Planktonic, prokaryotic, and eukaryotic photoautotrophs (phytoplankton) share a diverse and ancient evolutionary history, during which time they have played key roles in regulating marine food webs, biogeochemical cycles, and Earth's climate. Because phytoplankton represent the basis of marine ecosystems, the manner in which they die critically determines the flow and fate of photosynthetically fixed organic matter (and associated elements), ultimately constraining upper-ocean biogeochemistry. Programmed cell death (PCD) and associated pathway genes, which are triggered by a variety of nutrient stressors and are employed by parasitic viruses, play an integral role in determining the cell fate of diverse photoautotrophs in the modern ocean. Indeed, these multifaceted death pathways continue to shape the success and evolutionary trajectory of diverse phytoplankton lineages at sea. Research over the past two decades has employed physiological, biochemical, and genetic techniques to provide a novel, comprehensive, mechanistic understanding of the factors controlling this key process. Here, I discuss the current understanding of the genetics, activation, and regulation of PCD pathways in marine model systems; how PCD evolved in unicellular photoautotrophs; how it mechanistically interfaces with viral infection pathways; how stress signals are sensed and transduced into cellular responses; and how novel molecular and biochemical tools are revealing the impact of PCD genes on the fate of natural phytoplankton assemblages.


Article metrics loading...

Loading full text...

Full text loading...


Literature Cited

  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. 60:939–54 [Google Scholar]
  2. Agustí S. 2004. Viability and niche segregation of Prochlorococcus and Synechococcus cells across the Central Atlantic Ocean. Aquat. Microb. Ecol. 36:53–59 [Google Scholar]
  3. Agustí S, Sánchez MC. 2002. Cell viability in natural phytoplankton communities quantified by a membrane permeability probe. Limnol. Oceanogr. 47:818–28 [Google Scholar]
  4. Agustí S, Satta MP, Mura MP, Benavent E. 1998. Dissolved esterase activity as a trace of phytoplankton lysis: evidence of high phytoplankton lysis rates in the northwestern Mediterranean. Limnol. Oceanogr. 43:1836–49 [Google Scholar]
  5. Ameisen JC. 1998. The evolutionary origin and role of programmed cell death in single-celled organisms: a new view at executioners, mitochondria, host-pathogen interactions and the role of death in the process of natural selection. When Cells Die: A Comprehensive Evaluation of Apoptosis and Programmed Cell Death RA Lockshin, Z Zakeri, JL Tilly 3–56 New York: Wiley-Liss [Google Scholar]
  6. Ameisen JC. 2002. On the origin, evolution, and nature of programmed cell death: a timeline of four billion years. Cell Death Differ. 9:367–93 [Google Scholar]
  7. Ameisen JC, Idziorek T, Billaut-Mulot O, Loyens M, Tissier JP. et al. 1995. Apoptosis in a unicellular eukaryote (Trypazoma cruzi): implications for the evolutionary origin and role of programmed cell death in the control of cell proliferation, differentiation and survival. Cell Death Differ. 2:285–300 [Google Scholar]
  8. Aravind L, Dixit VM, Koonin EV. 1999. The domains of death: evolution of the apoptosis machinery. Trends Biochem. Sci. 24:47–53 [Google Scholar]
  9. Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D. et al. 2004. The genome of the diatom Thalassiosira pseudonana: ecology, evolution and metabolism. Science 306:79–86 [Google Scholar]
  10. Arnoult D, Akarid K, Grodet A, Petit PX, Estaquier J, Ameisen JC. 2002. On the evolution of programmed cell death: apoptosis of the unicellular eukaryote Leishmania major involves cysteine proteinase activation and mitochondrion permeabilization. Cell Death Differ. 9:65–81 [Google Scholar]
  11. Asplund-Samuelsson J, Bergman B, Larsson J. 2012. Prokaryotic caspase homologs: phylogenetic patterns and functional characteristics reveal considerable diversity. PLoS ONE 7:e49888 [Google Scholar]
  12. Azam F. 1998. Microbial control of oceanic carbon flux: The plot thickens. Science 280:694–96 [Google Scholar]
  13. Bar-Zeev E, Avishay I, Bidle KD, Berman-Frank I. 2013. Programmed cell death in the marine cyanobacterium Trichodesmium mediates carbon and nitrogen export. ISME J. 7:2340–48 [Google Scholar]
  14. Bar-Zeev E, Berman T, Rahav E, Dishon G, Herut B, Berman-Frank I. 2011. Transparent exopolymer particle (TEP) dynamics in the eastern Mediterranean Sea. Mar. Ecol. Prog. Ser. 431:107–18 [Google Scholar]
  15. Bayles KW. 2014. Bacterial programmed cell death: making sense of a paradox. Nat. Rev. Microbiol. 12:63–69 [Google Scholar]
  16. Beckman JS, Koppenol WH. 1996. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am. J. Physiol. 271:C1424–37 [Google Scholar]
  17. Belenghi B, Romero-Puertas MC, Vercammen D, Brackenier A, Inzé D. et al. 2007. Metacaspase actvity of Arabidopsis thaliana is regulated by S-nitrosylation of a critical cysteine residue. J. Biol. Chem. 282:1352–58 [Google Scholar]
  18. 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. 43:129–35 [Google Scholar]
  19. Berman-Frank I, Bidle KD, Haramaty L, Falkowski PG. 2004. The demise of the marine cyanobacterium, Trichodesmium spp., via an autocatalyzed cell death pathway. Limnol. Oceanogr. 49:997–1005 [Google Scholar]
  20. Berman-Frank I, Rosenberg G, Levitan O, Haramaty L, Mari X. 2007. Coupling between autocatalytic cell death and transparent exopolymeric particle production in the marine cyanobacterium Trichodesmium. Environ. Microbiol. 9:1415–22 [Google Scholar]
  21. Berman-Frank I, Zohary T, Erez J, Dubinsky Z. 1994. CO2 availability, carbonic-anhydrase, and the annual dinoflagellate bloom in Lake Kinneret. Limnol. Oceanogr. 39:1822–34 [Google Scholar]
  22. Best SM. 2008. Viral subversion of apoptotic enzymes: escape from death row. Annu. Rev. Microbiol. 62:171–92 [Google Scholar]
  23. Bidle KA, Haramaty L, Baggett N, Nannen J, Bidle KD. 2010. Tantalizing evidence for archaeal caspase-like protein expression and activity and its role in cellular stress response. Environ. Microbiol. 12:1161–72 [Google Scholar]
  24. Bidle KD, Azam F. 1999. Accelerated dissolution of diatom silica by natural marine bacterial assemblages. Nature 397:508–12 [Google Scholar]
  25. Bidle KD, Bender SJ. 2008. Iron starvation and culture age activate metacaspases and programmed cell death in the marine diatom, Thalassiosira pseudonana. Eukaryot. Cell 7:223–36 [Google Scholar]
  26. Bidle KD, Brzezinski MA, Long RA, Jones J, Azam F. 2003. Diminished efficiency in the oceanic silica pump caused by bacteria-mediated silica dissolution. Limnol. Oceanogr. 48:1855–68 [Google Scholar]
  27. Bidle KD, Falkowski PG. 2004. Cell death in planktonic photosynthetic microorganisms. Nat. Rev. Microbiol. 2:643–55 [Google Scholar]
  28. Bidle KD, Haramaty L, Barcelos-Ramos J, Falkowski PG. 2007. Viral activation and recruitment of metacaspases in the unicellular coccolithophorid, Emiliania huxleyi. Proc. Natl. Acad. Sci. USA 104:6049–54 [Google Scholar]
  29. Bidle KD, Vardi A. 2011. A chemical arms race at sea mediates algal host–virus interactions. Curr. Opin. Microbiol. 14:449–57 [Google Scholar]
  30. Biol. Chem. Oceanogr. Data Manag. Off 2014. Project: lipid lubrication of oceanic carbon and sulfur biogeochemistry via a host-virus chemical arms race http://www.bco-dmo.org/project/2136 [Google Scholar]
  31. Bowler C, Allen AE, Badger JH, Grimwood J, Jabbari K. et al. 2008. The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456:239–42 [Google Scholar]
  32. Boyce M, Degterev A, Yuan J. 2004. Caspases: an ancient cellular sword of Damocles. Cell Death Differ. 11:29–37 [Google Scholar]
  33. Boyd PW, Jickells T, Law CS, Blain S, Boyle EA. et al. 2007. Mesoscale iron enrichment experiments 1993–2005: synthesis and future directions. Science 315:612–17 [Google Scholar]
  34. Bozhkov PV, Suarez MF, Filonova LH, Daniel G, Zamyatnin AA Jr. et al. 2005. Cysteine protease mcII-Pa executes programmed cell death during plant embryogenesis. Proc. Natl. Acad. Sci USA 102:14463–68 [Google Scholar]
  35. Bratbak G, Egge JK, Heldal M. 1993. Viral mortality of the marine alga Emiliania huxleyi (Haptophyceae) and termination of algal blooms. Mar. Ecol. Prog. Ser. 93:39–48 [Google Scholar]
  36. Bratbak G, Wilson W, Heldal M. 1996. Viral control of Emiliania huxleyi blooms?. J. Mar. Syst. 9:75–81 [Google Scholar]
  37. Brügger B, Glass B, Haberkant P, Leibrecht I, Felix F. et al. 2006. The HIV lipidome: a raft with an unusual composition. Proc. Natl. Acad. Sci. USA 103:2641–46 [Google Scholar]
  38. Brussaard CPD, Noordeloos AAM, Riegman R. 1997. Autolysis kinetics of the marine diatom Ditylum brightwellii (Bacillariophyceae) under nitrogen and phosphorus limitation and starvation. J. Phycol. 33:980–87 [Google Scholar]
  39. Brussaard CPD, Riegman R, Noordeloos AAM, Cadée GC, Witte H. et al. 1995. Effects of grazing, sedimentation and phytoplankton cell lysis on the structure of a coastal pelagic food web. Mar. Ecol. Prog. Ser. 123:259–71 [Google Scholar]
  40. Brzezinski MA, Jones JL, Bidle KD, Azam F. 2003. The balance between silica production and silica dissolution in the sea: insights from Monterey Bay, California applied to the global data set. Limnol. Oceanogr. 48:1846–54 [Google Scholar]
  41. Brzezinski MA, Nelson DM. 1995. The annual silica cycle in the Sargasso Sea near Bermuda. Deep-Sea Res. I 42:1215–37 [Google Scholar]
  42. Caldwell GS, Olive PJW, Bentley MG. 2002. Inhibition of embryonic development and fertilization in broadcast spawning marine invertebrates by water soluble diatom extracts and the diatom toxin 2-trans,4-trans decadienal. Aquat. Toxicol. 60:123–37 [Google Scholar]
  43. Cambi A, Koopman M, Figdor CG. 2005. How C-type lectins detect pathogens. Cell. Microbiol. 7:481–88 [Google Scholar]
  44. Capone DG, Burns JA, Montoya JP, Subramaniam A, Mahaffey C. et al. 2005. Nitrogen fixation by Trichodesmium spp.: an important source of new nitrogen to the tropical and subtropical North Atlantic Ocean. Glob. Biogeochem. Cycles 19:GB2024 [Google Scholar]
  45. Capone DG, Zehr JP, Paerl H, Bergman B, Carpenter EJ. 1997. Trichodesmium, a globally significant marine cyanobacterium. Science 276:1221–29 [Google Scholar]
  46. Carmona-Gutierrez D, Fröhlich K-U, Kroemer G, Madeo F. 2010. Metacaspases are caspases. Doubt no more. Cell Death Differ. 17:377–78 [Google Scholar]
  47. 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 weissflogii (Bacillariophyceae). J. Phycol. 41:7–20 [Google Scholar]
  48. Castberg T, Thyrhaug R, Larsen A, Sandaa R-A, Heldal M. et al. 2002. Isolation and characterization of a virus that infects Emiliania huxleyi (Haptophyta). J. Phycol. 38:767–74 [Google Scholar]
  49. Chandra J, Samali A, Orrenius S. 2000. Triggering and modulation of apoptosis by oxidative stress. Free Radic. Biol. Med. 29:323–33 [Google Scholar]
  50. Chappell PD, Webb EA. 2010. A molecular assessment of the iron stress response in the two phylogenetic clades of Trichodesmium. Environ. Microbiol. 12:13–27 [Google Scholar]
  51. Chichkova NV, Shaw J, Galiullina RA, Drury GE, Tuzhikov AI. et al. 2010. Phytaspase, a relocalisable cell death promoting plant protease with caspase specificity. EMBO J. 29:1149–61 [Google Scholar]
  52. Choi CJ, Berges JA. 2013. New types of metacaspases in phytoplankton reveal diverse origins of cell death proteases. Cell Death Dis. 4:e490 [Google Scholar]
  53. Chung C-C, Hwang S-PL, Chang J. 2005. Cooccurrence of ScDSP gene expression, cell death, and DNA fragmentation in a marine diatom, Skeletonema costatum. Appl. Environ. Microbiol. 71:8744–51 [Google Scholar]
  54. Chung C-C, Hwang S-PL, Chang J. 2008. Nitric oxide as a signaling factor to upregulate the death-specific protein in a marine diatom, Skeletonema costatum, during blockage of electron flow in photosynthesis. Appl. Environ. Microbiol. 74:6521–27 [Google Scholar]
  55. Coffeen WC, Wolpert TJ. 2004. Purification and characterization of serine proteases that exhibit caspase-like activity and are associated with programmed cell death in Avena sativa. Plant Cell 16:857–73 [Google Scholar]
  56. Cohen GM. 1997. Caspases: the executioners of apoptosis. Biochem. J. 326:1–16 [Google Scholar]
  57. DalCorso G, Pesaresi P, Masiero S, Aseeva E, Schünemann D. et al. 2008. A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis. Cell 132:273–85 [Google Scholar]
  58. Darzynkiewicz Z, Li X, Gong J. 1994. Assays of cell viability: discrimination of cells dying by apoptosis. Methods Cell Biol. 41:15–38 [Google Scholar]
  59. Denton D, Nicolson S, Kumar S. 2011. Cell death by autophagy: facts and apparent artefacts. Cell Death Differ. 19:87–95 [Google Scholar]
  60. Dep. Energy Joint Genome Inst 2014a. Emiliania huxleyi CCMP1516 main genome assembly v1.0 Genome Portal. http://genome.jgi-psf.org/Emihu1/Emihu1.home.html [Google Scholar]
  61. Dep. Energy Joint Genome Inst 2014b. Thalassiosira pseudonana. Genome Portal. http://genome.jgi-psf.org/Thaps3/Thaps3.home.html [Google Scholar]
  62. Dixon SJ, Lemberg KM, Lamprecht MR, Skouta R, Zaitsev EM. et al. 2012. Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell 149:1060–72 [Google Scholar]
  63. Dugdale RC, Wilkerson FP. 1998. Silicate regulation of new production in the equatorial Pacific upwelling. Nature 391:270–73 [Google Scholar]
  64. Durand PM, Rashidi A, Michod RE. 2011. How an organism dies affects the fitness of its neighbors. Am. Nat. 177:224–32 [Google Scholar]
  65. Evans C, Kadner SV, Darroch LJ, Wilson WH, Liss PS, Malin G. 2007. The relative significance of viral lysis and microzooplankton grazing as pathways of dimethylsulfoniopropionate (DMSP) cleavage: an Emiliania huxleyi culture study. Limnol. Oceanogr. 52:1036–45 [Google Scholar]
  66. Evans C, Malin G, Mills GP, Wilson WH. 2006a. Viral infection of Emiliania huxyleyi (Prymnesiophyceae) leads to elevated production of reactive oxygen species. J. Phycol. 42:1040–47 [Google Scholar]
  67. Evans C, Malin G, Wilson WH, Liss PS. 2006b. Infectious titers of Emiliania huxleyi virus 86 are reduced by exposure to millimolar dimethyl sulfide and acrylic acid. Limnol. Oceanogr. 51:2468–71 [Google Scholar]
  68. Evans C, Wilson WH. 2008. Preferential grazing of Oxyrrhis marina on virus-infected Emiliania huxleyi. Limnol. Oceanogr 53:2035–40 [Google Scholar]
  69. Falciatore A, Ribera-d'Alcalà M, Croot P, Bowler C. 2000. Perception of environmental signals by a marine diatom. Science 288:2363–66 [Google Scholar]
  70. Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA. et al. 2004. The evolution of modern eukaryotic phytoplankton. Science 305:354–60 [Google Scholar]
  71. Falkowski PG, Knoll AH. 2007. Evolution of Primary Producers in the Sea New York: Academic [Google Scholar]
  72. Field CB, Behrenfeld MJ, Randerson JT, Falkowski PG. 1998. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281:237–40 [Google Scholar]
  73. Formigli L, Papucci L, Tani A, Shiavone N, Tempestini A. et al. 2000. Aponecrosis: morphological and biochemical exploration of a syncretic process of cell death sharing apoptosis and necrosis. J. Cell. Physiol. 182:41–49 [Google Scholar]
  74. Frada M, Schatz D, Farstey V, Sheyn U, Sabanay H. et al. 2014. Zooplankton may serve as transmission vectors for viruses infecting algal blooms in the ocean. Curr. Biol. In press. doi: 10.1016/j.cub.2014.09.031 [Google Scholar]
  75. Franklin DJ. 2014. Explaining the causes of cell death in cyanobacteria: what role for asymmetric division?. J. Plankton Res. 36:11–17 [Google Scholar]
  76. Franklin DJ, Berges JA. 2004. Mortality in cultures of the dinoflagellate Amphidinium carterae during culture senescence and darkness. Proc. Biol. Sci. 271:2099–107 [Google Scholar]
  77. 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 [Google Scholar]
  78. Franklin DJ, Steinke M, Young J, Probert I, Malin G. 2010. Dimethylsulphoniopropionate (DMSP), DMSP-lyase activity (DLA) and dimethylsulphide (DMS) in 10 species of coccolithophore. Mar. Ecol. Prog. Ser. 140:13–23 [Google Scholar]
  79. Fröhlich K-U, Madeo F. 2000. Apoptosis in yeast: A monocellular organism exhibits altruistic behaviour. FEBS Lett. 473:6–9 [Google Scholar]
  80. Fuhrman JA. 1999. Marine viruses and their biogeochemical and ecological effects. Nature 399:541–48 [Google Scholar]
  81. Fulton JM, Fredricks HF, Bidle KD, Vardi A, Kendrick J. et al. 2014. Novel molecular determinants of viral susceptibility and resistance in the lipidome of Emiliania huxleyi. Environ. Microbiol. 16:1137–49 [Google Scholar]
  82. Georgiou T, Yu Y-TN, Ekunwe S, Buttner MJ, Zuurmond A-M. et al. 1998. Specific peptide-activated proteolytic cleavage of Escherichia coli elongation factor Tu. Proc. Natl. Acad. Sci. USA 95:2891–95 [Google Scholar]
  83. Golstein P, Kroemer G. 2006. Cell death by necrosis: towards a molecular definition. Trends Biochem. Sci. 32:37–43 [Google Scholar]
  84. Graff van Creveld S, Rosenwasser S, Schatz D, Koren I, Vardi A. 2014. Early perturbation in mitochondria redox homeostasis in response to environmental stress predicts cell fate in diatoms. ISME J. In press. doi: 10.1038/ismej.2014.136 [Google Scholar]
  85. Guo FQ, Okamoto M, Crawford NM. 2003. Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302:100–3 [Google Scholar]
  86. Hamilton WD. 1964. The genetical evolution of social behavior. J. Theor. Biol. 7:1–52 [Google Scholar]
  87. Heath MC. 2000. Hypersensitive response-related death. Plant Mol. Biol. 44:321–34 [Google Scholar]
  88. Hengartner M. 2000. The biochemistry of apoptosis. Nature 407:770–76 [Google Scholar]
  89. Hewson I, Govil SR, Capone DG, Carpenter EJ, Fuhrman JA. 2004. Evidence of Trichodesmium viral lysis and potential significance for biogeochemical cycling in the oligotrophic ocean. Aquat. Microb. Ecol. 36:1–8 [Google Scholar]
  90. Hutchins DA, Bruland KW. 1998. Iron-limited diatom growth and Si:N uptake ratios in a coastal upwelling regime. Nature 393:561–64 [Google Scholar]
  91. Hutchins DA, Ditullio GR, Zhang Y, Bruland KW. 1998. An iron limitation mosaic in the California upwelling regime. Limnol. Oceanogr. 43:1037–54 [Google Scholar]
  92. Ianora A, Miralto A, Poulet SA, Carotenuto Y, Buttino I. et al. 2004. Aldehyde suppression of copepod recruitment in blooms of a ubiquitous planktonic diatom. Nature 429:403–7 [Google Scholar]
  93. Iglesias-Rodriguez MD, Brown CW, Doney SC, Kleypas JA, Kolber D. et al. 2002. Representing key phytoplankton functional groups in ocean carbon cycle models: coccolithophorids. Glob. Biogeochem. Cycles 16:1100–20 [Google Scholar]
  94. Inst. Mediterr. Oceanol 2014. VAHINE. http://mio.pytheas.univ-amu.fr/?VAHINE-Project
  95. Iyer LM, Aravind L, Koonin EV. 2001. Common origin of four diverse families of large eukaryotic DNA viruses. J. Virol. 75:11720–34 [Google Scholar]
  96. Jiang Q, Qin S, Wu Q-Y. 2010. Genome-wide comparative analysis of metacaspases in unicellular and filamentous cyanobacteria. BMC Genomics 11:198 [Google Scholar]
  97. Jiménez C, Capasso JM, Edelstein CL, Rivard CJ, Lucia S. et al. 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. 60:815–28 [Google Scholar]
  98. Johnson JG, Janech MG, Van Dolah FM. 2014. Caspase-like activity during aging and cell death in the toxic dinoflagellate Karenia brevis. Harmful Algae 31:41–53 [Google Scholar]
  99. Kahl LA, Vardi A, Schofield O. 2008. Effects of phytoplankton physiology on export flux. Mar. Ecol. Prog. Ser. 354:1–16 [Google Scholar]
  100. Karl DM. 1993. Microbial processes in the southern oceans. Antarctic Microbiology EI Friedmann 1–63 New York: Wiley-Liss [Google Scholar]
  101. Kegel JU, John U, Valentin K, Frickenhaus S. 2013. Genome variations associated with viral susceptibility and calcification in Emiliania huxleyi. PLoS ONE 8:e80684 [Google Scholar]
  102. Kerr JF, Wyllie AH, Currie AR. 1972. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26:239–57 [Google Scholar]
  103. Kirchman DL. 1999. Phytoplankton death in the sea. Nature 398:293–94 [Google Scholar]
  104. Koonin EV, Aravind L. 2002. Origin and evolution of eukaryotic apoptosis: the bacterial connection. Cell Death Differ. 9:394–404 [Google Scholar]
  105. Laporte C, Kosta A, Klein G, Aubry L, Lam D. et al. 2006. A necrotic cell death model in a protist. Cell Death Differ. 14:266–74 [Google Scholar]
  106. Lehahn Y, Koren I, Schatz D, Frada M, Sheyn U. et al. 2014. Decoupling physical from biological processes to assess the impact of viruses on a mesoscale algal bloom. Curr. Biol. 242041–46 [Google Scholar]
  107. Liu X, Kim CN, Yang J, Jemmerson R, Wang X. 1996. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86:147–57 [Google Scholar]
  108. Lockshin RA, Williams CM. 1965. Programmed cell death—V. Cytolytic enzymes in relation to the breakdown of the intersegmental muscles of silkmoths. J. Insect Physiol. 11:831–44 [Google Scholar]
  109. Mackinder LCM, Worthy CA, Biggi G, Hall M, Ryan KP. et al. 2009. A unicellular algal virus, Emiliania huxleyi virus 86, exploits an animal-like infection strategy. J. Gen. Virol. 90:2306–16 [Google Scholar]
  110. Mannick JB, Schonhoff C, Papeta N, Ghafourifar P, Szibor M. et al. 2001. S-nitrosylation of mitochondrial caspases. J. Cell Biol. 154:1111–16 [Google Scholar]
  111. Marchetti A, Schrutha DM, Durkina CA, Parkera MS, Kodnera RB. et al. 2012. Comparative metatranscriptomics identifies molecular bases for the physiological responses of phytoplankton to varying iron availability. Proc. Natl. Acad. Sci. USA 109:E317–25 [Google Scholar]
  112. Miralto A, Barone G, Romano G, Poulet SA, Ianora A. et al. 1999. The insidious effect of diatoms on copepod reproduction. Nat. Cell Biol. 402:173–76 [Google Scholar]
  113. Moharikar S, D'Souza JS, Kulkarni AB, Rao BJ. 2006. Apoptotic-like cell death pathway is induced in unicellular chlorophyte Chlamydomonas reinhardtii (Chlorophyceae) cells following UV irradiation: detection and functional analyses. J. Phycol. 42:423–33 [Google Scholar]
  114. Mohr A, Zwacka RM. 2007. In situ trapping of initiator caspases reveals intermediate surprises. Cell Biol. Int. 31:526–30 [Google Scholar]
  115. Munekage Y, Hashimoto M, Miyake C, Tomizawa K-I, Endo T. et al. 2004. Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429:579–82 [Google Scholar]
  116. Munekage Y, Hojo M, Meurer J, Endo T, Tasaka M, Shikanai T. 2002. PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110:361–71 [Google Scholar]
  117. Murik O, Kaplan A. 2009. Paradoxically, prior acquisition of antioxidant activity enhances oxidative stress-induced cell death. Environ. Microbiol. 11:2301–9 [Google Scholar]
  118. Neilan JG, Borca MV, Lu G, Kutish GF, Kleiboeker SB. et al. 1999. An African swine fever virus ORF with similarity to C-type lectins is non-essential for growth in swine macrophages in vitro and for virus virulence in domestic swine. J. Gen. Virol. 80:2693–97 [Google Scholar]
  119. Nelson DM, Goering JJ, Boisseau DW. 1981. Consumption and regeneration of silicic acid in three coastal upwelling systems. Coastal Upwelling FA Richards 242–56 Washington, DC: Am. Geophys. Union [Google Scholar]
  120. Nelson DM, Gordon LI. 1982. Production and pelagic dissolution of biogenic silica in the Southern Ocean. Geochim. Cosmochim. Acta 46:491–501 [Google Scholar]
  121. Nelson DM, Tréguer P, Brzezinski MA, Leynaert A, Quéguiner B. 1995. Production and dissolution of biogenic silica in the ocean: revised global estimates, comparison with regional data and relationship to biogenic sedimentation. Glob. Biogeochem. Cycles 9:359–72 [Google Scholar]
  122. Nimchuk Z, Eulgem T, Holt BF III, Dangl JL. 2003. Recognition and response in the plant immune system. Annu. Rev. Genet. 37:579–609 [Google Scholar]
  123. O'Neil JM. 1998. The colonial cyanobacterium Trichodesmium as a physical and nutritional substrate for the harpacticoid copepod Macrosetella gracilis. J. Plankton Res. 20:43–59 [Google Scholar]
  124. Ohki K. 1999. A possible role of temperate phage in the regulation of Trichodesmium biomass. Bull. Inst. Oceanogr. Monaco 19:287–91 [Google Scholar]
  125. Passow U. 2002. Transparent exopolymer particles (TEP) in aquatic environments. Prog. Oceanogr. 55:287–333 [Google Scholar]
  126. Paul C, Pohnert G. 2011. Interactions of the algicidal bacterium Kordia algicida with diatoms: regulated protease excretion for specific algal lysis. PLoS ONE 6:e21032 [Google Scholar]
  127. Peart JR, Mestre P, Lu R, Malcuit I, Baulcombe DC. 2005. NRG1, a CC-NB-LRR protein, together with N, a TIR-NB-LRR, mediates resistance against tobacco mosaic virus. Curr. Biol. 15:968–73 [Google Scholar]
  128. Peers G, Price NM. 2004. A role for manganese in superoxide dismutases and growth of iron-deficient diatoms. Limnol. Oceanogr. 49:1774–83 [Google Scholar]
  129. Pohnert G. 2002. Phospholipase A2 activity triggers the wound-activated chemical defense in the diatom Thalassiosira rotula. Plant Physiol. 129:103–11 [Google Scholar]
  130. Pokrzywinski KL, Place AR, Warner ME, Coyne KJ. 2012. Investigation of the algicidal exudate produced by Shewanella sp. IRI-160 and its effect on dinoflagellates. Harmful Algae 19:23–29 [Google Scholar]
  131. Poulsen N, Chesley PM, Kröger N. 2006. Molecular genetic manipulation of the diatom Thalassiosira pseudonana (Bacillariophyceae). J. Phycol. 42:1059–65 [Google Scholar]
  132. Raff MC. 1992. Social controls on cell survival and cell death. Nature 356:397–400 [Google Scholar]
  133. Ragueneau O, Schultes S, Bidle KD, Claquin P, Moriceau B. 2006. Si and C interactions in the world ocean: importance of ecological processes and implications for the role of diatoms in the biological pump. Glob. Biogeochem. Cycles 20:GB4SO2 [Google Scholar]
  134. Ray JL, Haramaty L, Thyrhaug R, Fredricks HF, Van Mooy BAS. et al. 2014. Virus infection of Haptolina ericina and Phaeocystis pouchetii implicates evolutionary conservation of programmed cell death induction in marine haptophyte–virus interactions. J. Plankton Res. 36:943–55 [Google Scholar]
  135. Read BA, Kegel J, Klute MJ, Kuo A, Lefebvre SC. et al. 2013. Pan genome of the phytoplankton Emiliania underpins its global distribution. Nature 499:209–13 [Google Scholar]
  136. Rice KC, Bayles KW. 2003. Death's toolbox: examining the molecular components of bacterial programmed cell death. Mol. Microbiol. 50:729–38 [Google Scholar]
  137. Richie DL, Miley MD, Bhabhra R, Rodson GD, Rhodes JC, Askew DS. 2007. The Aspergillus fumigatus metacaspases CasA and CasB facilitate growth under conditions of endoplasmic reticulum stress. Mol. Microbiol. 63:591–604 [Google Scholar]
  138. Rodier M, Borgne RL. 2008. Population dynamics and environmental conditions affecting Trichodesmium spp. (filamentous cyanobacteria) blooms in the south-west lagoon of New Caledonia. J. Exp. Mar. Biol. Ecol. 358:20–32 [Google Scholar]
  139. Rodier M, Borgne RL. 2010. Population and trophic dynamics of Trichodesmium thiebautii in the SE lagoon of New Caledonia: comparison with T. erythraeum in the SW lagoon. Mar. Pollut. Bull. 61:349–59 [Google Scholar]
  140. Rose SL, Fulton J, Brown CM, Natale F, Van Mooy BAS, Bidle KD. 2014. Isolation and characterization of lipid rafts in Emiliania huxleyi: a role for membrane microdomains in host-virus interactions. Environ. Microbiol. 16:1150–66 [Google Scholar]
  141. Rosenwasser S, Mausz MA, Schatz D, Sheyn U, Malitsky S. et al. 2014. Rewiring host lipid metabolism by large viruses determines the fate of Emiliania huxleyi, a bloom-forming alga in the ocean. Plant Cell 26:2689–707 [Google Scholar]
  142. Rousseaux C, Gregg W. 2013. Interannual variation in phytoplankton primary production at a global scale. Remote Sens. 6:1–19 [Google Scholar]
  143. Sakamoto H, Okamoto K, Aoki M, Kato H, Katsume A. et al. 2005. Host sphingolipid biosynthesis as a target for hepatitus C virus therapy. Nat. Chem. Biol. 1:333–37 [Google Scholar]
  144. Sanabria NM, Huang J-C, Dubery IA. 2010. Self/nonself perception in plants in innate immunity and defense.. Self Nonself 1:40–54 [Google Scholar]
  145. Sanmartín M, Jaroszewski L, Raikhel NV, Rojo E. 2005. Caspases. Regulating death since the origin of life. Plant Physiol. 137:841–47 [Google Scholar]
  146. Schatz D, Shemi A, Rosenwasser S, Sabanay H, Wolf SG. et al. 2014. Hijacking of an autophagy-like process is essential for the life cycle of a DNA virus infecting oceanic algal blooms. New Phytol In press [Google Scholar]
  147. Schieler BM, Bidle KD. 2014. The potential role of nitric oxide signaling in the infection of Emiliania huxleyi with coccolithoviruses. Presented at Ocean Sci. Meet., Honolulu, HI, Feb 23–28 [Google Scholar]
  148. Schievella AR, Chen JH, Graham JR, Lin L-L. 1997. MADD, a novel death domain protein that interacts with the type I tumor necrosis factor receptor and activates mitogen-activated protein kinase. J. Biol. Chem. 272:12069–75 [Google Scholar]
  149. Schroeder DC, Oke J, Malin G, Wilson WH. 2002. Coccolithovirus (Phycodnaviridae): characterization of a new large dsDNA algal virus that infects Emiliania huxleyi. Arch. Virol. 147:1685–98 [Google Scholar]
  150. Segovia M, Berges JA. 2005. Effect 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 [Google Scholar]
  151. Segovia M, Berges JA. 2009. Inhibition of caspase-like activities prevents the appearance of reactive oxygen species and dark-induced apoptosis in the unicellular chlorophyte Dunaliella tertiolecta. J. Phycol. 45:1116–26 [Google Scholar]
  152. Segovia M, Haramaty 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 [Google Scholar]
  153. Seth-Pasricha M, Bidle KA, Bidle KD. 2013. Specificity of archaeal caspase activity in the extreme halophile Haloferax volcanii. Environ. Microbiol. Rep. 5:263–71 [Google Scholar]
  154. Silva NF, Goring DR. 2002. The proline-rich, extensin-like receptor kinase-1 (PERK1) gene is rapidly induced by wounding. Plant Mol. Biol. 50:667–85 [Google Scholar]
  155. Skulachev VP. 2001. The programmed cell death phenomena, aging, and the Samurai law of biology. Exp. Gerontol. 36:995–1024 [Google Scholar]
  156. Sperandio S, de Belle I, Bredesen DE. 2000. An alternative, nonapoptotic form of programmed cell death. Proc. Natl. Acad. Sci USA 97:14376–81 [Google Scholar]
  157. Stamler JS, Lamas S, Fang FC. 2001. Nitrosylation: the prototypic redox-based signaling mechanism. Cell 106:675–83 [Google Scholar]
  158. Staskawicz BJ, Mudgett MB, Dangl JL, Galan JE. 2001. Common and contrasting themes of plant and animal diseases. Science 292:2285–89 [Google Scholar]
  159. Sukenik A, Eshkol R, Livne A, Hadas O, Rom M. et al. 2002. Inhibition of growth and photosynthesis of the dinoflagellate Peridinium gatunense by Microcystis sp. (cyanobacteria): a novel allelopathic mechanism. Limnol. Oceanogr. 47:1656–63 [Google Scholar]
  160. Summons RE, Jahnke LL, Hope JM, Logan GA. 1999. 2-Methylhopanoids as biomarkers for cyanobacterial oxygenic photosynthesis. Nature 400:555–57 [Google Scholar]
  161. Sunda W, Kieber DJ, Kiene RP, Huntsman S. 2002. An antioxidant function for DMSP and DMS in marine algae. Nature 418:317–20 [Google Scholar]
  162. Suttle CA. 2007. Marine viruses: major players in the global ecosystem. Nat. Rev. Microbiol. 5:801–12 [Google Scholar]
  163. Swiderski MR, Birker D, Jones JDG. 2009. The TIR domain of TIR-NB-LRR resistance proteins is a signaling domain involved in cell death induction. Mol. Plant-Microbe Interact. 22:157–65 [Google Scholar]
  164. Thamatrakoln K, Bailleul B, Brown CM, Gorbunov M, Kustka AB. et al. 2013. Death-specific protein in a marine diatom regulates photosynthetic responses to iron and light availability. Proc. Natl. Acad. Sci. USA 10:20123–28 [Google Scholar]
  165. Thamatrakoln K, Korenovska O, Niheu AK, Bidle KD. 2012. Whole-genome expression analysis reveals a role for death-related genes in stress acclimation of the diatom Thalassiosira pseudonana. Environ. Microbiol. 14:67–81 [Google Scholar]
  166. Thornberry NA, Lazebnik Y. 1998. Caspases: enemies within. Science 281:1312–16 [Google Scholar]
  167. Tilney CL, Pokrzywinski KL, Coyne KJ, Warner ME. 2014. Growth, death, and photobiology of dinoflagellates (Dinophyceae) under bacterial-algicide control. J. Appl. Phycol. 262117–27 [Google Scholar]
  168. Tu S, McStay GP, Boucher L-M, Mak T, Beere HM, Green DR. 2006. In situ trapping of activated initiator caspases reveals a role for caspase-2 in heat shock-induced apoptosis. Nat. Cell Biol. 8:72–77 [Google Scholar]
  169. Tyrell T, Merico A. 2004. Emiliania huxleyi: bloom observations and the conditions that induce them. Coccolithophores: From Molecular Processes to Global Impact HR Thierstein, JR Young 75–97 Berlin: Springer-Verlag [Google Scholar]
  170. Uren AG, O'Rourke K, 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 6:961–67 [Google Scholar]
  171. Valdez-Holguin JE, Alvarez-Borrego S, Mitchell BG. 1998. Photosynthetic parameters of phytoplankton. CalCOFI Rep. 39:148–58 [Google Scholar]
  172. Valiela I. 1995. Marine Ecological Processes New York: Springer-Verlag, 2nd ed.. [Google Scholar]
  173. van Boekel WHM, Hansen FC, Riegman R, Bak RPM. 1992. Lysis-induced decline of a Phaeocystis spring bloom and coupling with the microbial foodweb. Mar. Ecol. Prog. Ser. 81:269–76 [Google Scholar]
  174. Van Etten JL, Graves MV, Müller DG, Boland W, Delaroque N. 2002. Phycodnaviridae—large DNA algal viruses. Arch. Virol. 147:1479–516 [Google Scholar]
  175. Van Mooy BAS, Bidle KD, Johnson M, Mincer T, Vardi A. 2014. Infochemical control of microbial interactions and nutrient cycling in the North Atlantic. http://www.whoi.edu/page.do?pid=80539&tid=282&cid=174829 [Google Scholar]
  176. Van Valen L. 1973. A new evolutionary law. Evol. Theory 1:1–30 [Google Scholar]
  177. Vanlangenakker N, Vanden Berghe T, Vandenabeele P. 2011. Many stimuli pull the necrotic trigger, an overview. Cell Death Differ. 19:75–86 [Google Scholar]
  178. Vardi A. 2008. Cell signaling in marine diatoms. Commun. Integr. Biol. 1:134–36 [Google Scholar]
  179. 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. 9:1061–64 [Google Scholar]
  180. Vardi A, Bidle KD, Kwityn C, Hirsch DJ, Thompson SM. et al. 2008a. A diatom gene regulating nitric oxide signaling and susceptibility to diatom-derived aldehydes. Curr. Biol. 18:895–99 [Google Scholar]
  181. Vardi A, Eisenstadt D, Murik O, Berman-Frank I, Zohary T. et al. 2007. Synchronization of cell death in a dinoflagellate population is mediated by an excreted thiol protease. Environ. Microbiol. 9:360–69 [Google Scholar]
  182. Vardi A, Formiggini F, Casotti R, De Martino A, Ribalet F. et al. 2006. A stress surveillance system based on calcium and nitric oxide in marine diatoms. PLoS Biol. 4:e60 [Google Scholar]
  183. Vardi A, Haramaty L, Van Mooy BAS, Fredricks HF, Kimmance SA. et al. 2012. Host–virus dynamics and subcellular controls of cell fate in a natural coccolithophore population. Proc. Natl. Acad. Sci. USA 109:19327–32 [Google Scholar]
  184. Vardi A, Schatz D, Beeri K, Motro U, Sukenik A. et al. 2002. Dinoflagellate-cyanobacterium communication may determine the composition of phytoplankton assemblage in a mesotrophic lake. Curr. Biol. 12:1767–72 [Google Scholar]
  185. Vardi A, Thamatrakoln K, Bidle KD, Falkowski PG. 2008b. Diatom genomes come of age. Genome Biol. 9:245 [Google Scholar]
  186. Vardi A, Van Mooy BAS, Fredricks HF, Popendorf KJ, Ossolinski JE. et al. 2009. Viral glycosphingolipids induce lytic infection and cell death in marine phytoplankton. Science 326:861–65 [Google Scholar]
  187. Vartapetian AB, Tuzhikov AI, Chichkova NV, Taliansky M, Wolpert TJ. 2011. A plant alternative to animal caspases: subtilisin-like proteases. Cell Death Differ. 18:1289–97 [Google Scholar]
  188. Veldhuis M, Kraay G, Timmermans K. 2001. Cell death in phytoplankton: correlation between changes in membrane permeability, photosynthetic activity, pigmentation and growth. Eur. J. Phycol. 36:167–77 [Google Scholar]
  189. Vercammen D, Declercq W, Vandenabeele P, Van Breusegem. 2007. Are metacaspases caspases?. J. Cell Biol. 179:375–80 [Google Scholar]
  190. Vercammen D, van de Cotte B, de Jaeger G, Eeckhout D, Casteels P. et al. 2004. Type II metacaspases Atmc4 and Atmc9 of Arabidopsis thaliana cleave substrates after arginine and lysine. J. Biol. Chem. 279:45329–36 [Google Scholar]
  191. 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. 280:14691–99 [Google Scholar]
  192. Wilhelm SW, Suttle CA. 1999. Viruses and nutrient cycles in the sea. BioScience 49:781–88 [Google Scholar]
  193. Wilson WH, Schroeder DC, Allen MJ, Holden MTG, Parkhill J. et al. 2005. Complete genome sequence and lytic phase transcription profile of a Coccolithovirus. Science 309:1090–92 [Google Scholar]
  194. Wilson WH, Tarran GA, Schroeder D, Cox M, Oke J, Malin G. 2002. Isolation of viruses responsible for the demise of an Emiliania huxleyi bloom in the English Channel. J. Mar. Biol. Assoc. UK 82:369–77 [Google Scholar]
  195. Wolfe-Simon F, Starovoytov V, Reinfelder JR, Schofield O, Falkowski PG. 2006. Localization and role of manganese superoxide dismutase in marine diatoms. Plant Physiol. 142:1701–9 [Google Scholar]
  196. Yarmolinsky MB. 1995. Programmed cell death in bacterial populations. Science 267:836–37 [Google Scholar]
  197. Yoon HS, Hackett JD, Ciniglia C, Pinto G, Bhattacharya D. 2004. A molecular timeline for the origin of photosynthetic eukaryotes. Mol. Biol. Evol. 21:809–18 [Google Scholar]
  198. Zafiriou OC, McFarland M, Bromund RH. 1980. Nitric oxide in seawater. Science 207:637–39 [Google Scholar]
  199. Zemojtel T, Penzkofer T, Dandekar T, Schultz J. 2004. A novel conserved family of nitric oxide synthase?. Trends Biochem. Sci. 29:224–26 [Google Scholar]
  200. Zuppini A, Andreoli C, Baldan B. 2007. Heat stress: an inducer of programmed cell death in Chlorella saccharophila. Plant Cell Physiol. 48:1000–9 [Google Scholar]
  201. Zuppini A, Gerotto C, Moscatiello R, Bergantino E, Baldan B. 2009. Chlorella saccharophila cytochrome f and its involvement in the heat shock response. J. Exp. Bot. 60:4189–200 [Google Scholar]

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error