in

Iron and manganese co-limit the growth of two phytoplankton groups dominant at two locations of the Drake Passage

  • Sabine, C. L. et al. The oceanic sink for anthropogenic CO2. Science 305, 367–371 (2004).

    CAS 
    PubMed 

    Google Scholar 

  • Landschützer, P. et al. The reinvigoration of the Southern Ocean carbon sink. Science 349, 1221–1224 (2015).

    PubMed 

    Google Scholar 

  • Dunne, J. P., Sarmiento, J. L. & Gnanadesikan, A. A synthesis of global particle export from the surface ocean and cycling through the ocean interior and on the seafloor. Global Biogeochem. Cycles 21, https://doi.org/10.1029/2006GB002907 (2007).

  • Buesseler, K. O., Boyd, P. W., Black, E. E. & Siegel, D. A. Metrics that matter for assessing the ocean biological carbon pump. Proc. Natl Acad. Sci. USA 117, 9679–9687 (2020).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • de Baar, H. J. On iron limitation of the Southern Ocean: experimental observations in the Weddell and Scotia Seas. Mar. Ecol. Prog. Ser. 65, 105–122 (1990).

    Google Scholar 

  • Twining, B. S. & Baines, S. B. The trace metal composition of marine phytoplankton. Annu. Rev. Mar. Sci. 5, 191–215 (2013).

    Google Scholar 

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

    CAS 

    Google Scholar 

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

    CAS 
    PubMed 

    Google Scholar 

  • Sunda, W. Feedback interactions between trace metal nutrients and phytoplankton in the ocean. Front. Microbiol. 3, 204 (2012).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Martin, J. H. Glacial‐interglacial CO2 change: the iron hypothesis. Paleoceanography 5, 1–13 (1990).

    Google Scholar 

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

    CAS 

    Google Scholar 

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

    CAS 

    Google Scholar 

  • Behrenfeld, M. J. & Milligan, A. J. Photophysiological expressions of iron stress in phytoplankton. Annu. Rev. Mar. Sci. 5, 217–246 (2013).

    Google Scholar 

  • 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. 100, 565–575 (1992).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Raven, J. A., Evans, M. C. & Korb, R. E. The role of trace metals in photosynthetic electron transport in O2-evolving organisms. Photosynthesis Res. 60, 111–150 (1999).

    CAS 

    Google Scholar 

  • 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. N. Phytologist 116, 1–18 (1990).

    CAS 

    Google Scholar 

  • Wolfe-Simon, F., Grzebyk, D., Schofield, O. & Falkowski, P. G. The role and evolution of superoxide dismutases in algae 1. J. Phycol. 41, 453–465 (2005).

    CAS 

    Google Scholar 

  • Middag, R. D., De Baar, H. J. W., Laan, P., Cai, P. V. & Van Ooijen, J. C. Dissolved manganese in the Atlantic sector of the Southern Ocean. Deep Sea Res. Part II: Topical Stud. Oceanogr. 58, 2661–2677 (2011).

    CAS 

    Google Scholar 

  • Buma, A. G., De Baar, H. J., Nolting, R. F. & Van Bennekom, A. J. Metal enrichment experiments in the Weddell‐Scotia Seas: effects of iron and manganese on various plankton communities. Limnol. Oceanogr. 36, 1865–1878 (1991).

    CAS 

    Google Scholar 

  • Middag, R., de Baar, H. J., Klunder, M. B. & Laan, P. Fluxes of dissolved aluminum and manganese to the Weddell Sea and indications for manganese co‐limitation. Limnol. Oceanogr. 58, 287–300 (2013).

    CAS 

    Google Scholar 

  • Browning, T. J. et al. Strong responses of Southern Ocean phytoplankton communities to volcanic ash. Geophys. Res. Lett. 41, 2851–2857 (2014).

    CAS 

    Google Scholar 

  • Wu, M. et al. Manganese and iron deficiency in Southern Ocean Phaeocystis Antarctica populations revealed through taxon-specific protein indicators. Nat. Commun. 10, 1–10 (2019).

    Google Scholar 

  • Browning, T. J., Achterberg, E. P., Engel, A. & Mawji, E. Manganese co-limitation of phytoplankton growth and major nutrient drawdown in the Southern Ocean. Nat. Commun. 12, 884 (2021).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Viljoen, J. J. et al. Links between the phytoplankton community composition and trace metal distribution in summer surface waters of the Atlantic southern ocean. Front. Mar. Sci. 6, 295 (2019).

    Google Scholar 

  • Arrigo, K. R. Marine microorganisms and global nutrient cycles. Nature 437, 349–355 (2005).

    CAS 
    PubMed 

    Google Scholar 

  • De Baar, H. J. W. von Liebig’s law of the minimum and plankton ecology (1899–1991). Prog. Oceanogr. 33, 347–386 (1994).

    Google Scholar 

  • Saito, M. A., Goepfert, T. J. & Ritt, J. T. Some thoughts on the concept of colimitation: three definitions and the importance of bioavailability. Limnol. Oceanogr. 53, 276–290 (2008).

    CAS 

    Google Scholar 

  • Pausch, F., Bischof, K. & Trimborn, S. Iron and manganese co-limit growth of the Southern Ocean diatom Chaetoceros debilis. PLos ONE 14, e0221959 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hopkinson, B. M. et al. Iron limitation across chlorophyll gradients in the southern Drake Passage: phytoplankton responses to iron addition and photosynthetic indicators of iron stress. Limnol. Oceanogr. 52, 2540–2554 (2007).

    CAS 

    Google Scholar 

  • Trimborn, S., Hoppe, C. J., Taylor, B. B., Bracher, A. & Hassler, C. Physiological characteristics of open ocean and coastal phytoplankton communities of Western Antarctic Peninsula and Drake Passage waters. Deep Sea Res. Part I: Oceanographic Res. Pap. 98, 115–124 (2015).

    CAS 

    Google Scholar 

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

    PubMed 
    PubMed Central 

    Google Scholar 

  • Prézelin, B. B., Hofmann, E. E., Mengelt, C. & Klinck, J. M. The linkage between upper circumpolar deep water (UCDW) and phytoplankton assemblages on the west Antarctic Peninsula continental shelf. J. Mar. Res. 58, 165–202 (2000).

    Google Scholar 

  • Varela, M., Fernandez, E. & Serret, P. Size-fractionated phytoplankton biomass and primary production in the Gerlache and south Bransfield Straits (Antarctic Peninsula) in Austral summer 1995–1996. Deep Sea Res. Part II: Topical Stud. Oceanogr. 49, 749–768 (2002).

    CAS 

    Google Scholar 

  • Hoffmann, L. J., Peeken, I. & Lochte, K. Effects of iron on the elemental stoichiometry during EIFEX and in the diatoms Fragilariopsis kerguelensis and Chaetoceros dichaeta. Biogeosciences 4, 569–579 (2007).

    CAS 

    Google Scholar 

  • Blanco-Ameijeiras, S. et al. Exopolymeric substances control microbial community structure and function by contributing to both C and Fe nutrition in Fe-limited Southern Ocean provinces. Microorganisms 8, 1980 (2020).

    CAS 
    PubMed Central 

    Google Scholar 

  • Church, M. J., Hutchins, D. A. & Ducklow, H. W. Limitation of bacterial growth by dissolved organic matter and iron in the Southern Ocean. Appl. Environ. Microbiol. 66, 455–466 (2000).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Obernosterer, I., Fourquez, M. & Blain, S. Fe and C co-limitation of heterotrophic bacteria in the naturally fertilized region off the Kerguelen Islands. Biogeosciences 12, 1983–1992 (2015).

    Google Scholar 

  • Fourquez, M., Obernosterer, I., Davies, D. M., Trull, T. W. & Blain, S. Microbial iron uptake in the naturally fertilized waters in the vicinity of the Kerguelen Islands: phytoplankton–bacteria interactions. Biogeosciences 12, 1893–1906 (2015).

    Google Scholar 

  • Fourquez, M. et al. Microbial competition in the subpolar southern ocean: an Fe–C Co-limitation experiment. Front. Mar. Sci. 6, 776 (2020).

    Google Scholar 

  • Boyd, P. W. et al. A mesoscale phytoplankton bloom in the polar Southern Ocean stimulated by iron fertilization. Nature 407, 695–702 (2000).

    CAS 
    PubMed 

    Google Scholar 

  • De Baar, H. J. et al. Synthesis of iron fertilization experiments: from the iron age in the age of enlightenment. J. Geophys. Res. Oceans 110, https://doi.org/10.1029/2004JC002601 (2005).

  • Smetacek, V. & Naqvi, S. W. A. The next generation of iron fertilization experiments in the Southern Ocean. Philos. Trans. R. Soc. A: Math., Phys. Eng. Sci. 366, 3947–3967 (2008).

    CAS 

    Google Scholar 

  • Geider, R. J. & La Roche, J. The role of iron in phytoplankton photosynthesis, and the potential for iron-limitation of primary productivity in the sea. Photosynthesis Res. 39, 275–301 (1994).

    CAS 

    Google Scholar 

  • van Leeuwe, M. A. & Stefels, J. Effects of iron and light stress on the biochemical composition of Antarctic Phaeocystis sp. (Prymnesiophyceae). II. Pigment composition. J. Phycol. 34, 496–503 (1998).

    Google Scholar 

  • Hoffmann, L. J., Peeken, I., Lochte, K., Assmy, P. & Veldhuis, M. Different reactions of Southern Ocean phytoplankton size classes to iron fertilization. Limnol. Oceanogr. 51, 1217–1229 (2006).

    CAS 

    Google Scholar 

  • Koch, F., Beszteri, S., Harms, L. & Trimborn, S. The impacts of iron limitation and ocean acidification on the cellular stoichiometry, photophysiology, and transcriptome of Phaeocystis antarctica. Limnol. Oceanogr. 64, 357–375 (2019).

    CAS 

    Google Scholar 

  • Koch, F. & Trimborn, S. Limitation by Fe, Zn, Co, and B12 results in similar physiological responses in two antarctic phytoplankton species. Front. Mar. Sci. 6, 514 (2019).

    Google Scholar 

  • Peers, G. & Price, N. M. A role for manganese in superoxide dismutases and growth of iron‐deficient diatoms. Limnol. Oceanogr. 49, 1774–1783 (2004).

    CAS 

    Google Scholar 

  • Cefarelli, A. O. et al. Diversity of the diatom genus Fragilariopsis in the Argentine Sea and Antarctic waters: morphology, distribution and abundance. Polar Biol. 33, 1463–1484 (2010).

    Google Scholar 

  • Marchetti, A. & Harrison, P. J. Coupled changes in the cell morphology and elemental (C, N, and Si) composition of the pennate diatom Pseudo-nitzschia due to iron deficiency. Limnol. Oceanogr. 52, 2270–2284 (2007).

    CAS 

    Google Scholar 

  • Boyd, P. W. et al. Microbial control of diatom bloom dynamics in the open ocean. Geophys. Res. Lett. 39, https://doi.org/10.1029/2012GL053448 (2012).

  • Behrenfeld, M. J. & Kolber, Z. S. Widespread iron limitation of phytoplankton in the South Pacific Ocean. Science 283, 840–843 (1999).

    CAS 
    PubMed 

    Google Scholar 

  • Strzepek, R. F., Hunter, K. A., Frew, R. D., Harrison, P. J. & Boyd, P. W. Iron‐light interactions differ in Southern Ocean phytoplankton. Limnol. Oceanogr. 57, 1182–1200 (2012).

    CAS 

    Google Scholar 

  • Klunder, M. B. et al. Dissolved Fe across the Weddell Sea and Drake Passage: impact of DFe on nutrient uptake. Biogeosciences 11, 651–669 (2014).

    Google Scholar 

  • Trimborn, S. et al. Iron sources alter the response of Southern Ocean phytoplankton to ocean acidification. Mar. Ecol. Prog. Ser. 578, 35–50 (2017).

    CAS 

    Google Scholar 

  • Smith, W. O. & Lancelot, C. Bottom-up versus top-down control in phytoplankton of the Southern Ocean. Antarct. Sci. 16, 531–539 (2004).

    Google Scholar 

  • Schoffman, H., Lis, H., Shaked, Y. & Keren, N. Iron–nutrient interactions within phytoplankton. Front. Plant Sci. 7, 1223 (2016).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Meijers, A. J. S. The Southern Ocean in the coupled model intercomparison project phase 5. Philos. Trans. R. Soc. A: Math., Phys. Eng. Sci. 372, 20130296 (2014).

    CAS 

    Google Scholar 

  • Hauck, J. et al. On the Southern Ocean CO2 uptake and the role of the biological carbon pump in the 21st century. Glob. Biogeochem. Cycles 29, 1451–1470 (2015).

    CAS 

    Google Scholar 

  • Cabanes, D. J. et al. Using Fe chemistry to predict Fe uptake rates for natural plankton assemblages from the Southern Ocean. Mar. Chem. 225, 103853 (2020).

    CAS 

    Google Scholar 

  • Cutter, G. A. et al. Sampling and sample-handling protocols for GEOTRACES Cruises, Version 3.0 (2017).

  • Gerringa, L. J. A., De Baar, H. J. W. & Timmermans, K. R. A comparison of iron limitation of phytoplankton in natural oceanic waters and laboratory media conditioned with EDTA. Mar. Chem. 68, 335–346 (2000).

    CAS 

    Google Scholar 

  • Hoppe, C. J. et al. Iron limitation modulates ocean acidification effects on Southern Ocean phytoplankton communities. PLoS ONE 8, e79890 (2013).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Hathorne, E. C. et al. Online preconcentration ICP-MS analysis of rare earth elements in seawater. Geochemistry, Geophysics, Geosystems 13, https://doi.org/10.1029/2011GC003907 (2012).

  • Rapp, I., Schlosser, C., Rusiecka, D., Gledhill, M. & Achterberg, E. P. Automated preconcentration of Fe, Zn, Cu, Ni, Cd, Pb, Co, and Mn in seawater with analysis using high-resolution sector field inductively-coupled plasma mass spectrometry. Analytica Chim. Acta 976, 1–13 (2017).

    CAS 

    Google Scholar 

  • Utermöhl, H. Zur vervollkommnung der quantitativen phytoplankton-methodik: Mit 1 Tabelle und 15 abbildungen im Text und auf 1 Tafel. Int. Ver. f.ür. theoretische und Angew. Limnologie: Mitteilungen 9, 1–38 (1958).

    Google Scholar 

  • Edler, L. Recommendations on Methods for Marine Biological Studies in the Baltic Sea. Phytoplankton and Chlorophyll (Publication-Baltic Marine Biologists BMB (Sweden), 1979).

  • Tomas, C. R. & Haste, G. R. Identifying Marine Phytoplankton (Academic Press, 1997).

  • Olson, R. J., Zettler, E. R., Chisholm, S. W. & Dusenberry, J. A. in Particle Analysis in Oceanography 351–399 (Springer, 1991).

  • Koch, F., Sanudo-Wilhelmy, S. A., Fisher, N. S. & Gobler, C. J. Effect of vitamins B1 and B12 on bloom dynamics of the harmful brown tide alga, Aureococcus anophagefferens (Pelagophyceae). Limnol. Oceanogr. 58, 1761–1774 (2013).

    CAS 

    Google Scholar 

  • Welschmeyer, N. A. Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnol. Oceanogr. 39, 1985–1992 (1994).

    CAS 

    Google Scholar 

  • Oxborough, K. et al. Direct estimation of functional PSII reaction center concentration and PSII electron flux on a volume basis: a new approach to the analysis of Fast Repetition Rate fluorometry (FRRf) data. Limnol. Oceanogr.: Methods 10, 142–154 (2012).

    Google Scholar 

  • Schlitzer, R. Ocean Data View. (2015).


  • Source: Ecology - nature.com

    Sustainable strategies to treat urban runoff needed

    Q&A: Climate Grand Challenges finalists on building equity and fairness into climate solutions