Skip to main content
SpringerLink
Log in

Intra- and interspecific variation and phenotypic plasticity in thylakoid membrane properties across two Symbiodinium clades

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

Coral photosynthetic endosymbionts (Symbiodinium) are phylogenetically very diverse, yet the extent of inter- and intraspecific functional variation within clades remains largely underexplored. Understanding this variability will be critical for future research on climate change mediated responses. A properly functioning thylakoid membrane is essential for optimal photosynthetic performance both in free living and in hospite conditions. Here, we analyse the thylakoid membrane melting points of 13 Symbiodinium strains from species in Clades B and A, grown at both control (26 °C) and high temperature (31 °C). We observed a broad range of responses to thermal stress regardless of taxonomic rank. Our results support and augment a growing body of the literature demonstrating that functional differences among Symbiodinium spp. are as distinct at lower taxonomic levels (i.e. interspecific) as they are among major clades. These findings highlight the importance of assessing the variability of plastid traits across the Symbiodinium tree.

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

Similar content being viewed by others

References

  • Auld JR, Agrawal AA, Relyea RA (2010) Re-evaluating the costs and limits of adaptive phenotypic plasticity. Proc Biol Sci 277:503–511

    Article  PubMed  Google Scholar 

  • Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 661–689

  • Barber J, Ford R, Mitchell R, Millner P (1984) Chloroplast thylakoid membrane fluidity and its sensitivity to temperature. Planta 161:375–380

    Article  PubMed  CAS  Google Scholar 

  • Berry J, Bjorkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Biol 31:491–543

    Article  Google Scholar 

  • Blank R (1987) Cell architecture of the dinoflagellate Symbiodinium sp. inhabiting the Hawaiian stony coral Montipora verrucosa. Mar Biol 94:143–155

    Article  Google Scholar 

  • Blum A, Ebercon A (1981) Cell membrane stability as a measure of drought and heat tolerance in wheat. Crop Sci 21:43–47

    Article  Google Scholar 

  • Buxton L, Takahashi S, Hill R, Ralph PJ (2012) Variability in the primary site of photosynthetic damage in Symbiodinium sp. (dinophyceae) exposed to thermal stress. J Phycol 48:117–126

    Article  PubMed  CAS  Google Scholar 

  • Camejo D, Rodríguez P, Morales MA, Dell’Amico JM, Torrecillas A, Alarcón JJ (2005) High temperature effects on photosynthetic activity of two tomato cultivars with different heat susceptibility. Journal of plant physiology 162:281–289

    Article  PubMed  CAS  Google Scholar 

  • Coffroth MA, Santos SR (2005) Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156:19–34

    Article  PubMed  CAS  Google Scholar 

  • DeWitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81

    Article  PubMed  CAS  Google Scholar 

  • Díaz-Almeyda EM, Thomé P, El Hafidi M, Iglesias-Prieto R (2011) Differential stability of photosynthetic membranes and fatty acid composition at elevated temperature in Symbiodinium. Coral Reefs 30:217–225

    Article  Google Scholar 

  • Díaz-Almeyda EM, Prada C, Ohdera AH, Moran H, Civitello DJ, Iglesias-Prieto R, Carlo TA, LaJeunesse TC, Medina M (2017) Intraspecific and interspecific variation in thermotolerance and photoacclimation in Symbiodinium dinoflagellates. Proc R Soc B 284:20171767

    Article  PubMed  PubMed Central  Google Scholar 

  • Finney JC, Pettay DT, Sampayo EM, Warner ME, Oxenford HA, LaJeunesse TC (2010) The relative significance of host–habitat, depth, and geography on the ecology, endemism, and speciation of coral endosymbionts in the genus Symbiodinium. Microb Ecol 60:250–263

    Article  PubMed  Google Scholar 

  • Frade P, De Jongh F, Vermeulen F, Van Bleijswijk J, Bak R (2008) Variation in symbiont distribution between closely related coral species over large depth ranges. Mol Ecol 17:691–703

    Article  PubMed  CAS  Google Scholar 

  • Freudenthal HD (1962) Symbiodinium gen. nov. and Symbiodinium microadriaticum sp. nov., a Zooxanthella: Taxonomy, Life Cycle, and Morphology. J Eukaryot Microbiol 9:45–52

    Google Scholar 

  • Gates RD, Baghdasarian G, Muscatine L (1992) Temperature stress causes host cell detachment in symbiotic cnidarians: implications for coral bleaching. The Biological Bulletin 182:324–332

    Article  PubMed  CAS  Google Scholar 

  • Goulet TL, Cook CB, Goulet D (2005) Effect of short-term exposure to elevated temperatures and light levels on photosynthesis of different host-symbiont combinations in the Aiptasia pallida/Symbiodinium symbiosis. Limnol Oceanogr 50:1490–1498

    Article  CAS  Google Scholar 

  • Goyen S, Pernice M, Szabó M, Warner ME, Ralph PJ, Suggett DJ (2017) A molecular physiology basis for functional diversity of hydrogen peroxide production amongst Symbiodinium spp. (Dinophyceae). Mar Biol 164:46

    Article  CAS  Google Scholar 

  • Hennige S, Suggett DJ, Warner ME, McDougall K, Smith DJ (2009) Photobiology of Symbiodinium revisited: bio-physical and bio-optical signatures. Coral Reefs 28:179–195

    Article  Google Scholar 

  • Hill R, Ulstrup KE, Ralph PJ (2009) Temperature induced changes in thylakoid membrane thermostability of cultured, freshly isolated, and expelled zooxanthellae from scleractinian corals. Bull Mar Sci 85:223–244

    Google Scholar 

  • Hoegh-Guldberg O, McCloskey L, Muscatine L (1987) Expulsion of zooxanthellae by symbiotic cnidarians from the Red Sea. Coral Reefs 5:201–204

    Article  Google Scholar 

  • Hoegh-Guldberg O (2011) Coral reef ecosystems and anthropogenic climate change. Reg Environ Change 11:215–227

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Howells E, Beltran V, Larsen N, Bay L, Willis B, Van Oppen M (2012) Coral thermal tolerance shaped by local adaptation of photosymbionts. Nat Clim Chang 2:116–120

    Article  Google Scholar 

  • Hume BC, D’Angelo C, Smith EG, Stevens JR, Burt J, Wiedenmann J (2015) Symbiodinium thermophilum sp. nov., a thermotolerant symbiotic alga prevalent in corals of the world’s hottest sea, the Persian/Arabian Gulf. Scientific Reports 5:8562

  • Iglesias-Prieto R, Trench R (1997) Acclimation and adaptation to irradiance in symbiotic dinoflagellates. II. Response of chlorophyll–protein complexes to different photon-flux densities. Mar Biol 130:23–33

    Article  CAS  Google Scholar 

  • Iglesias-Prieto R, Matta JL, Robins WA, Trench RK (1992) Photosynthetic response to elevated temperature in the symbiotic dinoflagellate Symbiodinium microadriaticum in culture. Proc Natl Acad Sci U S A 89:10302–10305

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kolber ZS, Prášil O, Falkowski PG (1998) Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols. Biochim Biophys Acta Bioenerg 1367:88–106. https://doi.org/10.1016/S0005-2728(98)00135-2

    Article  CAS  Google Scholar 

  • Kusnetsov V, Mikulovich T, Kukina I, Cherepneva G, Herrmann R, Kulaeva O (1993) Changes in the level of chloroplast transcripts in pumpkin cotyledons during heat shock. FEBS Lett 321:189–193

    Article  PubMed  CAS  Google Scholar 

  • LaJeunesse TC (2001) Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region: in search of a “species” level marker. J Phycol 37:866–880

    Article  CAS  Google Scholar 

  • LaJeunesse TC, Lee SY, Gil-Agudelo DL, Knowlton N, Jeong HJ (2015) Symbiodinium necroappetens sp. nov. (Dinophyceae): an opportunist ‘zooxanthella’ found in bleached and diseased tissues of Caribbean reef corals. Eur J Phycol 50:223–238

    Article  Google Scholar 

  • LaJeunesse TC, Loh WK, Van Woesik R, Hoegh-Guldberg O, Schmidt GW, Fitt WK (2003) Low symbiont diversity in southern Great Barrier Reef corals, relative to those of the Caribbean. Limnol Oceanogr 48:2046–2054

    Article  Google Scholar 

  • LaJeunesse TC, Parkinson JE, Reimer JD (2012) A genetics-based description of Symbiodinium minutum sp. nov. and S. psygmophilum sp. nov. (Dinophyceae), two dinoflagellates symbiotic with cnidaria. J Phycol 48:1380–1391

    Article  PubMed  Google Scholar 

  • LaJeunesse TC, Wham DC, Pettay DT, Parkinson JE, Keshavmurthy S, Chen CA (2014) Ecologically differentiated stress-tolerant endosymbionts in the dinoflagellate genus Symbiodinium (Dinophyceae) Clade D are different species. Phycologia 53:305–319

    Article  Google Scholar 

  • Lajeunesse TC (2005) “Species” radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Mol Biol Evol 22:570–581

    Article  PubMed  CAS  Google Scholar 

  • Lee SY, Jeong HJ, Kang NS, Jang TY, Jang SH, Lajeunesse TC (2015) Symbiodinium tridacnidorum sp. nov., a dinoflagellate common to Indo-Pacific giant clams, and a revised morphological description of Symbiodinium microadriaticum Freudenthal, emended Trench & Blank. Eur J Phycol 50:155–172

    Article  Google Scholar 

  • Levin RA, Beltran VH, Hill R, Kjelleberg S, McDougald D, Steinberg PD, van Oppen MJ (2016) Sex, Scavengers, and Chaperones: Transcriptome Secrets of Divergent Symbiodinium Thermal Tolerances. Mol Biol Evol 33:2201–2215

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mayley G (1996) Landscapes, learning costs, and genetic assimilation. Evol Comput 4:213–234

    Article  Google Scholar 

  • McGinley MP, Aschaffenburg MD, Pettay DT, Smith RT, LaJeunesse TC, Warner ME (2012) Transcriptional response of two core photosystem genes in Symbiodinium spp. exposed to thermal stress. PLoS One 7:e50439

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Muller-Parker G, Davy SK (2001) Temperate and tropical algal-sea anemone symbioses. Invertebr Biol 120:104–123

    Article  Google Scholar 

  • Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27:454–460

    Article  Google Scholar 

  • Oliver TA, Palumbi SR (2009) Distributions of stress-resistant coral symbionts match environmental patterns at local but not regional scales. Mar Ecol Prog Ser 378:93–103

    Article  CAS  Google Scholar 

  • Parkinson JE, Coffroth MA, LaJeunesse TC (2015) New species of Clade B Symbiodinium (Dinophyceae) from the greater Caribbean belong to different functional guilds: S. aenigmaticum sp. nov., S. antillogorgium sp. nov., S. endomadracis sp. nov., and S. pseudominutum sp. nov. J Phycol 51:850–858

    Article  PubMed  Google Scholar 

  • Parkinson JE, Baumgarten S, Michell CT, Baums IB, LaJeunesse TC, Voolstra CR (2016) Gene Expression Variation Resolves Species and Individual Strains among Coral-Associated Dinoflagellates within the Genus Symbiodinium. Genome Biol Evol 8:665–680

    Article  PubMed  PubMed Central  Google Scholar 

  • Pochon X, Gates RD (2010) A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai’i. Mol Phylogenet Evol 56:492–497

    Article  PubMed  CAS  Google Scholar 

  • Pochon X, Pawlowski J, Zaninetti L, Rowan R (2001) High genetic diversity and relative specificity among Symbiodinium-like endosymbiotic dinoflagellates in soritid foraminiferans. Mar Biol 139:1069–1078

    Article  Google Scholar 

  • Prezelin BB, Sweeney BM (1977) Characterization of Photosynthetic Rhythms in Marine Dinoflagellates: II. Photosynthesis-Irradiance Curves and in Vivo Chlorophyll a Fluorescence. Plant Physiol 60:388–392

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ralph PJ, Gademann R, Larkum AW (2001) Zooxanthellae expelled from bleached corals at 33°C are photosynthetically competent. Mar Ecol Prog Ser 220:163–168

    Article  CAS  Google Scholar 

  • Rowan R (2004) Coral bleaching: thermal adaptation in reef coral symbionts. Nature 430:742–742.

  • Rowan R, Knowlton N, Baker A, Jara J (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388:265

    Article  PubMed  CAS  Google Scholar 

  • Rowan R, Powers DA (1991) Molecular genetic identification of symbiotic dinoflagellates (zooxanthellae). Mar Ecol Prog Ser 71:65–73

    Article  CAS  Google Scholar 

  • Rowan R, Knowlton N (1995) Intraspecific diversity and ecological zonation in coral-algal symbiosis. Proc Natl Acad Sci U S A 92:2850–2853

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Santos SR, Taylor DJ, Kinzie Iii RA, Hidaka M, Sakai K, Coffroth MA (2002) Molecular phylogeny of symbiotic dinoflagellates inferred from partial chloroplast large subunit (23S)-rDNA sequences. Mol Phylogenet Evol 23:97–111

    Article  PubMed  CAS  Google Scholar 

  • Savage A, Goodson M, Visram S, Trapido-Rosenthal H, Wiedenmann J, Douglas A (2002a) Molecular diversity of symbiotic algae at the latitudinal margins of their distribution: dinoflagellates of the genus Symbiodinium in corals and sea anemones. Mar Ecol Prog Ser 244:17–26

    Article  Google Scholar 

  • Savage A, Trapido-Rosenthal H, Douglas A (2002b) On the functional significance of molecular variation in Symbiodinium, the symbiotic algae of Cnidaria: photosynthetic response to irradiance. Mar Ecol Prog Ser 244:27–37

    Article  Google Scholar 

  • Sawall Y, Al-Sofyani A, Hohn S, Banguera-Hinestroza E, Voolstra CR, & Wahl M (2015) Extensive phenotypic plasticity of a Red Sea coral over a strong latitudinal temperature gradient suggests limited acclimatization potential to warming. Scientific Reports, 5: https://doi.org/10.1038/srep08940

  • Scheufen T, Krämer WE, Iglesias-Prieto R, Enríquez S (2017) Seasonal variation modulates coral sensibility to heat-stress and explains annual changes in coral productivity. Scientific Reports 7:4937

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schreiber U, Berry JA (1977) Heat-induced changes of chlorophyll fluorescence in intact leaves correlated with damage of the photosynthetic apparatus. Planta 136:233–238

    Article  PubMed  CAS  Google Scholar 

  • Sorek M, & Levy O (2012) The effect of temperature compensation on the circadian rhythmicity of photosynthesis in Symbiodinium, coral-symbiotic alga. Scientific Reports, 2: https://doi.org/10.1038/srep00536

  • Suggett DJ, Goyen S, Evenhuis C, Szabó M, Pettay DT, Warner ME, Ralph PJ (2015) Functional diversity of photobiological traits within the genus Symbiodinium appears to be governed by the interaction of cell size with cladal designation. New Phytol 208:370–381

    Article  PubMed  Google Scholar 

  • Suggett DJ, Warner ME, Leggat W (2017) Symbiotic dinoflagellate functional diversity mediates coral survival under ecological crisis. Trends Ecol Evol 32:735–745

    Article  PubMed  Google Scholar 

  • Swain TD, Chandler J, Backman V, Marcelino L (2017) Consensus thermotolerance ranking for 110 Symbiodinium phylotypes: an exemplar utilization of a novel iterative partial rank aggregation tool with broad application potential. Funct Ecol 31:172–183

    Article  Google Scholar 

  • Takahashi S, Yoshioka-Nishimura M, Nanba D, Badger MR (2013) Thermal acclimation of the symbiotic alga Symbiodinium spp. alleviates photobleaching under heat stress. Plant Physiol 161:477–485

    Article  PubMed  CAS  Google Scholar 

  • Tchernov D, Gorbunov MY, de Vargas C, Narayan Yadav S, Milligan AJ, Haggblom M, Falkowski PG (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci U S A 101:13531–13535

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Thornhill DJ, Kemp DW, Bruns BU, Fitt WK, Schmidt GW (2008) Correspondence between cold tolerance and temperate biogeography in a western Atlantic Symbiodinium (Dinophyta) lineage. J Phycol 44:1126–1135. https://doi.org/10.1111/j.1529-8817.2008.00567.x

    Article  PubMed  CAS  Google Scholar 

  • Valladares F, Gianoli E, Gómez JM (2007) Ecological limits to plant phenotypic plasticity. New Phytol 176:749–763

    Article  PubMed  Google Scholar 

  • Warner ME, & Suggett DJ. (2016). The Photobiology of Symbiodinium spp.: Linking Physiological Diversity to the Implications of Stress and Resilience. The Cnidaria, Past, Present and Future. Springer, pp. 489–509

  • Warner ME, Fitt WK, Schmidt GW (1999) Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc Natl Acad Sci U S A 96:8007–8012

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wilkinson, C (Ed.). (2008). Status of coral reefs of the world: 2008. Global Coral Reef Monitoring Network and Reef and Rainforest Research Centre,. Townsville, Australia,296

  • Ziegler M, Arif C, Burt JA, Dobretsov S, Roder C, LaJeunesse TC, Voolstra CR (2017) Biogeography and molecular diversity of coral symbionts in the genus Symbiodinium around the Arabian Peninsula. J Biogeogr 44:674–686

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank Todd C. LaJeunesse for providing input throughout the project as well as the Symbiodinium phylogeny. We thank Allison M. Lewis for preparing and sharing The LaJeunesse lab Symbiodinium cultures. We also thank the members of the Medina and Iglesias-Prieto labs for their support during the experiments and for input on the manuscript, as well as David Suggett and reviewers for reviewing and for providing comments that improved the manuscript. This document was written in partial fulfilment of Joost Mansour’s masters thesis at the University of Amsterdam. This work was supported by NSF Grants OCE 1442206 and OCE 1642311.

Author information

Authors and Affiliations

  1. University of Amsterdam, Amsterdam, The Netherlands

    Joost S. Mansour

  2. Department of Biology, Pennsylvania State University, 208 Mueller Lab, University Park, PA, 16802, USA

    F. Joseph Pollock, Roberto Iglesias-Prieto & Mónica Medina

  3. Emory University, Atlanta, GA, USA

    Erika Díaz-Almeyda

Authors
  1. Joost S. Mansour
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. F. Joseph Pollock
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Erika Díaz-Almeyda
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Roberto Iglesias-Prieto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mónica Medina
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Joost S. Mansour or Mónica Medina.

Additional information

Topic Editor Simon Davy

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM Fig. 1

Temperature-dependent melting curves of photosynthetic membranes for tested Symbiodinium strains. 8.33*104 cells ml−1 in 100 μl samples were incubated in a thermal cycler for five minutes at increasing temperatures. Photochemical efficiency (Fv/Fm) was measured after the five minutes of incubation at each temperature. Fluorescence parameters of PSII are plotted as relative to respective maximum. For each strain is depicted: Fv/Fm (dots); 4 parameter sigmoidal curve fit (line); 95% confidence limits of the 4p sigmoidal curve fit (dotted lines). In red are represented cultures with a high temperature treatment of 1.5 days at 31 °C, in blue cultures kept at 26 °C. Data was collected from three replicate experiments per temperature, using the same culture. (EPS 20694 kb)

ESM Fig. 2

Temperature-dependent melting curves of photosynthetic membranes for tested Symbiodinium species. Per species is depicted the mean Fv/Fm (dots) of data from all respective strains per replicate experiment; four-parameter sigmoidal curve fit (line); 95% confidence limits of the 4p sigmoidal curve fit (dotted lines). In red are represented cultures with a high temperature treatment of 1.5 days at 31 °C, in blue cultures kept at 26 °C. Data was collected from three replicate experiments per temperature, using the same culture. (EPS 5668 kb)

Supplementary material 3 (DOCX 35 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mansour, J.S., Pollock, F.J., Díaz-Almeyda, E. et al. Intra- and interspecific variation and phenotypic plasticity in thylakoid membrane properties across two Symbiodinium clades. Coral Reefs 37, 841–850 (2018). https://doi.org/10.1007/s00338-018-1710-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-018-1710-1

Keywords

Search

Navigation