Advertisement

Coral Reefs

, Volume 37, Issue 1, pp 145–152 | Cite as

Symbiont shuffling linked to differential photochemical dynamics of Symbiodinium in three Caribbean reef corals

  • Ross CunningEmail author
  • Rachel N. Silverstein
  • Andrew C. Baker
Report

Abstract

Dynamic symbioses with functionally diverse dinoflagellate algae in the genus Symbiodinium may allow some reef corals to alter their phenotypes through ‘symbiont shuffling’, or changes in symbiont community composition. In particular, corals may become more bleaching resistant by increasing the relative abundance of thermally tolerant Symbiodinium in clade D after bleaching. Despite the immediate relevance of this phenomenon to corals living in warming oceans—and to interventions aimed at boosting coral resilience—the mechanisms governing how, why, and when symbiont shuffling occurs are still poorly understood. Here, we performed controlled thermal bleaching and recovery experiments on three species of Caribbean corals hosting mixtures of D1a (S. trenchii) and other symbionts in clades B or C. We show that the degree of symbiont shuffling is related to (1) the duration of stress exposure and (2) the difference in photochemical efficiency (F v /F m) of co-occurring symbionts under stress (i.e., the ‘photochemical advantage’ of one symbiont over the other). The advantage of D1a under stress was greatest in Montastraea cavernosa, intermediate in Siderastrea siderea, and lowest in Orbicella faveolata and correlated positively with the magnitude of shuffling toward D1a. In holobionts where D1a had less of an advantage over co-occurring symbionts (i.e., only slightly higher F v /F m under stress), a longer stress duration was required to elicit commensurate increases in D1a abundance. In fact, across these three coral species, 92.9% of variation in the degree of symbiont shuffling could be explained by the time-integrated photochemical advantage of D1a under heat stress. Although F v /F m is governed by numerous factors that this study is unable to resolve mechanistically, its strong empirical relationship with symbiont shuffling helps elucidate general features that govern this process in reef corals, which will help refine predictions of coral responses to environmental change and inform interventions to manipulate symbiont communities to enhance coral resilience.

Keywords

Coral bleaching Symbiont shuffling qPCR Photochemical efficiency Mutualism Photophysiology 

Notes

Acknowledgements

RC and RNS were supported by NSF Graduate Research Fellowships and University of Miami Graduate Fellowships, with additional funding from RSMAS student awards, the Captain Harry D. Vernon Memorial Scholarship, and the Garden Club of America. Additional support was provided by NSF (OCE-0547169 and OCE-1358699), the Lenfest Ocean Program, a Pew Fellowship in Marine Conservation, and a University of Miami Provost Research Award in Natural Science and Engineering to ACB. We thank Z Schwartz, K Ondrasik, K Dziedzic, N Formel, K Montenero, P Jones, R Winter, R Okazaki, L Gordon, and N Guy for laboratory assistance. We also thank D Suggett, whose detailed review greatly improved an earlier draft.

References

  1. Aswani S, Mumby PJ, Baker AC, Christie P, McCook LJ, Steneck RS, Richmond RH (2015) Scientific frontiers in the management of coral reefs. Front Mar Sci 2:1–13CrossRefGoogle Scholar
  2. Baker AC (1999) The symbiosis ecology of reef-building corals. PhD thesis, University of Miami, FL, USAGoogle Scholar
  3. Baker AC (2001) Reef corals bleach to survive change. Nature 411:765–766CrossRefPubMedGoogle Scholar
  4. Baker AC (2003) Flexibility and specificity in coral–algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34:661–689CrossRefGoogle Scholar
  5. Baker AC, Starger C, McClanahan TR, Glynn PW (2004) Corals’ adaptive response to climate change. Nature 430:741CrossRefPubMedGoogle Scholar
  6. Baker AC, Glynn PW, Riegl B (2008) Climate change and coral reef bleaching: an ecological assessment of long-term impacts, recovery trends and future outlook. Estuar Coast Shelf Sci 80:435–471CrossRefGoogle Scholar
  7. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  8. Berkelmans R, van Oppen MJH (2006) 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 Lond B Biol Sci 273:2305–2312CrossRefGoogle Scholar
  9. Buddemeier RW, Fautin DG (1993) Coral bleaching as an adaptive mechanism. Bioscience 43:320–327CrossRefGoogle Scholar
  10. Couch CS, Burns JHR, Liu G, Steward K, Gutlay N, Kenyon J, Eakin CM, Kosaki RK (2017) Mass coral bleaching due to unprecedented marine heatwave in Papahānaumokuākea Marine National Monument (Northwestern Hawaiian Islands). PLoS One 12:e0185121CrossRefPubMedPubMedCentralGoogle Scholar
  11. Cunning R (2013) The role of algal symbiont community dynamics in reef coral responses to global climate change. PhD thesis, University of Miami, FL, USAGoogle Scholar
  12. Cunning R (2017) Data for: Symbiont shuffling linked to differential photochemical dynamics of Symbiodinium in three Caribbean reef corals (version v1.0.0). Zenodo.  http://doi.org/10.5281/zenodo.1044368
  13. Cunning R, Silverstein RN, Baker AC (2015a) Investigating the causes and consequences of symbiont shuffling in a multi-partner reef coral symbiosis under environmental change. Proc R Soc Lond B Biol Sci 282:20141725CrossRefGoogle Scholar
  14. Cunning R, Gillette P, Capo TR, Galvez K, Baker AC (2015b) Growth tradeoffs associated with thermotolerant symbionts in the coral Pocillopora damicornis are lost in warmer oceans. Coral Reefs 34:155–160CrossRefGoogle Scholar
  15. Cunning R, Ritson-Williams R, Gates RD (2016) Patterns of bleaching and recovery of Montipora capitata in Kāneohe Bay, Hawaii, USA. Mar Ecol Prog Ser 551:131–139CrossRefGoogle Scholar
  16. Fox J (2003) Effect displays in R for generalised linear models. J Stat Softw 8:1–27CrossRefGoogle Scholar
  17. Glynn PW (1993) Coral reef bleaching: ecological perspectives. Coral Reefs 12:1–17CrossRefGoogle Scholar
  18. 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 164:46CrossRefGoogle Scholar
  19. Grottoli AG, Warner ME, Levas SJ, Aschaffenburg MD, Schoepf V, McGinley MP, Baumann J, Matsui Y (2014) The cumulative impact of annual coral bleaching can turn some coral species winners into losers. Glob Chang Biol 20:3823–3833CrossRefPubMedGoogle Scholar
  20. 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 318:1737–1742CrossRefPubMedGoogle Scholar
  21. 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 546:82–90CrossRefPubMedGoogle Scholar
  22. Jokiel PL, Coles S (1977) Effects of temperature on the mortality and growth of Hawaiian reef corals. Mar Biol 43:201–208CrossRefGoogle Scholar
  23. Jones A, Berkelmans R (2010) Potential costs of acclimatization to a warmer climate: growth of a reef coral with heat tolerant vs. sensitive symbiont types. PLoS One 5:e10437CrossRefPubMedPubMedCentralGoogle Scholar
  24. Jones RJ, Yellowlees D (1997) Regulation and control of intracellular algae (= zooxanthellae) in hard corals. Philos Trans R Soc Lond B Biol Sci 352:457–468CrossRefPubMedCentralGoogle Scholar
  25. Jones A, Berkelmans R, van Oppen MJH, Mieog JC, Sinclair W (2008) A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proc R Soc Lond B Biol Sci 275:1359–1365CrossRefGoogle Scholar
  26. Kuznetsova A, Brockhoff PB, Christensen RHB (2015) lmerTest: tests in linear mixed effects models. R package version 2.0-33. https://CRAN.R-project.org/package=lmerTest
  27. LaJeunesse TC, Smith RT, Finney J, Oxenford HA (2009) Outbreak and persistence of opportunistic symbiotic dinoflagellates during the 2005 Caribbean mass coral’bleaching’ event. Proc R Soc Lond B Biol Sci 276:4139–4148CrossRefGoogle Scholar
  28. 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 53:305–319CrossRefGoogle Scholar
  29. Lenth RV (2016) Least-squares means: the R package lsmeans. J Stat Softw 69:1–33CrossRefGoogle Scholar
  30. Little A, van Oppen MJH, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304:1492–1494CrossRefPubMedGoogle Scholar
  31. Logan CA, Dunne JP, Eakin CM, Donner SD (2014) Incorporating adaptive responses into future projections of coral bleaching. Glob Chang Biol 20:125–139CrossRefPubMedGoogle Scholar
  32. McGinley MP, Aschaffenburg MD, Pettay DT, Smith RT, LaJeunesse TC, Warner ME (2012) Symbiodinium spp. in colonies of eastern Pacific Pocillopora spp. are highly stable despite the prevalence of low-abundance background populations. Mar Ecol Prog Ser 462:1–7CrossRefGoogle Scholar
  33. Miller FJ, Schlosser PM, Janszen DB (2000) Haber’s rule: a special case in a family of curves relating concentration and duration of exposure to a fixed level of response for a given endpoint. Toxicology 149:21–34CrossRefPubMedGoogle Scholar
  34. Osmond CB (1994) What is photoinhibition? Some insights from comparisons of shade and sun plants. In: Baker NR, Bowyer JR (eds) Photoinhibition of photosynthesis from molecular mechanisms to the field. BIOS Scientific Publishers, Oxford, pp 1–24Google Scholar
  35. Parkhill JP, Maillet G, Cullen JJ (2001) Fluorescence-based maximal quantum yield for PSII as a diagnostic of nutrient stress. J Phycol 37:517–529CrossRefGoogle Scholar
  36. Pettay DT, Wham DC, Smith RT, Iglesias-Prieto R, LaJeunesse TC (2015) Microbial invasion of the Caribbean by an Indo-Pacific coral zooxanthella. Proc Natl Acad Sci USA 112:7513–7518CrossRefPubMedPubMedCentralGoogle Scholar
  37. Pochon X, Gates RD, Vik D, Edmunds PJ (2014) Molecular characterization of symbiotic algae (Symbiodinium spp.) in soritid foraminifera (Sorites orbiculus) and a scleractinian coral (Orbicella annularis) from St John, US Virgin Islands. Mar Biol 161:2307–2318CrossRefGoogle Scholar
  38. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  39. Rowan R (2004) Coral bleaching: thermal adaptation in reef coral symbionts. Nature 430:742CrossRefPubMedGoogle Scholar
  40. Silverstein RN, Correa AMS, Baker AC (2012) Specificity is rarely absolute in coral–algal symbiosis: implications for coral response to climate change. Proc R Soc Lond B Biol Sci 239:2609–2618CrossRefGoogle Scholar
  41. Silverstein RN, Cunning R, Baker AC (2015) Change in algal symbiont communities after bleaching, not prior heat exposure, increases heat tolerance of reef corals. Glob Chang Biol 21:236–249CrossRefPubMedGoogle Scholar
  42. Silverstein RN, Cunning R, Baker AC (2017) Tenacious D: Symbiodinium in clade D remain in reef corals at both high and low temperature extremes despite impairment. J Exp Biol 220:1192–1196CrossRefPubMedGoogle Scholar
  43. Slavov C, Schrameyer V, Reus M, Ralph PJ (2016) Super-quenching state protects Symbiodinium from thermal stress: implications for coral bleaching. Biochim Biophys Acta 1857:840–847CrossRefPubMedGoogle Scholar
  44. Suggett DJ, Warner ME, Leggat W (2017) Symbiotic dinoflagellate functional diversity mediates coral survival under ecological crisis. Trends Ecol Evol 32:735–745CrossRefPubMedGoogle Scholar
  45. Suggett DJ, Moore CM, Hickman AE, Geider RJ (2009) Interpretation of fast repetition rate (FRR) fluorescence: signatures of phytoplankton community structure versus physiological state. Mar Ecol Prog Ser 376:1–19CrossRefGoogle Scholar
  46. Suggett DJ, Warner ME, Smith DJ, Hennige SJ, Baker NR (2008) Photosynthesis and production of hydrogen peroxide by Symbiodinium (Pyrrhophyta) phylotypes with different thermal tolerances. J Phycol 44:948–956CrossRefPubMedGoogle Scholar
  47. 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 208:370–381CrossRefPubMedGoogle Scholar
  48. Tansik AL, Fitt WK, Hopkinson BM (2017) Inorganic carbon is scarce for symbionts in scleractinian corals. Limnol Oceanogr 62:2045–2055CrossRefGoogle Scholar
  49. Thornhill DJ, LaJeunesse TC, Kemp DW, Fitt WK, Schmidt GW (2006) Multi-year, seasonal genotypic surveys of coral–algal symbioses reveal prevalent stability or post-bleaching reversion. Mar Biol 148:711–722CrossRefGoogle Scholar
  50. van Hooidonk R, Maynard JA, Liu Y, Lee SK (2015) Downscaled projections of Caribbean coral bleaching that can inform conservation planning. Glob Chang Biol 21:3389–3401CrossRefPubMedPubMedCentralGoogle Scholar
  51. van Oppen MJH, Oliver JK, Putnam HM, Gates RD (2015) Building coral reef resilience through assisted evolution. Proc Natl Acad Sci USA 112:2307–2313CrossRefPubMedPubMedCentralGoogle Scholar
  52. Wangpraseurt D, Larkum AWD, Ralph PJ, Kühl M (2012) Light gradients and optical microniches in coral tissues. Front Microbiol 3:316CrossRefPubMedPubMedCentralGoogle Scholar
  53. Wangpraseurt D, Pernice M, Guagliardo P, Kilburn MR, Clode PL, Polerecky L, Kühl M (2015) Light microenvironment and single-cell gradients of carbon fixation in tissues of symbiont-bearing corals. ISME J 10:788–792CrossRefPubMedPubMedCentralGoogle Scholar
  54. Warner ME, Fitt WK, Schmidt GW (1996) The effects of elevated temperature on the photosynthetic efficiency of zooxanthellae in hospite from four different species of reef coral: a novel approach. Plant Cell Envir 19:291–299CrossRefGoogle Scholar
  55. Wham DC, Ning G, LaJeunesse TC (2017) Symbiodinium glynnii sp. nov., a species of stress-tolerant symbiotic dinoflagellates from pocilloporid and montiporid corals in the Pacific Ocean. Phycologia 56:396–409CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Department of Marine Biology and Ecology, Rosenstiel School of Marine and Atmospheric ScienceUniversity of MiamiMiamiUSA
  2. 2.Miami WaterkeeperMiamiUSA

Personalised recommendations