Hostname: page-component-77c89778f8-7drxs Total loading time: 0 Render date: 2024-07-16T19:27:55.775Z Has data issue: false hasContentIssue false
  • English
  • Français

Symbiodinium thermophilum symbionts in Porites harrisoni and Cyphastrea microphthalma in the northern Persian Gulf, Iran

Published online by Cambridge University Press:  26 October 2017

Tooba Varasteh ,
Mohammad Reza Shokri ,
Hassan Rajabi-Maham ,
Safoura Behzadi  and
Benjamin C. C. Hume
Tooba Varasteh
Affiliation:
Faculty of Life Sciences and Biotechnology, Shahid Beheshti University, G.C., Evin, Tehran, 1983963113, IR Iran
Mohammad Reza Shokri*
Affiliation:
Faculty of Life Sciences and Biotechnology, Shahid Beheshti University, G.C., Evin, Tehran, 1983963113, IR Iran
Hassan Rajabi-Maham*
Affiliation:
Faculty of Life Sciences and Biotechnology, Shahid Beheshti University, G.C., Evin, Tehran, 1983963113, IR Iran
Safoura Behzadi
Affiliation:
Faculty of Life Sciences and Biotechnology, Shahid Beheshti University, G.C., Evin, Tehran, 1983963113, IR Iran
Benjamin C. C. Hume
Affiliation:
Coral Reef Laboratory, Ocean and Earth Science, University of Southampton, Waterfront Campus, National Oceanography Centre, Southampton SO14 3ZH, UK
*
Correspondence should be addressed to: M. R. Shokri and H. Rajabi-Maham, Faculty of Life Sciences and Biotechnology, Shahid Beheshti University, G.C., Evin, Tehran, 1983963113, IR Iran email: M_Shokri@sbu.ac.ir and H_Rajabi@sbu.ac.ir
Correspondence should be addressed to: M. R. Shokri and H. Rajabi-Maham, Faculty of Life Sciences and Biotechnology, Shahid Beheshti University, G.C., Evin, Tehran, 1983963113, IR Iran email: M_Shokri@sbu.ac.ir and H_Rajabi@sbu.ac.ir
Get access Rights & Permissions [Opens in a new window]

Abstract

Coral communities of the Persian Gulf (PG) withstand maximum and annual ranges of water temperatures that surpass those found on the majority of reefs elsewhere. As such, these communities may inform on how coral reefs might adapt to the warmer waters of the future. Depending on the algal symbiont (genus Symbiodinium) harboured, advantages in stress tolerance may be conferred to the coral holobiont. Characterizing the algal component is therefore critical in determining the coral holobiont's tolerance phenotype. Coral associations off the Arabian coastline of the PG have been characterized as biogeographically unique, containing a rare group of taxonomically ancestral and thermotolerant algal symbionts, the Symbiodinium thermophilum group. In contrast, waters off the Iranian coast remain poorly characterized with a notable lack of S. thermophilum group symbionts identified in coral associations to date. Here, we characterize the algal component of two reef building corals (Porites harrisoni and Cyphastrea microphthalma) predominant at three sites spanning almost the entire length of the PG's Iranian coast. Genotyping using the chloroplastic 23S and nuclear ITS2 genes, we demonstrate the presence of S. thermophilum group symbionts. We discuss the probable physical drivers of these associations and highlight the need for further research in these relatively understudied waters.

Keywords

SymbiodiniumPersian Gulfcoralclimate changeadaptationIran
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 98 , Special Issue 8: Special Section: European Marine Biology Symposium Papers 2018 , December 2018 , pp. 2067 - 2073
Copyright
Copyright © Marine Biological Association of the United Kingdom 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Baker, A.C. (1999) The symbiosis ecology of reef-building corals. PhD thesis. University of Miami, Miami, FL, USA.Google Scholar
Baker, A.C., Starger, C.J., McClanahan, T.R. and Glynn, P.W. (2004) Coral reefs: corals’ adaptive response to climate change. Nature 430, 741.Google Scholar
Coles, S.L. (2003) Coral species diversity and environmental factors in the Arabian Gulf and the Gulf of Oman: a comparison to the Indo-Pacific region. Atoll Research Bulletin 507, 1–19.Google Scholar
D'Angelo, C., Hume, B.C.C., Burt, J., Smith, E.G., Achterberg, E.P. and Wiedenmann, J. (2015) Local adaptation constrains the distribution potential of heat-tolerant Symbiodinium from the Persian/Arabian Gulf. International Society for Microbial Ecology 9, 2551–2560.Google Scholar
Forsman, Z.H., Barshis, D.J., Hunter, C.L. and Toonen, R.J. (2009) Shape-shifting corals: molecular markers show morphology is evolutionarily plastic in Porites. BMC Evolutionary Biology 9, 45.Google Scholar
Hume, B.C.C., D'Angelo, C., Burt, J., Baker, A.C., Riegl, B. and Wiedenmann, J. (2013) Corals from the Persian/Arabian Gulf as models for thermotolerant reef-builders: prevalence of clade C3 Symbiodinium, host fluorescence and ex situ temperature tolerance. Marine Pollution Bulletin 72, 313–322.Google Scholar
Hume, B.C.C., D'Angelo, C., Smith, E.G., Stevens, J.R., Burt, J. and 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.Google Scholar
Hume, B.C.C., Voolstra, C.R., Arif, C., D'Angelo, C., Burt, J.A., Eyal, G., Loya, Y. and Wiedenmann, J. (2016) Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change. Proceedings of the National Academy of Sciences USA 113, 4416–4421.Google Scholar
Johns, W.E., Jacobs, G.A., Kindle, J.C., Murray, S.P. and Carron, M. (1999) Arabian marginal seas and gulfs: Report of a workshop held at Stennis Space Center, Mississippi, May 11–13, 1999. University of Miami RSMAS Technical Report, 2000-01, 66 pp.Google Scholar
Jones, A.M. and Berkelmans, R. (2011) Tradeoffs to thermal acclimation: energetics and reproduction of a reef coral with heat tolerant Symbiodinium type-D. Journal of Marine Biology 2011, 885–890.Google Scholar
Jones, A.M., Berkelmans, R., van Oppen, M.J.H., Mieog, J.C. and Sinclair, W. (2008) A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proceedings of the Royal Society B: Biological Sciences 275, 1359–1365.Google Scholar
Koupaei, A.N., Dehghani, H., Mostafavi, P.G. and Mashini, A.G. (2016) Phylogeny of Symbiodinium populations in zoantharians of the northern Persian Gulf. Marine Pollution Bulletin 105, 553–557.Google Scholar
Krueger, T. and Gates, R.D. (2012) Cultivating endosymbionts – host environmental mimics support the survival of Symbiodinium C15 ex hospite. Journal of Experimental Marine Biology and Ecology 413, 169–176.Google Scholar
LaJeunesse, T.C., Smith, R.T., Finney, J. and Oxenford, H. (2009) Outbreak and persistence of opportunistic symbiotic dinoflagellates during the 2005 Caribbean mass coral ‘bleaching’ event. Proceedings of the Royal Society of London B: Biological Sciences 276, 4139–4148.Google Scholar
LaJeunesse, T.C., Smith, R., Walther, M., Pinzón, J.H., Pettay, T., McGinley, M., Aschaffenburg, M., Medina-Rosas, P., Cupul-Magana, A.L., Perez, A.L., Reyes-Bonilla, H. and Warner, M.E. (2010) Host-symbiont recombination vs. natural selection in the response of coral-dinoflagellate symbioses to environmental disturbance. Proceedings of the Royal Society of London B: Biological Science 277, 2925–2934.Google Scholar
LaJeunesse, T.C., Wham, D.C., Pettay, D.T., Parkinson, J.E., Keshavmurthy, S. and Chen, C.A. (2014) Ecologically differentiated stress tolerant endosymbionts in the dinoflagellate genus Symbiodinium Clade D are different species. Phycologia 53, 305–319.Google Scholar
Mahmoud, H.M. and Al-Sarraf, M. (2016) Molecular phylogeny and community fingerprinting of coral-associated Symbiodinium north of the Arabian Gulf. Marine Pollution Bulletin 108, 94–104.Google Scholar
Mashini, A.G., Parsa, S. and Mostafavi, P.G. (2015) Comparison of Symbiodinium populations in corals from subtidal region and tidal pools of northern coasts of Hengam Island, Iran. Journal of Experimental Marine Biology and Ecology 473, 202–206.Google Scholar
Mostafavi, P.G., Ashrafi, M.G. and Dehghani, H. (2013) Are symbiotic algae in corals in northern parts of the Persian Gulf resistant to thermal stress? Aquatic Ecosystem Health & Management 16, 177–182.Google Scholar
Mostafavi, P.G., Fatemi, S.M.R., Shahhosseiny, M.H., Hoegh-Guldberg, O. and Loh, W.K.W. (2007) Predominance of clade D Symbiodinium in shallow-water reef-building corals off Kish and Larak Islands (Persian Gulf, Iran). Journal of Marine Biology 153, 25–34.Google Scholar
Ortiz, J.C., Gonzalez-Rivero, M. and Mumby, P.J. (2013) Can a thermally tolerant symbiont improve the future of Caribbean coral reefs? Journal of Global Change Biology 19, 273–281.Google Scholar
Pettay, D.T., Wham, D.C., Smith, R.T., Iglesias-Prieto, R. and LaJeunesse, T.C. (2015) Microbial invasion of the Caribbean by an Indo-Pacific coral zooxanthella. Proceedings of the National Academy of Sciences USA 112, 7513–7518.Google Scholar
Pochon, X., Montoya-Burgos, J.I., Stadelmann, B. and Pawlowski, J. (2006) Molecular phylogeny, evolutionary rates, and divergence timing of the symbiotic dinoflagellate genus Symbiodinium. Journal of Molecular Phylogenetics and Evolution 38, 20–30.Google Scholar
Rahmani, S., Ghavam Mostafavi, P., Shahhosseiny, M.H., Vosoughi, G. and Faraji, A. (2011) Genetic identification of Symbiodinium in genus Acropora off Farur Island, Persian Gulf. International Journal of Marine Science and Engineering 1, 43–50.Google Scholar
Riegl, B.M. and Purkis, S.J. (2012) Coral reefs of the Gulf: adaptation to climatic extremes. Amsterdam: Springer.Google Scholar
Shahhosseiny, M.H., Mostafavi, P.G., Fatemi, S.M.R. and Karimi, E. (2011) Clade identification of symbiotic zooxanthellae of dominant scleractinian coral species of intertidal pools in Hengam Island. African Journal of Biotechnology 10, 1502–1506.Google Scholar
Sheppard, C., Al-Husiani, M., Al-Jamali, F., Al-Yamani, F., Baldwin, R., Bishop, J., Benzoni, F., Dutrieux, E., Dulvy, N.K., Durvasula, S.R.V., Jones, D.A., Loughland, R., Medio, D., Nithyanandan, M., Pilling, G.M., Polikarpov, I., Price, A.R.G., Purkis, S., Riegl, B., Saburova, M., Samimi-Namin, K., Taylor, O., Wilson, S. and Zainal, K. (2010) The Gulf: a young sea in decline. Marine Pollution Bulletin 60, 13–38.Google Scholar
Sheppard, C.R.C. (1993) Physical environment of the Gulf relevant to marine pollution – an overview. Marine Pollution Bulletin 27, 3–8.Google Scholar
Silverstein, R.N., Cunning, R. and Baker, A.C. (2015) Change in algal symbiont communities after bleaching, not prior heat exposure, increases heat tolerance of reef corals. Journal of Global Change Biology 21, 236–249.Google Scholar
Stat, M., Loh, W.K.W., LaJeunesse, T.C., Hoegh-Guldberg, O. and Carter, D.A. (2009) Stability of coral-endosymbiont associations during and after a thermal stress event in the southern Great Barrier Reef. Coral Reefs 28, 709–713.Google Scholar
Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Journal of Molecular Biology and Evolution 30, 2725–2729.Google Scholar
Warner, M.E., LaJeunesse, T.C., Robison, J.D. and Thur, R.M. (2006) The ecological distribution and comparative photobiology of symbiotic dinoflagellates from reef corals in Belize: potential implications for coral bleaching. Limnology and Oceanography 51, 1887–1897.Google Scholar
Yao, F.C. and Johns, W.E. (2010) A HYCOM modeling study of the Persian Gulf: 1. Model configurations and surface circulation. Journal of Geophysical Research: Oceans 115, 2156–2202.Google Scholar
Ziegler, M., Arif, C., Burt, J.A., Dobretsov, S., Roder, C., LaJeunesse, T.C. and Voolstra, C.R. (2017) Biogeography and molecular diversity of coral symbionts in the genus Symbiodinium around the Arabian Peninsula. Journal of Biogeography 44, 674–686.Google Scholar