Differential effects of ocean acidification on growth and photosynthesis among phylotypes of Symbiodinium (Dinophyceae)

Limnology and Oceanography

Volumn 56, Issue 3, 2011, Pages 927-938

  Brading, Patrick ^a   Warner, Mark E ^b   Davey, Phillip ^a   Smith, David J ^a   Achterberg, Eric P ^c   Suggett, David J ^a  

^a UNIVERSITY OF ESSEX   (United Kingdom)

^b UNIVERSITY OF DELAWARE   (United States)

^c UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDIFICATION; ALGA; CARBON; DINOFLAGELLATE; GROWTH RATE; PARTIAL PRESSURE; PHOTOSYNTHESIS; PHYLOGENETICS; PHYSIOLOGICAL RESPONSE; RESPIRATION; SYMBIOSIS;

ALGAE; CNIDARIA; DINOPHYCEAE; SYMBIODINIUM;

EID: 79956337218     PISSN: 00243590     EISSN: None     Source Type: Journal    
DOI: 10.4319/lo.2011.56.3.0927     Document Type: Article

References (64)

1. Al-Moghrabi, S., C. Goiran, D. Allemand, N. Speziale, and J. Jaubert. 1996. Inorganic carbon uptake for photosynthesis by the symbiotic coral-dinoflagellate association II. Mechanisms for bicarbonate uptake. J. Exp. Mar. Biol. Ecol. 199: 227-248, doi:10.1016/0022-0981(95)00202-2
2. Anderson, D., P. Glibert, and J. Burkholder. 2002. Harmful algal blooms and eutrophication: Nutrient sources, composition, and consequences. Estuar. Coasts 25: 704-726, doi:10.1007/BF02804901
3. Baker, A. 2003. Flexibility and specificity in coral-algal symbiosis: Diversity, ecology, and biogeography of Symbiodinium. Ann. Rev. Ecol. Evol. Syst. 34: 661-689, doi:10.1146/ annurev.ecolsys.34.011802.132417
4. 2 concentrating mechanisms, and their regulation. Funct. Plant Biol. 29: 335-347, doi:10.1071/PP01195
5. Berkelmans, R., and M. Van Oppen. 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: 2305-2312, doi:10.1098/ rspb.2006.3567
6. Bertucci, A., É. Tambutté, S. Tambutté, D. Allemand, and D. Zoccola. 2010. Symbiosis-dependent gene expression in coral-dinoflagellate association: Cloning and characterization of a P-type H+-ATPase gene. Proc. R. Soc. Lond. B Biol. Sci. 277: 87-95, doi:10.1098/rspb.2009.1266
7. 2 concentration, and cell size on the stable carbon isotope fractionation in marine phytoplankton. Geochim. Cosmochim. Acta 63: 3729-3741, doi:10.1016/ S0016-7037(99)00217-3
8. Caldeira, K., and M. Wickett. 2003. Anthropogenic carbon and ocean pH. Nature 425: 365-365, doi:10.1038/425365a
9. Coffroth, M., C. Lewis, S. Santos, J. Weaver, E. Sotka, and R. Thacker. 2006. Environmental populations of symbiotic dinoflagellates in the genus Symbiodinium can initiate symbioses with reef cnidarians. Curr. Biol. 16: R985-R987, doi:10.1016/j.cub.2006.10.049
10. Coffroth, M., and S. Santos. 2005. Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156: 19-34, doi:10.1016/j.protis.2005.02.004
11. Crawley, A., D. Kline, S. Dunn, K. Anthony, and S. Dove. 2010. The effect of ocean acidification on symbiont photorespiration and productivity in Acropora formosa. Glob. Change Biol. 16: 851-863, doi:10.1111/j.1365-2486.2009. 01943.x
12. Dubinsky, Z., and I. Berman-Frank. 2001. Uncoupling primary production from population growth in photosynthesizing organisms in aquatic ecosystems. Aquat. Sci. Res. Across Boundaries 63: 4-17.
13. 2 concentrations: a mesocosm experiment. Aquat. Microb. Ecol. 34: 93-104, doi:10.3354/ame034093
14. 2 concentration on a bloom of the coccolithophorid Emiliania huxleyi in mesocosm experiments. Limnol. Oceanogr. 50: 493-507, doi:10.4319/lo.2005.50.2.0493
15. Falkowski, P., and Y. Chen. 2003. Photoacclimation of light harvesting systems in eukaryotic algae, p. 423-447. In B. Green and W. Parson [eds.], Light-harvesting antennas in photosynthesis. Kluwer Academic.
16. Finney, J., D. Pettay, E. Sampayo, M. Warner, H. Oxenford, and T. Lajeunesse. 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, doi:10.1007/s00248-010-9681-y
17. Freudenthal, H. 1962. Symbiodinium gen. nov. and Symbiodinium microadriaticum sp. nov., a Zooxanthella: Taxonomy, life cycle, and morphology. J. Eukaryot. Microbiol. 9: 45-52, doi:10.1111/j.1550-7408.1962.tb02579.x
18. 2 on photosynthesis, growth, and elemental ratios in marine Synechococcus and Prochlorococcus (Cyanobacteria). J. Phycol. 43: 485-496, doi:10.1111/j.1529-8817.2007.00355.x
19. 2 and temperature effects on sympatric Heterosigma akashiwo and Prorocentrum minimum. Harmful Algae 7: 76-90, doi:10.1016/ j.hal.2007.05.006
20. Furla, P., I. Galgani, I. Durand, and D. Allemand. 2000. Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis. J. Exp. Biol. 203: 3445-3457.
21. 2 concentrating mechanisms in algae: Mechanisms, environmental modulation, and evolution. Ann. Rev. Plant Biol. 56: 99-131, doi:10.1146/annurev.arplant.56.032604.144052
22. 2 increases oceanic primary production. Nature 388: 526-527, doi:10.1038/41457
23. Hennige, S., D. Suggett, M. Warner, K. McDougall, and D. Smith. 2009. Photobiology of Symbiodinium revisited: Biophysical and bio-optical signatures. Coral Reefs 28: 179-195, doi:10.1007/s00338-008-0444-x
24. Hilton, J., H. Lishman, S. Mackness, and S. Heaney. 1986. An automated method for the analysis of particulate carbon and nitrogen in natural waters. Hydrobiologia 141: 269-271, doi:10.1007/BF00014221
25. Hurd, C., C. Hepburn, K. Currie, J. Raven, and K. Hunter. 2009. Testing the effects of ocean acidification on algal metabolism: Considerations for experimental designs. J. Phycol. 45: 1236-1251, doi:10.1111/j.1529-8817.2009.00768.x
26. 2 fixation, photosynthesis, growth rates, and elemental ratios: Implications for past, present, and future ocean biogeochemistry. Limnol. Oceanogr. 52: 1293-1304, doi:10.4319/lo.2007.52.4.1293
27. Iglesias-Prieto, R., V. Beltrán, T. Lajeunesse, H. ReyesBonilla, and P. Thomé. 2004. Different algal symbionts explain the vertical distribution of dominant reef corals in the Eastern Pacific. Proc. R. Soc. Lond. B Biol. Sci. 271: 1757-1763, doi:10.1098/rspb.2004.2757
28. Kana, T. 1990. Light-dependent oxygen cycling measured by an oxygen-18 isotope dilution technique. Mar. Ecol. Prog. Ser. 64: 293-300, doi:10.3354/meps064293
29. 2 concentration on growth of a natural phytoplankton assemblage in a controlled mesocosm experiment. Limnol. Oceanogr. 51: 1629-1636, doi:10.4319/lo.2006.51.4.1629
30. Lajeunesse, T. C. 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, doi:10.1046/j.1529-8817.2001.01031.x
31. Lajeunesse, T. C., and others. 2010. Long-standing environmental conditions, geographic isolation and host-symbiont specificity influence the relative ecological dominance and genetic diversification of coral endosymbionts in the genus Symbiodinium. J. Biogeogr. 37: 785-800, doi:10.1111/j.1365-2699. 2010.02273.x
32. Lajeunesse, T. C., L. William, and R. K. Trench. 2009. Do introduced endosymbiotic dinoflagellates 'take' to new hosts? Biol. Invasions 11: 995-1003, doi:10.1007/s10530-008-9311-5
33. 2 on photosynthesis and calcification of corals and interactions with seasonal change in temperature/irradiance and nutrient enrichment. J. Geophys. Res. 110: C09S07, doi:10.1029/ 2004JC002576
34. Leggat, W., M. Badger, and D. Yellowlees. 1999. Evidence for an inorganic carbon-concentrating mechanism in the symbiotic dinoflagellate Symbiodinium sp. Plant Physiol 121: 1247-1255, doi:10.1104/pp.121.4.1247
35. Leonardos, N., and R. Geider. 2005. Elevated atmospheric carbon dioxide increases organic carbon fixation by Emiliania huxleyi (Haptophyta), under nutrient-limited high-light conditions. J. Phycol. 41: 1196-1203, doi:10.1111/j.1529-8817. 2005.00152.x
36. 2 enhances nitrogen fixation and growth in the marine cyanobacterium Trichodesmium. Glob. Change Biol. 13: 531-538, doi:10.1111/j.1365-2486.2006.01314.x
37. Manning, M., and R. Gates. 2008. Diversity in populations of free-living Symbiodinium from a Caribbean and Pacific reef. Limnol. Oceanogr. 53: 1853-1861, doi:10.4319/lo.2008.53. 5.1853
38. Millero, F., T. Graham, F. Huang, H. Bustos-Serrano, and D. Pierrot. 2006. Dissociation constants of carbonic acid in seawater as a function of salinity and temperature. Mar. Chem. 100: 80-94, doi:10.1016/j.marchem.2005.12.001
39. 2 system calculations. ORNL/CDIAC-105 [Internet]. Oak Ridge (TN): Oak Ridge National Laboratory, Carbon Dioxide Information Analysis Center [accessed 15 April 2008]. Available from http://cdiac.ornl.gov/oceans/co2rprt.html
40. Platt, T., C. Gallegos, and W. Harrison. 1980. Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J. Mar. Res. 38: 687-701.
41. Pochon, X., M. Stat, M. Takabayashi, L. Chasqui, L. J. Chauka, D. D. K. Logan, and R. Gates. 2010. Comparison of endosymbiotic and free-living Symbiodinium (Dinophyceae) diversity in a Hawaiian reef environment. J. Phycol. 46: 53-65, doi:10.1111/j.1529-8817.2009.00797.x
42. Provasoli, L., J. McLaughlin, and M. Droop. 1957. The development of artificial media for marine algae. Arch. Microbiol. 25: 392-428.
43. Ragni, M., R. Airs, S. Hennige, D. Suggett, M. Warner, and R. Geider. 2010. PSII photoinhibition and photorepair in Symbiodinium (Pyrrhophyta) differs between thermally tolerant and sensitive phylotypes. Mar. Ecol. Prog. Ser. 406: 57-70, doi:10.3354/meps08571
44. 2-concentrating mechanisms of the potentially toxic dinoflagellate Protoceratium reticulatum (Dinophyceae, Gonyaulacales). J. Phycol. 43: 693-701, doi:10.1111/j.1529-8817.2007.00368.x
45. 2. Nature 407: 364-367, doi:10.1038/35030078
46. Ritchie, R. 2006. Consistent sets of spectrophotometric chlorophyll equations for acetone, methanol and ethanol solvents. Photosynth. Res. 89: 27-41, doi:10.1007/s11120-006-9065-9
47. Robison, J., and M. Warner. 2006. Differential impacts of photoacclimation and thermal stress on the photobiology of four different phylotypes of Symbiodinium (Pyrrhophyta). J. Phycol. 42: 568-579, doi:10.1111/j.1529-8817.2006.00232.x
48. Rogers, J., and R. Davis. 2006. Application of a new microculturing technique to assess the effects of temperature and salinity on specific growth rates of six Symbiodinium isolates. Bull. Mar. Sci. 79: 113-126.
49. Rost, B., K. Richter, U. Riebesell, and P. Hansen. 2006. Inorganic carbon acquisition in red tide dinoflagellates. Plant Cell Environ. 29: 810-822, doi:10.1111/j.1365-3040.2005. 01450.x
50. Rost, B., I. Zondervan, and D. Wolf-Gladrow. 2008. Sensitivity of phytoplankton to future changes in ocean carbonate chemistry: Current knowledge, contradictions and research directions. Mar. Ecol. Prog. Ser. 373: 227-237, doi:10.3354/ meps07776
51. Santos, S., and T. C. Lajeunesse. 2009. Searchable database of Symbiodinium diversity-geographic and ecological diversity [Internet]. Auburn (AL): Auburn University [accessed 10 June 2009]. Available from http://www.auburn.edu/, santosr/sd2_ged.htm
52. 2 promotes phytoplankton productivity. Ecol. Lett. 7: 446-451, doi:10.1111/j.1461-0248.2004.00597.x
53. Sheppard, C., S. Davy, and G. Pilling. 2009. The biology of coral reefs. Oxford Univ. Press.
54. Solomon, S., and others. [eds.]. 2007. Climate change 2007: The physical science basis, p. 996. In Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge Univ. Press.
55. Suggett, D., E. Le Floc'h, G. Harris, N. Leonardos, and R. Geider. 2007. Different strategies of photoacclimation by two strains of Emiliania huxleyi (Haptophyta). J. Phycol. 43: 1209-1222, doi:10.1111/j.1529-8817.2007.00406.x
56. Suggett, D., M. Warner, D. Smith, P. Davey, S. Hennige, and N. Baker. 2008. Photosynthesis and production of hydrogen peroxide by Symbiodinium (Pyrrhophyta) phylotypes with different thermal tolerances. J. Phycol. 44: 948-956, doi:10.1111/j.1529-8817.2008.00537.x
57. Taylor, F., M. Hoppenrath, and J. Saldarriaga. 2008. Dinoflagellate diversity and distribution. Biodivers. Conserv. 17: 407-418, doi:10.1007/s10531-007-9258-3
58. Tortell, P. 2000. Evolutionary and ecological perspectives on carbon acquisition in phytoplankton. Limnol. Oceanogr. 45: 744-750, doi:10.4319/lo.2000.45.3.0744
59. 2 effects on taxonomic composition and nutrient utilization in an Equatorial Pacific phytoplankton assemblage. Mar. Ecol. Prog. Ser. 236: 37-43, doi:10.3354/meps236037
60. Warner, M., T. Lajeunesse, J. Robison, and R. Thur. 2006. The ecological distribution and comparative photobiology of symbiotic dinoflagellates from reef corals in Belize: Potential implications for coral bleaching. Limnol. Oceanogr. 51: 1887-1897, doi:10.4319/lo.2006.51.4.1887
61. Weis, V., and W. Reynolds. 1999. Carbonic anhydrase expression and synthesis in the sea anemone Anthopleura elegantissima are enhanced by the presence of dinoflagellate symbionts. Physiol. Biochem. Zool. 72: 307-316, doi:10.1086/316674
62. Whitney, S., D. Shaw, and D. Yellowlees. 1995. Evidence that some dinoflagellates contain a ribulose-1,5-bisphosphate carboxylase/oxygenase related to that of the a-proteobacteria. Proc. R. Soc. Lond. B Biol. Sci. 259: 271-275, doi:10.1098/ rspb.1995.0040
63. Yellowlees, D., and others. 1993. Role of carbonic anhydrase in the supply of inorganic carbon to the giant clam-zooxanthellate symbiosis. Mar. Biol. 115: 605-611, doi:10.1007/ BF00349368
64. 2 concentration on the PIC/POC ratio in the coccolithophore Emiliania huxleyi grown under light-limiting conditions and different daylengths. J. Exp. Mar. Biol. Ecol. 272: 55-70, doi:10.1016/S0022-0981(02)00037-0