Effects of iron and copper deficiency on the expression of members of the light-harvesting family in the diatom Thalassiosira pseudonana (bacillariophyceae)

Journal of Phycology

Volumn 46, Issue 5, 2010, Pages 974-981

  Zhu, Song Hua ^a   Guo, Jian ^a   Maldonado, Maria T ^a   Green, Beverley R ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Copper deficiency; Diatom; Gene expression; Iron deficiency; Lhcx genes, LI818; Photoprotection; Photosystem I; Thalassiosira pseudonana

Indexed keywords

BACILLARIOPHYCEAE; BACILLARIOPHYTA; THALASSIOSIRA PSEUDONANA;

EID: 77957301015     PISSN: 00223646     EISSN: 15298817     Source Type: Journal    
DOI: 10.1111/j.1529-8817.2010.00884.x     Document Type: Article

References (57)

1. Allen A E, LaRoche J, Maheswari U, Lommer M, Schauer N, Lopez P J, Finazzi G, Fernie A R, Bowler C. Whole-cell response of the pennate diatom Phaeodactylum tricornutum to iron starvation. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:10438-43.
2. Amunts A, Nelson N. Functional organization of a plant photosystem I: evolution of a highly efficient photochemical machine. Plant Physiol. Biochem. 2008, 46:228-37.
3. Annett A L, Lapi S, Ruth T J, Maldonado M T. The effects of Cu and Fe availability on the growth and Cu:C ratios of marine diatoms. Limnol. Oceanogr. 2008, 53:2451-61.
4. Armbrust E V, Berges J A, Bowler C, Green B R, Martinez D, Putnam N H, Zhou S G. The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 2004, 306:79-86.
5. Bilger W, Bjorkman O. Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbency changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynth. Res. 1990, 25:173-85.
6. Boyd P W, Watson A J, Law C S, Abraham E R, Trull T, Murdoch R, Bakker D C E. A mesoscale phytoplankton bloom in the polar Southern Ocean stimulated by iron fertilization. Nature 2000, 407:695-702.
7. Brand L E, Guillard R R L, Murphy L S. A method for the rapid and precise determination of acclimated phytoplankton reproduction rates. J. Plankton Res. 1981, 3:193-202.
8. Bruland K W, Donat J R, Hutchins D A. Interactive influences of bioactive trace-metals on biological production in oceanic waters. Limnol. Oceanogr. 1991, 36:1555-77.
9. Chadd H E, Newman J, Mann N H, Carr N G. Identification of iron superoxide dismutase and a copper/zinc superoxide dismutase enzyme activity within the marine cyanobacterium Synechococcus sp. WH 7803. FEMS Microbiol. Lett. 1996, 138:161-5.
10. Coale K H, Johnson K S, Fitzwater S E, Gordon R M, Tanner S, Chavez F P, Ferioli L. A massive phytoplankton bloom induced by an ecosystem-scale iron fertilization experiment in the equatorial Pacific Ocean. Nature 1996, 383:495-501.
11. Debaar H J W, Dejong J T M, Bakker D C E, Loscher B M, Veth C, Bathmann U, Smetacek V. Importance of iron for plankton blooms and carbon-dioxide drawdown in the Southern Ocean. Nature 1995, 373:412-5.
12. Doan J M, Schoefs B, Ruban A V, Etienne A L. Changes in the LHCI aggregation state during iron repletion in the unicellular red alga Rhodella violacea. FEBS Lett. 2003, 533:59-62.
13. Gagne G, Guertin M. The early genetic response to light in the green unicellular alga Chlamydomonas eugametos grown under light dark cycles involves genes that represent direct responses to light and photosynthesis. Plant Mol. Biol. 1992, 18:429-45.
14. Geider R J, Laroche J. The role of iron in phytoplankton photosynthesis, and the potential for iron-limitation of primary productivity in the sea. Photosynth. Res. 1994, 39:275-301.
15. Geider R J, Laroche J, Greene R M, Olaizola M. Response of the photosynthetic apparatus of Phaeodactylum tricornutum (Bacillariophyceae) to nitrate, phosphate, or iron starvation. J. Phycol. 1993, 29:755-66.
16. Green B R. The evolution of light-harvesting antennas. Light-harvesting Antennas in Photosynthesis 2003, 129-68. Green B RParson W W. Eds, Kluwer Academic, Dordrecht, the Netherlands, pp
17. Green B R. Evolution of light-harvesting antennas in an oxygen world. Evolution of Primary Producers in the Sea 2007, 37-53. Falkowski P GKnoll A H. Eds, Elsevier, Burlington, Massachusetts, pp
18. Greene R M, Geider R J, Kolber Z, Falkowski P G. Iron-induced changes in light harvesting and photochemical energy-conversion processes in eukaryotic marine algae. Plant Physiol. 1992, 100:565-75.
19. Harnett J P. Isolation and characterization of photosystem I and the fucoxanthin-chlorophyll a/c proteins of the chromophyte alga Heterosigma carterae. 1998, MSc dissertation, University of British Columbia, Vancouver, pp
20. Hudson R J M, Morel F M M. Iron transport in marine-phytoplankton - kinetics of cellular and medium coordination reactions. Limnol. Oceanogr. 1990, 35:1002-20.
21. Ikeda Y, Komura M, Watanabe M, Minami C, Koike H, Itoh S, Kashino Y, Satoh K. Photosystem I complexes associated with fucoxanthin-chlorophyll-binding proteins from a marine centric diatom, Chaetoceros gracilis. Biochem. Biophys. Acta Bioenergetics 2008, 1777:351-61.
22. Im C S, Zhang Z D, Shrager J, Chang C W, Grossman A R. Analysis of light and CO2 regulation in Chlamydomonas reinhardtii using genome-wide approaches. Photosynth. Res. 2003, 75:111-25.
23. Johnson K S, Gordon R M, Coale K H. What controls dissolved iron concentrations in the world ocean? Mar. Chem. 1997, 57:137-61.
24. Kouřil R, Arteni A A, Lax J, Yeremenko N, D'Haene S, Rögner M, Matthijs H C P, Dekker J P, Boekema E J. Structure and functional role of supercomplexes of IsiA and photosystem I in cyanobacterial photosynthesis. FEBS Lett. 2005, 579:3253-7.
25. Koziol A G, Borza T, Ishida K I, Keeling P, Lee R W, Durnford D G. Tracing the evolution of the light-harvesting antennae in chlorophyll a/b-containing organisms. Plant Physiol. 2007, 143:1802-16.
26. La Fontaine S, Quinn J M, Nakamoto S S, Page M D, Göhre V, Moseley J L, Kropat J, Merchant S. Copper-dependent iron assimilation pathway in the model photosynthetic eukaryote Chlamydomonas reinhardtii. Eukaryot. Cell 2002, 1:736-57.
27. Maheswari U, Montsant A, Goll J, Krishnasamy S, Rajyashri K R, Patell V M, Bowler C. The diatom EST database. Nucleic Acids Res. 2005, 33:D344-7.
28. Maldonado M T, Allen A E, Chong J S, Lin K, Leus D, Karpenko N, Harris S L. Copper-dependent iron transport in coastal and oceanic diatoms. Limnol. Oceanogr. 2006, 51:1729-43.
29. Martin J H, Coale K H, Johnson K S, Fitzwater S E, Gordon R M, Tanner S J, Hunter C N. Testing the iron hypothesis in ecosystems of the equatorial Pacific Ocean. Nature 1994, 371:123-9.
30. Martin J H, Gordon R M, Fitzwater S E. Iron in Antarctic waters. Nature 1990, 345:156-8.
31. Merchant S S, Allen M D, Kropat J, Moseley J L, Long J C, Tottey S, Terauchi A M. Between a rock and a hard place: trace element nutrition in Chlamydomonas. Biochem. Biophys. Acta Mol. Cell Res. 2006, 1763:578-94.
32. Mock T, Samanta M P, Iverson V, Berthiaume C, Robison M, Holtermann K, Durkin C. Whole-genome expression profiling of the marine diatom Thalassiosira pseudonana identifies genes involved in silicon bioprocesses. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:1579-84.
33. Moseley J L, Allinger T, Herzog S, Hoerth P, Wehinger E, Merchant S, Hippler M. Adaptation to Fe-deficiency requires remodeling of the photosynthetic apparatus. EMBO (Eur. Mol. Biol. Organ.) J. 2002, 21:6709-20.
34. Moseley J L, Chang C W, Grossman A R. Genome-based approaches to understanding phosphorus deprivation responses and PSR1 control in Chlamydomonas reinhardtii. Eukaryot. Cell 2006, 5:26-44.
35. Naumann B, Busch A, Allmer J, Ostendorf E, Zeller M, Kirchhoff H, Hippler M. Comparative quantitative proteomics to investigate the remodeling of bioenergetic pathways under iron deficiency in Chlamydomonas reinhardtii. Proteomics 2007, 7:3964-79.
36. Naumann B, Stauber E J, Busch A, Sommer F, Hippler M. N-terminal processing of Lhca3 is a key step in remodeling of the photosystem I light-harvesting complex under iron deficiency in Chlamydomonas reinhardtii. J. Biol. Chem. 2005, 280:20431-41.
37. Peers G, Quesnel S A, Price N M. Copper requirements for iron acquisition and growth of coastal and oceanic diatoms. Limnol. Oceanogr. 2005, 50:1149-58.
38. Price N M, Harrison G I, Hering J G, Hudson R J, Nirel P M V, Palenik B, Morel F M M. Preparation and chemistry of the artificial algal culture medium Aquil. Biol. Oceanogr 1988/1989, 6:443-62.
39. Raven J A. Predictions of Mn and Fe use efficiencies of phototrophic growth as a function of light availability for growth and of C assimilation pathway. New Phytol. 1990, 116:1-18.
40. Raven J A, Evans M C W, Korb R E. The role of trace metals in photosynthetic electron transport in O2-evolving organisms. Photosynth. Res. 1999, 60:111-49.
41. Sandmann G, Reck H, Kessler E, Boger P. Distribution of plastocyanin and soluble plastidic cytochrome c in various classes of algae. Arch. Microbiol. 1983, 134:23-7.
42. Savard F, Richard C, Guertin M. The Chlamydomonas reinhardtii LI818 gene represents a distant relative of the cab I/II genes that is regulated during the cell cycle and in response to illumination. Plant Mol. Biol. 1996, 32:461-73.
43. Schreiber U, Endo T, Mi H L, Asada K. Quenching analysis of chlorophyll fluorescence by the saturation pulse method-particular aspects relating to the study of eukaryotic algae and cyanobacteria. Plant Cell Physiol. 1995a, 36:873-82.
44. Schreiber U, Hormann H, Neubauer C, Klughammer C. Assessment of photosystem II photochemical quantum yield by chlorophyll fluorescence quenching analysis. Aust. J. Plant. Physiol. 1995b, 22:209-20.
45. Stryer L. Biochemistry 1988, W. H. Freeman, New York, pp
46. Sunda W G, Huntsman S A. Iron uptake and growth limitation in oceanic and coastal phytoplankton. Mar. Chem. 1995, 50:189-206.
47. Sunda W G, Huntsman S A. Interrelated influence of iron, light and cell size on marine phytoplankton growth. Nature 1997, 390:389-92.
48. Tsuda A, Takeda S, Saito H, Nishioka J, Nojiri Y, Kudo I, Kiyosawa H. A mesoscale iron enrichment in the western subarctic Pacific induces a large centric diatom bloom. Science 2003, 300:958-61.
49. Vassiliev I R, Kolber Z, Wyman K D, Mauzerall D, Shukla V K, Falkowski P G. Effects of iron limitation on photosystem II composition and light utilization in Dunaliella tertiolecta. Plant Physiol. 1995, 109:963-72.
50. Veith T, Brauns J, Weisheit W, Mittag M, Büchel C. Identification of a specific fucoxanthin-chlorophyll protein in the light harvesting complex of photosystem I in the diatom Cyclotella meneghiniana. Biochem. Biophys. Acta Bioenergetics 2009, 1787:905-12.
51. Veith T, Büchel C. The monomeric photosystem I-complex of the diatom Phaeodactylum tricornutum binds specific fucoxanthin chlorophyll proteins (FCPs) as light-harvesting complexes. Biochem. Biophys. Acta Bioenergetics 2007, 1767:1428-35.
52. Westermann M, Rhiel E. Localisation of fucoxanthin chlorophyll a/c-binding polypeptides of the centric diatom Cyclotella cryptica by immuno-electron microscopy. Protoplasma 2005, 225:217-23.
53. Yamano T, Miura K, Fukuzawa H. Expression analysis of genes associated with the induction of the carbon-concentrating mechanism in Chlamydomonas reinhardtii. Plant Physiol. 2008, 147:340-54.
54. Zhang Z D, Shrager J, Jain M, Chang C W, Vallon O, Grossman A R. Insights into the survival of Chlamydomonas reinhardtii during sulfur starvation based on microarray analysis of gene expression. Eukaryot. Cell 2004, 3:1331-48.
55. Zhu S H. Characterization of LI818-like genes under various stress conditions in the marine diatom Thalassiosira pseudonana. 2009, PhD dissertation, University of British Columbia, Vancouver, pp
56. Zhu S H, Green B R. Light-harvesting and photoprotection in diatoms: identification and expression of LI818-like proteins. 2008, 261-4. Allen J F, Gantt EGolbeck J HOsmond B. Eds.] Photosynthesis. Energy from the Sun., Springer, Heidelberg, Germany, pp
57. Zhu S H, Green B R. Photoprotection in the diatom Thalassiosira pseudonana: role of LI818-like proteins in response to high light stress. Biochem. Biophys. Acta Bioenergetics 2010, 1797:1449-57.