Photosynthetic acclimation and photoprotective mechanism of Haematococcus pluvialis (Chlorophyceae) during the accumulation of secondary carotenoids at elevated irradiation

Phycologia

Volumn 45, Issue 2, 2006, Pages 117-126

  Qiu, Baosheng ^a   Li, Ying ^a  

^a CENTRAL CHINA NORMAL UNIVERSITY   (China)

Author keywords

Haematococcus pluvialis; Photoinhibition; Photoprotection; Photosynthesis; Secondary carotenoids

Indexed keywords

CHLOROPHYCEAE; HAEMATOCOCCUS PLUVIALIS;

EID: 33644955824     PISSN: 00318884     EISSN: None     Source Type: Journal    
DOI: 10.2216/04-99.1     Document Type: Article

References (58)

1. ANDERSSON B. & ARO E.M. 2001. Photodamage and D1 protein turnover in photosystem II. In: Regulation of photosynthesis - advances in photosynthesis and respiration, vol. 11 (Ed. by E.M. Aro & B. Andersson), pp. 377-393. Kluwer Academic Press, Dordrecht, The Netherlands.
2. ARO E.M., MCCAFFERY S. & ANDERSON J.M. 1993. Photoinhibition and D1 protein degradation in peas acclimated to different growth irradiances. Plant Physiology 103: 835-843.
3. BENEMANN J.R. 1992. Microalgae aquaculture feeds. Journal of Applied Phycology 4: 233-245.
4. BILGER W., BJÖRKMAN O. & THAYER S.S. 1989. Light-induced spectral absorbance changes in relation to photosynthesis and the epoxidation state of xanthophyll cycle components in cotton leaves. Plant Physiology 91: 542-551.
5. BOROWITZKA M.A., HUISMAN J.M. & OSBORN A. 1991. Culture of the astaxanthin-producing green alga Haematococcus pluvialis. 1. Effects of nutrients on growth and cell type. Journal of Applied Phycology 3: 295-304.
6. BOUSSIBA S. 2000. Carotenogenesis in the green alga Haematococcus pluvialis: cellular physiology and stress response. Physiologia Plantarum 108: 111-117.
7. BOUSSIBA S. & VONSHAK A. 1991. Astaxanthin accumulation in the green alga Haematococcus pluvialis. Plant and Cell Physiology 32: 1077-1082.
8. BOUSSIBA S., LU F. & VONSHAK A. 1992. Enhancement and determination of astaxanthin accumulation in green alga Haematococcus pluvialis. Methods in Enzymology 213: 386-391.
9. BOUSSIBA S., WANG B., YUAN J.P., ZARKA A. & CHEN F. 1999. Changes in pigments profile in the green alga Haematococcus pluvialis exposed to environmental stresses. Biotechnology Letters 21: 601-604.
10. CASPER-LINDLEY C. & BJÖRKMAN O. 1998. Fluorescence quenching in four unicellular algae with different light-harvesting and xanthophyll-cycle pigments. Photosynthesis Research 56: 277-289.
11. CZYGAN F.C. 1970. Blood-rain and blood-snow: nitrogen-deficient cells of Haematococcus pluvialis and Chlamydomonas nivalis. Archives of Microbiology 74: 69-76.
12. DAVIES B.H. 1976. Carotenoids. In: Chemistry and biochemistry of plant pigments (Ed. by T.W. Goodwin), pp. 38-166. Academic Press, London, UK.
13. DEMMIG-ADAMS B. & ADAMS W.W.III. 1993. The xanthophyll cycle, protein turnover, and the high light tolerance of sun-acclimated leaves. Plant Physiology 103: 1413-1420.
14. FRYXELL G.A. 1983. Survival strategies of the algae. Cambridge University Press, Cambridge, UK. 256 pp.
15. GRÜNEWALD K., HAGEN C. & BRAUNE W. 1997. Secondary carotenoid accumulation in flagellates of the green alga Haematococcus lacustris. European Journal of Phycology 32: 387-392.
16. GRÜNEWALD K., HIRSCHBERG J. & HAGEN C. 2001. Ketocarotenoid biosynthesis outside of plastids in the unicellular green alga Haematococcus pluvialis. Journal of Biological Chemistry 276: 6023-6029.
17. HAGEN C., BRAUNE W., BIRCKNER E. & NÜSKE J. 1993. Functional aspects of secondary carotenoids in Haematococcus lacustris [Girod] Rostafinski (Volvocales). I. The accumulation period as an active metabolic process. New Phylologist 125: 625-633.
18. HAGEN C., BRAUNE W. & BJÖRN L.O. 1994. Functional aspects of secondary carotenoids in Haematococcus lacustris (Volvocales). III. Action as a "sunshade." Journal of Phycology 30: 241-248.
19. HAGEN C., GRÜNEWALD K., SCHMIDT S. & MÜLLER J. 2000. Accumulation of secondary carotenoids in flagellates of Haematococcus pluvialis (Chlorophyta) is accompanied by an increase in per unit chlorophyll productivity of photosynthesis. European Journal of Phycology 35: 75-82
20. HARKER M., TSAVALOS A.J. & YOUNG A.J. 1995. Use of response surface methodology to optimise carotenogenesis in the microalga, Haematococcus pluvialis. Journal of Applied Phycology 7: 399-406.
21. HORTON P., RUBAN A.V. & WALTERS R.G. 1996. Regulation of light harvesting in green plants. Annual Review of Plant Physiology and Plant Molecular Biology 47: 655-684.
22. INSKEEP W.P. & BLOOM P.R. 1985. Extinction coefficients of chlorophyll a and b in N,N-dimethylformamide and 80% acetone. Plant Physiology 77: 483-485.
23. JOHNSON E.A. & AN G.H. 1991. Astaxanthin from microbial sources. Critical Reviews in Biotechnology 11: 297-326.
24. KOBAYASHI M. 2000. In vivo antioxidant role of astaxanthin under oxidative stress in the green alga Haematococcus pluvialis. Applied Microbiology and Biotechnology 54: 550-555.
25. KOBAYASHI M. 2003. Astaxanthin biosynthesis enhanced by reactive oxygen species in the green alga Haematococcus pluvialis. Biotechnology and Bioprocess Engineering 8: 322-330.
26. KOBAYASHI M., KAKIZONO T., NISHIO N. & NAGAI S. 1992. Effects of light intensity, light quality, and illumination cycle on astaxanthin formation in a green alga, Haematococcus pluvialis. Journal of Fermentation and Bioengineering 74: 61-63.
27. KOBAYASHI M., KAKIZONO T. & NAGAI S. 1993. Enhanced carotenoid biosynthesis by oxidative stress in acetate-induced cyst cells of a green unicellular alga, Haematococcus pluvialis. Applied and Environmental Microbiology 59: 867-873.
28. KOBAYASHI M., KURIMURA Y. & TSUJI Y. 1997. Light-independent, astaxanthin production by the green microalga Haematococcus pluvialis under salt stress. Biotechnology Letters 19: 507-509.
29. KRAUSE G.H. & WEIS E. 1991. Chlorophyll fluorescence and photosynthesis: the basics. Annual Review of Plant Physiology and Plant Molecular Biology 42: 313-349.
30. LEE Y.K. & SOH C.W. 1991. Accumulation of astaxanthin in Haematococcus lacustris (Chlorophyta). Journal of Phycology 27: 575-577.
31. LICHTENTHALER H.K. 1999. The 1-deoxy-D-xylulose-5-phosphate pathway of isoprenoid biosynthesis in plants. Annual Review of Plant Physiology and Plant Molecular Biology 50: 47-65.
32. LONG SP., HUMPHRIES S. & FALKOWSKI P.G. 1994. Photoinhibition of photosynthesis in Nature. Annual Review of Plant Physiology and Plant Molecular Biology 45: 633-662.
33. LORENZ R.T. & CYSEWSKI G.R. 2000. Commercial potential for Haematococcus microalgae as a natural source of astaxanthin. Trends in Biotechnology 18: 160-167.
34. LU F., VONSHAK A., ZARKA A. & BOUSSIBA S. 1998. Does astaxanthin protect Haematococcus against light damage? Zeitschrift für Naturforschung 53c: 93-100.
35. MASOJÍDEK J., KOPECKÝ J., KOBLÍ EK M. & TORZILLO G. 2004. The xanthophyll cycle in green algae (Chlorophyta): its role in the photosynthetic apparatus. Plant Biology 6: 342-349.
36. MATTOO A.K., GIARDI M.T., RASKIND A. & EDELMAN M. 1999. Dynamic metabolism of photosystem II reaction center proteins and pigments. Physiologia Plantarum 107: 454-461.
37. MIKI W. 1991. Biological functions and activities of animal carotenoids. Pure and Applied Chemistry 63: 141-146.
38. MÜLLER P., LI X.P. & NIYOGI K.K. 2001. Non-photochemical quenching. A response to excess light energy. Plant Physiology 125: 1558-1566.
39. NEUBAUER C. 1993. Multiple effects of DTT on non-photochemical fluorescence quenching in intact chloroplasts. Influence on violaxanthin de-epoxidase and ascorbate peroxidase activity. Plant Physiology 103: 575-583.
40. NISHIYAMA Y., YAMAMOTO H., ALLAKHVERDIEV S.I., INABA M., YOKOTA A. & MURATA N. 2001. Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. The EMBO Journal 20: 5587-5594.
41. PROCTOR V.W. 1957. Some controlling factors in the distribution of Haematococcus pluvialis. Ecology 38: 457-462.
42. PROCTOR M.C.F. & SMIRNOFF N. 2000. Rapid recovery of photosystems on rewetting desiccation-tolerant mosses: chlorophyll fluorescence and inhibitor experiments. Journal of Experimental Botany 51: 1695-1704.
43. QIU B.S. & LIU Q.F. 2000. The microalgae, Haematococcus: a review. Acta Hydrobiologica Sinica 24: 546-554.
44. RODRIGUES M.A., SANTOS C.P.D., YOUNG A.J., STRBAC D. & HALL D.O. 2002. A smaller and impaired xanthophyll cycle makes the deep sea macroalgae Laminaria abyssalis (Phaeophyceae) highly sensitive to daylight when compared with shallow water Laminaria digitata. Journal of Phycology 38: 939-947.
45. SANTOS M.F. & MESQUITA J.F. 1984. Ultrastructural study of Haematococcus lacustris [Girod.] Rostafinski (Volvocales). I. Some aspects of carotenogenesis. Cytologia 49: 215-228.
46. SHI T., CUNNINGHAM F.X., JR, YOUMANS M., GRABOWSKI B., SUN Z. & GANTT E. 1995. Cytochrome f loss in astaxanthin-accumulating red cells of Haematococcus pluvialis (Chlorophyceae): comparison of photosynthetic activity, photosynthetic enzymes, and thylakoid membrane polypeptides in red and green cells. Journal of Phycology 31: 897-905.
47. SOMMER T.R., POTTS W.T. & MORRISSY N.M. 1991. Utilization of microalgal astaxanthin by rainbow trout (Oncorhyncus mykiss). Aquaculture 94: 79-88.
48. SRIVASTAVA A., GUISSÉ B., GREPPIN H. & STRASSER R.J. 1997. Regulation of antenna structure and electron transport in photosystem II of Pisum sativum under elevated temperature probed by the fast polyphasic chlorophyll a fluorescence transient: OKJIP. Biochimica et Biophysica Acta 1320: 95-106.
49. STANIER R.Y., KUNISAWA M.M. & COHEN-BAZIRE G. 1971. Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriological Reviews 35: 171-201.
50. STEINBRENNER J. & LINDEN H. 2003. Light induction of carotenoid biosynthesis genes in the green alga Haematococcus pluvialis: regulation by photosynthetic redox control. Plant Molecular Biology 52: 343-356.
51. STRASSER B.J. & STRASSER R.J. 1995. Measuring fast fluorescence transients to address environmental questions: the JIP-test. In: Photosynthesis: from light to biosphere, vol. V (Ed. by P. Mathis), pp. 977-980. Kluwer Academic Press Publishers, Dordrecht, The Netherlands.
52. STRASSER R.J., SRIVASTAVA A. & TSIMILLI-MICHAEL M. 2000. The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Probing photosynthesis: mechanism, regulation and adaptation (Ed. by M. Yunus, U. Pathre & P. Mohanty), pp. 445-483. Taylor and Francis, London, UK.
53. TERAO J. 1989. Antioxidant activity of β-carotene-related carotenoids in solution. Lipids 24: 659-661.
54. TJAHJONO A.E., HAYAMA Y., KAKIZONO T., TERADA Y., NISHIO N. & NAGAI S. 1994. Hyper-accumulation of astaxanthin in a green alga Haematococcus pluvialis at elevated temperatures. Biotechnology Letters 16: 133-138.
55. TORZILLO G., GOKSAN T., FARALONI C., KOPECKY J. & MASOJÍDEK J. 2003. Interplay between photochemical activities and pigment composition in an outdoor culture of Haematococcus pluvialis during the shift from the green to red stage. Journal of Applied Phycology 15: 127-136.
56. WANG B., ZARKA A., TREBST A. & BOUSSIBA S. 2003. Astaxanthin accumulation in Haematococcus pluvialis (Chlorophyceae) as an active photoprotective process under high irradiance. Journal of Phycology 39: 1116-1124
57. YONG Y.Y.R. & LEE Y.K. 1991. Do carotenoids play a photoprotective role in the cytoplasm of Haematococcus lacustris (Chlorophyta). Phycologia 30: 257-261.
58. ZLOTNIK I., SUKENIK A. & DUBINSKY Z. 1993. Physiological and photosynthetic changes during the formation of red aplanospores in the Chlorophyte Haematococcus pluvialis. Journal of Phycology 29: 463-469.