The integral role of iron in ocean biogeochemistry

Abstract

The micronutrient iron is now recognized to be important in regulating the magnitude and dynamics of ocean primary productivity, making it an integral component of the ocean’s biogeochemical cycles. In this Review, we discuss how a recent increase in observational data for this trace metal has challenged the prevailing view of the ocean iron cycle. Instead of focusing on dust as the major iron source and emphasizing iron’s tight biogeochemical coupling to major nutrients, a more complex and diverse picture of the sources of iron, its cycling processes and intricate linkages with the ocean carbon and nitrogen cycles has emerged.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: A schematic representation of the first view of the processes governing the ocean iron cycle.
Figure 2: A revised representation of the major processes in the ocean iron cycle, with emphasis on the Atlantic Ocean.
Figure 3: Observations from a meridional section in the west Atlantic Ocean as a function of latitude and depth.
Figure 4: Processes controlling the oceanic distribution of iron.

References

  1. 1

    Falkowski, P. & Raven, J. A. Aquatic Photosynthesis 488 (Princeton Univ. Press, 2007)

  2. 2

    Ruud, J. T. Nitrates and phosphates in the Southern Seas. J. Conseil 5, 347–360 (1930)

    Google Scholar 

  3. 3

    Gran, H. H. On the conditions for the production of plankton in the sea. Conseil Permanent International pour l’Exploration de la Mer. Rapports et Procès-Verbaux des réunions 75, 37–46 (1931)

    Google Scholar 

  4. 4

    Hart, T. On the phytoplankton of the south-west Atlantic and the Bellingshausen Sea, 1929–31. Discov. Rep. VIII, 1–268 (1934)

    Google Scholar 

  5. 5

    Harvey, H. On the rate of diatom growth. J. Mar. Biol. Assoc. 19, 253–276 (1933)

    CAS  Google Scholar 

  6. 6

    Anderson, M. A. & Morel, F. M. M. The influence of aqueous iron chemistry on the uptake of iron by the coastal diatom Thalassiosira weissflogii. Limnol. Oceanogr. 27, 789–813 (1982)

    ADS  CAS  Google Scholar 

  7. 7

    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)

    ADS  CAS  Google Scholar 

  8. 8

    Cooper, L. H. N. Iron in the sea and in marine plankton. Proc. R. Soc. Lond. B 118, 419–438 (1935)

    ADS  CAS  Google Scholar 

  9. 9

    Goldberg, E. D. Marine geochemistry. 1. Chemical scavengers of the sea. J. Geol. 62, 249–265 (1954)

    ADS  CAS  Google Scholar 

  10. 10

    Williams, R. J. P. The Bakerian Lecture, 1981—Natural selection of the chemical elements. Proc. R. Soc. B 213, 361–397 (1981)

    ADS  CAS  Google Scholar 

  11. 11

    Raven, J. A. The iron and molybdenum use efficiencies of plant growth with different energy, carbon and nitrogen sources. New Phytol. 109, 279–287 (1988)

    CAS  Google Scholar 

  12. 12

    Moore, J. K., Doney, S. C., Glover, D. M. & Fung, I. Y. Iron cycling and nutrient-limitation patterns in surface waters of the World Ocean. Deep Sea Res. Part II 49, 463–507 (2002)

    ADS  CAS  Google Scholar 

  13. 13

    Bruland, K. W., Franks, R. P., Knauer, G. A. & Martin, J. H. Sampling and analytical methods for the determination of copper, cadmium, zinc, and nickel at the nanogram per liter level in sea water. Anal. Chim. Acta 105, 233–245 (1979)

    CAS  Google Scholar 

  14. 14

    Settle, D. & Patterson, C. Lead in albacore: guide to lead pollution in Americans. Science 207, 1167–1176 (1980)

    ADS  CAS  PubMed  Google Scholar 

  15. 15

    Gordon, R. M., Martin, J. H. & Knauer, G. A. Iron in Northeast Pacific waters. Nature 299, 611–612 (1982)

    ADS  CAS  Google Scholar 

  16. 16

    Landing, W. M. & Bruland, K. W. The contrasting biogeochemistry of iron and manganese in the Pacific Ocean. Geochim. Cosmochim. Acta 51, 29–43 (1987)

    ADS  CAS  Google Scholar 

  17. 17

    Martin, J. H., Gordon, R. M. & Fitzwater, S. E. Iron in Antarctic waters. Nature 345, 156–158 (1990)

    ADS  CAS  Google Scholar 

  18. 18

    Martin, J. H., Fitzwater, S. E. & Gordon, R. M. Iron deficiency limits phytoplankton growth in Antarctic waters. Glob. Biogeochem. Cycles 4, 5–12 (1990)

    ADS  CAS  Google Scholar 

  19. 19

    Martin, J. H. Glacial-interglacial CO2 change: the iron hypothesis. Paleoceanography 5, 1–13 (1990). This paper presented the iron hypothesis—that past variations in atmospheric carbon dioxide were driven by greater iron supply to the Southern Ocean.

    ADS  Google Scholar 

  20. 20

    Joos, F., Sarmiento, J. L. & Siegenthaler, U. Estimates of the effect of Southern Ocean iron fertilization on atmospheric CO2 concentrations. Nature 349, 772–775 (1991)

    ADS  CAS  Google Scholar 

  21. 21

    Cullen, J. J. Hypotheses to explain high-nutrient conditions in the open sea. Limnol. Oceanogr. 36, 1578–1599 (1991)

    ADS  CAS  Google Scholar 

  22. 22

    Martin, J. H. et al. Testing the iron hypothesis in ecosystems of the equatorial Pacific Ocean. Nature 371, 123–129 (1994)

    ADS  CAS  Google Scholar 

  23. 23

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

    ADS  CAS  PubMed  Google Scholar 

  24. 24

    Boyd, P. W. et al. A mesoscale phytoplankton bloom in the polar Southern Ocean stimulated by iron fertilization. Nature 407, 695–702 (2000). This paper reported results from the first in situ iron fertilization experiment from the Southern Ocean.

    ADS  CAS  PubMed  Google Scholar 

  25. 25

    Boyd, P. W. et al. Mesoscale iron enrichment experiments 1993–2005: synthesis and future directions. Science 315, 612–617 (2007)

    ADS  CAS  PubMed  Google Scholar 

  26. 26

    de Baar, H. J. W. et al. Synthesis of iron fertilization experiments: from the Iron Age in the Age of Enlightenment. J. Geophys. Res. 110, C09S16 (2005)

    Google Scholar 

  27. 27

    Moore, C. M. et al. Iron limits primary productivity during spring bloom development in the central North Atlantic. Glob. Change Biol. 12, 626–634 (2006)

    ADS  Google Scholar 

  28. 28

    Hutchins, D. A., DiTullio, G. R., Zhang, Y. & Bruland, K. W. An iron limitation mosaic in the California upwelling regime. Limnol. Oceanogr. 43, 1037–1054 (1998)

    ADS  CAS  Google Scholar 

  29. 29

    Hutchins, D. A. et al. Phytoplankton iron limitation in the Humboldt Current and Peru Upwelling. Limnol. Oceanogr. 47, 997–1011 (2002)

    ADS  Google Scholar 

  30. 30

    Johnson, K. S., Gordon, R. M. & Coale, K. H. What controls dissolved iron concentrations in the world ocean? Mar. Chem. 57, 137–161 (1997). This paper put forward the first conceptual and numerical model of the main processes driving the ocean iron cycle.

    CAS  Google Scholar 

  31. 31

    Gledhill, M. & van den Berg, C. M. G. Determination of complexation of iron(III) with natural organic complexing ligands in seawater using cathodic stripping voltammetry. Mar. Chem. 47, 41–54 (1994)

    CAS  Google Scholar 

  32. 32

    Rue, E. L. & Bruland, K. W. Complexation of iron(III) by natural organic ligands in the Central North Pacific as determined by a new competitive ligand equilibration/adsorptive cathodic stripping voltammetric method. Mar. Chem. 50, 117–138 (1995)

    CAS  Google Scholar 

  33. 33

    Sunda, W. G. & Huntsman, S. A. Interrelated influence of iron, light and cell size on marine phytoplankton growth. Nature 390, 389–392 (1997). This paper demonstrated how different environmental factors led to large variations in the phytoplankton iron uptake.

    ADS  CAS  Google Scholar 

  34. 34

    Archer, D. E. & Johnson, K. A model of the iron cycle in the ocean. Glob. Biogeochem. Cycles 14, 269–279 (2000)

    ADS  CAS  Google Scholar 

  35. 35

    Parekh, P., Follows, M. J. & Boyle, E. A. Decoupling of iron and phosphate in the global ocean. Glob. Biogeochem. Cycles 19, GB2020 (2005)

    ADS  Google Scholar 

  36. 36

    Jickells, T. D. et al. Global iron connections between desert dust, ocean biogeochemistry, and climate. Science 308, 67–71 (2005)

    ADS  CAS  PubMed  Google Scholar 

  37. 37

    de Baar, H. J. & de Jong, J. T. in The Biogeochemistry of Iron in Seawater Vol. 7 (eds Turner, D. R. & Hunter, K. A. ) 123–254 (2001)

    CAS  Google Scholar 

  38. 38

    Tagliabue, A. et al. How well do global ocean biogeochemistry models simulate dissolved iron distributions? Glob. Biogeochem. Cycles 30, 149–174 (2016). This paper was the first to critically appraise how well a range of state-of-the-art ocean models represented the ocean iron cycle.

    ADS  CAS  Google Scholar 

  39. 39

    Hain, M. P., Sigman, D. M. & Haug, G. H. Carbon dioxide effects of Antarctic stratification, North Atlantic Intermediate Water formation, and subantarctic nutrient drawdown during the last ice age: Diagnosis and synthesis in a geochemical box model. Glob. Biogeochem. Cycles 24, GB4023 (2010)

    ADS  Google Scholar 

  40. 40

    Watson, A. J., Bakker, D. C. E., Ridgwell, A. J., Boyd, P. W. & Law, C. S. Effect of iron supply on Southern Ocean CO2 uptake and implications for glacial atmospheric CO2 . Nature 407, 730–733 (2000)

    ADS  CAS  PubMed  Google Scholar 

  41. 41

    The GEOTRACES Group. The GEOTRACES Intermediate Data Product 2014. Mar. Chem. 177, 1–8 (2015). This paper reported the first release of high-quality iron data, alongside a range of other important datasets, from the GEOTRACES programme.

  42. 42

    Anderson, R. & Henderson, G. GEOTRACES—A global study of the marine biogeochemical cycles of trace elements and their isotopes. Oceanography 18, 76–79 (2005)

    Google Scholar 

  43. 43

    Johnson, K. S. et al. Developing standards for dissolved iron in seawater. Eos 88, 131–132 (2007)

    ADS  Google Scholar 

  44. 44

    Boyd, P. W. et al. FeCycle: attempting an iron biogeochemical budget from a mesoscale SF6 tracer experiment in unperturbed low iron waters. Glob. Biogeochem. Cycles 19, GB4S20 (2005)

    Google Scholar 

  45. 45

    Blain, S. et al. Effect of natural iron fertilization on carbon sequestration in the Southern Ocean. Nature 446, 1070–1074 (2007)

    ADS  CAS  PubMed  Google Scholar 

  46. 46

    Pollard, R. T. et al. Southern Ocean deep-water carbon export enhanced by natural iron fertilization. Nature 457, 577–580 (2009)

    ADS  CAS  PubMed  Google Scholar 

  47. 47

    Elrod, V. A., Berelson, W. M., Coale, K. H. & Johnson, K. S. The flux of iron from continental shelf sediments: a missing source for global budgets. Geophys. Res. Lett. 31, L12307 (2004)

    ADS  Google Scholar 

  48. 48

    Lam, P. J. & Bishop, J. K. B. The continental margin is a key source of iron to the HNLC North Pacific Ocean. Geophys. Res. Lett. 35, L07608 (2008)

    ADS  Google Scholar 

  49. 49

    Tagliabue, A., Aumont, O. & Bopp, L. The impact of different external sources of iron on the global carbon cycle. Geophys. Res. Lett. 41, 920–926 (2014)

    ADS  CAS  Google Scholar 

  50. 50

    Saito, M. A. et al. Slow-spreading submarine ridges in the South Atlantic as a significant oceanic iron source. Nat. Geosci. 6, 775–779 (2013)

    ADS  CAS  Google Scholar 

  51. 51

    Resing, J. A. et al. Basin-scale transport of hydrothermal dissolved metals across the South Pacific Ocean. Nature 523, 200–203 (2015). This paper was the first to demonstrate that the longevity of iron from hydrothermal vents was much longer than previously estimated.

    ADS  CAS  PubMed  Google Scholar 

  52. 52

    Klunder, M. B., Laan, P., Middag, R., De Baar, H. J. W. & van Ooijen, J. C. Dissolved iron in the Southern Ocean (Atlantic sector). Deep Sea Res. Part II 58, 2678–2694 (2011)

    ADS  CAS  Google Scholar 

  53. 53

    Klunder, M. B. et al. Dissolved iron in the Arctic shelf seas and surface waters of the central Arctic Ocean: impact of Arctic river water and ice-melt. J. Geophys. Res. Oceans 117, C01027 (2012)

    ADS  Google Scholar 

  54. 54

    Tagliabue, A. et al. Hydrothermal contribution to the oceanic dissolved iron inventory. Nat. Geosci. 3, 252–256 (2010)

    ADS  CAS  Google Scholar 

  55. 55

    Martinez-Garcia, A. et al. Iron fertilization of the Subantarctic ocean during the last ice age. Science 343, 1347–1350 (2014)

    ADS  CAS  PubMed  Google Scholar 

  56. 56

    Jaccard, S. L., Galbraith, E. D., Martinez-Garcia, A. & Anderson, R. F. Covariation of deep Southern Ocean oxygenation and atmospheric CO2 through the last ice age. Nature 530, 207–210 (2016)

    ADS  CAS  PubMed  Google Scholar 

  57. 57

    Sigman, D. M., Hain, M. P. & Haug, G. H. The polar ocean and glacial cycles in atmospheric CO2 concentration. Nature 466, 47–55 (2010)

    ADS  CAS  PubMed  Google Scholar 

  58. 58

    Lambert, F. et al. Dust fluxes and iron fertilization in Holocene and Last Glacial Maximum climates. Geophys. Res. Lett. 42, 6014–6023 (2015)

    ADS  CAS  Google Scholar 

  59. 59

    Conway, T. M. & John, S. G. Quantification of dissolved iron sources to the North Atlantic Ocean. Nature 511, 212–215 (2014). This paper was the first to use iron isotopes to fingerprint the importance of different iron sources in the North Atlantic Ocean.

    ADS  CAS  PubMed  Google Scholar 

  60. 60

    Moore, C. M. et al. Processes and patterns of oceanic nutrient limitation. Nat. Geosci. 6, 701–710 (2013)

    ADS  CAS  Google Scholar 

  61. 61

    Falkowski, P. G. Evolution of the nitrogen cycle and its influence on the biological sequestration of CO2 in the ocean. Nature 387, 272–275 (1997)

    ADS  CAS  Google Scholar 

  62. 62

    Moore, C. M. et al. Large-scale distribution of Atlantic nitrogen fixation controlled by iron availability. Nat. Geosci. 2, 867–871 (2009)

    ADS  CAS  Google Scholar 

  63. 63

    Schlosser, C. et al. Seasonal ITCZ migration dynamically controls the location of the (sub)tropical Atlantic biogeochemical divide. Proc. Natl Acad. Sci. USA 111, 1438–1442 (2014)

    ADS  CAS  PubMed  Google Scholar 

  64. 64

    Dutkiewicz, S., Ward, B. A., Monteiro, F. & Follows, M. J. Interconnection of nitrogen fixers and iron in the Pacific Ocean: theory and numerical simulations. Glob. Biogeochem. Cycles 26, GB1012 (2012)

    ADS  Google Scholar 

  65. 65

    Weber, T. & Deutsch, C. Local versus basin-scale limitation of marine nitrogen fixation. Proc. Natl Acad. Sci. USA 111, 8741–8746 (2014)

    ADS  CAS  PubMed  Google Scholar 

  66. 66

    Gledhill, M. & Buck, K. N. The organic complexation of iron in the marine environment: a review. Front. Microbiol. 3, 69 (2012)

    PubMed  PubMed Central  Google Scholar 

  67. 67

    Boyd, P. W. & Tagliabue, A. Using the L* concept to explore controls on the relationship between paired ligand and dissolved iron concentrations in the ocean. Mar. Chem. 173, 52–66 (2015)

    CAS  Google Scholar 

  68. 68

    Buck, K. N., Sohst, B. & Sedwick, P. N. The organic complexation of dissolved iron along the U.S. GEOTRACES (GA03) North Atlantic Section. Deep Sea Res. Part II 116, 152–165 (2015)

    CAS  Google Scholar 

  69. 69

    Gerringa, L. J. A., Rijkenberg, M. J. A., Schoemann, V., Laan, P. & de Baar, H. J. W. Organic complexation of iron in the West Atlantic Ocean. Mar. Chem. 177, 434–446 (2015)

    CAS  Google Scholar 

  70. 70

    Wozniak, A. S., Shelley, R. U., McElhenie, S. D., Landing, W. M. & Hatcher, P. G. Aerosol water soluble organic matter characteristics over the North Atlantic Ocean: implications for iron-binding ligands and iron solubility. Mar. Chem. 173, 162–172 (2015)

    CAS  Google Scholar 

  71. 71

    Cheize, M. et al. Iron organic speciation determination in rainwater using cathodic stripping voltammetry. Anal. Chim. Acta 736, 45–54 (2012)

    CAS  PubMed  Google Scholar 

  72. 72

    Mawji, E. et al. Production of siderophore type chelates in Atlantic Ocean waters enriched with different carbon and nitrogen sources. Mar. Chem. 124, 90–99 (2011)

    CAS  Google Scholar 

  73. 73

    Tagliabue, A., Williams, R. G., Rogan, N., Achterberg, E. P. & Boyd, P. W. A ventilation-based framework to explain the regeneration-scavenging balance of iron in the ocean. Geophys. Res. Lett. 41, 7227–7236 (2014)

    ADS  CAS  Google Scholar 

  74. 74

    Völker, C. & Tagliabue, A. Modeling organic iron-binding ligands in a three-dimensional biogeochemical ocean model. Mar. Chem. 173, 67–77 (2015)

    Google Scholar 

  75. 75

    Twining, B. S. & Baines, S. B. The trace metal composition of marine phytoplankton. Annu. Rev. Mar. Sci. 5, 191–215 (2013). This paper provides a state-of-the-art summary of the iron content of marine phytoplankton determined using a variety of different techniques.

    Google Scholar 

  76. 76

    Twining, B. S., Rauschenberg, S., Morton, P. L. & Vogt, S. Metal contents of phytoplankton and labile particulate material in the North Atlantic Ocean. Prog. Oceanogr. 137, 261–283 (2015)

    ADS  Google Scholar 

  77. 77

    Martiny, A. C. et al. Strong latitudinal patterns in the elemental ratios of marine plankton and organic matter. Nat. Geosci. 6, 279–283 (2013)

    ADS  CAS  Google Scholar 

  78. 78

    Boyd, P. W. et al. Why are biotic iron pools uniform across high- and low-iron pelagic ecosystems? Glob. Biogeochem. Cycles 29, 1028–1043 (2015)

    ADS  CAS  Google Scholar 

  79. 79

    Bowie, A. R. et al. Iron budgets for three distinct biogeochemical sites around the Kerguelen Archipelago (Southern Ocean) during the natural fertilisation study, KEOPS-2. Biogeosciences 12, 4421–4445 (2015)

    ADS  Google Scholar 

  80. 80

    Ratnarajah, L., Bowie, A. R., Lannuzel, D., Meiners, K. M. & Nicol, S. The biogeochemical role of baleen whales and krill in Southern Ocean nutrient cycling. PLoS One 9, e114067 (2014); correction 10(4), e0125134 (2015)

    ADS  PubMed  PubMed Central  Google Scholar 

  81. 81

    Twining, B. S. et al. Differential remineralization of major and trace elements in sinking diatoms. Limnol. Oceanogr. 59, 689–704 (2014)

    ADS  CAS  Google Scholar 

  82. 82

    Tagliabue, A. et al. Surface-water iron supplies in the Southern Ocean sustained by deep winter mixing. Nat. Geosci. 7, 314–320 (2014)

    ADS  CAS  Google Scholar 

  83. 83

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

    ADS  CAS  Google Scholar 

  84. 84

    Morel, F. M. M., Kustka, A. B. & Shaked, Y. The role of unchelated Fe in the iron nutrition of phytoplankton. Limnol. Oceanogr. 53, 400–404 (2008)

    ADS  CAS  Google Scholar 

  85. 85

    Schlosser, C., De La Rocha, C. L., Streu, P. & Croot, P. L. Solubility of iron in the Southern Ocean. Limnol. Oceanogr. 57, 684–697 (2012)

    ADS  CAS  Google Scholar 

  86. 86

    Liu, X. & Millero, F. J. The solubility of iron in seawater. Mar. Chem. 77, 43–54 (2002)

    CAS  Google Scholar 

  87. 87

    Tagliabue, A. & Arrigo, K. R. Processes governing the supply of iron to phytoplankton in stratified seas. J. Geophys. Res. 111, C06019 (2006)

    ADS  Google Scholar 

  88. 88

    Weber, L., Völker, C., Schartau, M. & Wolf-Gladrow, D. A. Modeling the speciation and biogeochemistry of iron at the Bermuda Atlantic Time-series Study site. Glob. Biogeochem. Cycles 19, GB1019 (2005)

    ADS  Google Scholar 

  89. 89

    Croot, P. L. et al. Retention of dissolved iron and Fe-II in an iron induced Southern Ocean phytoplankton bloom. Geophys. Res. Lett. 28, 3425–3428 (2001)

    ADS  CAS  Google Scholar 

  90. 90

    Moffett, J. W., Goepfert, T. J. & Naqvi, S. W. A. Reduced iron associated with secondary nitrite maxima in the Arabian Sea. Deep Sea Res. Part I 54, 1341–1349 (2007)

    Google Scholar 

  91. 91

    Sedwick, P. N., Sohst, B. M., Ussher, S. J. & Bowie, A. R. A zonal picture of the water column distribution of dissolved iron(II) during the U.S. GEOTRACES North Atlantic transect cruise (GEOTRACES GA03). Deep Sea Res. Part II 116, 166–175 (2015)

    CAS  Google Scholar 

  92. 92

    Strzepek, R. F., Maldonado, M. T., Hunter, K. A., Frew, R. D. & Boyd, P. W. Adaptive strategies by Southern Ocean phytoplankton to lessen iron limitation: uptake of organically complexed iron and reduced cellular iron requirements. Limnol. Oceanogr. 56, 1983–2002 (2011)

    ADS  CAS  Google Scholar 

  93. 93

    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. Part II 46, 2447–2473 (1999)

    ADS  CAS  Google Scholar 

  94. 94

    Rubin, M., Berman-Frank, I. & Shaked, Y. Dust- and mineral-iron utilization by the marine dinitrogen-fixer Trichodesmium. Nat. Geosci. 4, 529–534 (2011)

    ADS  CAS  Google Scholar 

  95. 95

    Shaked, Y., Kustka, A. B. & Morel, F. M. M. A general kinetic model for iron acquisition by eukaryotic phytoplankton. Limnol. Oceanogr. 50, 872–882 (2005)

    ADS  CAS  Google Scholar 

  96. 96

    Lis, H., Shaked, Y., Kranzler, C., Keren, N. & Morel, F. M. Iron bioavailability to phytoplankton: an empirical approach. ISME J. 9, 1003–1013 (2014)

    PubMed Central  Google Scholar 

  97. 97

    Saito, M. A. et al. Multiple nutrient stresses at intersecting Pacific Ocean biomes detected by protein biomarkers. Science 345, 1173–1177 (2014). This paper was the first to link data on resource stress from proteomic to field measurements of resource concentrations to demonstrate the transitions between iron and nitrogen limitation in the Pacific Ocean

    ADS  CAS  PubMed  Google Scholar 

  98. 98

    Rijkenberg, M. J. et al. The distribution of dissolved iron in the West Atlantic Ocean. PLoS One 9, e101323 (2014)

    ADS  PubMed  PubMed Central  Google Scholar 

  99. 99

    Dutkiewicz, S., Follows, M. J. & Parekh, P. Interactions of the iron and phosphorus cycles: a three-dimensional model study. Global Biogeochem. Cycles 19, GB1021 (2005)

    ADS  Google Scholar 

  100. 100

    Wagener, T., Guieu, C. & Leblond, N. Effects of dust deposition on iron cycle in the surface Mediterranean Sea: results from a mesocosm seeding experiment. Biogeosciences 7, 3769–3781 (2010)

    ADS  CAS  Google Scholar 

  101. 101

    Sohm, J. A. et al. Nitrogen fixation in the South Atlantic Gyre and the Benguela Upwelling System. Geophys. Res. Lett. 38, L16608 (2011)

    ADS  Google Scholar 

  102. 102

    Boyd, P. W. & Ellwood, M. J. The biogeochemical cycle of iron in the ocean. Nat. Geosci. 3, 675–682 (2010)

    ADS  CAS  Google Scholar 

  103. 103

    Slemons, L. O., Murray, J. W., Resing, J., Paul, B. & Dutrieux, P. Western Pacific coastal sources of iron, manganese, and aluminum to the Equatorial Undercurrent. Glob. Biogeochem. Cycles 24, GB3024 (2010)

    ADS  Google Scholar 

  104. 104

    Nishioka, J. et al. Iron supply to the western subarctic Pacific: importance of iron export from the Sea of Okhotsk. J. Geophys. Res. 112, C10012 (2007)

    ADS  Google Scholar 

  105. 105

    Tagliabue, A. et al. Quantifying the roles of ocean circulation and biogeochemistry in governing ocean carbon-13 and atmospheric carbon dioxide at the last glacial maximum. Clim. Past 5, 695–706 (2009)

    Google Scholar 

  106. 106

    Middleton, J. L., Langmuir, C. H., Mukhopadhyay, S., McManus, J. F. & Mitrovica, J. X. Hydrothermal iron flux variability following rapid sea level changes. Geophys. Res. Lett. 43, 3848–3856 (2016)

    ADS  CAS  Google Scholar 

  107. 107

    Lund, D. C. et al. Enhanced East Pacific Rise hydrothermal activity during the last two glacial terminations. Science 351, 478–482 (2016)

    ADS  CAS  PubMed  Google Scholar 

  108. 108

    Bopp, L. et al. Multiple stressors of ocean ecosystems in the 21st century: projections with CMIP5 models. Biogeosciences 10, 6225–6245 (2013)

    ADS  Google Scholar 

  109. 109

    Charette, M. A., Morris, P. J., Henderson, P. B. & Moore, W. S. Radium isotope distributions during the US GEOTRACES North Atlantic cruises. Mar. Chem. 177, 184–195 (2015)

    CAS  Google Scholar 

  110. 110

    Wu, J., Boyle, E., Sunda, W. & Wen, L. S. Soluble and colloidal iron in the oligotrophic North Atlantic and North Pacific. Science 293, 847–849 (2001)

    ADS  CAS  PubMed  Google Scholar 

  111. 111

    von der Heyden, B. P., Roychoudhury, A. N., Mtshali, T. N., Tyliszczak, T. & Myneni, S. C. Chemically and geographically distinct solid-phase iron pools in the Southern Ocean. Science 338, 1199–1201 (2012)

    ADS  CAS  PubMed  Google Scholar 

  112. 112

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

    ADS  CAS  Google Scholar 

  113. 113

    Bonnain, C., Breitbart, M. & Buck, K. N. The Ferrojan horse hypothesis: iron-virus interactions in the ocean. Front. Mar. Sci. 3, https://doi.org/10.3389/fmars.2016.00082 (2016)

  114. 114

    Mackey, K. R. et al. Divergent responses of Atlantic coastal and oceanic Synechococcus to iron limitation. Proc. Natl Acad. Sci. USA 112, 9944–9949 (2015)

    ADS  CAS  PubMed  Google Scholar 

  115. 115

    Hogle, S. L., Barbeau, K. A. & Gledhill, M. Heme in the marine environment: from cells to the iron cycle. Metallomics 6, 1107–1120 (2014)

    CAS  PubMed  Google Scholar 

  116. 116

    Jenkins, W. J., Smethie, W. M., Boyle, E. A. & Cutter, G. A. Water mass analysis for the U.S. GEOTRACES (GA03) North Atlantic sections. Deep Sea Res. Part II 116, 6–20 (2015)

    CAS  Google Scholar 

  117. 117

    Ito, T. & Follows, M. J. Preformed phosphate, soft tissue pump and atmospheric CO2 . J. Mar. Res. 63, 813–839 (2005)

    CAS  Google Scholar 

  118. 118

    Broecker, W. S., Takahashi, T. & Takahashi, T. Sources and flow patterns of deep-ocean waters as deduced from potential temperature, salinity, and initial phosphate concentration. J. Geophys. Res. 90, 6925–6939 (1985)

    ADS  CAS  Google Scholar 

  119. 119

    Duteil, O. et al. A novel estimate of ocean oxygen utilisation points to a reduced rate of respiration in the ocean interior. Biogeosciences 10, 7723–7738 (2013)

    ADS  Google Scholar 

  120. 120

    Waugh, D. W., Primeau, F., Devries, T. & Holzer, M. Recent changes in the ventilation of the southern oceans. Science 339, 568–570 (2013)

    ADS  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

A.T. acknowledges support from Natural Environment Research Council (NE/N0010791 and NE/N009525/1) and the Royal Society. A.R.B. acknowledges support from the Australian Research Council (FT130100037 and DP150100345) and the Antarctic Climate and Ecosystems Cooperative Research Centre. P.W.B. acknowledges support from the Australian Research Council (Laureate Fellowship FL160100131). K.N.B. acknowledges support from the National Science Foundation (OCE-1446327 and PLR-1443483). K.S.J. acknowledges support by the David and Lucile Packard Foundation. M.A.S. acknowledges support from National Science Foundation (NSF-1435-556) and the Gordon Betty Moore Foundation (3782).

Author information

Affiliations

Authors

Contributions

This review article was originated by A.T., who led the writing of the manuscript. All co-authors contributed to the ideas and the writing of the review.

Corresponding author

Correspondence to Alessandro Tagliabue.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

Reviewer Information Nature thanks K. Misumi, M. Moore and the other anonymous reviewer(s) for their contribution to the peer review of this work.

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Tagliabue, A., Bowie, A., Boyd, P. et al. The integral role of iron in ocean biogeochemistry. Nature 543, 51–59 (2017). https://doi.org/10.1038/nature21058

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing