The response of carotenoids and chlorophylls during virus infection of Emiliania huxleyi (Prymnesiophyceae)

Journal of Experimental Marine Biology and Ecology

Volumn 344, Issue 1, 2007, Pages 101-112

  Llewellyn, Carole A ^a   Evans, Claire ^a   Airs, Ruth L ^a   Cook, Isobel ^a   Bale, Nicole ^a   Wilson, William H ^a  

^a PLYMOUTH MARINE LABORATORY   (United Kingdom)

Author keywords

Algae; Carotenoids; Chlorophyll; Photophysiology; Virus infection; Xanthophyll cycle

Indexed keywords

CAROTENOID; CHLOROPHYLL; HOST-PATHOGEN INTERACTION; PHOTOOXIDATION; PHYSIOLOGICAL RESPONSE; PHYTOPLANKTON; VIRAL DISEASE;

ALGAE; EMILIANIA HUXLEYI; HAPTOPHYCEAE;

EID: 33947311177     PISSN: 00220981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jembe.2006.12.013     Document Type: Article

References (59)

1. Airs R.L., and Llewellyn C.A. Improved detection and characterisation of fucoxanthin-type carotenoids: novel pigments in Emiliania huxleyi (Prymnesiophyceae). J. Phycol. 42 (2006) 391-399
2. Balachandran S., Osmond C.B., and Daley P.F. Diagnosis of the earliest strain-specific interactions between tobacco mosaic virus and chloroplasts of tobacco leaves in vivo by means of chlorophyll fluorescence imaging. Plant Physiol. 104 (1994) 1059-1065
3. Barlow R.G., Cummings D.G., and Gibb S.W. Improved resolution of mono- and divinyl chlorophylls a and b and zeaxanthin and lutein in phytoplankton extracts using reverse phase C-8 HPLC. Mar. Ecol. Prog. Ser. 161 (1997) 303-307
4. Bratbak G., Egge J.K., and Heldal M. Viral mortality of the marine algae Emiliania huxleyi (Haptophyceae) and termination of algal blooms. Mar. Ecol. Prog. Ser. 93 (1993) 39-48
5. Brussaard C.P.D. Viral control of phytoplankton populations-a review. J. Eukaryot. Microbiol. 51 (2004) 125-138
6. Brussaard C.P.D., Thyrhaug R., Marie D., and Bratbak G. Flow cytometric analysis of viral infection in two marine phytoplankton species, Micromonas pusilla (Prasinophyceae) and Phaeocystis pouchetii (Prymnesiophyceae). J. Phycol. 35 (1999) 941-948
7. Castberg T., Thyrhang R., Larsen A., Sandaa R., Heldal M., Van Etten J.L., and Bratbak G. Isolation and characterisation of a virus that infects Emiliania huxleyi (Haptophyta). J. Phycol. 38 (2002) 767-774
8. Demmig-Adams B., and Adams III W.W. The xanthophyll cycle. In: Young A., and Britton G. (Eds). Carotenoids in Photosynthesis (1993), Chapman & Hall, London 206-251
9. Demmig-Adams B., and Adams III W.W. The role of xanthophylls cycle carotenoids in the protection of photosynthesis. Trends in Plant Sci. 1 (1996) 21-26
10. Edge R., McGarvey D.J., and Truscott T.G. The carotenoids as anti-oxidants-a review. J. Photochem. Photobiol., B Biol. 41 (1997) 189-200
11. Evans, C., 2005. The influence of marine viruses on the production of dimethyl sulphide (DMS) and related compounds from Emiliania huxleyi. PhD thesis. University of East Anglia.
12. Evans C., Malin G., Mills G.P., and Wilson W.H. Viral infection of Emiliania huxleyi (Prymnesiophyceae) leads to elevated production of reactive oxygen species. J. Phycol. 42 (2006) 1040-1047
13. Fiedor J., Fiedor L., Winkler J., Scherz A., and Scheer H. Photodynamics of the bacteriochlorophyll-carotenoid system. 1. Bacteriochlorophyll-photosensitized oxygenation of β-carotene in acetone. Photochem. Photobiol. 74 (2001) 64-71
14. Fiedor J., Fiedor L., Haessner R., and Scheer H. Cyclic endoperoxides of beta-carotene, potential pro-oxidants, as products of chemical quenching of singlet oxygen. BBA-Bioenergetics vol. 1709 (2005) 1-4
15. Foote C.S., and Denny R.W. Chemistry of singlet oxygen 7. Quenching by beta-carotene. J. Am. Chem. Soc. 90 (1968) 6233
16. Frank H.A. Incorporation of carotenoids into reaction center and light-harvesting pigment-protein complexes. In: Frank H.A., Young A.J., Britton G., and Cogdell R.J. (Eds). The Photochemistry of the Carotenoids, Advances in Photosynthesis (1999), Kluwer Academic, Dordrecht 235-244
17. Fuhrman J.A. Marine viruses and their biogeochemical and ecological effects. Nature 39 (1999) 541-548
18. Garrido J.L., Otero J., Maestro M.A., and Zapata M. The main nonpolar chlorophyll c from Emiliania huxleyi (Prymnesiophyceae) is a chlorophyll c(2)-monogalactosyldiacylglyceride ester: a mass spectrometry study. J. Phycol. 36 (2000) 497-505
19. 2-labelling kinetics of carotenoids. J. Phycol. 28 (1992) 507-517
20. Guillard R.R.L. Culture of phytoplankton for feeding marine invertebrates. In: Smith W.L., and Chanley M.H. (Eds). Culture of Marine Invertebrate Animals (1975), Academic Press, New York 29-60
21. Hallegraeff G.M., and Jeffrey S.W. Description of new chlorophyll-a alteration products in marine phytoplankton. Deep-Sea Res. 32 (1985) 697-705
22. Head E.J.H., and Harris L.R. Chlorophyll and carotenoids transformation and destruction by Calanus spp grazing on diatoms. Mar. Ecol. Prog. Ser. 86 (1992) 229-238
23. Henriksen P., Riemann B., Kaas H., Sørensen H.M., and Sørensen H.L. Effects of nutrient-limitation and irradiance on marine phytoplankton pigments. J. Plankton Res. 24 (2002) 835-858
24. Hodgson R.A.J., Beachy R.N., and Pakrasi H.B. Selective inhibition of photosystem II in spinach by tobacco mosaic virus: an effect of the viral coat protein. FEBS Lett. 245 (1989) 267-270
25. Holligan P.M., Fernandez E., Aiken J., Balch W.M., Boyd P., Burkill P.H., Finch M., Groom S.B., Malin G., Muller K., Purdie D.A., Robinson C., Trees C.C., Turner S.M., and Vanderwal P. A biogeochemical study of the Coccolithophore, Emiliania huxleyi, in the North-Atlantic. Global Biogeochem. Cycles 7 (1993) 879-900
26. Jacquet S., Heldal M., Iglesias-Rodriguez D., Larsen A., Wilson W., and Bratbak G. Flow cytometric analysis of an Emiliania huxleyi bloom terminated by viral infection. Aquat. Microb. Ecol. 27 (2002) 11-124
27. Jeffrey S.W., Llewellyn C.A., Barlow R.G., and Mantoura R.F.C. Pigment processes in the sea: a selected bibliography. In: Jeffrey S.W., Mantoura R.F.C., and Wright S.W. (Eds). Phytoplankton in Oceanography (1997), UNESCO Publishing, Paris 167-178
28. Jeffrey S.W., Mantoura R.F.C., and Bjφrnland T. Data for the identification of 47 key phytoplankton pigments. In: Jeffrey S.W., Mantoura R.F.C., and Wright S.W. (Eds). Phytoplankton in Oceanography (1997), UNESCO Publishing, Paris 449-559
29. Juneau P., Lawrence J.E., Suttle C.A., and Harrison P.J. Effects of viral infection on photosynthetic processes in the bloom-forming alga Heterosigma akashiwo. Aquat. Microb. Ecol. 31 (2003) 9-17
30. Keller M.D. Dimethyl sulphide production and marine phytoplankton: the importance of species composition and cell size. Biol. Oceanogr. 6 (1989) 375-382
31. Krinsky N.I. Function. In: Isler O. (Ed). Carotenoids (1971), Birkhäuser Verlag, Basel 669-716
32. Krinsky N.I. Carotenoid protection against oxidation. Pure Appl. Chem. 51 (1979) 649-660
33. Larsen A., Flaten G.A.F., Sandaa R.A., Castberg T., Thyrhaug R., Erga S.R., Jacquet S., and Bratbak G. Spring phytoplankton bloom dynamics in Norwegian coastal waters: microbial community succession and diversity. Limnol. Oceanogr. 49 (2004) 180-190
34. LeRouzic B., Bertru G., and Brient L. HPLC analysis of chlorophyll-a breakdown products to interpret microalgae dynamics in a shallow bay. Hydrobiology 302 (1995) 71-80
35. Lohr M., and Wilhelm C. Algae displaying the diadinoxanthin cycle also possess the violaxanthin cycle. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 8784-8789
36. Lohr M., and Wilhelm C. Xanthophyll synthesis in diatoms: quantification of putative intermediates and comparison of pigment conversion kinetics with rate constants derived from a model. Planta 212 (2001) 382-391
37. Mackey M.D., Mackey D.J., Higgins H.W., and Wright S.W. CHEMTAX-a program for estimating class abundances from chemical markers: application to HPLC measurements of phytoplankton. Mar. Ecol. Prog. Ser. 144 (1996) 265-283
38. Mallick N., and Mohn F.H. Reactive oxygen species: response of algal cells. J. Plant Physiol. 157 (2000) 183-193
39. Marie D., Brussaard C.P.D., Thyrhaug R., Bratbak G., and Vaulot D. Enumeration of marine viruses in cultures and nature by flow cytometry. Appl. Environ. Microb. 65 (1999) 45-52
40. Muller P., Li X.P., and Niyogi K.K. Non-photochemical quenching. A response to excess light energy. Plant Physiol. 125 (2001) 1558-1566
41. Naidu R.A., Krishnan M., Nayuda M.V., and Gnaman A. Studies on peanut green mosaic virus infected peanut (Arackis kypogaeu L.) leaves. II. Chlorophyll-protein complexes and polypeptide composition of thylakoid membranes. Physiol. Plant Pathol. 25 (1984) 191-198
42. Naidu R.A., Krishnan M., Ramanujan P., Gnaman A., and Nayuda M.V. Studies on peanut green mosaic virus infected peanut (Arackis hypogaeu L.) leaves. I. Photosynthesis and photochemical reactions. Physiol. Plant Pathol. 25 (1984) 181-190
43. Polivka T., Herek J.L., Zigmantas D., Åkerland H.-E., and Sundström V. Direct observation of the (forbidden) S1 state in carotenoids. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 4914-4917
44. Reinero A., and Beachy R.N. Reduced photosystem I1 activity and accumulation of viral coat protein in chloroplasts of leaves infected with tobacco mosaic virus. Plant Physiol. 89 (1989) 111-116
45. Roy S., Chanut J.P., Gosselin M., and SimeNgando T. Characterization of phytoplankton communities in the lower St Lawrence estuary using HPLC-detected pigments and cell microscopy. Mar. Ecol. Prog. Ser. 142 (1996) 55-73
46. Schlüter L., Møhlenberg F., Havskum H., and Larsen S. The use of phytoplankton pigments for identifying and quantifying phytoplankton groups in coastal areas: testing the influence of light and nutrients on pigment/chlorophyll a ratios. Mar. Ecol. Prog. Ser. 19 (2000) 49-63
47. Seaton G.G.R., Lee K., and Rohozinski J. Photosynthetic shutdown in ChlorellaNC64A associated with the infection cycle of Paramecium bursaria Chlorellavirus-1. Plant Physiol. 108 (1995) 1431-1438
48. Seaton G.G.R., Hurry V.M., and Rohozinski J. Novel amplification of non-photochemical chlorophyll fluorescence quenching following viral infection in Chlorella. FEBS Lett. 3 (1996) 19-323
49. Short S.M., and Suttle C.A. Temporal dynamics of natural communities of marine algal viruses and eukaryotes. Aquat. Microb. Ecol. 32 (2003) 107-119
50. Stratton S.P., Schaefer W.H., and Liebler D.C. Isolation and Identification of singlet oxygen oxidation-products of beta-carotene. Chem. Res. Toxicol. 6 (1993) 542-547
51. Suttle C.A. Viruses in the sea. Nature 437 (2005) 356-361
52. Szabo I., Bergantino E., and Giacometti G.M. Light and oxygenic photosynthesis: energy dissipation as a protection mechanisms against photo-oxidation. EMBO Rep. 6 (2005) 629-634
53. Thyrhaug R., Larsen A., Thingstad T.F., and Bratbak G. Stable coexistence in marine algal host-virus systems. Mar. Ecol. Prog. Ser. 254 (2003) 27-35
54. Wilhelm S.W., and Suttle C.A. Viruses and nutrient cycles in the sea. Bioscience 49 (1999) 781-788
55. Wilson W.H., Tarran G.A., Schroeder D., Cox M., Oke J., and Malin G. Isolation of viruses responsible for the demise of an Emiliania huxleyi bloom in the English Channel. J. Mar. Biol. Assoc. U. K. 82 (2002) 369-377
56. Wilson W.H., Schroeder D.C., Allen M.J., Holden M.T.G., Parkhill J., Barrell B.G., Churcher C., Harnlin N., Mungall K., Norbertczak H., Quail M.A., Price C., Rabbinowitsch E., Walker D., Craigon M., Roy D., and Ghazal P. Complete genome sequence and lytic phase transcription profile of a Coccolithovirus. Science 309 (2005) 1090-1092
57. Yamamoto H.Y. Xanthophyll cycles. Methods Enzymol. 110 (1985) 303-312
58. Young A.J. Carotenoids in pigment-protein complexes. In: Young A.J., and Britton G. (Eds). Carotenoids in Photosynthesis (1993), Chapman & Hall, London 72-95
59. Young A.J., Phillip D., Ruban A.V., Horton P., and Frank H.A. The xanthophylls cycle and carotenoid-mediated dissipation of excess excitation energy in photosynthesis. Pure Appl. Chem. 69 (1997) 2125-2130