Saccharides enhance iron bioavailability to Southern Ocean phytoplankton

Iron limits primary productivity in vast regions of the ocean. Given that marine phytoplankton contribute up to 40% of global biological carbon fixation, it is important to understand what parameters control the availability of iron (iron bioavailability) to these organisms. Most studies on iron bioavailability have focused on the role of siderophores; however, eukaryotic phytoplankton do not produce or release siderophores. Here, we report on the pivotal role of saccharides—which may act like an organic ligand—in enhancing iron bioavailability to a Southern Ocean cultured diatom, a prymnesiophyte, as well as to natural populations of eukaryotic phytoplankton. Addition of a monosaccharide (>2 nM of glucuronic acid, GLU) to natural planktonic assemblages from both the polar front and subantarctic zones resulted in an increase in iron bioavailability for eukaryotic phytoplankton, relative to bacterioplankton. The enhanced iron bioavailability observed for several groups of eukaryotic phytoplankton (i.e., cultured and natural populations) using three saccharides, suggests it is a common phenomenon. Increased iron bioavailability resulted from the combination of saccharides forming highly bioavailable organic associations with iron and increasing iron solubility, mainly as colloidal iron. As saccharides are ubiquitous, present at nanomolar to micromolar concentrations, and produced by biota in surface waters, they also satisfy the prerequisites to be important constituents of the poorly defined “ligand soup,” known to weakly bind iron. Our findings point to an additional type of organic ligand, controlling iron bioavailability to eukaryotic phytoplankton—a key unknown in iron biogeochemistry.

[1]  K. Porter,et al.  The use of DAPI for identifying and counting aquatic microflora1 , 1980 .

[2]  B. Nair,et al.  Studies on the nature of interaction of iron(III) with alginates. , 2004, Biochimica et biophysica acta.

[3]  F. Morel,et al.  AQUIL: A CHEMICALLY DEFINED PHYTOPLANKTON CULTURE MEDIUM FOR TRACE METAL STUDIES 1 2 , 1979 .

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

[5]  P. Statham,et al.  The role of polysaccharides and diatom exudates in the redox cycling of Fe and the photoproduction of hydrogen peroxide in coastal seawaters , 2009 .

[6]  R. Benner,et al.  Abundance and distribution of carbohydrates in the ocean , 1994 .

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

[8]  R. Benner,et al.  Carbohydrates in phytoplankton and freshly produced dissolved organic matter , 1998 .

[9]  J. Nishioka,et al.  Enhanced carbohydrate production by Southern Ocean phytoplankton in response to in situ iron fertilization , 2005 .

[10]  P. Worsfold,et al.  Hydroxamate siderophores: occurrence and importance in the Atlantic Ocean. , 2008, Environmental science & technology.

[11]  P. Boyd,et al.  Iron-binding ligands and their role in the ocean biogeochemistry of iron , 2007 .

[12]  M. Gretz,et al.  DIATOM EXTRACELLULAR POLYMERIC SUBSTANCES: FUNCTION, FINE STRUCTURE, CHEMISTRY, AND PHYSIOLOGY , 1993 .

[13]  S. Wilhelm.  Ecology of iron-limited cyanobacteria: a review of physiological responses and implications for aquatic systems , 1995 .

[14]  Crystal S. Thomas,et al.  Computer-assisted high-performance liquid chromatography method development with applications to the isolation and analysis of phytoplankton pigments. , 2001, Journal of chromatography. A.

[15]  P. Boyd,et al.  Spinning the “Ferrous Wheel”: The importance of the microbial community in an iron budget during the FeCycle experiment , 2005 .

[16]  Christoph Völker,et al.  Physical limits on iron uptake mediated by siderophores or surface reductases , 1999 .

[17]  David L. Kirchman,et al.  The oceanic gel phase: a bridge in the DOM-POM continuum , 2004 .

[18]  S. Bertilsson,et al.  Iron enrichment and photoreduction of iron under UV and PAR in the presence of hydroxycarboxylic acid: implications for phytoplankton growth in the Southern Ocean , 2004 .

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

[20]  C. Hassler,et al.  Bioavailability of trace metals to aquatic microorganisms: importance of chemical, biological and physical processes on biouptake. , 2006, Biochimie.

[21]  J. Bowman,et al.  Chemical Characterization of Exopolysaccharides from Antarctic Marine Bacteria , 2005, Microbial Ecology.

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

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

[24]  C. Hung,et al.  Control of acid polysaccharide production and 234Th and POC export fluxes by marine organisms , 2003 .

[25]  D. Hutchins,et al.  A trace metal clean reagent to remove surface-bound iron from marine phytoplankton , 2003 .

[26]  K. Arrigo,et al.  Processes governing the supply of iron to phytoplankton in stratified seas , 2006 .

[27]  P. Boyd,et al.  Does planktonic community structure determine downward particulate organic carbon flux in different oceanic provinces , 1999 .

[28]  A. Decho,et al.  Microbial exopolymer secretions in ocean environments: their role(s) in food webs and marine processes , 1990 .

[29]  C. Carrano,et al.  Photolysis of iron–siderophore chelates promotes bacterial–algal mutualism , 2009, Proceedings of the National Academy of Sciences.

[30]  C. Lancelot,et al.  Carbohydrates in the North Sea during spring blooms of Phaeocystis : A specific fingerprint , 1996 .

[31]  M. T. Maldonado,et al.  The effect of Fe and Cu on growth and domoic acid production by Pseudo-nitzschia multiseries and Pseudo‐nitzschia australis , 2002 .

[32]  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 .

[33]  Janet G. Hering,et al.  Principles and Applications of Aquatic Chemistry , 1993 .

[34]  Chen Xu,et al.  Chemical composition and 234Th (IV) binding of extracellular polymeric substances (EPS) produced by the marine diatom Amphora sp. , 2008 .

[35]  Laodong Guo,et al.  Phase partitioning and solubility of iron in natural seawater controlled by dissolved organic matter , 2004 .

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

[37]  R. Sempéré,et al.  Analytical methods for the determination of sugars in marine samples: A historical perspective and future directions , 2005 .

[38]  Béla Gyurcsik,et al.  Carbohydrates as ligands: coordination equilibria and structure of the metal complexes , 2000 .

[39]  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 .

[40]  G. Battaglia,et al.  Determination of humic substances in natural waters by cathodic stripping voltammetry of their complexes with iron. , 2007, Analytica chimica acta.

[41]  T. Waite,et al.  Use of superoxide as an electron shuttle for iron acquisition by the marine cyanobacterium Lyngbya majuscula. , 2005, Environmental science & technology.

[42]  P. Croot,et al.  Determination of Iron Speciation by Cathodic Stripping Voltammetry in Seawater Using the Competing Ligand 2‐(2‐Thiazolylazo)‐p‐cresol (TAC) , 2000 .

[43]  A. J. Watson,et al.  Testing the iron hypothesis in ecosystems of the equatorial Pacific Ocean , 1994, Nature.

[44]  K. Bruland,et al.  Domoic acid binds iron and copper: a possible role for the toxin produced by the marine diatom Pseudo-nitzschia , 2001 .

[45]  S. Markager.  Practical guidelines for the analysis of seawater , 2010 .

[46]  C. Lancelot,et al.  Effects of photosynthesis on the accumulation of Mn and Fe by Phaeocystis colonies , 2001 .

[47]  E. Boyle,et al.  Mesoscale Iron Enrichment Experiments 1993-2005: Synthesis and Future Directions , 2007, Science.

[48]  Roman Stocker,et al.  Rapid chemotactic response enables marine bacteria to exploit ephemeral microscale nutrient patches , 2008, Proceedings of the National Academy of Sciences.

[49]  Robert F. Chen,et al.  A major biopolymeric component to dissolved organic carbon in surface sea water , 1997, Nature.

[50]  J. Moffett,et al.  Thermodynamic characterization of the partitioning of iron between soluble and colloidal species in the Atlantic Ocean , 2006 .