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Iron acquisition by photosynthetic marine phytoplankton from ingested bacteria

Nature volume 396, pages 248–251 (1998)Cite this article

Abstract

Iron is unique among biologically essential trace metals in having a higher particulate than dissolved concentration in ocean surface waters1. Uptake of dissolved iron is generally considered to be the norm for phytoplankton, as even the smallest iron-bearing particles are unavailable for transport into cells2,3. But the oceanic dissolved fraction is so small, and the particulate fraction so inert2, that phytoplankton production is limited by a dearth of available iron in some regions4. Here we use incubation experiments to show that Ochromonas sp., a common photosynthetic flagellate from the Pacific Ocean, can obtain iron directly in particulate form, by ingesting bacteria. Iron acquisition is highly efficient; Ochromonas assimilates 30% of the ingested ration, acquiring a high intracellular iron concentration and maintaining a significantly faster growth rate than when iron is provided in the dissolved phase. Phytoplankton capable of such phagotrophy (so-called mixotrophic species) may thus be able to assimilate iron in both particulate and dissolved forms in the ocean. Moreover, when iron availability is limited, the iron ‘cost’ of growth is diminished because Ochromonas derives a greater fraction of its energy from the bacteria. Analysis of standing stocks and clearance rates of plankton in the equatorial Pacific shows that the iron flux through mixotrophic flagellates can amount to 35–58% of the total Fe uptake by the entire autotrophic community. Our results suggest that the phagotrophic ingestion of bacteria may be an effective adaptive strategy for photosynthetic organisms to obtain iron for growth in iron-limited regions of the sea.

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Figure 1: Utilization of dissolved and particulate Fe by Ochromonas.

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References

  1. Johnson, K. S., Gordon, R. M. & Coale, K. H. What controls dissolved iron concentrations in the world ocean? Mar. Chem. 57, 137–161 (1997).

    Article  CAS  Google Scholar 

  2. Rich, H. W. & Morel, F. M. M. Availability of well-defined iron colloids to the marine diatom Thalassiosira weissflogii. Limnol. Oceanogr. 35, 652–662 (1990).

    Article  ADS  CAS  Google Scholar 

  3. Price, N. M. & Morel, F. M. M. in Iron Transport and Storage in Microorganisms Plants and Animals: Metal Ions in Biological Systems (eds Sigel, A. & Sigel, H.) 1–36 (Decker, New York, 1998).

    Google Scholar 

  4. Coale, K. H. et al. Amassive phytoplankton bloom induced by an ecosystem-scale iron fertilisation experiment in the equatorial Pacific. Nature 383, 495–501 (1996).

    Article  ADS  CAS  Google Scholar 

  5. Hudson, R. J. M. & Morel, F. M. M. Iron transport in marine phytoplankton: Kinetics of cellular and medium control reactions. Limnol. Oceanogr. 35, 1002–1020 (1990).

    Article  ADS  CAS  Google Scholar 

  6. Maldonado, M. T. & Price, N. M. Utilization of iron bound to strong organic ligands by plankton communities in the subarctic Pacific Ocean. Deep-Sea Res. (in the press).

  7. Rothhaupt, K. O. Utilization of substitutable carbon and phosphorus sources by the mixotrophic chrysophyte Ochromonas sp. Ecology 77, 706–715 (1996).

    Article  Google Scholar 

  8. Caron, D. A. et al. Light-dependent phagotrophy in the freshwater mixotrophic chrysophyte Dinobyron cylindricum. Microb. Ecol. 25, 93–111 (1993).

    Article  CAS  Google Scholar 

  9. Raven, J. A. Phagotrophy in phototrophs. Limnol. Oceanogr. 42, 198–205 (1997).

    Article  ADS  CAS  Google Scholar 

  10. Tortell, P. D., Maldonado, M. T. & Price, N. M. The role of heterotrophic bacteria in iron-limited ocean ecosystems. Nature 383, 330–332 (1996).

    Article  ADS  CAS  Google Scholar 

  11. Chase, Z. & Price, N. M. Metabolic consequences of Fe deficiency in heterotrophic marine protozoa. Limnol. Oceanogr. 42, 1673–1684 (1997).

    Article  ADS  CAS  Google Scholar 

  12. Hutchins, D. A., DiTullio, G. R. & Bruland, K. W. Iron and regenerated production—evidence for biological iron recycling in two marine environments. Limnol. Oceanogr. 38, 1242–1255 (1993).

    Article  ADS  CAS  Google Scholar 

  13. Sunda, W. G. & Huntsman, S. A. Iron uptake and growth limitation in oceanic and coastal phytoplankton. Mar. Chem. 50, 189–206 (1995).

    Article  CAS  Google Scholar 

  14. Raven, J. A. The iron and molybdenum use efficiencies of plant growth with different energy, carbon and nitrogen sources. New Phytol. 116, 1–18 (1988).

    Article  Google Scholar 

  15. 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).

    Article  ADS  CAS  Google Scholar 

  16. Barbeau, K., Moffett, J. W., Caron, D. A., Croot, P. L. & Erdner, D. L. Role of protozoan grazing in relieving iron limitation of phytoplankton. Nature 380, 61–64 (1996).

    Article  ADS  CAS  Google Scholar 

  17. Twiss, M. R. & Campbell, P. G. C. Regeneration of trace metals from picoplankton by nanoflagellate grazing. Limnol. Oceanogr. 40, 1418–1429 (1995).

    Article  ADS  CAS  Google Scholar 

  18. Sanders, R. W. Mixotrophic protists in marine and freshwater ecosystems. J. Protozool. 38, 76–81 (1991).

    Article  Google Scholar 

  19. La Roche, J., Boyd, P. W., McKay, M. L. & Geider, R. J. Flavodoxin as an in situ marker for iron stress in phytoplankton. Nature 382, 802–805 (1996).

    Article  ADS  CAS  Google Scholar 

  20. Chavez, F. P., Buck, K. R., Service, S. K., Newton, J. & Barber, R. T. Phytoplankton variability in the central and eastern tropical Pacific. Deep Sea Res. II 43, 835–870 (1996).

    Article  ADS  CAS  Google Scholar 

  21. Strøm, S. & Welschmeyer, N. A. Pigment-specific rates of phytoplankton growth and microzooplankton grazing in the open subarctic Pacific Ocean. Limnol. Oceanogr. 36, 50–63 (1991).

    Article  ADS  Google Scholar 

  22. Constantinou, J. Mixotrophic Nanoflagellates in Marine Microbial Food Webs. Thesis, Univ. Hawaii (1994).

    Google Scholar 

  23. Stoecker, D. K., Gustason, D. E. & Verity, P. G. Micro- and mesoprotozooplankton at 140° W in the equatorial Pacific: heterotrophs and mixotrophs. Aquat. Microb. Ecol. 10, 273–282 (1996).

    Article  Google Scholar 

  24. Price, N. M. et al. Preparation and chemistry of the artificial algal culture media Aquil. Biol. Oceanogr. 6, 443–462 (1988/89).

    Google Scholar 

  25. Hudson, R. J. M. & Morel, F. M. M. Distinguishing between extra- and intracellular iron in marine phytoplankton. Limnol. Oceanogr. 34, 1113–1120 (1989).

    Article  ADS  CAS  Google Scholar 

  26. Børsheim, K. Y. & Bratbak, G. Cell volume to cell carbon conversion factors for a bacterivorous Monas sp. enriched from seawater. Mar. Ecol. Prog. Ser. 36, 171–175 (1987).

    Article  ADS  Google Scholar 

  27. Peters, F. The prediction of planktonic protistan grazing rates. Limnol. Oceanogr. 39, 195–205 (1994).

    Article  ADS  Google Scholar 

  28. Bjørnsen, P. K. & Kuparinen, J. Growth and herbivory by heterotrophic dinoflagellates in the Southern Ocean, studied by mesocosm experiments. Mar. Biol. 109, 397–405 (1991).

    Article  Google Scholar 

  29. Barber, R. T. et al. Primary productivity and its regulation in the equatorial Pacific during and following the 1991–1992 El Niño. Deep Sea Res. II 43, 933–969 (1996).

    Article  ADS  CAS  Google Scholar 

  30. Binder, B. J., Chisholm, S. W., Olson, R. J., Frankel, S. L. & Worden, A. Z. Dynamics of picophytoplankton, ultraphytoplankton and bacteria in the central equatorial Pacific. Deep-Sea Res. II 43, 907–931 (1996).

    Article  ADS  Google Scholar 

  31. McCarthy, J. J., Garside, C., Nevins, J. L. & Barber, R. T. New production along the 140° W in the equatorial Pacific during and following an El Niño event. Deep-Sea Res. II 43, 1065–1093 (1996).

    Article  ADS  Google Scholar 

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Acknowledgements

We thank M. T. Maldonado and J. Granger for technical advice and comments on the manuscript, and D. M. Karl for discussion. Technical assistance was provided by P. Fenwick and A.Soucisse. R.M. was supported by a FCAR (Quebec) student scholarship. This work was funded by NSERC (Canada) grants to D.F.B. and N.M.P., and by the McGill Faculty of Graduate Studies and Research. This is a contribution to the Canadian JGOFS program and to the GRIL.

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Authors and Affiliations

  1. Département des sciences biologiques, Université du Québec à Montréal, CP 8888, succ. Centre-ville, Montéral, H3C 3P8, QC, Canada

    R. Maranger & D. F. Bird

  2. Department of Biology, McGill University, 1205 Avenue Dr. Penfield, Montéral, H3A 1B1, QC, Canada

    N. M. Price

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Correspondence to N. M. Price.

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Maranger, R., Bird, D. & Price, N. Iron acquisition by photosynthetic marine phytoplankton from ingested bacteria. Nature 396, 248–251 (1998). https://doi.org/10.1038/24352

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