Marine Biotechnology

, Volume 21, Issue 2, pp 151–160 | Cite as

Gene Expression Profiles of Two Coral Species with Varied Resistance to Ocean Acidification

  • Xiangcheng YuanEmail author
  • Hui HuangEmail author
  • Weihua Zhou
  • Yajuan Guo
  • Tao Yuan
  • Sheng Liu
Original Article


Recent studies have indicated that various corals might have different degrees of resistance to elevated CO2 levels. However, the underlying molecular mechanism accounting for these differences is still poorly understood. In this study, RNA-seq data were analyzed to identify differentially expressed genes in two coral species (Acropora austera and Acropora cerealis) in response to high CO2 levels. The calcification rates were higher in high CO2 treatment than the control in A. austera, but was not significantly different in A. cerealis. A KEGG database search revealed that in both coral species, most Ca2+ transporters were present in the calcium signaling pathway, which could be important in the CO2 regulation of coral calcification. The gene expression levels of many CO2 and HCO3 transporters were not affected by elevated CO2. Nevertheless, high CO2 levels did have an effect on the expression of certain Ca2+ transporters. The upregulation of Ca2+ transporters likely explained the higher resistance of A. austera to high CO2 than A. cerealis.


Calcium signaling pathway CO2 Coral Coral calcifying fluid Oceanic acidification 



We thank the Strategic Priority Research Program of the Chinese Academy of Sciences and the National Key Technology R&D Program for their financial assistance (Grant Nos. XDA13020403 and 2014BAC01B03, respectively). Thank Y.L. Gao for comments.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflicts of interest.

Supplementary material

10126_2018_9864_MOESM1_ESM.docx (1.3 mb)
ESM 1 (DOCX 1324 kb)


  1. Albright R (2011) Reviewing the effects of ocean acidification on sexual reproduction and early life history stages of reef-building corals. J Mar Biol 14:1–14CrossRefGoogle Scholar
  2. Bertucci A, Moya A, Tambutté S, Allemand D, Supuran CT, Zoccola D (2013) Carbonic anhydrases in anthozoan corals-a review. Bioorg Med Chem 21:1437–1450CrossRefGoogle Scholar
  3. Cohen AL, Mccorkle DC, Putron SD, Gaetani GA, Rose KA (2009) Morphological and compositional changes in the skeletons of new coral recruits reared in acidified seawater: insights into the biomineralization response to ocean acidification. Geochem Geophy Geosyst 10:217–222CrossRefGoogle Scholar
  4. Comeau S, Tambutté E, Carpenter RC, Edmunds PJ, Evensen NR, Allemand D, Ferrier-Pagès C, Tambutté S, Venn AA (2017) Coral calcifying fluid pH is modulated by seawater carbonate chemistry not solely seawater pH. Proc Biol Sci 284.
  5. De Beer D, Kühl M, Stambler N, Vaki L (2000) A microsensor study of light enhanced Ca2+ uptake and photosynthesis in the reef-building hermatypic coral Favia sp. Mar Ecol Prog Ser 194:75–85CrossRefGoogle Scholar
  6. Desalvo MK, Voolstra CR, Sunagawa S, Schwarz JA, Stillman JH, Coffroth MA, Szmant AM, Medina M (2008) Differential gene expression during thermal stress and bleaching in the Caribbean coral Montastraea faveolata. Mol Ecol 17:3952–3971CrossRefGoogle Scholar
  7. Dickson AG, Sabine CL, Christian JR (2007) Determination of total alkalinity in sea water using an open-cell titration: guide to best practices for ocean CO2 measurements. Pices Special Publication 3, IOCCP Report No 8:1–16Google Scholar
  8. 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 18:710CrossRefGoogle Scholar
  9. Georgiou L, Falter J, Trotter J, Kline DI, Holcomb M, Dove SG, Hoegh-Guldberg O, Mcculloch M (2015) pH homeostasis during coral calcification in a free ocean CO2 enrichment (FOCE) experiment, Heron Island reef flat, Great Barrier Reef. Proc Natl Acad Sci U S A 112:13219CrossRefGoogle Scholar
  10. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Xian A, Fan L, Raychowdhury R, Zeng Q (2011) Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nat Biotechnol 29:644CrossRefGoogle Scholar
  11. Guppy M, Withers P (1999) Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biol Rev Camb Philos Soc 74:1–40CrossRefGoogle Scholar
  12. Hou J, Xu T, Su D, Wu Y, Cheng L, Wang J, Zhou Z, Wang Y (2018) RNA-Seq reveals extensive transcriptional response to heat stress in the stony coral Galaxea fascicularis. Front Genet 9:37CrossRefGoogle Scholar
  13. Huang H, Yuan X, Cai W, Zhang C, Li X, Liu S (2014) Positive and negative responses of coral calcification to elevated pCO2: case studies of two coral species and the implications of their responses. Mar Ecol Prog Ser 502:145–156CrossRefGoogle Scholar
  14. Inoue N, Ishibashi R, Ishikawa T, Atsumi T, Aoki H, Komaru A (2011) Gene expression patterns in the outer mantle epithelial cells associated with pearl sac formation. Mar Biotechnol 13:474–483CrossRefGoogle Scholar
  15. Kanehisa M, Goto S, Sato Y, Kawashima M, Furumichi M, Tanabe M (2014) Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res 42:199–205CrossRefGoogle Scholar
  16. Kaniewska P, Campbell PR, Kline DI, Rodriguez-Lanetty M, Miller DJ, Dove S, Hoegh-Guldberg O (2012) Major cellular and physiological impacts of ocean acidification on a reef building coral. PLoS One 7:ARTN e34659CrossRefGoogle Scholar
  17. Kenkel CD, Matz MV (2016) Gene expression plasticity as a mechanism of coral adaptation to a variable environment. Nat Ecol Evol 1:14CrossRefGoogle Scholar
  18. Kleypas JA, Feely RA, Fabry VJ, Langdon C, Sabine CLRobbins LL (2006) Impacts of ocean acidification on coral reefs and other marine calcifiers. A Guide for Future Research. Report of a workshop sponsored by NSF, NOAA & USGSGoogle Scholar
  19. Kleypas JA, Anthony K, Gattuso JP (2011) Coral reefs modify their seawater carbon chemistry–case study from a barrier reef (Moorea, French Polynesia). Glob Chang Biol 17:3667–3678CrossRefGoogle Scholar
  20. Langdon C, Atkinson M (2005) Effect of elevated pCO2 on photosynthesis and calcification of corals and interactions with seasonal change in temperature/irradiance and nutrient enrichment. J Geophys Res 110:C09S07CrossRefGoogle Scholar
  21. Lee STM, Keshavmurthy S, Fontana S, Takuma M, Chou WH, Chen CA (2018) Transcriptomic response in Acropora muricata under acute temperature stress follows preconditioned seasonal temperature fluctuations. BMC Res Notes 11:119CrossRefGoogle Scholar
  22. Levy O, Karako-Lampert S, Ben-Asher HW, Zoccola D, Pages G, Ferrier-Pages C (2016) Molecular assessment of the effect of light and heterotrophy in the scleractinian coral Stylophora pistillata. Proc Biol Sci 283:Artn20153025CrossRefGoogle Scholar
  23. Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12:323CrossRefGoogle Scholar
  24. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408CrossRefGoogle Scholar
  25. Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550CrossRefGoogle Scholar
  26. Masako N, Masaya M, Haruko K, Satoshi M (2012) Expression of hsp70,hsp90 and hsf1in the reef coral Acropora digitifera under prospective acidified conditions over the next several decades. Biol Open 1:75–81CrossRefGoogle Scholar
  27. Mayfield AB, Wang YB, Chen CS, Chen SH, Lin CY (2016) Dual-compartmental transcriptomic+proteomic analysis of a marine endosymbiosis exposed to environmental change. Mol Ecol 25.
  28. Mcculloch M, Falter J, Trotter J, Montagna P (2012) Coral resilience to ocean acidification and global warming through pH up-regulation. Nat Clim Chang 2:623–627CrossRefGoogle Scholar
  29. Moya A, Huisman L, Foret S, Gattuso JP, Hayward DC, Ball EE, Miller DJ (2015) Rapid acclimation of juvenile corals to CO2-mediated acidification by upregulation of heat shock protein and Bcl-2 genes. Mol Ecol 24:438–452CrossRefGoogle Scholar
  30. Ogawa D, Bobeszko T, Ainsworth T, Leggat W (2013) The combined effects of temperature and CO2 lead to altered gene expression in Acropora aspera. Coral Reefs 32:895–907CrossRefGoogle Scholar
  31. Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL (2011) Projecting coral reef futures under global warming and ocean acidification. Science 333:418CrossRefGoogle Scholar
  32. Pertea G, Huang X, Liang F, Antonescu V, Sultana R, Karamycheva S, Lee Y, White J, Cheung F, Parvizi B (2003) TIGR gene indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics 19:651–652CrossRefGoogle Scholar
  33. Pierrot, D., Lewis, E., Wallace, R., Wallace, D., Wallace, W. Wallace, D.W.R. (2006). MS excel program developed for CO2 system calculationsGoogle Scholar
  34. Putnam HM, Mayfield AB, Fan TY, Chen CS, Gates RD (2013) The physiological and molecular responses of larvae from the reef-building coral Pocillopora damicornis exposed to near-future increases in temperature and pCO2. Mar Biol 160:2157–2173CrossRefGoogle Scholar
  35. Reyes-Bermudez A, Lin ZY, Hayward DC, Miller DJ, Ball EE (2009) Differential expression of three galaxin-related genes during settlement and metamorphosis in the scleractinian coral Acropora millepora. BMC Evol Biol 9.
  36. Riebesell U, Fabry VJ, Hansson L, Gattuso JP (2011) Guide to best practices for ocean acidification research and data reporting. Oceanography 22:260Google Scholar
  37. Ries JB (2011) A physicochemical framework for interpreting the biological calcification response to CO2-induced ocean acidification. Geochim Cosmochim Acta 75:4053–4064CrossRefGoogle Scholar
  38. Rocker MM, Noonan S, Humphrey C, Moya A, Willis BL, Bay LK (2015) Expression of calcification and metabolism-related genes in response to elevated pCO2 and temperature in the reef-building coral Acropora millepora. Mar Genomics 24:313–318CrossRefGoogle Scholar
  39. Schoepf V, Grottoli AG, Warner ME, Cai WJ, Melman TF, Hoadley KD, Pettay DT, Hu X, Li Q, Xu H, Wang Y, Matsui Y, Baumann JH (2013) Coral energy reserves and calcification in a high-CO2 world at two temperatures. PLoS One 8:e75049CrossRefGoogle Scholar
  40. Schoepf V, Jury CP, Toonen RJ, Mcculloch MT (2017) Coral calcification mechanisms facilitate adaptive responses to ocean acidification. Proc Biol Sci 284:20172117CrossRefGoogle Scholar
  41. Takeuchi T, Yamada L, Shinzato C, Sawada H, Satoh N (2016) Stepwise evolution of coral biomineralization revealed with genome-wide proteomics and transcriptomics. PLoS One 11:e0156424CrossRefGoogle Scholar
  42. Tambutté, , Allemand, D., Mueller, E. Jaubert, J. (1996). A compartmental approach to the mechanism of calcification in hermatypic corals. J Exper Biol 199:1029–1041Google Scholar
  43. Wall M, Fietzke J, Schmidt GM, Fink A, Hofmann LC, De BD, Fabricius KE (2016) Internal pH regulation facilitates in situ long-term acclimation of massive corals to end-of-century carbon dioxide conditions. Sci Rep 6:30688CrossRefGoogle Scholar
  44. Wang L, Feng Z, Wang X, Wang X, Zhang X (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26:136–138CrossRefGoogle Scholar
  45. Weber MX, Medina M (2012) The role of microalgal symbionts (Symbiodinium) in holobiont physiology. Adv Bot Res 64:119–140CrossRefGoogle Scholar
  46. Xiang LX, Ding H, Dong WR, Zhang YW, Shao JZ (2010) Deep sequencing-based transcriptome profiling analysis of bacteria-challenged Lateolabrax japonicus reveals insight into the immune-relevant genes in marine fish. BMC Genomics 11:472CrossRefGoogle Scholar
  47. Yuan X, Yuan T, Huang H, Jiang L, Zhou W, Liu S (2018) Elevated CO2 delays the early development of scleractinian coral Acropora gemmifera. Sci Rep 8:2787CrossRefGoogle Scholar
  48. Zhang Y, Sun J, Mu H, Lun JC, Qiu JW (2017) Molecular pathology of skeletal growth anomalies in the brain coral Platygyra carnosa: a meta-transcriptomic analysis. Mar Pollut Bull 124(2):660–667CrossRefGoogle Scholar
  49. Zoccola D, Tambutté E, Sénégas-Balas F, Michiels JF, Failla JP, Jaubert J, Allemand D (1999) Cloning of a calcium channel α1 subunit from the reef-building coral, Stylophora pistillata. Gene 227:157–167CrossRefGoogle Scholar
  50. Zoccola D, Tambutte E, Kulhanek E, Puverel S, Scimeca JC, Allemand D, Tambutte S (2004) Molecular cloning and localization of a PMCA P-type calcium ATPase from the coral Stylophora pistillata. BBA-Biomembranes 1663:117–126Google Scholar
  51. Zoccola D, Ganot P, Bertucci A, Caminiti-Segonds N, Techer N, Voolstra CR, Aranda M, Tambutte E, Allemand D, Casey JR, Tambutte S (2015) Bicarbonate transporters in corals point towards a key step in the evolution of cnidarian calcification. Sci Rep 5.

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Key Laboratory of Tropical Marine Bio-resources and Ecology, South China Sea Institute of OceanologyChinese Academy of SciencesGuangzhouChina
  2. 2.Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of OceanologyChinese Academy of SciencesGuangzhouChina
  3. 3.Tropical Marine Biological Research Station in HainanChinese Academy of SciencesSanyaChina
  4. 4.Equipment Public Service Center, South China Sea Institute of OceanologyChinese Academy of SciencesGuangzhouChina

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