Implication of nitric oxide in the heat-stress-induced cell death of the symbiotic alga Symbiodinium microadriaticum

Marine Biology

Volumn 156, Issue 11, 2009, Pages 2209-2220

  Bouchard, Josée Nina ^a,b   Yamasaki, Hideo ^a  

^a UNIVERSITY OF THE RYUKYUS   (Japan)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GLOBAL WARMING; HEAT SHOCK; MICROALGA; MORTALITY; NITRIC OXIDE; PHYTOPLANKTON; SEA SURFACE TEMPERATURE; SURVIVAL; SYMBIONT;

ALGAE; MAMMALIA; SYMBIODINIUM MICROADRIATICUM;

EID: 71349086617     PISSN: 00253162     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00227-009-1249-3     Document Type: Article

References (79)

1. Affenzeller MJ, Darehshouri A, Andosch A, Lütz C, Lütz-Meindl U (2009) Salt stress-induced cell death in the unicellular green alga Micrasterias denticulata. J Exp Bot 60: 939-954.
2. Almeida B, Buttner S, Ohlmeier S, Silva A, Mesquita A, Sampaio-Marques B, Osório NS, Kollau A, Mayer B, Leão C, Laranjinha J, Rodrigues F, Madeo F, Ludovico P (2007) NO-mediated apoptosis in yeast. J Cell Sci 120: 3279-3288.
3. Berges JA, Falkowski PG (1998) Physiological stress and cell death in marine phytoplankton: induction of proteases in response to nitrogen or light limitation. Limnol Oceanogr 43: 129-135.
4. Berman-Frank I, Bidle KD, Haramaty L, Falkowski PG (2004) The demise of the marine cyanobacterium Trichodesmium spp., via an autocatalysed cell death pathway. Limnol Oceanogr 49: 997-1005.
5. Bidle KD, Bender SJ (2008) Iron starvation and culture age activate metacaspases and programmed cell death in the marine diatom Thalassiosira pseudonana. Eukaryot Cell 7: 223-236.
6. Bidle KD, Falkowski PG (2004) Cell death in planktonic, photosynthetic microorganisms. Nat Rev 2: 643-655.
7. Bidle KD, Hamaraty L, Barcelos e Ramos J, Falkowski P (2007) Viral activation and recruitment of metacaspases in the unicellular coccolithophore, Emiliania huxleyi. Proc Natl Acad Sci USA 104: 6049-6054.
8. Bonneau L, Ge Y, Drury GE, Gallois P (2008) What happened to plant caspases? J Exp Bot 59(3): 491-499. doi: 10. 1093/jxb/erm352.
9. Bouchard JN, Yamasaki H (2008) Heat stress stimulates nitric oxide production in Symbiodinium microadriaticum: a possible linkage between nitric oxide and the coral bleaching phenomenon. Plant Cell Physiol 49: 641-652.
10. Bozhkov PV, Suarez MF, Filonova LH, Daniel G, Zamyatnin AA Jr, Rodriguez-Nieto S, Zhivotovsky B, Smertenko A (2005) Cysteine protease mcII-Pa executes programmed cell death during plant embryogenesis. Proc Natl Acad Sci USA 102: 14463-14468.
11. Brüne B (2003) Nitric oxide: NO apoptosis or turning it ON. Cell Death Differ 10: 864-869.
12. Brussaard CPD, Marie D, Thyrhaug R, Bratbak G (2001) Flow cytometric analysis of phytoplankton viability following viral infection. Aquat Microb Ecol 26: 157-166.
13. Buma AG, Zemmerlink HJ, Sjollema K, Gieskes WWC (1996) UVB radiation modifies protein and photosynthetic pigment content, volume and ultrastructure of marine diatoms. Mar Ecol Prog Ser 142: 47-54.
14. Chung C-C, Hwang S-PL, Chang J (2008) Nitric oxide as a signalling factor to upregulate the death-specific protein in a marine diatom, Skeletonema costatum, during blockage of electron flow in photosynthesis. Appl Env Microbiol 74: 6521-6527.
15. Clarke A, Desikan R, Hurst RD, Hancock JT, Neill SJ (2000) NO way back: nitric oxide and programmed cell death in Arabidopsis thaliana suspension cultures. Plant J 24: 667-677.
16. Coles SL, Brown BE (2003) Coral bleaching-capacity for acclimatization and adaptation. Adv Mar Biol 46: 183-223.
17. Darehshouri A, Affenzeller M, Lütz-Meindl U (2008) Cell death upon H2O2 induction in the unicellular green alga Micrasterias. Plant Biol 10: 32-745.
18. de Pinto MC, Tommasi F, De Gara L (2002) Changes in the antioxidant systems as part of the signaling pathway responsible for the programmed cell death activated by nitric oxide and reactive oxygen species in tobacco bright-yellow 2 cells. Plant Physiol 130: 1-11.
19. Delledonne M (2005) NO news is good news for plants. Curr Opin Plant Biol 8: 390-396.
20. Delledonne M, Xia Y, Dixon RA, Lamb C (1998) Nitric oxide functions as a signal in plant disease resistance. Nature 394: 585-588.
21. Delledonne M, Zeier J, Marocco A, Lamb C (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc Natl Acad Sci USA 98: 13454-13459.
22. Deponte M (2008) Programmed cell death in protists. Biochem Biophys Acta 1783(7): 1396-1405. doi: 10. 1016/j. bbamcr. 2008. 01. 018.
23. Dunn SR, Bythell JC, Le Tissier MDA, Burnett WJ, Thomason JC (2002) Programmed cell death and cell necrosis activity during hyperthermic stress-induced bleaching of the sea anemone Aiptasia sp. J Exp Mar Biol Ecol 272: 29-53.
24. Dunn SR, Thomason JC, Le Tissier MDA, Bythell JC (2004) Heat stress induces different forms of cell death in sea anemones and their endosymbiotic algae depending on temperature and duration. Cell Death Differ 11: 1213-1222.
25. Dunn SR, Schnitzler CE, Weis VM (2007) Apoptosis and autophagy as mechanisms of dinoflagellate symbiont release during cnidarian bleaching: every way you lose. Proc R Soc B 274: 3079-3085.
26. Esch P, Techel D, Schimmoller N, Rensing L (1995) Heat shock effects on the circadian rhythm of protein synthesis and phosphorylation of ribosomal proteins in Gonyaulax polyedra. Chronobiol Int 12: 369-381.
27. Frada M, Probert I, Allen MJ, Wilson WH, de Vargas C (2008) The "Cheshire Cat" escape strategy of the coccolithophore Emiliania huxleyi in response to viral infection. Proc Natl Acad Sci USA 105: 15944-15949.
28. Franklin DJ, Berges JA (2004) Mortality in cultures of the dinoflagellate Amphidinium carterae during culture senescence and darkness. Proc Biol Sci 271: 2099-2107.
29. Franklin DJ, Hoegh-Guldberg O, Jones RJ, Berges JA (2004) Cell death and degeneration in the symbiotic dinoflagellates of the coral Stylophora pistillata during bleaching. Mar Ecol Progr Ser 272: 117-130.
30. Franklin DJ, Brussaard CPD, Berges JA (2006) What is the role and nature of programmed cell death in phytoplankton ecology? Eur J Phycol 41: 1-14.
31. Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds) Culture of marine invertebrate animals. Plenum Press, New York, pp 26-60.
32. Hoegh-Guldberg O (1999) Climate change and World's coral reefs: implications for the Great Barrier Reef. Mar Freshw Res 50: 839-866.
33. Hong JK, Yun B-W, Kang J-G, Raja MU, Kwon E, Sorhagen K, Chu C, Wang Y, Loake GJ (2008) Nitric oxide function and signaling in plant disease resistance. J Exp Bot 59: 147-154.
34. Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c and c2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz 167: 191-194.
35. Jiménez C, Capasso JM, Edelstein CL, Rivard CJ, Lucia S, Breusegem S, Berl T, Segovia M (2009) Different ways to die: cell death modes of the unicellular chlorophyte Dunaliella viridis exposed to various environmental stresses are mediated by the caspase-like activity DEVDase. J Exp Bot 60(3): 815-828. doi: 10. 1093/jxb/ern330.
36. Kirchman DL (1999) Phytoplankton death in the sea. Nature 398: 293-294.
37. Kojima H, Urano Y, Kikuchi K, Higuchi T, Hirata Y, Nagano T (1999) Fluorescent indicators for imaging nitric oxide production. Angew Chem Int Ed 38: 3209-3212.
38. Lesser MP, Farrell JH (2004) Exposure to solar radiation increases damage to both host tissues and algal symbionts of corals during thermal stress. Coral Reefs 23: 367-377.
39. Madeo F, Herker E, Maldener C, Wissing S, Lächelt S, Herlan M, Fehr M, Lauber K, Sigrist SJ, Wesselborg S, Fröhlich KU (2002) A caspase-related protease regulates apoptosis in yeast. Mol Cell 9: 911-917.
40. Miller-Morey JS, van Dolah FM (2004) Differential responses of stress proteins, antioxidant enzymes, and photosynthetic efficiency to physiological stresses in the Florida red tide dinoflagellate, Karenia brevis. Comp Biochem Physiol C 138: 493-505.
41. Murgia I, Tarantino D, Vannini C, Bracale M, Carravieri S, Soave C (2004a) Arabidopsis thaliana plants overexpressing thylakoidal ascorbate peroxidase show increased resistance to Paraquat-induced photooxidative stress and to nitric oxide-induced cell death. Plant J 38: 940-953.
42. Murgia I, Concetta de Pinto M, Delledonne M, Soave C, De Gara L (2004b) Comparative effects of various nitric oxide donors on ferritin regulation, programmed cell death, and cell redox state in plant cells. J. Plant Physiol 161: 777-783.
43. Nedelcu AM, Miles IH, Fagir AM, Karol K (2008) Adaptive eukaryote-to-eukaryote lateral gene transfer: stress-related genes of algal origin in the closest unicellular relatives of animals. J Evol Biol 21: 1852-1860.
44. Neill S, Bright J, Desikan R, Hancock J, Harrison J, Wilson I (2008) Nitric oxide evolution and perception. J Exp Bot 59: 25-35.
45. Nicholson DW (1999) Caspase structure, proteolytic substrates, and function during apoptotic cell death. Cell Death Differ 6: 1028-1042.
46. Nicholson DW, Ali A, Thornberry NA, Vaillancourt JP, Ding CK, Gallant M, Gareau Y, Griffin PR, Labelle M, Lazebnik YA, Munday NA, Raju AM, Smulson ME, Yamin T-T, Yu VL, Miller DK (1995) Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 376: 37-43.
47. Parker MS, Mock T, Armbrust EV (2008) Genomic insights into marine microalgae. Annu Rev Genet 42: 619-645.
48. Pedroso MC, Magalhaes JR, Durzan D (2000) A nitric oxide burst precedes apoptosis in angiosperm and gymnosperm callus cells and foliar tissues. J Exp Bot 51: 1027-1036.
49. Perez S, Weis V (2006) Nitric oxide and cnidarian bleaching: an eviction notice mediates breakdown of a symbiosis. J Exp Biol 209: 2804-2810.
50. Piszczek E, Gutman W (2007) Caspase-like proteases and their role in programmed cell death in plants. Acta Physiol Plant 29: 391-398.
51. Richier S, Sabourault C, Courtiade J, Zucchini N, Allemand D (2006) Oxidative stress and apoptotic events during thermal stress in the symbiotic sea anemone, Anemonia viridis. FEBS J 273: 4186-4198.
52. Ross C, Santiago-Vázquez L, Paul V (2006) Toxin release in response to oxidative stress and programmed cell death in the cyanobacterium Microcystis aeruginosa. Aquat Toxicol 78: 66-73.
53. Saunders BK, Muller-Parker G (1997) The effects of temperature and light on two algal populations in the temperate sea anemone Anthopleura elegantissima (Brandt, 1835). J Exp Mar Biol Ecol 211: 213-224.
54. Saviani EE, Orsi CH, Oliveira JFP, Pinto-Maglio CAF, Salgado I (2002) Participation of the mitochondrial permeability transition pore in nitric oxide-induced plant cell death. FEBS Lett 510: 136-140.
55. Scheiner SM, Gurevitch J (2001) Design and analysis of ecological experiments, 2nd edn. Oxford University Press, New York, p 415.
56. Segovia M (2008) Programmed cell death in dinoflagellates. In: Pérez Martin JM (ed) Programmed cell death in protozoa. Landes Bioscience, Austin, pp 126-142.
57. Segovia M, Berges JA (2005) Effects of inhibitors of protein synthesis and DNA replication on the induction of proteolytic activities, caspase-like activities and cell death in the unicellular chlorophyte Dunaliella tertiolecta. Eur J Phycol 40: 21-30.
58. Segovia M, Haramati L, Berges JA, Falkowski PG (2003) Cell death in the unicellular chlorophyte Dunaliella tertiolecta. A hypothesis on the evolution of apoptosis in higher plants and metazoans. Plant Physiol 132: 99-105.
59. Takahashi S, Nakamura T, Sakamizu M, van Woesik R, Yamasaki H (2004) Repair machinery of symbiotic photosynthesis as the primary target of heat stress for reef-building corals. Plant Cell Physiol 45: 251-255.
60. Thornberry NA (1999) Caspases: a decade of death research. Cell Death Differ 6: 1023-1027.
61. Thornberry NA, Lazebnik Y (1998) Caspases: enemies within. Science 281: 1312-1316.
62. Timmermans KR, Veldhuis MJW, Brussaard CPD (2007) Cell death in three marine diatom species in response to different irradiance levels, silicate or iron concentrations. Aquat Microb Ecol 46: 253-261.
63. Trapido-Rosenthal HG, Sharp KH, Galloway TS, Morrall CE (2001) Nitric oxide and cnidarian-dinoflagellate symbioses: pieces of a puzzle. Am Zool 41: 247-257.
64. Uren AG, O'Rourke K, Aravind L, Pisabarro MT, Seshagiri S, Koonin EV, Dixit VM (2000) Identification of paracaspases and metacaspases: two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma. Mol Cell 6: 961-967.
65. Vardi A, Berman-Frank I, Rozenberg T, Hadas O, Kaplan A, Levine A (1999) Programmed cell death of the dinoflagellate Peridinium gatunense is mediated by CO2 limitation and oxidative stress. Curr Biol 9: 1061-1064.
66. Vardi A, Eisenstadt D, Murik O, Berman-Frank I, Zohary T, Levine A, Kaplan A (2007) Synchronisation of cell death in a dinoflagellate population is mediated by an excreted thiol protease. Environ Microbiol 9: 360-369.
67. Vardi A, Bidle D, Kwityn C, Hirsh DJ, Thompson SM, Callow JA, Falkowski P, Bowler C (2008) A diatom gene regulating nitric-oxide signaling and susceptibility to diatom-derived aldehydes. Curr Biol 18: 895-899.
68. Veldhuis MJW, Cucci TL, Sieracki ME (1997) Cellular DNA content of marine phytoplankton using two new fluorochromes: taxonomic and ecological implications. J Phycol 33: 527-541.
69. Veldhuis MJW, Kraay GW, Timmermans KR (2001) Cell death in phytoplankton: correlation between changes in membrane permeability, photosynthetic activity, pigmentation and growth. Eur J Phycol 36: 167-177.
70. Vercammen D, van de Cotte B, De Jaeger G, Eeckhout D, Casteels P, Vandepoele K, Vandenberghe I, van Beeumen J, Inzé D, van Breusegem F (2004) Type II metacaspases Atmc4 and Atmc9 of Arabidopsis thaliana cleave substrates after arginine and lysine. J Biol Chem 44: 45329-45336.
71. Vincent W (1983) Fluorescence properties of the freshwater phytoplankton: three algal classes compared. Br Phycol J 18: 5-21.
72. Warner ME, Fitt WK, Schmidt GW (1996) The effect of elevated temperature on the photosynthetic efficiency of zooxanthellae in hospite from four different species of reef coral: a novel approach. Plant Cell Environ 19: 291-299.
73. Watanabe N, Lam E (2005) Two Arabidopsis metacaspases AtMCP1b and AtMCP2b are arginine/lysine-specific cysteine proteases and activate apoptosis-like cell death in yeast. J Biol Chem 280: 14691-14699.
74. Weis VM (2008) Cellular mechanisms of cnidarian bleaching: stress causes the collapse of symbiosis. J Exp Biol 211: 3059-3066.
75. Wilkerson FP, Muller Parker G, Muscatine L (1983) Temporal patterns of cell division in natural populations of endosymbiotic algae. Limnol Oceanogr 28: 1009-1014.
76. Wink DA, Cook JA, Pacelli R, DeGraff W, Gamson J, Liebmann J, Krishna MA, Mitchell JB (1996) The effect of various nitric oxide-donor agents on hydrogen peroxide-mediated toxicity: a direct correlation between nitric oxide formation and protection. Arch Biochem Biophys 331: 241-248.
77. Zago E, Morsa S, Dat JF, Alard P, Ferrarini A, Inzé D, Delledonne M, van Breusegem F (2006) Nitric oxide- and hydrogen peroxide-responsive gene regulation during cell death induction in tobacco. Plant Physiol 141: 404-411.
78. Zheng-Bin Z, Chun-Ying L, Zhen-Zhen W, Lei X, Pei-Feng L (2006) Detection of nitric oxide in culture media and studies on nitric oxide formation by marine microalgae. Med Sci Monit 12: BR75-BR85.
79. Zuppini A, Andreoli C, Baldan B (2007) Heat stress: an inducer of programmed cell death in Chlorella saccarophila. Plant Cell Physiol 48: 1000-1009.