Abstract
The supply of some essential metals to pelagic ecosystems is less than the demand, so many phytoplankton have slow rates of photosynthetic production and restricted growth1. The types and amounts of metals required by phytoplankton depends on their evolutionary history2 and on their adaptations to metal availability3,4, which varies widely among ocean habitats. Diatoms, for example, need considerably less iron (Fe) to grow than chlorophyll-b-containing taxa2, and the oceanic species demand roughly one-tenth the amount of coastal strains5,6,7. Like Fe, copper (Cu) is scarce in the open sea, but notably higher concentrations of it are required for the growth of oceanic than of coastal isolates8. Here we report that the greater Cu requirement in an oceanic diatom, Thalassiosira oceanica, is entirely due to a single Cu-containing protein, plastocyanin, which—until now—was only known to exist in organisms with chlorophyll b and cyanobacteria. Algae containing chlorophyll c, including the closely related coastal species T. weissflogii, are thought to lack plastocyanin and contain a functionally equivalent Fe-containing homologue, cytochrome c6 (ref. 9). Copper deficiency in T. oceanica inhibits electron transport regardless of Fe status, implying a constitutive role for plastocyanin in the light reactions of photosynthesis in this species. The results suggest that selection pressure imposed by Fe limitation has resulted in the use of a Cu protein for photosynthesis in an oceanic diatom. This biochemical switch reduces the need for Fe and increases the requirement for Cu, which is relatively more abundant in the open sea.
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References
Morel, F. M. M. & Price, N. M. The biogeochemical cycles of trace metals in the oceans. Science 300, 944–947 (2003)
Quigg, A. et al. The evolutionary inheritance of elemental stoichiometry in marine phytoplankton. Nature 425, 291–293 (2003)
Cullen, J. T., Lane, T. W., Morel, F. M. M. & Sherrell, R. M. Modulation of cadmium uptake in phytoplankton by seawater CO2 concentration. Nature 402, 165–167 (1999)
Strzepek, R. F. & Harrison, P. J. Photosynthetic architecture differs in coastal and oceanic diatoms. Nature 431, 689–692 (2004)
Ryther, J. H. & Kramer, D. D. Relative iron requirements of some coastal and offshore plankton algae. Ecology 42, 444–446 (1961)
Sunda, W. G., Swift, D. G. & Huntsman, S. A. Low iron requirements for growth in oceanic phytoplankton. Nature 351, 55–57 (1991)
Maldonado, M. T. & Price, N. M. Influence of N substrate on Fe requirements of marine centric diatoms. Mar. Ecol. Prog. Ser. 141, 161–172 (1996)
Peers, G., Quesnel, S.-A. & Price, N. M. Copper requirements for iron acquisition and growth of coastal and oceanic diatoms. Limnol. Oceanogr. 50, 1149–1158 (2005)
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. 60, 111–149 (1999)
Brand, L. E., Sunda, W. G. & Guillard, R. R. L. Limitation of marine phytoplankton reproductive rates by zinc, manganese, and iron. Limnol. Oceanogr. 28, 1182–1198 (1983)
Bruland, K. W. Oceanographic distributions of cadmium, zinc, nickel, and copper in the North Pacific. Earth Planet. Sci. Lett. 47, 176–198 (1980)
Moffett, J. W., Brand, L. E., Croot, P. L. & Barbeau, K. A. Cu speciation and cyanobacterial distribution in harbors subject to anthropogenic Cu inputs. Limnol. Oceanogr. 42, 789–799 (1997)
Tortell, P. D. & Price, N. M. Cadmium toxicity and zinc limitation in centric diatoms of the genus Thalassiosira. Mar. Ecol. Prog. Ser. 138, 245–254 (1996)
Sunda, W. G. & Huntsman, S. A. Regulation of copper concentrations in the oceanic nutricline by phytoplankton uptake and regeneration cycles. Limnol. Oceanogr. 40, 132–137 (1995)
Inda, L. A., Erdner, D. L., Peleato, M. L. & Anderson, D. M. Cytochrome c6 isolated from the marine diatom Thalassiosira weissflogii. Phytochemistry 51, 1–4 (1999)
Papageorgiou, G. C. & Govindjee (eds) Chlorophyll a Fluorescence: A Signature of Photosynthesis (Kluwer Academic, Dordrecht, 2004)
Weigel, M. et al. Plastocyanin is indispensable for photosynthetic electron flow in Arabidopsis thaliana. J. Biol. Chem. 278, 31286–31289 (2003)
Quinn, J. M. & Merchant, S. Copper-responsive gene expression during adaptation to copper deficiency. Methods Enzymol. 297, 263–279 (1998)
Schottler, M. A., Kirchhoff, H. & Weis, E. The role of plastocyanin in the adjustment of the photosynthetic electron transport to the carbon metabolism in tobacco. Plant Physiol. 136, 4265–4274 (2004)
da Silva, J. J. R. F. & Williams, R. J. P. The Biological Chemistry of the Elements (Oxford Univ. Press, New York, 2001)
La Fontaine, S. et al. Copper-dependent iron assimilation pathway in the model photosynthetic eukaryote Chlamydomonas reinhardtii. Eukaryot. Cell 1, 736–757 (2002)
Armbrust, E. V. & Galindo, H. M. Rapid evolution of a sexual reproduction gene in centric diatoms of the genus Thalassiosira. Appl. Environ. Microbiol. 67, 3501–3513 (2001)
Archibald, J. M., Rogers, M. B., Topp, M., Ishida, K. & Keeling, P. J. Lateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga Bigelowiella natans. Proc. Natl Acad. Sci. USA 100, 7678–7683 (2003)
Strzepek, R. F. Photosynthetic Iron Requirements of Marine Diatoms. Thesis, Univ. British Columbia (2003)
Moffett, J. W., Zika, R. G. & Brand, L. E. Distribution and potential sources and sinks of copper chelators in the Sargasso Sea. Deep-Sea Res. 37, 27–36 (1990)
Coale, K. H. & Bruland, K. W. Copper complexation in the Northeast Pacific. Limnol. Oceanogr. 33, 1084–1101 (1988)
Bruland, K. W., Donat, J. R. & Hutchins, D. A. Interactive influences of bioactive trace metals on biological production in oceanic waters. Limnol. Oceanogr. 36, 1555–1577 (1991)
Peers, G. & Price, N. M. A role for manganese in superoxide dismutases and growth of Fe-deficient diatoms. Limnol. Oceanogr. 49, 1774–1783 (2004)
Chang, S. I. & Reinfelder, J. R. Bioaccumulation, subcellular distribution, and trophic transfer of copper in a coastal marine diatom. Environ. Sci. Technol. 34, 4931–4935 (2000)
Navarro, J. A., Hervas, M. & De la Rosa, M. A. in Photosynthesis Research Protocols (ed. Carpentier, R.) 79–93 (Humana, Totowa, New Jersey, 2004)
Acknowledgements
We thank R. Popovic for use of the PEA and M. R. Di Falco for purifying the trypsin-digested peptides. This work was supported by grants from the Natural Sciences and Engineering Research Council (NSERC) of Canada and the Centre for Environmental Bio-Inorganic Chemistry (CEBIC, Princeton University).
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The sequences reported here have been deposited in the UniProt knowledgebase under accession number P84800. Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.
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Peers, G., Price, N. Copper-containing plastocyanin used for electron transport by an oceanic diatom. Nature 441, 341–344 (2006). https://doi.org/10.1038/nature04630
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DOI: https://doi.org/10.1038/nature04630
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