What is the role and nature of programmed cell death in phytoplankton ecology?

European Journal of Phycology

Volumn 41, Issue 1, 2006, Pages 1-14

  Franklin, Daniel J ^a   Brussaard, Corina P D ^b   Berges, John A ^c  

^a UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^b ROYAL NETHERLANDS INSTITUTE FOR SEA RESEARCH   (Netherlands)

^c UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

Author keywords

Apoptosis; Cell lysis; Microalgae; Necrosis; Phytoplankton mortality; Programmed cell death (PCD)

Indexed keywords

PHYTOPLANKTON;

ALGAE; ANIMALIA; BACTERIA (MICROORGANISMS); CHLOROPHYTA; CYANOBACTERIA; DINOPHYCEAE; METAZOA;

EID: 33644927576     PISSN: 09670262     EISSN: 14694433     Source Type: Journal    
DOI: 10.1080/09670260500505433     Document Type: Review

References (119)

1. ADAMEC, F., KAFTAN, D. & NEDBAL, L. (2005). Stress-induced filament fragmentation of Calothrix elenkinii (Cyanobacteria) is facilitated by death of high-fluorescence cells. J. Phycol., 41: 835-839.
2. AGUSTÍ, S. (2004). Viability and niche segregation of Prochlorococcus and Synechococcus cells across the Central Atlantic Ocean. Aquat. Microb. Ecol., 36: 53-59.
3. AGUSTÍ, S., SATTA, M.P., MURA, M.P. & BENAVENT, E. (1998). Dissolved esterase activity as a tracer of phytoplankton lysis: evidence of high phytoplankton lysis rates in the northwestern Mediterranean. Limnol. Oceanogr., 43: 1836-1849.
4. ALDSWORTH, T.G., SHARMAN, R.L. & DODD, C.E.R. (1999). Bacterial suicide through stress. Cell. Mol. Life Sci., 56: 378-383.
5. AMEISEN, J.C. (2002). On the origin, evolution, and nature of programmed cell death: a timeline of four billion years. Cell Death Diff., 9: 367-393.
6. ARAVIND, L., DIXIT, V.M. & KOONIN, E.V. (2001). Apoptotic molecular machinery: vastly increased complexity in vertebrates revealed by genome comparisons. Science, 291: 1279-1284.
7. ARMBRUST, J.C., BERGES, J.A., BOWLER, C., GREEN, B.R., MARTINEZ, D. & PUTNAM, N.H. (2004). The genome of the diatom Thalassiosira pseudonana: ecology, evolution and metabolism. Science, 306: 79-86.
8. ARNOULT, D., TATISCHEFF, I., ESTAQUIER, J., GIRARD, M., SUREAU, F., TISSIER, J.P., GRODET, A., DELLINGER, M., TRAINCARD, F., KAHN, A., AMEISEN, J. & PETIT, P.X. (2001). On the evolutionary conservation of the cell death pathway: Mitochondrial release of an apoptosis-inducing factor during Dictyostelium discoideum cell death. Mol. Biol. Cell, 12: 3016-3030.
9. BAULCOMBE, D. (2002). Viral supression of systemic silencing. Trends in Microbiol., 10: 306-308.
10. BEHRENDT, H. & NIXDORF, B. (1993). The carbon balance of phytoplankton production and loss processes based on in situ measurements in a shallow lake. Int. Rev. Gesamt. Hydrobiol., 78: 439-458.
11. BERGES, J.A. & FALKOWSKI, P.G. (1998). Physiological stress and cell death in marine phytoplankton: Induction of proteases in response to nitrogen or light limitation. Limnol. Oceanogr., 43: 129-135.
12. BERMAN, T., KAPLAN, B., CHAVA, S., VINER, Y., SHERR, B.F. & SHERR, E.B. (2001). Metabolically active bacteria in Lake Kinneret. Aquat. Microb. Ecol., 23: 213-224.
13. BERMAN-FRANK, I., BIDLE, K.D., HARAMATY, L. & FALKOWSKI, P.G. (2004). The demise of the cyanobacterium, Trichodesmium spp., via an autocatalyzed cell death pathway. Limnol. Oceanogr., 49: 997-1005.
14. BIDLE, K.D. & FALKOWSKI, P.G. (2004). Cell death in planktonic, photosynthetic microorganisms. Nature Rev. Microbiol., 2: 643-655.
15. BIDLE, K.D., HARAMATY, L. & FALKOWSKI, P.G. (2005). Roads to ruin: the development and relationship of programmed cell death and viral infection in phytoplankton. ASLO conference presentation. Santiago, Spain, June 2005.
16. BRUSSAARD, C.P.D. (2004). Viral control of phytoplankton populations - a review. J. Eukaryotic Microbiol., 51: 125-138.
17. BRUSSAARD, C.P.D. & RIEGMAN, R. (1998). Influence of bacteria on phytoplankton cell mortality with phosphorus or nitrogen as the algal-growth-limiting nutrient. Aquat. Microbial Ecol., 14: 271-280.
18. BRUSSAARD, C.P.D., RIEGMAN, R., NOORDELOOS, A.A.M., CADEE, G.C., WITTE, H., KOP, A.J., NIEUWLAND, G., VAN DUYL, F.C. & BAK, R.P.M. (1995). Effects of grazing, sedimentation and phytoplankton cell lysis on the structure of a coastal pelagic food web. Mar. Ecol. Prog. Ser., 123: 259-271.
19. BRUSSAARD, C.P.D., NOORDELOOS, A.A.M. & RIEGMAN, R. (1997). Autolysis kinetics of the marine diatom Ditylum brightwellii (Bacillariophyceae) under nitrogen and phosphorus limitation and starvation. J. Phycol., 33: 980-997.
20. BRUSSAARD, C.P.D., MARIE, D., THYRHAUG, R. & BRATBAK, G. (2001). Flow cytometric analysis of phytoplankton viability following viral infection. Aquat. Microbial Ecol., 26: 157-166.
21. CANTER, H.M. (1979). Fungal and protozoan parasites and their importance in the ecology of the phytoplankton. Rep. Freshwat. Biol. Ass., 47: 43-50.
22. CASOTTI, R., MAZZA, S., BRUNET, C., VANTREPOTTE, V., IANORA, A. & MIRALTO, A. (2005). Growth inhibition and toxicity of the diatom aldehyde 2-trans, 4-trans-decadienal on Thalassiosira weissfloggi (Bacillariophyceae). J. Phycol., 41: 7-20.
23. COHEN, G.M. (1997). Caspases: the executioners of apoptosis. Biochem. J., 326: 1-16.
24. COLE, J.J. (1982). Interactions between bacteria and algae in aquatic ecosystems. Annu. Rev. Ecol. Syst., 13: 291-314.
25. COSTAS, E., AGUILERA, A., GONZALEZ-GIL, S. & LOPEZ-RODAS, V. (1993). Contact inhibition: also a control for cell proliferation in unicellular algae?. Biol. Bull., 184: 1-5.
26. COVENEY, M.F., CRONBERG, G., ENELL, M., LARSSON, K. & OLOFSSON, L. (1977). Phytoplankton, zooplankton and bacteria - standing crop and production relationships in a eutrophic lake. Oikos, 29: 5-21.
27. CRUMPTON, W.G. & WETZEL, R.G. (1982). Effects of differential growth and mortality in the seasonal succession of phytoplankton populations in Lawrence Lake, Michigan. Ecology, 63: 1729-1739.
28. DUNN, S.R., BYTHELL, J.C., LE TISSIER, M.D.A., BURNETT, W.J. & THOMASON, J.C. (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.
29. ELOFF, J.N., STEINITZ, Y. & SHILO, M. (1976). Photooxidation of cyanobacteria in natural conditions. Appl. Environ. Microbiol., 31: 119-126.
30. ESTEP, K.W. & MACINTYRE, F. (1989). Taxonomy, life-cycle, distribution and dasmotrophy of Chrysochromulina - a theory accounting for scales, haptonema, muciferous bodies and toxicity. Mar. Ecol. Prog. Ser., 57: 11-21.
31. FASHAM, M.J.R., DUCKLOW, H.W. & MCKELVIE, D.S. (1990). A nitrogen-based model of plankton dynamics in the oceanic mixed layer. J. Mar. Res., 48: 591-639.
32. FRANKLIN, D.J. & BERGES, J.A. (2004). Mortality in cultures of the dinoflagellate Amphidinium carterae during culture senescence and darkness. Proc. R. Soc. Lond. B, 271: 2099-2107.
33. FROHLICH, K.U. & MADEO, F. (2000). Apoptosis in yeast - a monocellular organism exhibits altruistic behaviour. FEBS Letters, 473: 6-9.
34. FOGG, G.E. & THAKE, B. (1987). Algal Cultures and Phytoplankton Physiology. University of Wisconsin Press, Wisconsin.
35. FORSBERG, B.R. (1985). The fate of planktonic primary production. Limnol. Oceanogr., 30: 807-819.
36. FREUDENTHAL, H.D. (1962). Symbiodinium gen. nov. and Symbiodinium microadriaticum sp. nov., a zooxanthella: Taxonomy, life cycle, and morphology. J. Protozool., 9: 45-52.
37. GALLAGHER, J.C. (1980). Population genetics of Skeletonema costatum (Bacillariophyceae) in Narragansett Bay. J. Phycol., 16: 464-474.
38. GEIDER, R.J., DELUCIA, E.H., FALKOWSKI, P.G., FINZI, A.C., GRIME, J.P., GRACE, J., KANA, T.M., LA ROCHE, J., LONG, S.P., OSBORNE, B.A., PLATT, T., PRENTICE, I.C., RAVEN, J.A., SCHLESINGER, W.H., SMETACEK, V., STUART, V., SATHYENDRANATH, S., THOMAS, R.B., VOGELMANN, T.C., WILLIAMS, P. & WOODWARD, F.I. (2001). Primary productivity of planet earth: biological determinants and physical constraints in terrestrial and aquatic habitats. Global Change Biology, 7: 849-882.
39. GOMEZ, M.P., HARRIS, J.B. & WALNE, P.L. (1974). Studies of Euglena gracilis in aging cultures. I. Light microscopy and cytochemistry. Br. Phycol. J., 9: 163-174.
40. GOODNIGHT, C.J. & STEVENS, L. (1997). Experimental studies of group selection: what do they tell us about group selection in nature?. Am. Nat., 150: S59-S79.
41. GRASLKRAUPP, B., RUTTKAYNEDECKY, B., KOUDELKA, H., BUKOWSKA, K., BURSCH, W. & SCHULTEHERMANN, R. (1995). In-situ detection of fragmented DNA (TUNEL assay) fails to discriminate among apoptosis, necrosis, and autolytic cell death - a cautionary note. Hepatology, 21: 1465-1468.
42. HAGEN, G. & KOCHERT, G. (1980). Protein synthesis in a new system for the study of senescence. Exp. Cell Res., 127: 451-457.
43. HEISKANEN, A.S. (1993). Mass encystment and sinking of dinoflagellates during a spring bloom. Mar. Biol., 116: 161-167.
44. HEISKANEN, A. & KONONEN, K. (1994). Sedimentation of vernal and late summer phytoplankton communities in the coastal Baltic sea. Arch. Hydrobiol., 131: 175-198.
45. HOLFELD, H. (1998). Fungal infections of the phytoplankton: seasonality, minimal host density, and specificity in a mesotrophic lake. New Phytol., 138: 507-517.
46. HORN, H. & HORN, W. (2000). Sedimentation: the main loss factor in waters dominated by diatoms. Results of long-term investigations. Int. Rev. Hydrobiol., 85: 191-208.
47. IMAI, I., ISHIDA, Y. & HATA, Y. (1993). Killing of marine phytoplankton by a gliding bacterium Cytophaga sp., isolated from the coastal Sea of Japan. Mar. Biol., 116: 527-532.
48. JABS, T., DIETRICH, R.A. & DANGL, J.L. (1996). Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science, 273: 1853-1856.
49. JASSBY, A.D. & GOLDMAN, C.R. (1974). Loss rates from a lake phytoplankton community. Limnol. Oceanogr., 19: 618-627.
50. JEROME, K.R., VALLAN, C. & JAGGI, R. (2000). The TUNEL assay in the diagnosis of graft-versus-host disease: caveats for interpretation. Pathology, 32: 186-190.
51. JEWSON, D.H., RIPPEY, B.H. & GILMORE, W.K. (1981). Loss rates from sedimentation, parasitism, and grazing during the growth, nutrient limitation, and dormancy of a diatom crop. Limnol. Oceanogr., 26: 1045-1056.
52. JOINT, I., TAIT, K., CALLOW, M.E., CALLOW, J.A., MILTON, D., WILLIAMS, P. & CAMARA, M. (2002). Cell-to cell communication across the prokaryote-eukaryote boundary. Science, 298: 1207.
53. JONES, A.M. (2001). Programmed cell death in development and defense. Plant Physiol., 125: 94-97.
54. KALFF, J. & KNOECHEL, R. (1978). Phytoplankton and their dynamics in oligotrophic and eutrophic lakes. Annu. Rev. Ecol. Syst., 9: 475-495.
55. KANDUC, D., MITTELMAN, A., SERPICO, R., SINIGAGLIA, E., SINHA, A.A., NATALE, C., SANTACROCE, R., DI CORCIA, M.G., LUCCHESE, A., DINI, L., PANI, P., SANTACROCE, S., SIMONE, S., BUCCI, R. & FARBER, E. (2002). Cell death: apoptosis versus necrosis (review). Int. J. Oncol., 21: 165-170.
56. KERR, J.F.R., WYLLIE, A.H. & CURRIE, A.R. (1972). Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer, 26: 239-257.
57. KIRCHMAN, D.L. (1999). Phytoplankton death in the sea. Nature, 398: 293-294.
58. KIRK, D.L. (1998). Volvox. Molecular-genetic Origins of Multicellularity and Cellular Differentiation. Cambridge University Press, Cambridge.
59. KUHN, S. (1998). Infection of Coscinodiscus spp. by the parasitoid nanoflagellate Pirsonia diadema: II. Selective infection behaviour for host species and individual host cells. J. Plankton Res., 20: 443-454.
60. LABAT-MOLEUR, F., GUILLERMET, C., LORIMIER, P., ROBERT, C., LANTUEJOUL, S., BRAMBILLA, E. & NEGOESCU, A. (1998). TUNEL apoptotic detection in tissue sections: critical evaluation and improvement. Histochem. Cytochem., 46: 327-334.
61. LAM, E., KATO, N. & LAWTON, M. (2001). Programmed cell death, mitochondria and the plant hypersensitive response. Nature, 411: 848-853.
62. LAUN, P., PICHOVA, A., MADEO, F., FUCHS, J., ELLINGER, A., KOHLWEIN, S., DAWES, I., FROHLICH, K.U. & BREITENBACH, M. (2001). Aged mother cells of Saccharomyces cerevisiae show markers of oxidative stress and apoptosis. Mol. Microbiol., 39: 1166-1173.
63. LEDERMAN, L. (2004). Apoptosis: one way to die. BioTechniques, 37: 520-521.
64. LEE, D. & RHEE, G. (1999). Circadian rhythm in growth and death of Anabaena flos-aquae (Cyanobacteria). J. Phycol., 35: 694-699.
65. LEE, N., BERTHOLET, S., DEBRABANT, A., MULLER, J., DUNCAN, R. & NAKHASI, H.L. (2002). Programmed cell death in the unicellular protozoan parasite Leishmania. Cell Death Diff., 9: 53-64.
66. LEHMAN, J.T. & SANDGREN, C.D. (1985). Species-specific rates of growth and grazing loss among freshwater algae. Limnol. Oceanogr., 30: 34-46.
67. LEOPOLD, A.C. (1961). Senescence in plant development. Science, 134: 1727-1732.
68. LEWIS, K. (2000). Programmed cell death in bacteria. Microbiol. Mol. Biol. Ann. Rev., 64: 503-514.
69. LINDAHL, O. (1983). On the development of a Gyrodinium aureolum occurrence on the Swedish west coast in 1982. Mar. Biol., 77: 143-150.
70. LOWE, C.D., DAY, A., KEMP, S.J. & MONTAGNES, D.J.S. (2005). There are high levels of functional and genetic diversity in Oxyrrhis marina. J. Eukaryot. Microbiol., 52: 250-257.
71. MADEO, F., FROHLICH, E. & FROHLICH, K. (1997). A yeast mutant showing diagnostic markers of early and late apoptosis. J. Cell Biol., 139: 729-734.
72. MADEO, F., FROHLICH, E., LIGR, M., GREY, M., SIGRIST, S.J., WOLF, D.H. & FROHLICH, K.U. (1999). Oxygen stress: A regulator of apoptosis in yeast. J. Cell Biol., 145: 757-767.
73. MALMUSI, M. & ACKERMAN, A.B. (1999). A critical review of apoptosis in historical perspective. Ardor scribendi. Philadelphia.
74. MARTIN, S.J., REUTELINGSPERGER, C.P.M., MCGAHON, A.J., RADER, J.A., VAN SCHIE, R.C.A.A., LAFACE, D.M. & GREEN, D.R. (1995). Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 ande Abl. J. Exp. Med., 182: 1545-1556.
75. MASON, C.A., HAMER, G. & BRYERS, J.D. (1986). The death and lysis of microorganisms in environmental processes. FEMS Microbiol. Rev., 39: 373-401.
76. MEDLIN, L.K., LANGE, M. & NOTHIG, E.M. (2000). Genetic diversity in the marine phytoplankton: a review and a consideration of Antarctic phytoplankton. Antarctic Sci., 12: 325-333.
77. NEDELCU, A.M., MARCU, O. & MICHOD, R.E. (2004). Sex as a response to oxidative stress: a twofold increase in cellular reactive oxygen species activates sex genes. Proc. R. Soc. Lond. B., 271: 1591-1596.
78. NING, S.B., GUO, H.L., WANG, L. & SONG, Y.C. (2002). Salt stress induces programmed cell death in prokaryotic organism Anabaena. J. Appl. Microbiol., 93: 15-28.
79. NOJI, T., PASSOW, U. & SMETACEK, V. (1986). Interaction between pelagial and benthal during autumn in Kiel Bight. I. Development and sedimentation of phytoplankton blooms. Ophelia, 26: 333-349.
80. OLESKIN, A.V., BOTVINKO, I.V. & TSAVKELOVA, E.A. (2000). Colonial organisation and intracellular communication in microorganisms. Mikrobiologiya, 69: 249-265.
81. OLIE, R.A., DURRIEU, F., CORNILLON, S., LOUGHRAN, G., GROSS, J., EARNSHAW, W.C. & GOLSTEIN, P. (1998). Apparent caspase independence of programmed cell death in Dictyostelium. Curr. Biol., 8: 955-958.
82. PATEL, T., ARORA, A. & GORES, G.J. (1995). A fluorometric assay for quantitating DNA strand breaks during apoptosis. Anal. Biochem., 229: 229-235.
83. POLLINGHER, U. (1988). Freshwater armored dinoflagellates: growth, reproduction strategies and population dynamics. In Growth and reproductive strategies of freshwater phytoplankton (Sandgren, C.D., editor). Cambridge University Press, Cambridge.
84. POMMERVILLE, J.C. & KOCHERT, G.D. (1981). Changes in somatic cell structure during senescence of Volvox carteri. Eur. J. Cell Biol., 24: 236-243.
85. PREZELIN, B.B. (1982). Effects of light intensity on aging of the dinoflagellate Gonyaulax polyedra. Mar. Biol., 69: 129-135.
86. RAFF, M.C. (1992). Social controls on cell survival and cell death. Nature, 356: 397-400.
87. RATEL, D., BOISSEAU, S., NASSER, V., BERGER, F. & WION, D. (2001). Programmed cell death or cell death programme? That is the question. J. Theor. Biol., 208: 385-386.
88. REDDY, P.M., YUMNAM, D.D. & IMCHEN, T.Y. (1987). Regulation of differentiation of multiple heterocysts in a blue-green alga, Anabaena variabilis. Arch. Hydrobiol., 73: 559-574.
89. REGUERA, B. & GONZALEZ-GIL, S. (2001). Small cell and intermediate cell formation in species of Dinophysis (Dinophyceae, Dinophysiales). J. Phycol., 37: 318-333.
90. REYNOLDS, C.S. (1984). The Ecology of Freshwater Phytoplankton. Cambridge University Press, Cambridge.
91. RYNEARSON, T.A. & ARMBRUST, E.V. (2005). Maintenance of clonal diversity during a spring bloom of the centric diatom Ditylum brightwellii. Mol. Ecol., 14: 1631-1640.
92. SAKAMOTO, T., DELGAIZO, V.B. & BRYANT, D.A. (1998). Growth on urea can trigger death and peroxidation of the cyanobacterium Synechococcus sp. strain PCC 7002. Appl. Environ. Microbiol., 64: 2361-2366.
93. SANDERSON, B.L. & FROST, T.M. (1996). Regulation of dinoflagellate populations: Relative importance of grazing, resource limitation and recruitment from sediments. Can. J. Fish. Aquat. Sci., 53: 1409-1417.
94. SCAVIA, D. & FAHNENSTIEL, G.L. (1987). Dynamics of Lake Michigan phytoplankton: mechanisms controlling epilimnetic communities. J. Great Lakes Res., 13: 103-120.
95. SEGOVIA, M., HARAMATY, L., BERGES, J.A. & FALKOWSKI, P.G. (2003). Cell death in the unicellular chlorophyte Dunaliella tertiolecta. A hypothesis on the evolution of apoptosis in higher plants and metazoans. Plant Physiol., 132: 1-7.
96. SHELDRAKE, R. (1974). The ageing, growth and death of cells. Nature, 250: 381-385.
97. SHRAGER, J., CHANG, C.W., HAUSER, E., HARRIS, R., TAMSE, R., DAVIES, J., ZHANG, Z. & GROSSMAN, A.R. (2003). Chlamydomonas reinhardtii genome project: sequence analysis, assembly and annotation. Plant Physiol., 131: 401-408.
98. SILVA, E.S. & FAUST, M.A. (1995). Small cells in the life history of dinoflagellates (Dinophyceae): a review. Phycologia, 34: 396-408.
99. SLOAN WILSON, D. (1997). Introduction: multilevel selection theory comes of age. Am. Nat., 150: S1-S4.
100. SPERANDIO, S., DE BELLE, I. & BREDESEN, D.E. (2000). An alternative, nonapoptotic form of programmed cell death. Proc. Natl. Acad. Sci. USA, 97: 14376-14381.
101. STEELE, J.H. (1974). The Structure of Marine Ecosystems. Harvard University Press, Harvard.
102. SUGINAKA, K., YAMAMOTO, K., ASHIDA, H., SAWA, Y. & SHIBATA, H. (1999). Effect of intracellular glutathione on heat-induced cell death in the cyanobacterium, Synechocystis PCC 6803. Biosci. Biotechnol. Biochem., 63: 1112-1115.
103. SUTTLE, C.A. (2005). Viruses in the sea. Nature, 437: 356-361.
104. TATISCHEFF, I., PETIT, P.X., GRODET, A., TISSIER, J., DUBAND-GROULET, I. & AMEISEN, J. (2001). Inhibition of multicellular development switches cell death of Dictyostelium discoideum towards mammalian-like unicellular apoptosis. Eur. J. Cell Biol., 80: 428-441.
105. THORNTON, D.C.O. (2002). Individuals, clones or groups? Phytoplankton behaviour and units of selection. Ethol. Ecol. Evol., 14: 165-173.
106. TILZER, M.M. (1984). Estimation of phytoplankton loss rates from daily photosynthetic rates and observed biomass changes in Lake Constance. J. Plankton Res., 6: 309-324.
107. TOTH, G.B., NORÉN, F., SELANDER, E. & PAVIA, H. (2004). Marine dinoflagellates show induced life-history shifts to escape parasite infection in response to water-borne signals. Proc. R. Soc. Lond. B, 271: 733-738.
108. UCHIDA, T., YAMAGUCHI, M., MATSUYAMA, Y. & HONJO, T. (1995). The red-tide dinoflagellate Heterocapsa sp. kills Gyrodinium instriatum by cell contact. Mar. Ecol. Prog. Ser., 118: 301-303.
109. UREN, A.G., O'ROURKE, K.O., ARAVIND, L., PISABARRO, M.T., SESHAGIRI, S., KOONIN, E.V. & DIXIT, M.V. (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.
110. USUP, G. & AZANZA, R.V. (1988). Physiology and bloom dynamics of the tropical dinoflagellate Pyrodinium bahamense. In Physiological Ecology of Harmful Algal Blooms (Anderson, D.M., Cembella, A.D., and Hallegraeff, G.M., editors). 81-94. Springer Verlag, Heidelberg.
111. 2 limitation and oxidative stress. Curr. Biol., 9: 1061-1064.
112. VARDI, A., SCHATZ, D., BEERI, K., MOTRO, U., SUKENIK, A., LEVINE, A. & KAPLAN, A. (2002). Dinoflagellate-cyanobacterium communication may determine the composition of phytoplankton assemblage in a mesotrophic lake. Curr. Biol., 12: 1767-1772.
113. VAUX, D.L. & KORSMEYER, S.J. (1999). Cell death in development. Cell, 96: 245-254.
114. VELDHUIS, M.J.W., KRAAY, G.W. & TIMMERMANS, K.R. (2001). Cell death in phytoplankton: correlation between changes in membrane permeability, photosynthetic activity, pigmentation and growth. Eur. J. Phycol., 36: 167-177.
115. VONSHAK, A., TORZILLO, G., ACCOLLA, P. & TOMASELLI, L. (1996). Light and oxygen stress in Spirulina platensis (cyanobacteria) grown outdoors in tubular reactors. Physiol. Plant., 97: 175-179.
116. WALSH, J.J. (1983). Death in the sea: Enigmatic phytoplankton losses. Prog. Oceanogr., 12: 1-86.
117. WEBB, J.S., THOMPSON, L.S., JAMES, S., CHARLTON, T., TOLKER-NIELSEN, T., KOCH, B., GIVSKOV, M. & KJELLEBERG, S. (2003). Cell death in Pseudomonas aeruginosa biofilm development. J. Bacteriol., 185: 4585-4592.
118. YOSHIDA, Y. (1962). Nuclear control of chloroplast activity in Elodea leaf cells. Protoplasma, 54: 476-492.
119. ZANGGER, H., MOTTRAM, J.C. & FASEL, N. (2002). Cell death in Leishmania induced by stress and differentiation: programmed cell death or necrosis? Cell Death Diff., 9: 1126-1139.