Adaptive strategies by Southern Ocean phytoplankton to lessen iron limitation: Uptake of organically complexed iron and reduced cellular iron requirements

Limnology and Oceanography

Volumn 56, Issue 6, 2011, Pages 1983-2002

  Strzepek, Robert F ^a   Maldonado, Maria T ^b   Hunter, Keith A ^a   Frew, Russell D ^a   Boyd, Philip W ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; ALGA; CONCENTRATION (COMPOSITION); DIATOM; GROWTH RATE; IRON; LABORATORY METHOD; LIGAND; MARINE ECOSYSTEM; NUTRIENT AVAILABILITY; NUTRIENT LIMITATION; NUTRIENT UPTAKE; NUTRITIONAL REQUIREMENT; PHYTOPLANKTON; SIDEROPHORE;

SOUTHERN OCEAN;

ALGAE; BACILLARIOPHYTA; EUCAMPIA ANTARCTICA; FRAGILARIOPSIS KERGUELENSIS; PHAEOCYSTIS; PHAEOCYSTIS ANTARCTICA; PROBOSCIA INERMIS; THALASSIOSIRA ANTARCTICA; THALASSIOSIRA PSEUDONANA; THALASSIOSIRA WEISSFLOGII;

EID: 80052865950     PISSN: 00243590     EISSN: None     Source Type: Journal    
DOI: 10.4319/lo.2011.56.6.1983     Document Type: Article

References (59)

1. AUMONT, O., E. Maier-Reimer, S. BLAIN, and P. MONFRAY. 2003. An ecosystem model of the global ocean including Fe, Si, P colimitations. Glob. Biogeochem. Cycles 17: 1060, doi:10.1029/2001GB001745
2. BARBEAU, K., E. L. RUE, K. W. BRULAND, and A. BUTLER. 2001. Photochemical cycling of iron in the surface ocean mediated by microbial iron(III)-binding ligands. Nature 413: 409-413, doi:10.1038/35096545
3. BARBEAU, K., E. L. RUE, C. G. TRICK, K. W. BRULAND, and A. BUTLER. 2003. Photochemical reactivity of siderophores produced bymarine heterotrophic bacteria and cyanobacteria based on characteristic Fe(III) binding groups. Limnol. Oceanogr. 48: 1069-1078, doi:10.4319/lo.2003.48.3.1069
4. BOYD, P. W., and M. J. ELLWOOD. 2010. The biogeochemical cycle of iron in the ocean. Nat. Geosci. 3: 675-682, doi:10.1038/ngeo964
5. BOYD, P. W., and OTHERS. 2007. Mesoscale iron enrichment experiments 1993-2005: Synthesis and future directions. Science 315: 612-617, doi:10.1126/science.1131669
6. BOYE, M., C.M.G. van den Berg, J. T.M. De Jong, H. Leach, P.L. Croot, and H. J. W. De Baar. 2001. Organic complexation of iron in the Southern Ocean. Deep-Sea Res. Part I 48: 1477-1497.
7. BUESSELER, K. O., and OTHERS. 2001. Upper ocean export of particulate organic carbon and biogenic silica in the Southern Ocean along 170uW. Deep-Sea Res. Part II 48: 4275-4297.
8. COALE, K. H., WANG, X., TANNER, S. J., and K. S. JOHNSON. 2003. Phytoplankton growth and biological response to iron and zinc addition in the Ross Sea and Antarctic Circumpolar Current along 170uW. Deep-Sea Res. Part II 50: 6335-653.
9. De Baar, H. J. W., L. J. A. GERRINGA, P. LAAN, and K. R. TIMMERMANS. 2008. Efficiency of carbon removal per added iron in ocean iron fertilization. Mar. Ecol. Prog. Ser. 364: 269-282, doi:10.3354/meps07548
10. DITULLIO, G. R., and OTHERS. 2000. Rapid and early export of Phaeocystis antarctica blooms in the Ross Sea, Antarctica. Nature 404: 595-598, doi:10.1038/35007061
11. FAN, S. M. 2008. Photochemical and biochemical controls on reactive oxygen and iron speciation in the pelagic surface ocean. Mar. Chem. 109: 152-164, doi:10.1016/j.marchem. 2008.01.005
12. FUKUDA, R., H. OGAWA, T. NAGATA, and I. KOIKE. 1998. Direct determination of carbon and nitrogen contents of natural bacterial assemblages in marine environments. Appl. Environ. Microbiol. 64: 3352-3358.
13. HARRIS, W. R., C. J. CARRANO, and K. N. RAYMOND. 1979. Coordination chemistry of microbial iron transport compounds: 16. Isolation, characterization, and formation-constants of ferric aerobactin. J. Am. Chem. Soc. 101: 2722-2727, doi:10.1021/ja00504a038
14. HASSLER, C. S., and V. SCHOEMANN. 2009. Bioavailability of organically bound Fe to model phytoplankton of the Southern Ocean. Biogeosciences 6: 2281-2296, doi:10.5194/bg-6-2281-2009
15. HUDSON, R. J. M., and F. M. M. MOREL. 1990. Iron transport in marine phytoplankton: Kinetics of cellular and medium coordination reactions. Limnol. Oceanogr. 35: 1002-1020, doi:10.4319/lo.1990.35.5.1002
16. HUTCHINS, D. A., A. E. WITTER, A. BUTLER, and G. W. LUTHER. 1999. Competition among marine phytoplankton for different chelated iron species. Nature 400: 858-861, doi:10.1038/23680
17. KÜPPER, F. C., C. J. CARRANO, J. KUHN, and A. BUTLER. 2006. Photoreactivity of iron(III)-aerobactin: Photoproduct structure and iron(III) coordination. Inorg. Chem. 45: 6028-6033, doi:10.1021/ic0604967
18. LANE, E. S., D. M. SEMENIUK, R. F. STRZEPEK, J. T. CULLEN, and M. T. MALDONADO. 2009. Effects of iron limitation on intracellular cadmium of cultured phytoplankton: Implications for surface dissolved cadmium to phosphate ratios. Mar. Chem. 115: 155-162, doi:10.1016/j.marchem.2009.07.008
19. MACRELLIS, H. M., C. G. TRICK, E. L. RUE, G. SMITH, and K. W. BRULAND. 2001. Collection and detection of natural ironbinding ligands from seawater. Mar. Chem. 76: 175-187, doi:10.1016/S0304-4203(01)00061-5
20. MALDONADO, M. T., and N. M. PRICE. 1996. Influence of N substrate on Fe requirements of marine centric diatoms. Mar. Ecol. Prog. Ser. 141: 161-172, doi:10.3354/meps141161
21. MALDONADO, M. T., and N. M. PRICE. 2000. Nitrate regulation of Fe reduction and transport by Fe-limited Thalassiosira oceanica. Limnol. Oceanogr. 45: 814-826, doi:10.4319/lo.2000.45.4.0814
22. MALDONADO, M. T., and N. M. PRICE. 2001. Reduction and transport of organically bound iron by Thalassiosira oceanica (Bacillariophyceae). J. Phycol. 37: 298-309, doi:10.1046/j.1529-8817.2001.037002298.x
23. MALDONADO, M. T., R. F. STRZEPEK, S. SANDER, and P. W. BOYD. 2005. Acquisition of iron bound to strong organic complexes, with different Fe-binding groups and photochemical reactivities, by plankton communities in Fe-limited sub-Antarctic waters. Glob. Biogeochem. Cycles 19: GB4S23, doi:10.1029/2005GB002481
24. MARTIN, J. H., S. E. FITZWATER, and R. M. GORDON. 1990. Iron deficiency limits phytoplankton growth in Antarctic waters. Glob. Biogeochem. Cycles 4: 5-12, doi:10.1029/GB004i001p00005
25. MAWJI, E., and OTHERS. 2008. Hydroxamate siderophores: Occurrence and importance in the Atlantic Ocean. Environ. Sci. Technol. 42: 8675-8680, doi:10.1021/es801884r
26. MEASURES, C. I., and S. VINK. 2001. Dissolved Fe in the upper waters of the Southern Ocean during the 1997/98 US-JGOFS cruises. Deep-Sea Res. Part II 48: 2787-2809.
27. Menden-Deuer, S., and E. J. LESSARD. 2000. Carbon to volume relationships for dinoflagellates, diatoms, and other protest plankton. Limnol. Oceanogr. 45: 569-579, doi:10.4319/lo.2000.45.3.0569
28. MONGIN, M., D. M. NELSON, P. PONDAVEN, and P. TRÉGUER. 2006. Simulation of upper-ocean biogeochemistry with a flexiblecomposition phytoplankton model: C, N and Si cycling and Fe limitation in the Southern Ocean. Deep-Sea Res. Part II 53: 601-619.
29. MOORE, J. K., and O. BRAUCHER. 2008. Sedimentary and mineral dust sources of dissolved iron to the world ocean. Biogeosciences 5: 631-656, doi:10.5194/bg-5-631-2008
30. MOORE, J. K., S. C. DONEY, J. A. KLEYPAS, D. M. GLOVER, and I. Y. FUNG. 2002. An intermediate complexity marine ecosystem model for the global domain. Deep-Sea Res. Part II 49: 403-462.
31. MOREL, F. M. M. 2008. The co-evolution of phytoplankton and trace element cycles in the oceans. Geobiol. 6: 318-324, doi:10.1111/j.1472-4669.2008.00144.x
32. PRICE, N. M., G. HARRISON, J. HERING, R. J. HUDSON, P. M. V. NIREL, B. PALENICK, and F. M. M. MOREL. 1988/1989. Preparation and chemistry of the artificial algal culture medium Aquil. Biol. Oceanogr. 6: 443-461.
33. RAVEN, J. A. 1990. 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. 116: 1-18, doi:10.1111/j.1469-8137.1990.tb00505.x
34. RAYMOND, K. N., E. A. DERTZ, and S. S. KIM. 2003. Enterobactin: An archetype for microbial iron transport. Proc. Natl. Acad. Sci. USA. 100: 3584-3588, doi:10.1073/pnas.0630018100
35. REAY, D. S., J. PRIDDLE, D. B. NEDWELL, M. J. WHITEHOUSE, J. C. Ellis-Evans, C. DEUBERT, and D. P. CONNELLY. 2001. Regulation by low temperature of phytoplankton growth and nutrient uptake in the Southern Ocean. Mar. Ecol. Prog. Ser. 219: 51-64, doi:10.3354/meps219051
36. ROSE, J. M., and OTHERS. 2009. Synergistic effects of iron and temperature on Antarctic phytoplankton and microzooplankton assemblages. Biogeosciences 6: 3131-3147, doi:10.5194/bg-6-3131-2009
37. SALMON, T. P., A. L. ROSE, B. A. NEILAN, and T. D. WAITE. 2006. The FeL model of iron acquisition: Nondissociative reduction of ferric complexes in the marine environment. Limnol. Oceanogr. 51: 1744-1754, doi:10.4319/lo.2006.51.4.1744
38. SARMIENTO, J. L., T.M.C. HUGHES, R. J. STOUFFER, and S. MANABE. 1998. Simulated response of the ocean carbon cycle to anthropogenic climate warming. Nature 393: 245-249, doi:10.1038/30455
39. SARTHOU, G., K. R. TIMMERMANS, S. BLAIN, and P. TRÉGUER. 2005. Growth physiology and fate of diatoms in the ocean: A review. J. Sea Res. 53: 25-42, doi:10.1016/j.seares.2004.01.007
40. SHAKED, Y., A. B. KUSTKA, and F. M. M. MOREL. 2005. A general kineticmodel for iron acquisition by eukaryotic phytoplankton. Limnol. Oceanogr. 50: 872-882, doi:10.4319/lo.2005.50.3.0872
41. SIGMAN, D. M., and E. A. BOYLE. 2000. Glacial/interglacial variations in atmospheric carbon dioxide. Nature 407: 859-869, doi:10.1038/35038000
42. Soria-Dengg, S., and U. HORSTMANN. 1995. Ferrioxamines B and E as iron sources for the marine diatom Phaeodactylum tricornutum. Mar. Ecol. Prog. Ser. 127: 269-277, doi:10.3354/meps127269
43. STRZEPEK, R. F., and P. J. HARRISON. 2004. Photosynthetic architecture differs in coastal and oceanic diatoms. Nature 431: 689-692, doi:10.1038/nature02954
44. STRZEPEK, R. F., M. T. MALDONADO, J. L. HIGGINS, J. HALL, K. SAFI, S. W. WILHELM, and P. W. BOYD. 2005. Spinning the ''Ferrous Wheel'': The importance of the microbial community in an iron budget during the FeCycle experiment. Glob. Biogeochem. Cycles 19: GB4S26, doi:10.1029/2005GB002490
45. STRZEPEK, R. F., and N. M. PRICE. 2000. Influence of irradiance and temperature on the iron content of the marine diatom Thalassiosira weissflogii (Bacillariophyceae). Mar. Ecol. Prog. Ser. 206: 107-117, doi:10.3354/meps206107
46. SUNDA, W. G. 1997. Control of dissolved iron concentrations in the world ocean: A comment. Mar. Chem. 57: 169-172, doi:10.1016/S0304-4203(97)00045-5
47. SUNDA, W. G., and S. A. HUNTSMAN. 1995. Iron uptake and growth limitation in oceanic and coastal phytoplankton. Mar. Chem. 50: 189-206, doi:10.1016/0304-4203(95)00035-P
48. SUNDA, W. G., and S. A. HUNTSMAN. 1997. Interrelated influence of iron, light and cell size on marine phytoplankton growth. Nature 390: 389-392, doi:10.1038/37093
49. SUNDA, W. G., and S. A. HUNTSMAN. 2003. Effect of pH, light, and temperature on Fe-EDTA chelation and Fe hydrolysis in seawater. Mar. Chem. 84: 35-47, doi:10.1016/S0304-4203(03)00101-4
50. TAGLIABUE, A., and K. R. ARRIGO. 2005. Iron in the Ross Sea: 1. Impact of CO2 fluxes via variation in phytoplankton functional group and non-Redfield stoichiometry. J. Geophys. Res. 110: C03009, doi:10.1029/2004JC002531
51. TAGLIABUE, A., L. BOPP, O. AUMONT, and K. R. ARRIGO. 2008. Influence of light and temperature on the marine iron cycle: From theoretical to global modeling. Glob. Biogeochem. Cycles 23: GB2017, doi:10.1029/2008GB003214
52. TIAN, F., R. D. FREW, S. SANDER, K. A. HUNTER, and M. J. ELLWOOD. 2006. Organic iron(III) speciation in surface transects across a frontal zone: The Chatham Rise, New Zealand. Mar. Freshw. Res. 57: 533-544, doi:10.1071/MF05209
53. Timmermans, K. R., L. J. A. Gerringa, H. J. W. de Baar, B. van der Wagt, M. J. W. Veldhuis, J. T. M. De Jong, and P. L. Croot. 2001. Growth rates of large and small Southern Ocean diatoms in relation to availability of iron in natural seawater. Limnol. Oceanogr. 46: 260-266, doi:10.4319/lo.2001.46.2.0260
54. Timmermans, K. R., B. Van Der Wagt, and H. J. W. de Baar. 2004. Growth rates, half-saturation constants, and silicate, nitrate, and phosphate depletion in relation to iron availability of four large, open-ocean diatoms from the Southern Ocean. Limnol. Oceanogr. 49: 2141-2151, doi:10.4319/lo.2004.49.6.2141
55. Timmermans, K. R., M. J. W. VELDHUIS, P. LANN, and C. P. D. BRUSSAARD. 2008. Probing natural iron fertilization near the Kerguelen (Southern Ocean) using natural phytoplankton assemblages and diatom cultures. Deep-Sea Res. Part II 55: 693-705.
56. TWINING, B. S., S. B. BAINES, N. S. FISHER, and M. R. LANDRY. 2004. Cellular iron contents of plankton during the Southern Ocean Iron Experiment (SOFeX). Deep-Sea Res. Part I 51: 1827-1850.
57. WAGENER, T., C. GUIEU, R. LOSNO, S. BONNET, and N. MAHOWALD. 2008. Revisiting atmospheric dust export to the Southern Hemisphere ocean: Biogeochemical implications. Glob. Biogeochem. Cycles 22: GB2006, doi:10.1029/2007GB002984
58. WELLS, M. L. 1999. Manipulating iron availability in nearshore waters. Limnol. Oceanogr. 44: 1002-1008, doi:10.4319/lo.1999.44.4.1002
59. WITTER, A. E., D. A. HUTCHINS, A. BUTLER, and G. W. LUTHER, III. 2000. Determination of conditional stability constants and kinetic constants for strong model Fe-binding ligands in seawater. Mar. Chem. 69: 1-17, doi:10.1016/S0304-4203(99)00087-0