Can the xanthophyll cycle help extract the essence of the microalgal functional response to a variable light environment?

Journal of Plankton Research

Volumn 32, Issue 12, 2010, Pages 1609-1617

  Brunet, Christophe ^a   Lavaud, Johann ^b  

^a STAZIONE ZOOLOGICA ANTON DOHRN   (Italy)

^b UNIVERSITÉ DE LA ROCHELLE   (France)

Author keywords

ecophysiology; photosynthesis; phytoplankton

Indexed keywords

ADAPTATION; ECOPHYSIOLOGY; FUNCTIONAL RESPONSE; HYDRODYNAMICS; LIGHT EFFECT; MARINE ECOSYSTEM; MICROALGA; PELAGIC ENVIRONMENT; PHOTOSYNTHESIS; PHYTOPLANKTON;

EID: 78149452536     PISSN: 01427873     EISSN: 14643774     Source Type: Journal    
DOI: 10.1093/plankt/fbq104     Document Type: Article

References (92)

1. Alderkamp, A.-C., de Baar, H. J. W., Visser, R. J. W. et al. (2010) Can photoinhibition control phytoplankton abundance in deeply mixed water columns of the Southern Ocean? Limnol. Oceanogr., 55, 1248-1264.
2. Allen, A. E., LaRoche, J., Maheswari, U. et al. (2008) Whole-cell response of the pennate diatom Phaeodactylum tricornutum to iron starvation. Proc. Natl Acad. Sci. USA, 105, 10438-10443.
3. Armbrust, E. V. (2009) The life of diatoms in the world's oceans. Nature, 459, 185-192.
4. Arsalane, W., Rousseau, B. and Duval, J.-C. (1994) Influence of the pool size of the xanthophyll cycle on the effects of light stress in a diatom: competition between photoprotection and photoinhibition. Photochem. Photobiol., 60, 237-243.
5. Bastow Wilson, J. (1990) Mechanisms of species coexistence: twelve explanations for Hutchinson's "paradox of the plankton": evidence from New Zealand plant communities. N. Z. J. Ecol., 13, 17-42.
6. Bailey, S. and Grossman, A. (2008) Photoprotection in cyanobacteria: regulation of light harvesting. Photochem. Photobiol., 84, 1410-1420.
7. Bidigare, R. R., Smith, R. C., Baker, K. S. et al. (1987) Oceanic primary production estimates from measurements of spectral irradiance and pigment concentrations. Global Biogeochem. Cycles, 1, 171-186.
8. Brown, J. H., Gillooly, J. F., Allen, A. P. et al. (2004) Toward a metabolic theory of ecology. Ecology, 85, 1771-1789.
9. Brunet, C. and Lizon, F. (2003) Tidal and diel periodicities of size fractioned phytoplankton pigment signatures at an offshore station in South-Eastern English Channel. Estuarine Coastal Shelf Sci., 56, 835-845.
10. Brunet, C., Brylinski, J. M. and Lemoine, Y. (1993) In situ variations of the xanthophylls diadinoxanthin and diatoxanthin: photoadaptation and relationships with an hydrodynamical system of the Eastern English Channel. Mar. Ecol. Prog. Ser., 102, 69-77. (Pubitemid 24430342)
11. Brunet, C., Casotti, R., Aronne, B. et al. (2003) Measured photophysiological parameters used as tools to estimate vertical water movements in the coastal Mediterranean. J. Plankton Res., 25, 1413-1425.
12. Brunet, C., Casotti, R., Vantrepotte, V. et al. (2006) Picophytoplankton diversity and photophysiology in the Strait of Sicily (Mediterranean Sea) in summer. I. Mesoscale variations. Aquat. Microbiol. Ecol., 44, 127-141.
13. Brunet, C., Casotti, R., Vantrepotte, V. et al. (2007) Vertical variability and diel dynamics of picophytoplankton in the Strait of Sicily (Mediterranean Sea) in summer. Mar. Ecol. Prog. Ser., 346, 15-26.
14. Brunet, C., Casotti, R. and Vantrepotte, V. (2008) Phytoplankton diel and vertical variability in photobiological responses at a coastal station in the Mediterranean Sea. J. Plankton Res., 30, 645-654.
15. Brunet, C., Johnsen, G., Lavaud, J. et al. (in press) Selected pigment applications in oceanography Pigments and photoacclimation processes. In Roy, S., Johnsen, G., Llewellyn, C. and Skarstad, E. (eds), Phytoplankton Pigments in Oceanography: Guidelines to Modern Methods, Series: Oceanographic Methodologies. Vol. 2. SCOR-UNESCO Publishing, Cambridge University Press.
16. Casotti, R., Mazza, S., Brunet, C. et al. (2005) Growth inhibition and toxicity of the diatom aldehyde 2-trans-4-trans decadienal on Thalassiosira weissflogii (Bacillariophyceae). J. Phycol., 41, 7-20.
17. Chevalier, E. M., Gévaert, F. and Créach, A. (2010) In situ photosynthetic activity and xanthophylls cycle development of undisturbed microphytobenthos in an intertidal mudflat. J. Exp. Mar. Biol. Ecol., 385, 44-49.
18. Claustre, H., Kerhervé, P., Marty, J.-C. et al. (1994) Phytoplankton photoadaptation related to some frontal physical processes. J. Mar. Syst., 5, 251-265.
19. Coesel, S., Obornik, M., Varela, J. et al. (2008) Evolutionary origins and functions of the carotenoid biosynthetic pathway in marine diatoms. PLoS ONE, 3, e2896.
20. Cogdell, R. J. (2006) The structural basis of non-photochemical quenching is revealed? TRENDS Plant Sci., 11, 59-60.
21. Demmig-Adams, B. and Adams, W. W. III (2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytol., 172, 11-21.
22. Dimier, C., Corato, F., Saviello, G. et al. (2007a) Photophysiological properties of the marine picoeukaryote Picochlorum RCC237 (Trebouxiophyceae, Chlorophyta). J. Phycol., 43, 275-283.
23. Dimier, C., Corato, F., Tramontano, F. et al. (2007b) Photoprotection and xanthophyll cycle activity in three diatoms. J. Phycol., 43, 937-947.
24. Dimier, C., Brunet, C., Geider, J. R. et al. (2009a) Growth and photoregulation dynamics of the picoeukaryote Pelagomonas calceolata in fluctuating light. Limnol. Oceanogr., 54, 823-836.
25. Dimier, C., Saviello, G., Tramontano, F. et al. (2009b) Comparative ecophysiology of the xanthophyll cycle in six marine phytoplanktonic species. Protist, 160, 397-411.
26. D'ortenzio, F., Iudicone, D., Boyer Montegut, C. et al. (2005) Seasonal variability of the mixed layer depth in the Mediterranean Sea as derived from in situ profiles. Geophys. Res. Lett., 32, L12605, doi:1.1029/2005GL022463.
27. Dubinsky, Z. and Schofield, O. (2010) From the light to the darkness: thriving at the light extremes in the oceans. Hydrobiologia, 639, 153-171.
28. Eisner, L. B., Twardowski, M. S., Cowles, T. J. et al. (2003) Resolving phytoplankton photoprotective: photosynthetic carotenoid ratios on fine scales using in situ absorption measurements. Limnol. Oceanogr., 48, 632-646.
29. Falkowski, P. G. and Raven, J. A. (2007) Aquatic Photosynthesis. Blackwell Science Publishers, Malden, USA, 375 pp.
30. Finkel, Z. (2001) Light absorption and size scaling of light-limited metabolism in marine diatoms. Limnol. Oceanogr., 46, 86-94.
31. Flöder, S. U. J. and Kawabata, Z.-I. (2002) The influence of fluctuating light intensities on species composition and diversity of natural phytoplankton communities. Oecologia, 133, 395-401.
32. Fujiki, T., Toda, T., Kikuchi, T. et al. (2003) Photoprotective response of xanthophyll pigments during phytoplankton blooms in Sagami Bay, Japan. J. Plankton Res., 25, 317-322.
33. Goss, R. and Jakob, T. (2010) Regulation and function of xanthophyll cycle-dependent photoprotection in algae. Photosynth. Res., doi:10.1007/s11120- 010-9536-x.
34. Griffith, G. P., Vennell, R. and Williams, M. J. M. (2010) An algal photoprotection index and vertical mixing in the Southern Ocean. J. Plankton Res., 32, 515-528.
35. Grobbelaar, J. (2006) Photosynthetic response and acclimation of microalgae to light fluctuations. In: Subba Rao, D. V. (ed.), Algal Cultures Analogues of Blooms and Applications. Science Publishers, Enfield, USA, pp. 671-683.
36. Gundermann, K. and Büchel, C. (2008) The fluorescence yield of the trimeric fucoxanthin chlorophyll-protein FCPa in the diatom Cyclotella meneghiniana is dependent on the amount of bound diatoxanthin. Photosynth. Res., 95, 229-235.
37. Huisman, J., Johansson, A. M., Folmer, E. O. et al. (2001) Towards a solution of the plankton paradox: the importance of physiology and life history. Ecol. Lett., 4, 408-411.
38. Hutchinson, G. E. (1961) The paradox of the plankton. Am. Nat., 95, 137-145.
39. Kashino, Y., Kudoh, S., Hayashi, Y. et al. (2002) Strategies of phytoplankton to perform effective photosynthesis in the North water. Deep-Sea Res. II, 49, 5049-5061.
40. Key, T., McCarthy, A., Campbell, D. A. et al. (2010) Cell size trade-off govern light exploitation strategies in marine phytoplankton. Environ. Microbiol., 12, 95-104.
41. Kirilovsky, D. (2007) Photoprotection in cyanobacteria: the orange carotenoid protein (OCP)-related non-photochemical-quenching mechanism. Photosynth. Res., 93, 7-16.
42. Kooistra, W. C. F., Gersonde, R., Medlin, L. K. et al. (2007) The origin and evolution of the diatoms: their adaptation to a planktonic existence. In: Falkowski, P. G. and Knoll, A. H. (eds.), Evolution of planktonic photoautotrophs. Academic Press Inc., pp. 207-250.
43. Kropuenske, L. R., Mills, M. M., van Dijken, G. L. et al. (2009) Photophysiology in two major Southern Ocean phytoplankton taxa: Photoprotection in Phaeocystis antarctica and Fragillariopsis cylindrus. Limnol. Oceanogr., 54, 1176-1196.
44. Laurion, I. and Roy, S. (2009) Growth and photoprotection in three dinoflagellates (including two strains of Alexandrium tamarense) and one diatom exposed to four weeks of natural and enhanced ultraviolet-B radiation. J. Phycol., 45, 16-33.
45. Lavaud, J. (2007) Fast regulation of photosynthesis in diatoms: mechanisms, evolution and ecophysiology. Funct. Plant Sci. Biotech., 1, 267-287.
46. Lavaud, J. and Kroth, P. G. (2006) In diatoms, the transthylakoid proton gradient regulates the photoprotective non-photochemical fluorescence quenching beyond its control on the xanthophyll cycle. Plant Cell Physiol., 47, 1010-1016.
47. Lavaud, J., Rousseau, B., van Gorkom, H. J. et al. (2002a) Influence of the diadinoxanthin pool size on photoprotection in the marine planktonic diatom Phaeodactylum tricornutum. Plant Physiol., 129, 1398-1406.
48. Lavaud, J., Rousseau, B. and Etienne, A.-L. (2002b) In diatoms, a transthylakoidal proton gradient alone is not sufficient for nonphotochemical fluorescence quenching. FEBS Lett., 523, 163-166.
49. Lavaud, J., Rousseau, B. and Etienne, A.-L. (2003) Enrichment of the light-harvesting complex in diadinoxanthin and implications for the nonphotochemical quenching fluorescence quenching in diatoms. Biochemistry, 42, 5802-5808.
50. Lavaud, J., Rousseau, B. and Etienne, A.-L. (2004) General features of photoprotection by energy dissipation in planktonic diatoms (Bacillariophyceae). J. Phycol., 40, 130-137.
51. Lavaud, J., Strzepeck, R. F. and Kroth, P. G. (2007) Photoprotection capacity differs among diatoms: possible consequences on the spatial distribution of diatoms related to fluctuations in the underwater light climate. Limnol. Oceanogr., 52, 1188-1194.
52. Lewis, M. R., Cullen, J. J. and Platt, T. (1984) Relationships between vertical mixing and photoadaptation of phytoplankton: similarity criteria. Mar. Ecol. Prog. Ser., 15, 141-149.
53. Li, Z., Wakao, S., Fischer, B. B. et al. (2009) Sensing and responding to excess light. Annu. Rev. Plant Biol., 60, 239-260.
54. Liess, A., Lange, K., Schulz, F. et al. (2009) Light, nutrients and grazing interact to determine diatom species richness via change to productivity, nutrient state and grazing activity. J. Ecol., doi: 10.1111/j.1365-2745.2008.01463.x.
55. Litchman, E. (2000) Growth rate of phytoplankton under fluctuating light. Freshwater Biol., 44, 223-235.
56. Litchman, E. and Klausmeier, C. A. (2001) Competition of phytoplankton under fluctuating irradiance. Am. Nat., 157, 170-187.
57. Litchman, E. and Klausmeier, C. A. (2008) Trait-based community ecology of phytoplankton. Annu. Rev. Ecol. Evol. Syst., 39, 615-639.
58. Long, S. P., Humphries, S. and Falkowsi, P. G. (1994) Photoinhibition of photosynthesis in nature. Ann. Rev. Plant Physiol. Plant Mol. Biol., 45, 633-662.
59. MacIntyre, H. L., Kana, T. M. and Geider, J. R. (2000) The effect of water motion on the short-term rates of photosynthesis by marine phytoplankton. TRENDS Plant Sci., 5, 12-17.
60. Mangoni, O., Carrada, G. C., Modigh, M. et al. (2009) Photoacclimation in Antarctic bottom ice algae: an experimental approach. Polar Biol., 32, 325-335.
61. Materna, A. C., Sturm, S., Kroth, P. G. et al. (2009) First induced plastid genome mutations in an alga with secondary plastids: psbA mutations in the diatom Phaeodactylum tricornutum (Bacillariophyceae) reveal consequences on the regulation of photosynthesis. J. Phycol., 45, 838-846.
62. Meyer, A. A., Tackx, M. and Daro, N. (2000) Xanthophyll cycling in Phaeocystis globosa and Thalassiosira sp.: a possible mechanism for species succession. J. Sea Res., 43, 373-384.
63. Mitrovic, S. M., Howden, C. G., Bowling, L. C. et al. (2003) Unusual allometry between in situ growth of freshwater phytoplankton under static and fluctuating light environments: possible implications for dominance. J. Plankton Res., 25, 517-526.
64. Moline, M. A. (1998) Photoadaptative response during the development of a coastal Antarctic diatom bloom and relationship to water column stability. Limnol. Oceanogr., 43, 146-153.
65. Müller, A. M. and Wasmund, N. (2003). Photophysiology of surface phytoplankton communities in a transect from the mouth of the Peene-strom to the Arkona Sea (Baltic). Internat. Rev. Hydrobiol., 88, 482-497.
66. Mullineaux, C. W. and Emlyn-Jones, E. (2004) State-transitions: an example of acclimation to low-light stress. J. Exp. Bot., 56, 389-393.
67. Nymark, M., Valle, K. C., Brembu, T. et al. (2009) An integrated analysis of molecular acclimation to high light in marine diatom Phaeodactylum tricornutum. PLoS ONE, 4, e7743.
68. Olaizola, M., Bienfang, P. K. and Ziemann, D. A. (1992) Pigment analysis of phytoplankton during a subarctic bloom: xanthophylls cycling. J. Exp. Mar. Biol. Ecol., 158, 59-74.
69. Peers, G., Truong, T. B., Ostendorf, E. et al. (2009) An ancient lightharvesting protein is critical for the regulation of algal photosynthesis. Nature, 462, 518-521.
70. Raven, J. A. and Kübler, J. A. (2002) New light on the scaling of metabolic rate with the size of algae. J. Phycol., 38, 11-16.
71. Raven, J. A. and Geider, J. R. (2003) Adaptation, acclimation and regulation in algal photosynthesis. In Larkum, W. D., Douglas, S. E. and Raven, J. A. (eds.), Photosynthesis in Algae. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 385-412.
72. Rost, B. and Riebesell, U. (2004) Coccolithophores and the biological pump: responses to environmental changes. In Thierstein, H. R. and Young, J. R. (eds), Coccolithophores: From Molecular Processes to Global Impact. Springer, Berlin, Germany, pp. 99-125.
73. Ruban, A. V. and Johnson, M. P. (2009) Dynamics of higher plant photosystem cross-section associated with state-transitions. Photosynth. Res., 99, 173-183.
74. Schumann, A., Goss, R., Jakob, T. et al. (2007) Investigations on the quenching efficiency of diatoxanthin in cells of Phaeodactylum tricornutum (Bacillariophyceae) with different pool sizes of xanthophylls cycle pigments. Phycologia, 46, 113-117.
75. Serodio, J., Cruz, S., Vieira, S. et al. (2005) Non-photochemical quenching of chlorophyll fluorescence and operation of the xanthophyll cycle in estuarine microphytobenthos. J. Exp. Mar. Biol. Ecol., 326, 157-169.
76. Six, C., Finkel, Z. V., Irwin, A. J. et al. (2007) Light variability illuminates niche partitioning among marine picocyanobacteria. PLoS ONE, 2, e1341.
77. Six, C., Finkel, Z., Rodriguez, F. et al. (2008) Contrasting photoacclimation costs in ecotypes of the marine eukaryote picoplankter Ostreococcus. Limnol. Oceanogr., 53, 255-265.
78. Six, C., Sherrard, R., Lionard, M. et al. (2009) Photosystem II and pigment dynamics among ecotypes of the Green Alga Ostreococcus. Plant Physiol., 151, 379-390.
79. Sommer, U. (1995) An experimental test of the intermediate disturbance hypothesis using cultures of marine phytoplankton. Limnol. Oceanogr., 40, 1271-1277. (Pubitemid 3016472)
80. Staehr, P. A., Henriksen, P. and Markager, S. (2002) Photoacclimation of four marine phytoplankton species to irradi.ance and nutrient availability. Mar. Ecol. Prog. Ser., 238, 47-59.
81. Strzepek, R. F. and Harrison, P. J. (2004) Photosynthetic architecture differs in costal and oceanic diatoms. Nature, 431, 689-692.
82. Timmermans, K. R., van der Wagt, B., Veldhuis, M. J. W. et al. (2005) Physiological responses of three species of marine picophytoplankton to ammonium, phosphate, iron and light limitation. J. Sea Res., 53, 109-120.
83. van de Poll, W. H. and Buma, A. G. J. (2009) Does ultraviolet radiation affect the xanthophyll cycle in marine phytoplankton? Photochem. Photobiol. Sci., 8, 1295-1301.
84. van de Poll, W. H., van Leeuwe, M. A., Roggeveld, J. et al. (2005) Nutrient limitation and high irradiance reduce PAR and UV-induced viability loss in the Antarctic diatom Chaetoceros brevis (Bacillariophyceae). J. Phycol., 41, 840-850.
85. van de Poll, W. H., Visser, R. J. W. and Buma, A. G. J. (2007) Acclimation to a dynamic irradiance regime changes excessive irradiance sensitivity of Emiliana huxleyi and Thalassiosira weissflogii. Limnol. Oceanogr., 52, 1430-1438.
86. van de Poll, W. H., Buma, A. G. J., Visser, R. J. W. et al. (2010) Xanthophyll cycle activity and photosynthesis of Dunaliella tertiolecta (Chlorophyceae) and Thalassiosira weissflogii (Bacillariophyceae) during fluctuating solar radiation. Phycologia, 49, 249-259.
87. van Leeuwe, M. A., van Sikkelerus, B., Gieskes, W. W. C. et al. (2005) Taxon specific differences in photoacclimation to fluctuating irradiance in an Antarctic diatom and a green flagellate. Limnol. Oceanogr., 288, 9-19.
88. van Leeuwe, M. A., Brotas, V., Consalvey, M. et al. (2008) Photoacclimation in microphytobenthos and the role of the xanthophylls cycle. Eur. J. Phycol., 43, 123-132.
89. Wagner, H., Jakob, T. and Wilhelm, C. (2006) Balancing the energy flow from captured light to biomass under fluctuating light conditions. New Phytol., 169, 95-108.
90. Welschmeyer, N. A. and Hoepffner, N. (1986) Rapid xanthophylls cycling: an in situ tracer for mixing in the upper ocean. EOS. Trans. Am. Geophys. Union, 67, 969.
91. Wilhelm, C., Büchel, C., Fisahn, J. et al. (2006) The regulation of carbon and nutrient assimilation in diatoms is significantly different from green algae. Protist, 157, 91-124.
92. Wilson, A., Ajlani, G., Verbavatz, J. M. et al. (2006) A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria. Plant Cell, 18, 992-1007.