Contrasting modes of inorganic carbon acquisition amongst Symbiodinium (Dinophyceae) phylotypes

New Phytologist

Volumn 200, Issue 2, 2013, Pages 432-442

  Brading, Patrick ^a   Warner, Mark E ^b   Smith, David J ^a   Suggett, David J ^a  

^a UNIVERSITY OF ESSEX   (United Kingdom)

^b UNIVERSITY OF DELAWARE   (United States)

Author keywords

Carbon acquisition; Carbon concentrating mechanism (CCM); Dinoflagellate; Microalgae; Ocean acidification; Symbiodinium

Indexed keywords

ACIDIFICATION; CARBON DIOXIDE; CARBON FIXATION; CORAL; DINOFLAGELLATE; ENVIRONMENTAL CONDITIONS; INORGANIC CARBON; MICROALGA; OCEAN;

ANTHOZOA; DINOPHYCEAE; SYMBIODINIUM;

CARBON DIOXIDE; CHLOROPHYLL; CHLOROPHYLL A; RIBULOSEBISPHOSPHATE CARBOXYLASE;

ADAPTATION; ANIMAL; ANTHOZOA; ARTICLE; CARBON ACQUISITION; CARBON CYCLE; CARBON-CONCENTRATING MECHANISM (CCM); DINOFLAGELLATE; ELECTRON TRANSPORT; GROWTH, DEVELOPMENT AND AGING; LIGHT; METABOLISM; MICROALGA; OCEAN ACIDIFICATION; PARASITOLOGY; PHOTOSYNTHESIS; PHYSIOLOGY; RADIATION EXPOSURE; SPECIES DIFFERENCE; SYMBIODINIUM; SYMBIOSIS;

CARBON ACQUISITION; CARBON-CONCENTRATING MECHANISM (CCM); DINOFLAGELLATE; MICROALGAE; OCEAN ACIDIFICATION; SYMBIODINIUM;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANTHOZOA; CARBON CYCLE; CARBON DIOXIDE; CHLOROPHYLL; DINOFLAGELLIDA; ELECTRON TRANSPORT; LIGHT; MICROALGAE; PHOTOSYNTHESIS; RIBULOSE-BISPHOSPHATE CARBOXYLASE; SPECIES SPECIFICITY; SYMBIOSIS;

EID: 84884411984     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12379     Document Type: Article

References (63)

1. Al-Moghrabi S, Goiran C, Allemand D, Speziale N, Jaubert J. 1996. Inorganic carbon uptake for photosynthesis by the symbiotic coral-dinoflagellate association II. Mechanisms for bicarbonate uptake. Journal of Experimental Marine Biology and Ecology 199: 227-248.
2. Bailey S, Melis A, Mackey KRM, Cardol P, Finazzi G, van Dijken G, Berg GM, Arrigo K, Shrager J, Grossman A. 2008. Alternative photosynthetic electron flow to oxygen in marine Synechococcus. Biochimica et Biophysica Acta 1777: 269-276.
3. Berkelmans R, van Oppen M. 2006. The role of zooxanthellae in the thermal tolerance of corals: a 'nugget of hope' for coral reefs in an era of climate change. Proceedings of the Royal Society B: Biological Sciences 273: 2305-2312.
4. +-ATPase gene. Proceedings of the Royal Society B: Biological Sciences 277: 87-95.
5. Brading P, Warner ME, Davey P, Smith DJ, Achterberg EP, Suggett DJ. 2011. Differential effects of ocean acidification on growth and productivity and photosynthesis among phylotypes of Symbiodinium (Dinophyceae). Limnology and Oceanography 56: 927-938.
6. Brown CM, MacKinnon JD, Cockshutt AM, Villareal TA, Campbell DA. 2008. Flux capacities and acclimation costs in Trichodesmium from the Gulf of Mexico. Marine Biology 57: 413-422.
7. Brownlee C. 2009. pH regulation in symbiotic anemones and corals: a delicate balancing act. Proceedings of the National Academy of Sciences, USA 106: 16541-16542.
8. 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. Journal of Phycology 48: 117-126.
9. Carpenter EJ, Roenneberg T. 1995. The marine planktonic cyanobacteria Trichodesmium spp.: photosynthetic rate measurements in the SW Atlantic Ocean. Marine Ecology Progress Series 118: 267-273.
10. Colman B, Huertas IE, Bhatti S, Dason JS. 2002. The diversity of inorganic carbon acquisition mechanisms in eukaryotic microalgae. Functional Plant Biology 29: 261-270.
11. Dason JS, Huertas IE, Colman B. 2004. Source of inorganic carbon for photosynthesis in two marine dinoflagellates. Journal of Phycology 40: 285-292.
12. 2 problem. Annual Review of Marine Science 1: 169-192.
13. Espie GS, Colman B. 1986. Inorganic carbon uptake during photosynthesis. Plant Physiology 80: 863-869.
14. 2 and temperature effects on sympatric Heterosigma akashiwo and Prorocentrum minimum. Harmful algae 7: 76-90.
15. Gattuso J-P, Allemand D, Frankignoulle M. 1999. Photosynthesis and calcification at cellular, organismal and community levels in coral reefs: a review on interactions and control by carbonate chemistry. American Zoologist 39: 160-183.
16. Geider RJ, Osborne BA. 1992. Algal photosynthesis: the measurement of algal gas exchange. London, UK: Chapman and Hall.
17. 2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annual Review of Plant Biology 56: 99-131.
18. Goiran C, Al-Moghrabi S, Allemand D, Jaubert J. 1996. Inorganic carbon uptake for photosynthesis by the symbiotic coral-dinoflagellate association II. Bicarbonate absorption by animal host. Journal of Experimental Marine Biology and Ecology 199: 207-225.
19. Guinotte JM, Fabry VJ. 2008. Ocean acidification and its potential effects on marine ecosystems. Annals NY Academy of Sciences 1134: 320-342.
20. 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.
21. Hurd C, Hepburn C, Currie K, Raven J, Hunter K. 2009. Testing the effects of ocean acidification on algal metabolism: considerations for experimental designs. Journal of Phycology 45: 1236-1251.
22. Iglesias-Prieto R, Beltrán V, Lajeunesse T, Reyes-Bonilla H, Thomé P. 2004. Different algal symbionts explain the vertical distribution of dominant reef corals in the Eastern Pacific. Proceedings of the Royal Society B: Biological Sciences 271: 1757-1763.
23. Johnson KS. 1982. Carbon dioxide hydration and dehydration kinetics in seawater. Limnology and Oceanography 27: 849-855.
24. 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. Journal of Phycology 37: 866-880.
25. Leggat W, Badger M, Yellowlees D. 1999. Evidence for an inorganic carbon-concentrating mechanism in the symbiotic dinoflagellate Symbiodinium sp. Plant Physiology 121: 1247-1255.
26. Leggat W, Marendy EM, Baillie B, Whitney SM, Lugwig M, Badger MR, Yellowlees D. 2002. Dinoflagellate symbioses: strategies and adaptations for the acquisition and fixation of inorganic carbon. Functional Plant Biology 29: 309-322.
27. Lesser MP. 1996. Exposure of symbiotic dinoflagellates to elevated temperatures and ultraviolet radiation causes oxidative stress and inhibits photosynthesis. Limnology and Oceanography 41: 271-283.
28. Lilley RM, Ralph PJ, Larkum AWD. 2010. The determination of activity of the enzyme Rubisco in cell extracts of the dinoflagellate alga Symbiodinium sp. by manganese chemiluminescence and its response to short-term thermal stress of the alga. Plant, Cell & Environment 33: 995-1004.
29. MacIntyre HL, Sharkey TD, Geider RJ. 1997. Activation and deactivation of ribulose-1, 5-bisphosphate carboxylase/oxygenase (Rubisco) in three marine microalgae. Photosynthesis Research 51: 93-106.
30. Mackey KRM, Paytan A, Grossman AR, Bailey S. 2008. A photosynthetic strategy for coping in a high-light, low-nutrient environment. Limnology and Oceanography 53: 900-913.
31. Martin CL, Tortell PD. 2006. Bicarbonate transport and extracellular carbonic anhydrase activity in Bering Sea phytoplankton assemblages: results from isotopic disequilibrium experiments. Limnology and Oceanography 51: 2111-2121.
32. McCabe-Reynolds J, Bruns BU, Fitt WK, Schmidt GW. 2008. Enhanced photoprotection pathways in symbiotic dinoflagellates of shallow-water corals and other cnidarians. Proceedings of the National Academy of Sciences, USA 105: 13673-13678.
33. 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.
34. Millero F, Graham T, Huang F, Bustos-Serrano H, Pierrot D. 2006. Dissociation constants of carbonic acid in seawater as a function of salinity and temperature. Marine Chemistry 100: 80-94.
35. Moore CM, Suggett DJ, Hickman AE, Kim YN, Tweddle JF, Sharples J, Geider RJ, Holligan PM. 2006. Phytoplankton photoacclimation and photoadaptation in response to environmental gradients in a shelf sea. Limnology and Oceanography 51: 936-949.
36. Morse D, Salois P, Markovic P, Hastings JW. 1995. A nuclear-encoded form II Rubisco in dinoflagellates. Science 268: 1622-1624.
37. Muscatine L, Goiran C, Land L, Jaubert J, Cuif JP, Allemand D. 2005. Stable isotopes (δC-13 and δN-15) of organic matrix from coral skeleton. Proceedings of the National Academy of Sciences, USA 102: 1525-1530.
38. Niyogi KK. 2000. Safety valves for photosynthesis. Current Opinion in Biology 3: 455-460.
39. 2 as an alternative electron sink in photosynthesis? Current Opinion in Plant Biology 5: 193-198.
40. 2 system calculations. ORNL/CDIAC-105. [WWW document] URL http://cdiac.ornl.gov/oceans/co2rprt.html [accessed 1 February 2011].
41. Platt T, Gallegos C, Harrison W. 1980. Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. Journal of Marine Research 38: 687-701.
42. Portis AR, Li C, Wang D, Salvucci ME. 2008. Regulation of Rubisco activase and its interaction with Rubisco. Journal of Experimental Botany 59: 1597-1604.
43. Provasoli L, McLaughlin J, Droop M. 1957. The development of artificial media for marine algae. Archives of Microbiology 25: 392-428.
44. Ragni M, Airs R, Hennige S, Suggett DJ, Warner ME, Geider RJ. 2010. PSII photoinhibition and photorepair in Symbiodinium (Pyrrhophyta) differs between thermally tolerant and sensitive phylotypes. Marine Ecology Progress Series 406: 57-70.
45. Reinfelder JR. 2011. Carbon concentrating mechanisms in eukaryotic marine phytoplankton. Annual Review of Marine Science 3: 291-315.
46. Ritchie R. 2006. Consistent sets of spectrophotometric chlorophyll equations for acetone, methanol and ethanol solvents. Photosynthesis Research 89: 27-41.
47. Robison J, Warner ME. 2006. Differential impacts of photoacclimation and thermal stress on the photobiology of four different phylotypes of Symbiodinium (Pyrrhophyta). Journal of Phycology 42: 568-579.
48. Rost B, Kranz SA, Richter KU, Tortell PD. 2007. Isotope disequilibrium and mass spectrometric studies of inorganic carbon acquisition by phytoplankton. Limnology and Oceanography: Methods 5: 328-337.
49. Rost B, Zondervan I, Wolf-Gladrow D. 2008. Sensitivity of phytoplankton to future changes in ocean carbonate chemistry: current knowledge, contradictions and research directions. Marine Ecology Progress Series 373: 227-237.
50. Ryan-Keogh TJ, Macey AI, Cockshutt AM, Moore CM, Bibby TC. 2012. The cyanobacterial chlorophyll-binding-protein IsiA acts to increase the in vivo effective absorption cross-section of PSI under iron limitation. Journal of Phycology 48: 145-154.
51. Schägger H. 2006. Tricine-SDS-PAGE. Nature Protocols 1: 16-22.
52. Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL, eds. 2007. Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, UK.
53. Suggett DJ, MacInytre HL, Kana TM, Geider RJ. 2009. Comparing electron transport with gas exchange: parameterising exchange rates between alternative photosynthetic currencies for eukaryotic phytoplankton. Aquatic Microbial Ecology 56: 147-162.
54. Suggett DJ, Warner ME, Smith DJ, Davey P, Hennige S, Baker NR. 2008. Photosynthesis and production of hydrogen peroxide by Symbiodinium (Pyrrhophyta) phylotypes with different thermal tolerances. Journal of Phycology 44: 948-956.
55. Tabita FR, Satagopan S, Hanson TE, Kreel NE, Scott SS. 2008. Distinct form I, II, III, and IV Rubisco proteins from the three kingdoms of life provide clues about Rubisco evolution and structure/function relationships. Journal of Experimental Botany 59: 1515-1524.
56. Tortell P. 2000. Evolutionary and ecological perspectives on carbon acquisition in phytoplankton. Limnology and Oceanography 45: 744-750.
57. 2 gradients. Journal of Phycology 46: 433-443.
58. Venn AA, Tambutté E, Lotto S, Zoccola D, Allemand D, Tambutté S. 2009. Imaging intracellular pH in a reef coral and symbiotic anemone. Proceedings of the National Academy of Sciences, USA 106: 16574-16579.
59. Whitney S, Shaw D, Yellowlees D. 1995. Evidence that some dinoflagellates contain a ribulose-1, 5-bisphosphate carboxylase/oxygenase related to that of the a-proteobacteria. Proceedings of the Royal Society B: Biological Sciences 259: 271-275.
60. Wooldridge SA. 2009. A new conceptual model for the warm-water breakdown of the coral-algae endosymbiosis Marine and Freshwater Research 60: 483-496.
61. Wooldridge SA. 2010. Is the coral-algae symbiosis really 'mutually beneficial' for the partners? BioEssays 32: 615-625.
62. 2 specificity of single-subunit ribulose-bisphosphate carboxylase from the dinoflagellate, Amphidinium carterae. Australian Journal of Plant Physiology 25: 131-138.
63. Yellowlees D, Dionisio-Sese ML, Masuda K, Maruyama T, Abe T, Baillie B, Tsuzuki M, Miyachi S. 1993. Role of carbonic anhydrase in the supply of inorganic carbon to the giant clam-zooxanthellate symbiosis. Marine Biology 115: 605-611.