Chasing iron bioavailability in the Southern Ocean: Insights from Phaeocystis antarctica and iron speciation

Dissolved iron (dFe) availability limits the uptake of atmospheric CO2 by the Southern Ocean (SO) biological pump. Hence, any change in bioavailable dFe in this region can directly influence climate. On the basis of Fe uptake experiments with Phaeocystis antarctica, we show that the range of dFe bioavailability in natural samples is wider (<1 to ~200% compared to free inorganic Fe′) than previously thought, with higher bioavailability found near glacial sources. The degree of bioavailability varied regardless of in situ dFe concentration and depth, challenging the consensus that sole dFe concentrations can be used to predict Fe uptake in modeling studies. Further, our data suggest a disproportionately major role of biologically mediated ligands and encourage revisiting the role of humic substances in influencing marine Fe biogeochemical cycling in the SO. Last, we describe a linkage between in situ dFe bioavailability and isotopic signatures that, we anticipate, will stimulate future research.

[1]  J. Fitzsimmons,et al.  Novel Insights into Marine Iron Biogeochemistry from Iron Isotopes. , 2022, Annual review of marine science.

[2]  D. Siegel,et al.  Quantifying the Ocean's Biological Pump and Its Carbon Cycle Impacts on Global Scales. , 2022, Annual review of marine science.

[3]  C. Hassler,et al.  Phytoplankton Responses to Bacterially Regenerated Iron in a Southern Ocean Eddy , 2022, Microorganisms.

[4]  I. Berman‐Frank,et al.  Assessing the contribution of diazotrophs to microbial Fe uptake using a group specific approach in the Western Tropical South Pacific Ocean , 2022, ISME Communications.

[5]  D. Repeta,et al.  Slow Kinetics of Iron Binding to Marine Ligands in Seawater Measured by Isotope Exchange Liquid Chromatography-Inductively Coupled Plasma Mass Spectrometry. , 2022, Environmental science & technology.

[6]  T. Horner,et al.  A decade of progress in understanding cycles of trace elements and their isotopes in the oceans , 2021 .

[7]  D. König,et al.  Constraints on the Cycling of Iron Isotopes From a Global Ocean Model , 2021, Global biogeochemical cycles.

[8]  C. Hassler,et al.  Isotopic fingerprinting of biogeochemical processes and iron sources in the iron-limited surface Southern Ocean , 2021 .

[9]  M. T. Maldonado,et al.  Probing the Bioavailability of Dissolved Iron to Marine Eukaryotic Phytoplankton Using In Situ Single Cell Iron Quotas , 2021, Global biogeochemical cycles.

[10]  C. Bowler,et al.  Iron metabolism strategies in diatoms , 2021, Journal of experimental botany.

[11]  K. Arrigo,et al.  Massive Southern Ocean phytoplankton bloom fed by iron of possible hydrothermal origin , 2021, Nature Communications.

[12]  C. Hassler,et al.  Exopolymeric Substances Control Microbial Community Structure and Function by Contributing to both C and Fe Nutrition in Fe-Limited Southern Ocean Provinces , 2020, Microorganisms.

[13]  J. Camadro,et al.  Iron Uptake Mechanisms in Marine Phytoplankton , 2020, Frontiers in Microbiology.

[14]  D. Hutchins,et al.  Independent iron and light limitation in a low-light-adapted Prochlorococcus from the deep chlorophyll maximum , 2020, The ISME journal.

[15]  C. Hassler,et al.  Using Fe chemistry to predict Fe uptake rates for natural plankton assemblages from the Southern Ocean , 2020 .

[16]  D. Wolf-Gladrow,et al.  Iron organic speciation during the LOHAFEX experiment: Iron ligands release under biomass control by copepod grazing , 2020 .

[17]  P. Boyd,et al.  Contribution of Electroactive Humic Substances to the Iron‐Binding Ligands Released During Microbial Remineralization of Sinking Particles , 2020, Geophysical Research Letters.

[18]  C. Hassler,et al.  Trace metal and nutrient dynamics across broad biogeochemical gradients in the Indian and Pacific sectors of the Southern Ocean , 2020, Marine Chemistry.

[19]  S. Sander,et al.  Importance of refractory ligands and their photodegradation for iron oceanic inventories and cycling , 2020 .

[20]  P. Boyd,et al.  Distinct iron cycling in a Southern Ocean eddy , 2020, Nature Communications.

[21]  M. T. Maldonado,et al.  Insights into the bioavailability of oceanic dissolved Fe from phytoplankton uptake kinetics , 2020, The ISME Journal.

[22]  C. Hassler,et al.  Electrochemical evaluation of iron-binding ligands along the Australian GEOTRACES southwestern Pacific section (GP13) , 2020 .

[23]  R. Anderson.  GEOTRACES: Accelerating Research on the Marine Biogeochemical Cycles of Trace Elements and Their Isotopes. , 2020, Annual review of marine science.

[24]  C. Hassler,et al.  Cycling of zinc and its isotopes across multiple zones of the Southern Ocean: Insights from the Antarctic Circumnavigation Expedition , 2020, Geochimica et Cosmochimica Acta.

[25]  C. Hassler,et al.  High-resolution Cd isotope systematics in multiple zones of the Southern Ocean from the Antarctic Circumnavigation Expedition , 2019 .

[26]  K. Bischof,et al.  Susceptibility of Two Southern Ocean Phytoplankton Key Species to Iron Limitation and High Light , 2019, Front. Mar. Sci..

[27]  P. Boyd,et al.  Photosynthetic adaptation to low iron, light, and temperature in Southern Ocean phytoplankton , 2019, Proceedings of the National Academy of Sciences.

[28]  R. Raiswell,et al.  Iron in Glacial Systems: Speciation, Reactivity, Freezing Behavior, and Alteration During Transport , 2018, Front. Earth Sci..

[29]  F. Koch,et al.  The impacts of iron limitation and ocean acidification on the cellular stoichiometry, photophysiology, and transcriptome of Phaeocystis antarctica , 2018, Limnology and Oceanography.

[30]  Giacomo R. DiTullio,et al.  Colony formation in Phaeocystis antarctica: connecting molecular mechanisms with iron biogeochemistry , 2018, Biogeosciences.

[31]  Bogumil J. Karas,et al.  Carbonate-sensitive phytotransferrin controls high-affinity iron uptake in diatoms , 2018, Nature.

[32]  M. Saito,et al.  Distinct Siderophores Contribute to Iron Cycling in the Mesopelagic at Station ALOHA , 2018, Front. Mar. Sci..

[33]  K. Johnson,et al.  The integral role of iron in ocean biogeochemistry , 2017, Nature.

[34]  C. Hassler,et al.  Toward a Regional Classification to Provide a More Inclusive Examination of the Ocean Biogeochemistry of Iron-Binding Ligands , 2017 .

[35]  D. Mende,et al.  Siderophore-based microbial adaptations to iron scarcity across the eastern Pacific Ocean , 2016, Proceedings of the National Academy of Sciences.

[36]  Martin Frank,et al.  The GEOTRACES Intermediate Data Product 2017 , 2018, Chemical Geology.

[37]  C. Völker,et al.  Modeling organic iron-binding ligands in a three-dimensional biogeochemical ocean model , 2015 .

[38]  F. Poitrasson,et al.  Iron isotope fractionation during Fe(II) and Fe(III) adsorption on cyanobacteria , 2015 .

[39]  S. Sander,et al.  Iron stable isotopes track pelagic iron cycling during a subtropical phytoplankton bloom , 2014, Proceedings of the National Academy of Sciences.

[40]  F. Morel,et al.  Iron bioavailability to phytoplankton: an empirical approach , 2014, The ISME Journal.

[41]  P. Boyd,et al.  Surface-water iron supplies in the Southern Ocean sustained by deep winter mixing , 2014 .

[42]  Scott C. Doney,et al.  Marine Ecosystem Dynamics and Biogeochemical Cycling in the Community Earth System Model [CESM1(BGC)]: Comparison of the 1990s with the 2090s under the RCP4.5 and RCP8.5 Scenarios , 2013 .

[43]  F. Morel,et al.  Preparation and chemistry of the artificial algal culture medium aquil , 2013 .

[44]  C. Hassler,et al.  Measurement of iron chemical speciation in seawater at 4 °C: The use of competitive ligand exchange–adsorptive cathodic stripping voltammetry , 2013 .

[45]  F. Poitrasson,et al.  Extreme iron isotope fractionation between colloids and particles of boreal and temperate organic-rich waters , 2013 .

[46]  S. Baines,et al.  The trace metal composition of marine phytoplankton. , 2013, Annual review of marine science.

[47]  I. Obernosterer,et al.  A method for the use of the radiotracer 55Fe for microautoradiography and CARD-FISH of natural bacterial communities. , 2012, FEMS microbiology letters.

[48]  Y. Shaked,et al.  Disassembling Iron Availability to Phytoplankton , 2012, Front. Microbio..

[49]  K. Buck,et al.  The Organic Complexation of Iron in the Marine Environment: A Review , 2012, Front. Microbio..

[50]  A. King,et al.  Quasi-Lagrangian drifter studies of iron speciation and cycling off Point Conception, California , 2012 .

[51]  David M Schruth,et al.  Comparative metatranscriptomics identifies molecular bases for the physiological responses of phytoplankton to varying iron availability , 2012, Proceedings of the National Academy of Sciences.

[52]  P. Boyd,et al.  Adaptive strategies by Southern Ocean phytoplankton to lessen iron limitation: Uptake of organically complexed iron and reduced cellular iron requirements , 2011 .

[53]  C. Völker,et al.  Towards accounting for dissolved iron speciation in global ocean models , 2011 .

[54]  Meinrat O. Andreae,et al.  Modulation of the Southern Ocean cadmium isotope signature by ocean circulation and primary productivity , 2011 .

[55]  C. Hassler,et al.  Saccharides enhance iron bioavailability to Southern Ocean phytoplankton , 2010, Proceedings of the National Academy of Sciences.

[56]  A. Anbar,et al.  Fe isotope fractionation during equilibration of Fe-organic complexes. , 2010, Environmental science & technology.

[57]  Dennis A. Hansell,et al.  Dissolved Organic Matter in the Ocean: A Controversy Stimulates New Insights , 2009 .

[58]  C. Hassler,et al.  Bioavailability of organically bound Fe to model phytoplankton of the Southern Ocean , 2009 .

[59]  C. Hassler,et al.  Discriminating between intra‐ and extracellular metals using chemical extractions: an update on the case of iron , 2009 .

[60]  Olivier Aumont,et al.  Influence of light and temperature on the marine iron cycle: From theoretical to global modeling , 2009 .

[61]  Cathy W. S. Chen,et al.  Bayesian Estimation for Parsimonious Threshold Autoregressive Models in R , 2009 .

[62]  C. M. G. van den Berg,et al.  Evidence for geochemical control of iron by humic substances in seawater , 2009 .

[63]  R. Geider,et al.  Interpretation of fast repetition rate (FRR) fluorescence: signatures of phytoplankton community structure versus physiological state , 2009 .

[64]  S. Tulaczyk,et al.  Bioavailable iron in the Southern Ocean: the significance of the iceberg conveyor belt , 2008, Geochemical transactions.

[65]  J. Baker,et al.  Equilibrium Fe isotope fractionation between inorganic aqueous Fe(III) and the siderophore complex, Fe(III)-desferrioxamine B , 2008 .

[66]  A. Kustka,et al.  The role of unchelated Fe in the iron nutrition of phytoplankton , 2008 .

[67]  E. Boyle,et al.  GEOTRACES – An international study of the global marine biogeochemical cycles of trace elements and their isotopes , 2007 .

[68]  P. Sedwick,et al.  Evidence for high iron requirements of colonial Phaeocystis antarctica at low irradiance , 2007 .

[69]  F. Morel,et al.  Distinguishing between cellular and Fe-oxide-associated trace elements in phytoplankton , 2006 .

[70]  S. Sander,et al.  Acquisition of iron bound to strong organic complexes, with different Fe binding groups and photochemical reactivities, by plankton communities in Fe‐limited subantarctic waters , 2005 .

[71]  F. Morel,et al.  A general kinetic model for iron acquisition by eukaryotic phytoplankton , 2005 .

[72]  A. Anbar,et al.  Fe isotopic fractionation during mineral dissolution with and without bacteria , 2004 .

[73]  K. Arrigo,et al.  Phytoplankton dynamics within 37 Antarctic coastal polynya systems , 2003 .

[74]  K. Bruland,et al.  Collection and detection of natural iron-binding ligands from seawater , 2001 .

[75]  N. M. Price,et al.  Utilization of iron bound to strong organic ligands by plankton communities in the subarctic Pacific Ocean , 1999 .

[76]  A. Butler,et al.  Competition among marine phytoplankton for different chelated iron species , 1999, Nature.

[77]  S. Myklestad,et al.  A sensitive and rapid method for analysis of dissolved mono- and polysaccharides in seawater , 1997 .

[78]  D. Kirchman.  Microbial ferrous wheel , 1996, Nature.

[79]  W. Sunda,et al.  Iron uptake and growth limitation in oceanic and coastal phytoplankton , 1995 .

[80]  K. Bruland,et al.  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 , 1995 .

[81]  F. Morel,et al.  lron transport in marine phytoplankton: Kinetics of cellular and medium coordination reactions , 1990 .

[82]  John H. Martin.  glacial-interglacial Co2 change : the iron hypothesis , 1990 .

[83]  C. Hassler,et al.  Iron bioavailability in the Southern Ocean , 2012 .

[84]  M. Lohan.  Marine Biogeochemical Cycles of Trace Elements and their Isotopes , 2010 .

[85]  Christiane Lancelot,et al.  Phaeocystis blooms in the global ocean and their controlling mechanisms: a review , 2005 .

[86]  F. Millero,et al.  The solubility of iron in seawater , 2002 .