid hydrolysis and aminolysis that contributed to up-regulation in gluconeogenesis to meet energy demand for basic survival; (2) pantothenate and panthenol, two essential intermediates in tricarboxylic acid (TCA) cycle, were up-regulated, implying enhanced efficiency in energy production; (3) small peptides (e.g., Glu-Leu and Glu-Glu-Glu-Glu) and lyso-platelet-activating factor (lysoPAF) possibly implicated a strengthened coral immune response; (4) the down-regulation of betaine and trimethylamine N-oxide (TMAO), known as osmolyte compounds for maintaining holobiont homeostasis, might be the result of disruption of coral holobiont.

Graphical abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Ainsworth TD, Heron SF, Ortiz JC, Mumby PJ, Grech A, Ogawa D, Eakin CM, Leggat W. Climate change disables coral bleaching protection on the Great Barrier Reef. Science. 2016;352(6283):338–42.

    CAS  PubMed  Google Scholar 

  2. Kwiatkowski L, Cox P, Halloran PR, Mumby PJ, Wiltshire AJ. Coral bleaching under unconventional scenarios of climate warming and ocean acidification. Nat Clim Change. 2015;5(8):777–81.

    CAS  Google Scholar 

  3. Hughes TP, Kerry JT, Simpson T. Large-scale bleaching of corals on the Great Barrier Reef. Ecology. 2018;99(2):501–601.

    CAS  PubMed  Google Scholar 

  4. Hughes TP, Kerry JT, Alvarez-Noriega M, Alvarez-Romero JG, Anderson KD, Baird AH, Babcock RC, Beger M, Bellwood DR, Berkelmans R, Bridge TC, Butler IR, Byrne M, Cantin NE, Comeau S, Connolly SR, Cumming GS, Dalton SJ, Diaz-Pulido G, Eakin CM, Figueira WF, Gilmour JP, Harrison HB, Heron SF, Hoey AS, Hobbs JPA, Hoogenboom MO, Kennedy EV, Kuo CY, Lough JM, Lowe RJ, Liu G, Cculloch MTM, Malcolm HA, Mcwilliam MJ, Pandolfi JM, Pears RJ, Pratchett MS, Schoepf V, Simpson T, Skirving WJ, Sommer B, Torda G, Wachenfeld DR, Willis BL, Wilson SK. Global warming and recurrent mass bleaching of corals. Nature. 2017;543(7645):373–7.

    CAS  PubMed  Google Scholar 

  5. Hughes TP, Rodrigues MJ, Bellwood DR, Ceccarelli D, Hoegh-Guldberg O, McCook L, Moltschaniwskyj N, Pratchett MS, Steneck RS, Willis B. Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr Biol. 2007;17(4):360–5.

    CAS  PubMed  Google Scholar 

  6. Cziesielski MJ, Liew YJ, Cui GX, Schmidt-Roach S, Campana S, Marondedze C, Aranda M. Multi-omics analysis of thermal stress response in a zooxanthellate cnidarian reveals the importance of associating with thermotolerant symbionts. Proc R Soc B Biol Sci. 1877;2018(285):20172654.

    Google Scholar 

  7. Parkinson JE, Baker AC, Baums IB, Davies SW, Grottoli AG, Kitchen SA, Matz MV, Miller MW, Shantz AA, Kenkel CD. Molecular tools for coral reef restoration: beyond biomarker discovery. Conserv Lett. 2020;13(1): e12687.

    Google Scholar 

  8. Lesser MP. Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol. 2006;68:253–78.

    CAS  PubMed  Google Scholar 

  9. Gruning NM, Lehrach H, Ralser M. Regulatory crosstalk of the metabolic network. Trends Biochem Sci. 2010;35(4):220–7.

    PubMed  Google Scholar 

  10. Rivest EB, Chen CS, Fan TY, Li HH, Hofmann GE. Lipid consumption in coral larvae differs among sites: a consideration of environmental history in a global ocean change scenario. Proc R Soc B Biol Sci. 1853;2017(284):20162825.

    Google Scholar 

  11. Herrmann J, Abou Fayad A, Muller R. Natural products from myxobacteria: novel metabolites and bioactivities. Nat Prod Rep. 2017;34(2):135–60.

    CAS  PubMed  Google Scholar 

  12. Roychoudhury A, Bieker A, Haussinger D, Oesterhelt F. Membrane protein stability depends on the concentration of compatible solutes - a single molecule force spectroscopic study. Biol Chem. 2013;394(11):1465–74.

    CAS  PubMed  Google Scholar 

  13. Hill RW, Li C, Jones AD, Gunn JP, Frade PR. Abundant betaines in reef-building corals and ecological indicators of a photoprotective role. Coral Reefs. 2010;29(4):869–80.

    Google Scholar 

  14. Hillyer KE, Tumanov S, Villas-Boas S, Davy SK. Metabolite profiling of symbiont and host during thermal stress and bleaching in a model cnidarian-dinoflagellate symbiosis. J Exp Biol. 2016;219(4):516–27.

    PubMed  Google Scholar 

  15. 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. Metabolomics of reef benthic interactions reveals a bioactive lipid involved in coral defence. Proc R Soc B Biol Sci. 1829;2016(283):20160469.

    Google Scholar 

  16. Sogin EM, Putnam HM, Anderson PE, Gates RD. Metabolomic signatures of increases in temperature and ocean acidification from the reef-building coral. Pocillopora damicornis Metabolomics. 2016;12(4):1–12.

    CAS  Google Scholar 

  17. Hillyer KE, Dias DA, Lutz A, Wilkinson SP, Roessner U, Davy SK. Metabolite profiling of symbiont and host during thermal stress and bleaching in the coral Acropora aspera. Coral Reefs. 2017;36(1):105–18.

    Google Scholar 

  18. Roach TNF, Dilworth J, Martin CH, Jones AD, Quinn RA, Drury C. Metabolomic signatures of coral bleaching history. Nat Ecol Evol. 2021;5(4):495–503.

    PubMed  Google Scholar 

  19. Williams A, Chiles EN, Conetta D, Pathmanathan JS, Cleves PA, Putnam HM, Su XY, Bhattacharya D. Metabolomic shifts associated with heat stress in coral holobionts. Sci Adv. 2021;7(1):eabd4210.

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Farag MA, Meyer A, Ali SE, Salem MA, Giavalisco P, Westphal H, Wessjohann LA. Comparative metabolomics approach detects stress-specific responses during coral bleaching in soft corals. J Proteome Res. 2018;17(6):2060–71.

    CAS  PubMed  Google Scholar 

  21. Boroujerdi AFB, Vizcaino MI, Meyers A, Pollock EC, Huynh SL, Schock TB, Morris PJ, Bearden DW. NMR-based microbial metabolomics and the temperature-dependent coral pathogen Vibrio coralliilyticus. Environ Sci Technol. 2009;43(20):7658–64.

    CAS  PubMed  Google Scholar 

  22. Wang MX, Carver JJ, Phelan VV, Sanchez LM, Garg N, Peng Y, Nguyen DD, Watrous J, Kapono CA, Luzzatto-Knaan T, Porto C, Bouslimani A, Melnik AV, Meehan MJ, Liu WT, Criisemann M, Boudreau PD, Esquenazi E, Sandoval-Calderon M, Kersten RD, Pace LA, Quinn RA, Duncan KR, Hsu CC, Floros DJ, Gavilan RG, Kleigrewe K, Northen T, Dutton RJ, Parrot D, Carlson EE, Aigle B, Michelsen CF, Jelsbak L, Sohlenkamp C, Pevzner P, Edlund A, McLean J, Piel J, Murphy BT, Gerwick L, Liaw CC, Yang YL, Humpf HU, Maansson M, Keyzers RA, Sims AC, Johnson AR, Sidebottom AM, Sedio BE, Klitgaard A, Larson CB, Boya CA, Torres-Mendoza D, Gonzalez DJ, Silva DB, Marques LM, Demarque DP, Pociute E, O’Neill EC, Briand E, Helfrich EJN, Granatosky EA, Glukhov E, Ryffel F, Houson H, Mohimani H, Kharbush JJ, Zeng Y, Vorholt JA, Kurita KL, Charusanti P, McPhail KL, Nielsen KF, Vuong L, Elfeki M, Traxler MF, Engene N, Koyama N, Vining OB, Baric R, Silva RR, Mascuch SJ, Tomasi S, Jenkins S, Macherla V, Hoffman T, Agarwal V, Williams PG, Dai JQ, Neupane R, Gurr J, Rodriguez AMC, Lamsa A, Zhang C, Dorrestein K, Duggan BM, Almaliti J, Allard PM, Phapale P, Nothias LF, Alexandrovr T, Litaudon M, Wolfender JL, Kyle JE, Metz TO, Peryea T, Nguyen DT, VanLeer D, Shinn P, Jadhav A, Muller R, Waters KM, Shi WY, Liu XT, Zhang LX, Knight R, Jensen PR, Palsson BO, Pogliano K, Linington RG, Gutierrez M, Lopes NP, Gerwick WH, Moore BS, Dorrestein PC, Bandeira N. Sharing and community curation of mass spectrometry data with Global Natural Products Social Molecular Networking. Nat Biotechnol. 2016;34(8):828–37.

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Hartmann AC, Petras D, Quinn RA, Protsyuk I, Archer FI, Ransome E, Williams GJ, Bailey BA, Vermeij MJA, Alexandrov T, Dorrestein PC, Rohwer FL. Meta-mass shift chemical profiling of metabolomes from coral reefs. Proc Natl Acad Sci USA. 2017;114(44):11685–90.

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Ros M, Suggett DJ, Edmondson J, Haydon T, Hughes DJ, Kim M, Guagliardo P, Bougoure J, Pernice M, Raina JB, Camp EF. Symbiont shuffling across environmental gradients aligns with changes in carbon uptake and translocation in the reef-building coral Pocillopora acuta. Coral Reefs. 2021;40(2):595–607.

    Google Scholar 

  25. Yu XP, Yu KF, Liao ZH, Liang JY, Deng CQ, Huang W, Huang YH. Potential molecular traits underlying environmental tolerance of Pavona decussata and Acropora pruinosa in Weizhou Island, northern South China Sea. Mar Pollut Bull. 2020;156: 111199.

    CAS  PubMed  Google Scholar 

  26. Yu WJ, Wang WH, Yu KF, Wang YH, Huang XY, Huang RY, Liao ZH, Xu SD, Chen XY. Rapid decline of a relatively high latitude coral assemblage at Weizhou Island, northern South China Sea. Biodivers Conserv. 2019;28(14):3925–49.

    Google Scholar 

  27. Qin ZJ, Yu KF, Wang YH, Xu LJ, Huang XY, Chen B, Li Y, Wang WH, Pan ZL. Spatial and intergeneric variation in physiological indicators of corals in the south china sea: insights into their current state and their adaptability to environmental stress. J Geophys Res-Oceans. 2019;124(5):3317–32.

    Google Scholar 

  28. Grottoli AG, Toonen RJ, van Woesik R, Thurber RV, Warner ME, McLachlan RH, Price JT, Bahr KD, Baums IB, Castillo KD, Coffroth MA, Cunning R, Dobson KL, Donahue MJ, Hench JL, Iglesias-Prieto R, Kemp DW, Kenkel CD, Kline DI, Kuffner IB, Matthews JL, Mayfield AB, Padilla-Gamino JL, Palumbi S, Voolstra CR, Weis VM, Wu HC. Increasing comparability among coral bleaching experiments. Ecol Appl. 2021;31(4): e0226.

    Google Scholar 

  29. Xia JG, Psychogios N, Young N, Wishart DS. MetaboAnalyst: a web server for metabolomic data analysis and interpretation. Nucleic Acids Res. 2009;37:W652–60.

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Malul D, Holzman R, Shavit U. Coral tentacle elasticity promotes anout-of-phasemotion that improves mass transfer. Proc R Soc B Biol Sci. 1929;2020(287):20200180.

    Google Scholar 

  31. Sikorskaya TV, Ermolenko EV, Imbs AB. Effect of experimental thermal stress on lipidomes of the soft coral Sinularia sp. and its symbiotic dinoflagellates. J Exp Mar Biol Ecol. 2020;524:151295.

    Google Scholar 

  32. Kabeya N, Fonseca MM, Ferrier DEK, Navarro JC, Bay LK, Francis DS, Tocher DR, Castro LFC, Monroig O. Genes for de novo biosynthesis of omega-3 polyunsaturated fatty acids are widespread in animals. Sci Adv. 2018;4(5):eaar6849.

    PubMed  PubMed Central  Google Scholar 

  33. Imbs AB, Latyshev NA, Dautova TN, Latypov YY. Distribution of lipids and fatty acids in corals by their taxonomic position and presence of zooxanthellae. Mar Ecol Prog Ser. 2010;409:65–77.

    CAS  Google Scholar 

  34. Graham EM, Baird AH, Connolly SR, Sewell MA, Willis BL. Uncoupling temperature-dependent mortality from lipid depletion for scleractinian coral larvae. Coral Reefs. 2017;36(1):97–104.

    Google Scholar 

  35. Oku H, Yamashiro H, Onaga K. Lipid biosynthesis from [C-14]-glucose in the coral Montipora digitata. Fisheries Sci. 2003;69(3):625–31.

    CAS  Google Scholar 

  36. Yamashiro H, Oku H, Onaga K. Effect of bleaching on lipid content and composition of Okinawan corals. Fisheries Sci. 2005;71(2):448–53.

    CAS  Google Scholar 

  37. Davy SK, Allemand D, Weis VM. Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol Mol Biol R. 2012;76(2):229–61.

    CAS  Google Scholar 

  38. Rosset S, Koster G, Brandsma J, Hunt AN, Postle AD, D’Angelo C. Lipidome analysis of Symbiodiniaceae reveals possible mechanisms of heat stress tolerance in reef coral symbionts. Coral Reefs. 2019;38(6):1241–53.

    Google Scholar 

  39. Berkelmans R, van Oppen MJH. The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change. Proc R Soc B Biol Sci. 2006;273(1599):2305–12.

    Google Scholar 

  40. Nunez-Pons L, Bertocci I, Baghdasarian G. Symbiont dynamics during thermal acclimation using cnidarian-dinoflagellate model holobionts. Mar Environ Res. 2017;130:303–14.

    CAS  PubMed  Google Scholar 

  41. d’Auriac IG, Quinn RA, Maughan H, Nothias LF, Little M, Kapono CA, Cobian A, Reyes BT, Green K, Quistad SD, Leray M, Smith JE, Dorrestein PC, Rohwer F, Deheyn DD, Hartmann AC. Before platelets: the production of platelet-activating factor during growth and stress in a basal marine organism. Proc R Soc B Biol Sci. 1884;2018(285):20181307.

    Google Scholar 

  42. van de Water JAJM, Ainsworth TD, Leggat W, Bourne DG, Willis BL, van Oppen MJH. The coral immune response facilitates protection against microbes during tissue regeneration. Mol Ecol. 2015;24(13):3390–404.

    PubMed  Google Scholar 

  43. Gombos Z, Wada H, Hideg E, Murata N. The unsaturation of membrane lipids stabilizes photosynthesis against heat stress. Plant Physiol. 1994;104(2):563–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Quinn PJ, Joo F, Vigh L. The role of unsaturated lipids in membrane structure and stability. Prog Biophys Mol Biol. 1989;53(2):71–103.

    CAS  PubMed  Google Scholar 

  45. Tchernov D, Gorbunov MY, de Vargas C, Yadav SN, Milligan AJ, Haggblom M, Falkowski PG. Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci USA. 2004;101(37):13531–5.

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Sila A, Bougatef A. Antioxidant peptides from marine by-products: Isolation, identification and application in food systems. A review J Funct Foods. 2016;21:10–26.

    CAS  Google Scholar 

  47. Wang YG, Zhu FR, Han FS, Wang HA. Purification and characterization of antioxidative peptides from Salmon protamine hydrolysate. J Food Biochem. 2008;32(5):654–71.

    CAS  Google Scholar 

  48. Sato K, Egashira Y, Ono S, Mochizuki S, Shimmura Y, Suzuki Y, Nagata M, Hashimoto K, Kiyono T, Park EY, Nakamura Y, Itabashi M, Sakata Y, Furuta S, Sanada H. Identification of a hepatoprotective peptide in wheat gluten hydrolysate against d-galactosamine-induced acute hepatitis in rats. J Agr Food Chem. 2013;61(26):6304–10.

    CAS  Google Scholar 

  49. Wada S, Sato K, Ohta R, Wada E, Bou Y, Fujiwara M, Kiyono T, Park EY, Aoi W, Takagi T, Naito Y, Yoshikawa T. Ingestion of low dose pyroglutamyl leucine improves dextran sulfate sodium-induced colitis and intestinal microbiota in mice. J Agr Food Chem. 2013;61(37):8807–13.

    CAS  Google Scholar 

  50. Tanzi RE, Moir RD, Wagner SL. Clearance of Alzheimer’s A beta peptide: the many roads to perdition. Neuron. 2004;43(5):605–8.

    CAS  PubMed  Google Scholar 

  51. Lodwig EM, Hosie AHF, Bordes A, Findlay K, Allaway D, Karunakaran R, Downie JA, Poole PS. Amino-acid cycling drives nitrogen fixation in the legume - Rhizobium symbiosis. Nature. 2003;422(6933):722–6.

    CAS  PubMed  Google Scholar 

  52. Pernice M, Meibom A, Van Den Heuvel A, Kopp C, Domart-Coulon I, Hoegh-Guldberg O, Dove S. A single-cell view of ammonium assimilation in coral-dinoflagellate symbiosis. Isme J. 2012;6(7):1314–24.

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Nandi PK, Bera A, Sizaret PY. Osmolyte trimethylamine N-oxide converts recombinant alpha-helical prion protein to its soluble beta-structured form at high temperature. J Mol Biol. 2006;362(4):810–20.

    CAS  PubMed  Google Scholar 

  54. Raymond JA, DeVries AL. Elevated concentrations and synthetic pathways of trimethylamine oxide and urea in some teleost fishes of McMurdo Sound. Antarctica Fish Physiol Biochem. 1998;18(4):387–98.

    CAS  Google Scholar 

  55. Wu WK, Chen CC, Liu PY, Panyod S, Liao BY, Chen PC, Kao HL, Kuo HC, Kuo CH, Chiu THT, Chen RA, Chuang HL, Huang YT, Zou HB, Hsu CC, Chang TY, Lin CL, Ho CT, Yu HT, Sheen LY, Wu MS. Identification of TMAO-producer phenotype and host-diet-gut dysbiosis by carnitine challenge test in human and germ-free mice. Gut. 2019;68(8):1439–49.

    CAS  PubMed  Google Scholar 

  56. Bourne D, Iida Y, Uthicke S, Smith-Keune C. Changes in coral-associated microbial communities during a bleaching event. Isme J. 2008;2(4):350–63.

    CAS  PubMed  Google Scholar 

Download references

Funding

This work was supported by the National Natural Science Foundation of China (Nos. 42090041, 21665003, 42030502) and the Guangxi Natural Science Fund Project (Nos. 2018GXNSFAA281354, AD17129063, and AA17204074).

Author information

Authors and Affiliations

  1. Coral Reef Research Center of China, Guangxi Laboratory On the Study of Coral Reefs in the South China Sea, School of Marine Sciences, Guangxi University, Nanning, Guangxi, 530000, People’s Republic of China

    Ji-Ying Pei, Wen-Feng Yu, Jing-Jing Zhang, Jun-Jie Hu & Ke-Fu Yu

  2. Department of Chemistry, National Taiwan University, Taipei, 10617, Taiwan

    Ting-Hao Kuo, Hsin-Hsiang Chung & Cheng-Chih Hsu

  3. Southern Marine Science and Engineering Guangdong Laboratory, Zhuhai, Guangdong, 519080, People’s Republic of China

    Ke-Fu Yu

Authors
  1. Ji-Ying Pei
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wen-Feng Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jing-Jing Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ting-Hao Kuo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hsin-Hsiang Chung
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jun-Jie Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Cheng-Chih Hsu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ke-Fu Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceived the project: J. Y. Pei, K. F. Yu. Obtained funding: K. F. Yu, J. Y. Pei. Mentorship: K. F. Yu. Field collections and indoor cultivation of corals: J. J. Zhang, W. F. Yu, J. J. Hu. Instrumental analysis: H. H. Chung. Bioinformatic analyses: J. Y. Pei, T. H. Kuo. Wrote the paper: J. Y. Pei, K. F. Yu, C. C. Hsu, T. H. Kuo.

Corresponding author

Correspondence to Ke-Fu Yu.

Ethics declarations

Ethics approval

All the animal protocols were approved by the Animal Care and Use Committee of Guangxi University (approval no. GXU–2022285).

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 2.55 MB)

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pei, JY., Yu, WF., Zhang, JJ. et al. Mass spectrometry–based metabolomic signatures of coral bleaching under thermal stress. Anal Bioanal Chem 414, 7635–7646 (2022). https://doi.org/10.1007/s00216-022-04294-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00216-022-04294-y

Keywords

Search

Navigation