Assessing the role of caspase activity and metacaspase expression on viral susceptibility of the coccolithophore, emiliania huxleyi (haptophyta)

Journal of Phycology

Volumn 48, Issue 5, 2012, Pages 1079-1089

  Bidle, Kay D ^a   Kwityn, Clifford J ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

Caspase; Coccolithovirus; Metacaspase; Programmed cell death; Resistance; Sensitivity; Virus infection

Indexed keywords

COCCOLITHOVIRUS; EMILIANIA HUXLEYI; HAPTOPHYCEAE;

EID: 84867213767     PISSN: 00223646     EISSN: 15298817     Source Type: Journal    
DOI: 10.1111/j.1529-8817.2012.01209.x     Document Type: Article

References (43)

1. Balch, W. M., Kilpatrick, K. A. & Trees, C. C. 1996. The 1991 coccolithophore bloom in the central North Atlantic. 1. Optical properties and factors affecting their distribution. Limnol. Oceanogr. 41:1669-83.
2. Berman-Frank, I., Bidle, K., Haramaty, L. & Falkowski, P. 2004. The demise of the marine cyanobacterium, Trichodesmium spp., via an autocatalyzed cell death pathway. Limnol. Oceanogr. 49:997-1005.
3. Bidle, K. D. & Bender, S. J. 2008. Iron starvation and culture age activate metacaspases and programmed cell death in the marine diatom, Thalassiosira pseudonana. Eukaryot. Cell 7:223-36.
4. Bidle, K. D. & Falkowski, P. G. 2004. Cell death in planktonic photosynthetic microorganisms. Nature Rev. Microbiol. 2:643-55.
5. Bidle, K. D., Haramaty, L., Barcelos-Ramos, J. & Falkowski, P. G. 2007. Viral activation and recruitment of metacaspases in the unicellular coccolithophorid, Emiliania huxleyi. Proc. Natl. Acad. Sci. USA 104:6049-54.
6. Bidle, K. D. & Vardi, A. 2011. A chemical arms race at sea mediates algal host-virus interactions. Curr. Opin. Microbiol. 14:1-9.
7. Bozhkov, P. V., Suarez, M. F., Filonova, L. H., Daniel G, Zamyatnin A.A. 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 102:14463-8.
8. Bratbak, G., Egge, J. K. & Heldal, M. 1993. Viral mortality of the marine alga Emiliania huxleyi (Haptophyceae) and termination of algal blooms. Mar. Ecol. Prog. Ser. 93:39-48.
9. Bratbak, G., Wilson, W. & Heldal, M. 1996. Viral control of Emiliania huxleyi blooms? J. Mar. Syst. 9:75-81.
10. Chandra, J., Samali, A. & Orrenius, S. 2000. Triggering and modulation of apoptosis by oxidative stress. Free Radical Biol. Med. 29:323-33.
11. Cohen, G. M. 1997. Caspases: the executioners of apoptosis. Biochem. J. 326:1-16.
12. Evans, C., Malin, G., Mills, G. P. & Wilson, W. H. 2006a. Viral infection of Emiliania huxyleyi (Prymnesiophyceae) leasd to elevated production of reactive oxygen species J. Phycol. 42:1040-7.
13. Evans, C., Malin, G., Wilson, W. H. & Liss, P. S. 2006b. Infectious titers of Emiliania huxleyi virus 86 are reduced by exposure to millimolar dimethyl sulfide and acrylic acid. Limnol. Oceanogr. 51:2468-71.
14. Fuhrman, J. A. 1999. Marine viruses and their biogeochemical and ecological effects. Nature 399:541-8.
15. Holligan, P. M., Fernandez, E., Aiken, J., Balch, W. M., Boyd, P., Burkill, P. H., Finch, M., Groom, S. B., Malin, G. & Muller, K. 1993. A biogeochemical study of the coccolithophore, Emiliana huxleyi, in the North Atlantic. Global Biogeochem. Cycles 7:879-900.
16. Iglesias-Rodriguez, M. D., Brown, C. W., Doney, S. C., Kleypas, J., Kolber, D., Kolber, Z., Hayes, P. K. & Falkowski, P. 2002. Representing key phytoplankton functional groups in ocean carbon cycle models: Coccolithophorids. Global Biogeochem. Cycles 16:1100.
17. Jacquet, S., Heldal, M., Iglesias-Rodriguez, D., Larsen, A., Wilson, W. & Bratbak, G. 2002. Flow cytometric analysis of an Emiliania huxleyi bloom terminated by viral infection. Aquat. Microb. Ecol. 27:111-24.
18. Leblanc, K., Hare, C. E., Feng, Y., Berg, G. M., DiTullio, G. R., Neeley, A., Benner, I. et al. 2009. Distribution of calcifying and silicifying phytoplankton in relation to environmental and biogeochemical parameters during the late stages of the 2005 North East Atlantic Spring Bloom. Biogeosciences 6:2155-79.
19. Liao, W. 2010. Further characterization of metacaspase expression and activity in marine phytoplankton. Rutgers University, M.S., 77 pp.
20. Madeo, F., Herker, E., Maldener, C., Wissing, S., Lächelt, S., Herlan, M., Fehr, M., Lauber, K., Sigrist, S. J., Wesselborg, S. & Fröhlich, K.-U. 2002. A caspase-related protease regulates apoptosis in yeast. Mol. Cell 9:911-7.
21. Martinez-Martinez, J., Schroeder, D. C., Larsen, A., Bratbak, G. & Wilson, W. H. 2007. Molecular dynamics of Emiliania huxleyi and cooccurring viruses during two separate mesocosm studies. Appl. Environ. Microbiol. 73:554-62.
22. Richie, D. L., Miley, M. D., Bhabhra, R., Rodson, G. D., Rhodes, J. C. & Askew, D. S. 2007. The Aspergillus fumigatus metacaspases CasA and CasB facilitate growth under conditions of endoplasmic reticulum stress. Mol. Microbiol. 63:591-604.
23. Schroeder, D. C., Oke, J., Hall, M., Malin, G. & Wilson, W. H. 2003. Virus succession observed during an Emiliania huxleyi bloom. Appl. Environ. Microbiol. 69:2484-90.
24. Schroeder, D. C., Oke, J., Malin, G. & Wilson, W. H. 2002. Coccolithovirus (Phycodnaviridae): characterization of a new large dsDNA algal virus that infects Emiliania huxleyi. Arch. Virol. 147:1685-98.
25. Segovia, M. & Berges, J. A. 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.
26. Segovia, M. Ã., 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. 132:99-105.
27. Soosaar, J. L. M., Burch-Smith, T. M. & Dinesh-Kumar, S. P. 2005. Mechanisms of plant resistance to viruses. Nat. Rev. Microbiol. 3:789-98.
28. Steinke, M., Wolfe, G. V. & Kirst, G. O. 1998. Partial characterisation of dimethylsulfoniopropionate (DMSP) lyase isozymes in 6 strains of Emiliania huxleyi. Mar. Ecol. Prog. Ser. 175:215-25.
29. Stennicke, H. R. & Salvesen, G. S. 1998. Properties of the caspases. Biochim. Biophys. Acta 1387:17-31.
30. Strom, S., Wolfe, G., Holmes, J., Stecher, H., Shimeneck, C., Lambert, S. & Moreno, E. 2003. Chemical defense in the microplankton I: Feeding and growth rates of heterotrophic protists on the DMS-producing phytoplankter Emiliania huxleyi. Limnol. Oceanogr. 48:217-29.
31. Sunda, W., Kieber, D. J., Kiene, R. P. & Huntsman, S. 2002. An antioxidant function for DMSP and DMS in marine algae. Nature 418:317-20.
32. Suttle, C. A. 2007. Marine viruses: major players in the global ecosystem. Nat. Rev. Microbiol. 5:801-12.
33. Szallies, A., Kubata, B. K. & Duszenko, M. 2002. A metacaspase of Trypanosoma brucei causes loss of respiration competence and clonal death in the yeast Saccharomyces cerevisiae. FEBS Lett. 517:144-50.
34. Thamatrakoln, K., Korenovska, O., Niheu, A. K. & Bidle, K. D. 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.
35. Thornberry, N. A. & Lazebnik, Y. 1998. Caspases: enemies within. Science 281:1312-6.
36. Uren, A. G., O'Rourke, K., Pisabarro, M. T., Seshagiri, S., Koonin, E. V. & Dixit, V. M. 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 6:961-7.
37. Vardi, A., Bidle, K., Kwityn, C., Hirsch, D. J., Thompson, S. M., Callow, J. A., Falkowski, P. & Bowler, C. 2008. A diatom gene regulating nitric oxide signaling and susceptibility to diatom-derived aldehydes. Curr. Biol. 18:1-5.
38. Vardi, A., Formiggini, F., Casotti, R., deMartino, A., Ribalet, F., Miralto, A. & Bowler, C. 2006. A stress surveillance system based on calcium and nitric oxide in marine diatoms. PLoS Biol. 4:e60.
39. Vardi, A., Mooy, B. A. S. V., Fredricks, H. F., Popendorf, K. J., Ossolinski, J. E., Haramaty, L. & Bidle, K. D. 2009. Viral glycosphingolipids induce lytic infection and cell death in marine phytoplankton. Science 326:861-5.
40. Vercammen, D., Cotte, B. v. d., Jaeger, G. D., Eeckhout, D., Casteels, P., Vandepoele, K., Vandenberghe, I., Beeumen, J. V., Inzé, D. & Breusegem, F. V. 2004. Type II metacaspases Atmc4 and Atmc9 of Arabidopsis thaliana cleave substrates after arginine and lysine. J. Biol. Chem. 279:45329-36.
41. Vercammen, D., Declercq, W., Vandenabeele, P. & Breusegem, F. V. 2007. Are metacaspases caspases? J. Cell Biol. 179:375-80.
42. 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. 280:14691-9.
43. Wilson, W. H., Tarran, G. A., 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. Bio. Assoc. UK 82:369-77.