• Adrian MarchettiEmail author
  • Maria T. Maldonado
Part of the Developments in Applied Phycology book series (DAPH, volume 6)


Iron is essential for algal growth, metabolism and function. Numerous proteins and enzymes require iron, including those involved in photosynthesis, respiration, as well as nitrogen assimilation and fixation. A variety of sources and sinks of iron in marine and freshwater ecosystems lead to a wide range of dissolved iron concentrations, from iron-limiting to iron-replete, for microalgal growth. Decades of physiological and molecular research, in combination with recent genomic advances, have made way for breakthroughs in our understanding of the critical roles iron plays in microalgal metabolism and how iron is acquired in aqueous environments. Herein, we review and integrate these studies to compare and contrast the iron requirements, acquisition abilities and strategies, as well as storage capacities of microalgae, with a particular emphasis on diatoms, green algae and cyanobacteria. These include the ability to perform substitution or the permanent replacement of iron-requiring proteins for non-iron containing functional equivalents, the presence of a high-affinity uptake system and the capacity to store iron in excess of cellular demand. We also include a discussion of iron-related topics of current significance, including iron-light co-limitation, effects of iron limitation on cellular elemental composition, large-scale iron fertilization experiments, and climate change effects on iron bioavailability. Lastly, a brief overview of some common laboratory and field techniques employed to study microalgal iron physiology is provided.


Iron Requirements Transport Storage Limitation Fertilization 



We thank W.G. Sunda, P.J. Harrison and J.A. Raven for their helpful comments and insights on the manuscript. Supported by NSF-OCE 1334935 (A.M.).


  1. Allen MD, del Campo JA, Kropat J, Merchant SS (2007) FEA1, FEA2, and FRE1, encoding two homologous secreted proteins and a candidate ferrireductase, are expressed coordinately with FOX1 and FTR1 in iron-deficient Chlamydomonas reinhardtii. Eukaryot Cell 6:1841–1852PubMedPubMedCentralCrossRefGoogle Scholar
  2. Allen A, LaRoche J, Maheswari U, Lommer M, Schauer N, Lopez P, Finazzi G, Fernie A, Bowler C (2008) Whole-cell response of the pennate diatom Phaeodactylum tricornutum to iron starvation. Proc Natl Acad Sci 105:10438–10443PubMedPubMedCentralCrossRefGoogle Scholar
  3. Allnutt FCT, Bonner WD Jr (1987a) Characterization of iron uptake from ferrioxamine B by Chlorella vulgaris. Plant Physiol 85:746–750PubMedPubMedCentralCrossRefGoogle Scholar
  4. Allnutt FCT, Bonner WD (1987b) Evaluation of reductive release as a mechanism for iron uptake from ferrioxamine B by Chlorella vulgaris. Plant Physiol 85:751–756PubMedPubMedCentralCrossRefGoogle Scholar
  5. Anbar AD, Knoll AH (2002) Proterozoic ocean chemistry and evolution: a bioinorganic bridge? Science 297:1137–1142PubMedCrossRefGoogle Scholar
  6. Andersen RA (1992) Diversity of eukaryotic algae. Biodivers Conserv 1:267–292CrossRefGoogle Scholar
  7. Anderson MA, Morel FMM (1982) The influence of aqueous iron chemistry on the uptake of iron by the coastal diatom Thalassiosira weissflogii. Limnol Oceanogr 27:789–813CrossRefGoogle Scholar
  8. Annett AL, Lapi S, Ruth TJ, Maldonado MT (2008) The effects of Cu and Fe availability on the growth and Cu: C ratios of marine diatoms. Limnol Oceanogr 53:2451–2461CrossRefGoogle Scholar
  9. Armbrust E (2009) The life of diatoms in the world’s oceans. Nature 459:185–192PubMedCrossRefGoogle Scholar
  10. Askwith CC, de Silva D, Kaplan J (1996) Molecular biology of iron acquisition in Saccharomyces cerevisiae. Mol Microbiol 20:27–34PubMedCrossRefGoogle Scholar
  11. Assmy P, Smetacek V, Montresor M, Klaas C, Henjes J, Strass VH, Arrieta JM, Bathmann U, Berg GM, Breitbarth E, Cisewski B, Friedrichs L, Fuchs N, Herndl GJ, Jansen S, Kragefsky S, Latasa M, Peeken I, Rottgers R, Scharek R, Schuller SE, Steigenberger S, Webb A, Wolf-Gladrow D (2013) Thick-shelled, grazer-protected diatoms decouple ocean carbon and silicon cycles in the iron-limited Antarctic Circumpolar Current. Proc Natl Acad Sci 110:20633–20638PubMedPubMedCentralCrossRefGoogle Scholar
  12. Baines SB, Twining BS, Vogt S, Balch WM, Fisher NS, Nelson DM (2011) Elemental composition of equatorial Pacific diatoms exposed to additions of silicic acid and iron. Deep Sea Res II 58:512–523CrossRefGoogle Scholar
  13. Banse K (1991) Iron availability, nitrate uptake, and exportable new production in the Subarctic Pacific. J Geophys Res Oceans 96:741–748CrossRefGoogle Scholar
  14. Barbeau K, Rue EL, Bruland KW, Butler A (2001) Photochemical cycling of iron in the surface ocean mediated by microbial iron(III)-binding ligands. Nature 413:409–413PubMedCrossRefGoogle Scholar
  15. Barbeau K, Rue EL, Trick CG, Bruland KT, Butler A (2003) Photochemical reactivity of siderophores produced by marine heterotrophic bacteria and cyanobacteria based on characteristic Fe(III) binding groups. Limnol Oceanogr 48:1069–1078CrossRefGoogle Scholar
  16. Behrenfeld MJ, Milligan AJ (2013) Photophysiological expressions of iron stress in phytoplankton. Ann Rev Mar Sci 5:217–246PubMedCrossRefGoogle Scholar
  17. Behrenfeld MJ, Worthington K, Sherrell RM, Chavez FP, Strutton P, McPhaden M, Shea DM (2006) Controls on tropical Pacific Ocean productivity revealed through nutrient stress diagnostics. Nature 442:1025–1028PubMedCrossRefGoogle Scholar
  18. Behrenfeld MJ, Westberry TK, Boss ES, O’Malley RT, Siegel DA, Wiggert JD, Franz BA, McClain CR, Feldman GC, Doney SC, Moore JK, Dall’Olmo G, Milligan AJ, Lima I, Mahowald N (2009) Satellite-detected fluorescence reveals global physiology of ocean phytoplankton. Biogeosciences 6:779–794CrossRefGoogle Scholar
  19. Beiderbeck H, Taraz K, Budzikiewicz H, Walsby AE (2000) Anachelin, the siderophore of the cyanobacterium Anabaena cylindrica CCAP 1403/2A. Zeitschr Naturf C 55:681–687Google Scholar
  20. Beja O, Aravind L, Koonin EV, Suzuki MT, Hadd A, Nguyen LP, Jovanovich S, Gates CM, Feldman RA, Spudich JL, Spudich EN, DeLong EF (2000) Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 289:1902–1906PubMedCrossRefGoogle Scholar
  21. Berman-Frank I, Quigg A, Finkel ZV, Irwin AJ, Haramaty L (2007) Nitrogen-fixation strategies and Fe requirements in cyanobacteria. Limnol Oceanogr 52:2260–2269CrossRefGoogle Scholar
  22. Bertrand EM, Saito MA, Rose JM, Riesselman CR, Lohan MC, Noble AE, Lee PA, DiTullio GR (2007) Vitamin B12 and iron colimitation of phytoplankton growth in the Ross Sea. Limnol Oceanogr 52:1079–1093CrossRefGoogle Scholar
  23. Bibby TS, Nield J, Barber J (2001) Iron deficiency induces the formation of an antenna ring around trimeric photosystem I in cyanobacteria. Nature 412:743–745PubMedCrossRefGoogle Scholar
  24. Blaby-Haas CE, Merchant SS (2012) The ins and outs of algal metal transport. Biochim Biophys Acta-Mol Cell Res 1823:1531–1552CrossRefGoogle Scholar
  25. Blain S, Sedwick PN, Griffiths FB, Queguiner B, Bucciarelli E, Fiala M, Pondaven P, Treguer P (2002) Quantification of algal iron requirements in the Subantarctic Southern Ocean (Indian sector). Deep-Sea Res II 49:3255–3273CrossRefGoogle Scholar
  26. Blain S, Queguiner B, Armand L, Belviso S, Bombled B, Bopp L, Bowie A, Brunet C, Brussaard C, Carlotti F, Christaki U, Corbiere A, Durand I, Ebersbach F, Fuda JL, Garcia N, Gerringa L, Griffiths B, Guigue C, Guillerm C, Jacquet S, Jeandel C, Laan P, Lefevre D, Lo Monaco C, Malits A, Mosseri J, Obernosterer I, Park YH, Picheral M, Pondaven P, Remenyi T, Sandroni V, Sarthou G, Savoye N, Scouarnec L, Souhaut M, Thuiller D, Timmermans K, Trull T, Uitz J, van Beek P, Veldhuis M, Vincent D, Viollier E, Vong L, Wagener T (2007) Effect of natural iron fertilization on carbon sequestration in the Southern Ocean. Nature 446:1070–U1071PubMedCrossRefGoogle Scholar
  27. Bleuel C, Grosse C, Taudte N, Scherer J, Wesenberg D, Krauss GJ, Nies DH, Grass G (2005) TolC is involved in enterobactin efflux across the outer membrane of Escherichia coli. J Bacteriol 187:6701–6707PubMedPubMedCentralCrossRefGoogle Scholar
  28. Boekema EJ, Hifney A, Yakushevska AE, Piotrowski M, Keegstra W, Berry S, Michel KP, Pistorius EK, Kruip J (2001) A giant chlorophyll-protein complex induced by iron deficiency in cyanobacteria. Nature 412:745–748PubMedCrossRefGoogle Scholar
  29. Borowitzka MA (2016) Systematics, taxonomy and species names: do they matter? In: Borowitzka MA, Beardall J, Raven JA (eds) The physiology of microalgae. Springer, Dordrecht, pp 655–681Google Scholar
  30. Boukhalfa H, Crumbliss AL (2002) Chemical aspects of siderophore mediated iron transport. Biometals 15:325–339PubMedCrossRefGoogle Scholar
  31. Boyd PW, Jickells T, Law CS, Blain S, Boyle EA, Buesseler KO, Coale KH, Cullen JJ, de Baar HJW, Follows M, Harvey M, Lancelot C, Levasseur M, Owens NPJ, Pollard R, Rivkin RB, Sarmiento J, Schoemann V, Smetacek V, Takeda S, Tsuda A, Turner S, Watson AJ (2007) Mesoscale iron enrichment experiments 1993–2005: synthesis and future directions. Science 315:612–617PubMedCrossRefGoogle Scholar
  32. Boyle E (1998) Pumping iron makes thinner diatoms. Nature 393:733–734CrossRefGoogle Scholar
  33. Boyle E, Edmond J, Sholkovitz E (1976) The mechanism of iron removal in estuaries. Geochim Cosmochim Acta 41:1313–1324CrossRefGoogle Scholar
  34. Breitbarth E, Bellerby RJ, Neill CC, Ardelan MV, Meyerhöfer M, Zöllner E, Croot PL, Riebesell U (2010) Ocean acidification affects iron speciation during a coastal seawater mesocosm experiment. Biogeosciences 7:1065–1073CrossRefGoogle Scholar
  35. Bruland KW, Orians KJ, Cowen JP (1994) Reactive trace metals in the stratified central North Pacific. Geochim Cosmochim Acta 58:3171–3182CrossRefGoogle Scholar
  36. Bruland KW, Lohan MC, Aguilar-Islas AM, Smith GJ, Sohst B, Baptista A (2008) Factors influencing the chemistry of the near-field Columbia River plume: nitrate, silicic acid, dissolved Fe, and dissolved Mn. J Geophys Res Oceans 113:C00B02. DOI: 10.1029/2007JC004702
  37. Bruland KW, Middag R, Lohan MC (2014) Controls of trace metals in seawater. In: Holland HD, Tureklan KK (eds) Treatise on geochemistry, vol 8, 2nd edn. Elsevier, Oxford, pp 19–51CrossRefGoogle Scholar
  38. Brzezinski MA, Baines SB, Balch WM, Beucher C, Chai F, Dugdale RC, Krause JW, Landry MR, Marchi A, Measures C, Nelson DM, Parker A, Poulton A, Selph KE, Strutton P, Taylor AG, Twining BS (2011) Co-limitation of diatoms by iron and silicic acid in the equatorial Pacific. Deep-Sea Res II:493–511Google Scholar
  39. Bucciarelli E, Pondaven P, Sarthou G (2010) Effects of an iron-light co-limitation on the elemental composition (Si, C, N) of the marine diatoms Thalassiosira oceanica and Ditylum brightwellii. Biogeosciences 7:657–669CrossRefGoogle Scholar
  40. Castruita M, Casero D, Karpowicz SJ, Kropat J, Vieler A, Hsieh SI, Yan W, Cokus S, Loo JA, Benning C (2011) Systems biology approach in Chlamydomonas reveals connections between copper nutrition and multiple metabolic steps. Plant Cell Online 23:1273–1292CrossRefGoogle Scholar
  41. Cellier MFM, Bergevin I, Boyer E, Richer E (2001) Polyphyletic origins of bacterial Nramp transporters. Trends Genet 17:365–370PubMedCrossRefGoogle Scholar
  42. Chase Z, Strutton PG, Hales B (2007) Iron links river runoff and shelf width to phytoplankton biomass along the U.S. West Coast. Geophys Res Lett 34:L04607. DOI: 10.1029/2006GL028069
  43. Chauhan D, Folea IM, Jolley CC, Kouril R, Lubner CE, Lin S, Kolber D, Wolfe-Simon F, Golbeck JH, Boekema EJ (2011) A novel photosynthetic strategy for adaptation to low-iron aquatic environments. Biochemistry 50:686–692PubMedCrossRefGoogle Scholar
  44. Chavez FP, Buck KR, Coale KH, Martin JH, Ditullio GR, Welschmeyer NA, Jacobson AC, Barber RT (1991) Growth-rates, grazing, sinking, and iron limitation of Equatorial Pacific phytoplankton. Limnol Oceanogr 36:1816–1833CrossRefGoogle Scholar
  45. Chimento DP, Kadner RJ, Wiener MC (2005) Comparative structural analysis of TonB-dependent outer membrane transporters: implications for the transport cycle. Proteins 59:240–251PubMedCrossRefGoogle Scholar
  46. Coale KH, Fitzwater SE, Gordon RM, Johnson KS, Barber RT (1996) Control of community growth and export production by upwelled iron in the equatorial Pacific Ocean. Nature 379:621–624CrossRefGoogle Scholar
  47. Coale KH, Wang X, Tanner SJ, Johnson KS (2003) Phytoplankton growth and biological response to iron and zinc addition in the Ross Sea and Antarctic Circumpolar Current along 170 W. Deep Sea Res II 50:635–653CrossRefGoogle Scholar
  48. Coale KH, Johnson KS, Chavez FP, Buesseler KO, Barber RT, Brzezinski MA, Cochlan WP, Millero FJ, Falkowski PG, Bauer JE, Wanninkhof RH, Kudela RM, Altabet MA, Hales BE, Takahashi T, Landry MR, Bidigare RR, Wang XJ, Chase Z, Strutton PG, Friederich GE, Gorbunov MY, Lance VP, Hilting AK, Hiscock MR, Demarest M, Hiscock WT, Sullivan KF, Tanner SJ, Gordon RM, Hunter CN, Elrod VA, Fitzwater SE, Jones JL, Tozzi S, Koblizek M, Roberts AE, Herndon J, Brewster J, Ladizinsky N, Smith G, Cooper D, Timothy D, Brown SL, Selph KE, Sheridan CC, Twining BS, Johnson ZI (2004) Southern ocean iron enrichment experiment: carbon cycling in high- and low-Si waters. Science 304:408–414PubMedCrossRefGoogle Scholar
  49. Cochlan WP, Bronk DA, Coale KH (2002) Trace metals and nitrogenous nutrition of Antarctic phytoplankton: experimental observations in the Ross Sea. Deep-Sea Res II 49:3365–3390CrossRefGoogle Scholar
  50. Conway TM, John SG (2014) Quantification of dissolved iron sources to the North Atlantic Ocean. Nature 511:212–215PubMedCrossRefGoogle Scholar
  51. Crawford DW, Lipsen MS, Purdie DA, Lohan MC, Statham PJ, Whitney FA, Putland JN, Johnson WK, Sutherland N, Peterson TD, Harrison PJ, Wong CS (2003) Influence of zinc and iron enrichments on phytoplankton growth in the northeastern subarctic Pacific. Limnol Oceanogr 48:1583–1600CrossRefGoogle Scholar
  52. Cullen JJ (1991) Hypotheses to explain high-nutrient conditions in the open sea. Limnol Oceanogr 36:1578–1599CrossRefGoogle Scholar
  53. Cullen JT, Chase Z, Coale KH, Fitzwater SE, Sherrell RM (2003) Effect of iron limitation on the cadmium to phosphorus ratio of natural phytoplankton assemblages from the Southern Ocean. Limnol Oceanogr 48:1079–1087CrossRefGoogle Scholar
  54. Dang TC, Fujii M, Rose AL, Bligh M, Waite TD (2012) Characteristics of the freshwater cyanobacterium Microcystis aeruginosa grown in iron-limited continuous culture. Appl Environ Microbiol 78:1574–1583PubMedPubMedCentralCrossRefGoogle Scholar
  55. de Baar HJW, Boyd PW, Coale KH, Landry MR, Tsuda A, Assmy P, Bakker DCE, Bozec Y, Barber RT, Brzezinski MA, Buesseler KO, Boye M, Croot PL, Gervais F, Gorbunov MY, Harrison PJ, Hiscock WT, Laan P, Lancelot C, Law CS, Levasseur M, Marchetti A, Millero FJ, Nishioka J, Nojiri Y, van Oijen T, Riebesell U, Rijkenberg MJA, Saito H, Takeda S, Timmermans KR, Veldhuis MJW, Waite AM, Wong CS (2005) Synthesis of iron fertilization experiments: from the iron age in the age of enlightenment. J Geophys Res 110:C09S16. doi: 10.1029/2004JC002601 Google Scholar
  56. Desai DK, Desai FD, LaRoche J (2012) Factors influencing the diversity of iron uptake systems in aquatic microorganisms. Front Microbiol 3:362. doi: 10.3389/fmicb.2012.00362 PubMedPubMedCentralGoogle Scholar
  57. Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Annu Rev Mar Sci 1:169–192CrossRefGoogle Scholar
  58. Doney SC, Ruckelshaus M, Emmett Duffy J, Barry JP, Chan F, English CA, Galindo HM, Grebmeier JM, Hollowed AB, Knowlton N, Polovina J, Rabalais NN, Sydeman WJ, Talley LD (2012) Climate change impacts on marine ecosystems. Annu Rev Mar Sci 4:11–37CrossRefGoogle Scholar
  59. Doucette GJ, Harrison PJ (1991) Aspects of iron and nitrogen nutrition in the red tide dinoflagellate Gymnodinium sanguineum. Mar Biol 110:165–173CrossRefGoogle Scholar
  60. Doucette GJ, Erdner DL, Peleato ML, Hartman JJ, Anderson DM (1996) Quantitative analysis of iron-stress related proteins in Thalassiosira weissflogii: measurement of flavodoxin and ferredoxin using HPLC. Mar Ecol Prog Ser 130:269–276CrossRefGoogle Scholar
  61. Droop MR (1970) Vitamin B12 and marine ecology V. Continuous culture as an approach to nutritional kinetics. Helgol Wiss Meeresun 20:629–636CrossRefGoogle Scholar
  62. Dugdale RC, Wilkerson FP (1991) Low specific nitrate uptake rate – a common feature of high-nutrient, low-chlorophyll marine ecosystems. Limnol Oceanogr 36:1678–1688CrossRefGoogle Scholar
  63. Dugdale RC, Wilkerson FP (1998) Silicate regulation of new production in the equatorial Pacific upwelling. Nature 391:270–273CrossRefGoogle Scholar
  64. Eckhardt U, Buckhout TJ (1998) Iron assimilation in Chlamydomonas reinhardtii involves ferric reduction and is similar to Strategy I higher plants. J Exp Bot 49:1219–1226Google Scholar
  65. Ehrenreich IM, Waterbury JB, Webb EA (2005) Distribution and diversity of natural product genes in marine and freshwater cyanobacterial cultures and genomes. Appl Environ Microbiol 71:7401–7413PubMedPubMedCentralCrossRefGoogle Scholar
  66. Eide D, Broderius M, Fett J, Guerinot ML (1996) A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc Natl Acad Sci 93:5624–5628PubMedPubMedCentralCrossRefGoogle Scholar
  67. Eldridge ML, Trick CG, Alm MB, DiTullio GR, Rue EL, Bruland KW, Hutchins DA, Wilhelm SW (2004) Phytoplankton community response to a manipulation of bioavailable iron in HNLC waters of the subtropical Pacific Ocean. Aquat Microb Ecol 35:79–91CrossRefGoogle Scholar
  68. Falkowski PG, Owens TG, Ley AC, Mauzerall DC (1981) Effects of growth irradiance levels on the ratio of reaction centers in 2 species of marine phytoplankton. Plant Physiol 68:969–973PubMedPubMedCentralCrossRefGoogle Scholar
  69. Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA, Schofield O, Taylor FJR (2004) The evolution of modern eukaryotic phytoplankton. Science 305:354–360PubMedCrossRefGoogle Scholar
  70. Faraldo-Gomez JD, Sansom MSP (2003) Acquisition of siderophores in gram-negative bacteria. Nat Rev Mol Cell Biol 4:105–116PubMedCrossRefGoogle Scholar
  71. Faraldo-Gomez JD, Smith GR, Sansom MSP (2003) Molecular dynamics simulations of the bacterial outer membrane protein FhuA: a comparative study of the ferrichrome-free and bound states. Biophys J 85:1406–1420PubMedPubMedCentralCrossRefGoogle Scholar
  72. Finkel ZV, Quigg AS, Raven JA, Reinfelder JR, Schofield OE, Falkowski PG (2006) Irradiance and the elemental stoichiometry of marine phytoplankton. Limnol Oceanogr 51:2690–2701CrossRefGoogle Scholar
  73. Firme GF, Rue EL, Weeks DA, Bruland KW, Hutchins DA (2003) Spatial and temporal variability in phytoplankton iron limitation along the California coast and consequences for Si, N, and C biogeochemistry. Global Biogeochem Cycles 17:1016CrossRefGoogle Scholar
  74. Fitzwater SE, Coale KH, Gordon RM, Johnson KS, Ondrusek ME (1996) Iron deficiency and phytoplankton growth in the equatorial Pacific. Deep-Sea Res II 43:995–1015CrossRefGoogle Scholar
  75. Fuhrman JA, Schwalbach MS, Stingl U (2008) Proteorhodopsins: an array of physiological roles? Nat Rev Microbiol 6:488–494PubMedGoogle Scholar
  76. Fujii M, Dang TC, Rose AL, Omura T, Waite TD (2011) Effect of light on iron uptake by the freshwater cyanobacterium Microcystis aeruginosa. Environ Sci Technol 45:1391–1398PubMedCrossRefGoogle Scholar
  77. Gademann K, Portmann C (2008) Secondary metabolites from cyanobacteria: complex structures and powerful bioactivities. Curr Org Chem 12:326–341CrossRefGoogle Scholar
  78. Gaither LA, Eide DJ (2001) Eukaryotic zinc transporters and their regulation. Biometals 14:251–270PubMedCrossRefGoogle Scholar
  79. Garcia NS, Sedwick PN, DiTullio GR (2009) Influence of irradiance and iron on the growth of colonial Phaeocystis antarctica: implications for seasonal bloom dynamics in the Ross Sea, Antarctica. Aquat Microb Ecol 57:203–220CrossRefGoogle Scholar
  80. Geider RJ (1987) Light and temperature dependence of the carbon to chlorophyll a ratio in microalgae and cyanobacteria: implications for physiology and growth of phytoplankton. New Phytol 106:1–34CrossRefGoogle Scholar
  81. Geider RJ, LaRoche J (1994) The role of iron in phytoplankton photosynthesis, and the potential for iron limitation of primary productivity in the sea. Photosynth Res 39:275–301PubMedCrossRefGoogle Scholar
  82. Geider RJ, La Roche J, Greene R, Olaizola M (1993) Response of the photosynthetic apparatus of Phaeodactylum tricornutum (Bacillariophyceae) to nitrate, phosphate or iron limitation. J Phycol 29:755–766CrossRefGoogle Scholar
  83. Gledhill M, Buck KN (2012) The organic complexation of iron in the marine environment: a review. Front Microbiol 3:69. doi: 10.3389/fmicb.2012.00069 PubMedPubMedCentralGoogle Scholar
  84. Gledhill M, van den Berg CMG (1994) Determination of complexation of iron(III) with natural organic complexing ligands in seawater using cathodic stripping voltammetry. Mar Chem 47:41–54CrossRefGoogle Scholar
  85. Glover HF (1977) Effects of iron deficiency on the physiology and biochemistry of Isochrysis galbana (Chrysophyceae) and Phaedactylum tricornutum (Bacillariophyceae). J Phycol 13:208–212Google Scholar
  86. Greene RM, Geider RJ, Falkowski PG (1991) Effect of iron limitation on photosynthesis in a marine diatom. Limnol Oceanogr 36:1772–1782CrossRefGoogle Scholar
  87. Greene RM, Geider RJ, Kolber Z, Falkowski PG (1992) Iron-induced changes in light harvesting and photochemical energy conversion processes in eukaryotic marine algae. Plant Physiol 100:565–575PubMedPubMedCentralCrossRefGoogle Scholar
  88. Groussman RD, Parker MS, Armbrust EV (2015) Diversity and evolutionary history of iron metabolism genes in diatoms. PLoS ONE 10:e0129081PubMedPubMedCentralCrossRefGoogle Scholar
  89. Guo J, Annett AL, Taylor RL, Lapi S, Ruth TJ, Maldonado MT (2010) Copper uptake kinetics of coastal and oceanic diatoms. J Phycol 46:1218–1228CrossRefGoogle Scholar
  90. Guo J, Lapi S, Ruth TJ, Maldonado MT (2012) The effects of iron and copper availability on the copper stoichiometry of marine phytoplankton. J Phycol 48:312–325CrossRefGoogle Scholar
  91. Guo J, Green BR, Maldonado MT (2015) Sequence analysis and gene expression of potential components of copper transport and homeostasis in Thalassiosira pseudonana. Protist 166:58–77PubMedCrossRefGoogle Scholar
  92. Hamm CE, Merkel R, Springer O, Jurkojc P, Maier C, Prechtel K, Smetacek V (2003) Architecture and material properties of diatom shells provide effective mechanical protection. Nature 421:841–843PubMedCrossRefGoogle Scholar
  93. Harris JE (1992) Weathering of rock, corrosion of stone and rusting of iron. Meccanica 27:233–250CrossRefGoogle Scholar
  94. Harrison PJ, Berges JA (2005) Marine culture media. In: Andersen RA (ed) Algal culturing techniques. Elsevier Academic Press, San Diego, pp 21–34Google Scholar
  95. Harrison GI, Morel FMM (1986) Response of the marine diatom Thalassiosira weissflogii to iron stress. Limnol Oceanogr 31:989–997CrossRefGoogle Scholar
  96. Harrison PJ, Whitney FA, Tsuda A, Saito H, Tadokoro K (2004) Nutrient and plankton dynamics in the NE and NW gyres of the subarctic Pacific Ocean. J Oceanogr 60:93–117CrossRefGoogle Scholar
  97. Hart TJ (1934) On the phytoplankton of the Southwest Atlantic and the Bellingshausen Sea. Discov Rep 8:1–268Google Scholar
  98. Hartnett A, Bottger LH, Matzanke BF, Carrano CJ (2012a) Iron transport and storage in the coccolithophore: Emiliania huxleyi. Metallomics 4:1160–1166PubMedCrossRefGoogle Scholar
  99. Hartnett A, Bottger LH, Matzanke BF, Carrano CJ (2012b) A multidisciplinary study of iron transport and storage in the marine green alga Tetraselmis suecica. J Inorg Biochem 116:188–194PubMedCrossRefGoogle Scholar
  100. Havens SM, Hassler CS, North RL, Guildford SJ, Silsbe G, Wilhelm SW, Twiss MR (2012) Iron plays a role in nitrate drawdown by phytoplankton in Lake Erie surface waters as observed in lake-wide assessments. Can J Fish Aquat Sci 69:369–381CrossRefGoogle Scholar
  101. Herbik A, Bolling C, Buckhout TJ (2002a) The involvement of a multicopper oxidase in iron uptake by the green algae Chlamydomonas reinhardtii. Plant Physiol 130:2039–2048PubMedPubMedCentralCrossRefGoogle Scholar
  102. Herbik A, Haebel S, Buckhout TJ (2002b) Is a ferroxidase involved in the high-affinity iron uptake in Chlamydomonas reinhardtii. Plant Soil 241:1–9CrossRefGoogle Scholar
  103. Hill KL, Merchant S (1995) Coordinate expression of coproporphyrinogen oxidase and cytochrome c6 in the green alga Chlamydomonas reinhardtii in response to changes in copper availability. EMBO J 14:857–865PubMedPubMedCentralGoogle Scholar
  104. Ho T-Y, Quigg A, Finkel ZV, Milligan AJ, Wyman K, Falkowski PG, Morel FMM (2003) The elemental composition of some marine phytoplankton. J Phycol 39:1145–1159CrossRefGoogle Scholar
  105. Hoffmann LJ, Breitbarth E, Boyd PW, Hunter KA (2012) Influence of ocean warming and acidification on trace metal biogeochemistry. Mar Ecol Prog Ser 470:191–205CrossRefGoogle Scholar
  106. Hopkinson B, Barbeau K (2008) Interactive influences of iron and light limitation on phytoplankton at subsurface chlorophyll maxima in the eastern North Pacific. Limnol Oceanogr 53:1303–1318CrossRefGoogle Scholar
  107. Hopkinson BM, Barbeau KA (2012) Iron transporters in marine prokaryotic genomes and metagenomes. Environ Microbiol 14:114–128PubMedCrossRefGoogle Scholar
  108. Hopkinson BM, Morel FMM (2009) The role of siderophores in iron acquisition by photosynthetic marine microorganisms. Biometals 22:659–669PubMedCrossRefGoogle Scholar
  109. Hopkinson BM, Xu Y, Shi D, McGinn PJ, Morel FMM (2010) The effect of CO2 on the photosynthetic physiology of phytoplankton in the Gulf of Alaska. Limnol Oceanogr 55:2011–2024CrossRefGoogle Scholar
  110. Hoppe CJM, Hassler CS, Payne CD, Tortell PD, Rost B, Trimborn S (2013) Iron limitation modulates ocean acidification effects on Southern Ocean phytoplankton communities. PLoS ONE 8:e79890PubMedPubMedCentralCrossRefGoogle Scholar
  111. Hudson RJM, Morel FMM (1989) Distinguishing between extra- and intracellular iron in marine phytoplankton. Limnol Oceanogr 34:111–1120CrossRefGoogle Scholar
  112. Hudson RJM, Morel FMM (1990) Iron transport in marine phytoplankton – kinetics of cellular and medium coordination reactions. Limnol Oceanogr 35:1002–1020CrossRefGoogle Scholar
  113. Hudson RJM, Morel FMM (1993) Trace-metal transport by marine microorganisms – implications of metal coordination kinetics. Deep-Sea Res I 40:129–150CrossRefGoogle Scholar
  114. Hutchins DA (1995) Iron and the marine phytoplankton community. Phycol Res 11:1–49Google Scholar
  115. Hutchins DA, Bruland KW (1998) Iron-limited diatom growth and Si:N uptake ratios in a coastal upwelling regime. Nature 393:561–564CrossRefGoogle Scholar
  116. Hutchins DA, DiTullio GR, Zhang Y, Bruland KW (1998) An iron limitation mosaic in the California upwelling regime. Limnol Oceanogr 43:1037–1054CrossRefGoogle Scholar
  117. Hutchins DA, Franck VM, Brzezinski MA, Bruland KW (1999a) Inducing phytoplankton iron limitation in iron-replete coastal waters with a strong chelating ligand. Limnol Oceanogr 44:1009–1018CrossRefGoogle Scholar
  118. Hutchins DA, Witter AE, Butler A, Luther GW (1999b) Competition among marine phytoplankton for different chelated iron species. Nature 400:858–861CrossRefGoogle Scholar
  119. Hutchins DA, Hare CE, Weaver RS, Zhang Y, Firme GF, DiTullio GR, Alm MB, Riseman SF, Maucher JM, Geesey ME (2002) Phytoplankton iron limitation in the Humboldt Current and Peru Upwelling. Limnol Oceanogr 47:997–1011CrossRefGoogle Scholar
  120. Hyenstrand P, Rydin E, Gunnerhed M (2000) Response of pelagic cyanobacteria to iron additions – enclosure experiments from Lake Erken. J Plankton Res 22:1113–1126CrossRefGoogle Scholar
  121. Ito Y, Butler A (2005) Structure of synechobactins, new siderophores of the marine cyanobacterium Synechococcus sp. PCC 7002. Limnol Oceanogr 50:1918CrossRefGoogle Scholar
  122. Johnson KS, Gordon RM, Coale KH (1997) What controls dissolved iron concentrations in the world ocean? Mar Chem 57:137–161CrossRefGoogle Scholar
  123. Johnson KS, Chavez FP, Friederich GE (1999) Continental-shelf sediment as a primary source of iron for coastal phytoplankton. Nature 398:697–700CrossRefGoogle Scholar
  124. Jones GJ, Palenik BP, Morel FMM (1987) Trace metal reduction by phytoplankton: the role of plasmalemma redox enzymes. J Phycol 23:237–244CrossRefGoogle Scholar
  125. Katoh H, Hagino N, Grossman AR, Ogawa T (2001a) Genes essential to iron transport in the cyanobacterium Synechocystis sp strain PCC 6803. J Bacteriol 183:2779–2784PubMedPubMedCentralCrossRefGoogle Scholar
  126. Katoh H, Hagino N, Ogawa T (2001b) Iron-binding activity of FutA1 subunit of an ABC-type iron transporter in the cyanobacterium Synechocystis sp strain PCC 6803. Plant Cell Physiol 42:823–827PubMedCrossRefGoogle Scholar
  127. Klunder MB, Bauch D, Laan P, de Baar HJW, van Heuven S, Ober S (2012) 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 117:C01027Google Scholar
  128. Koch F, Marcoval MA, Panzeca C, Bruland KW, Sanudo-Wilhelmy SA, Gobler CJ (2011) The effect of vitamin B12 on phytoplankton growth and community structure in the Gulf of Alaska. Limnol Oceanogr 56:1023–1034CrossRefGoogle Scholar
  129. Kranzler C, Lis H, Shaked Y, Keren N (2011) The role of reduction in iron uptake processes in a unicellular, planktonic cyanobacterium. Environ Microbiol 13:2990–2999PubMedCrossRefGoogle Scholar
  130. Kranzler C, Rudolf M, Keren N, Schleiff E (2013) Iron in cyanobacteria. Adv Bot Res 65:57–105CrossRefGoogle Scholar
  131. Kranzler C, Lis H, Finkel OM, Schmetterer G, Shaked Y, Keren N (2014) Coordinated transporter activity shapes high-affinity iron acquisition in cyanobacteria. ISME J 8:409–417PubMedPubMedCentralCrossRefGoogle Scholar
  132. Krewulak KD, Vogel HJ (2011) TonB or not TonB: is that the question? Biochem Cell Biol 89:87–97PubMedCrossRefGoogle Scholar
  133. Kudo I, Harrison PJ (1997) Effect of iron nutrition on the marine cyanobacterium Synechococcus grown on different N sources and irradiances. J Phycol 33:232–240CrossRefGoogle Scholar
  134. Kudo I, Noiri Y, Nishioka J, Taira Y, Kiyosawa H, Tsuda A (2006) Phytoplankton community response to Fe and temperature gradients in the NE (SERIES) and NW (SEEDS) subarctic Pacific Ocean. Deep Sea Res II 53:2201–2213CrossRefGoogle Scholar
  135. Kuma K et al (1992) Photo-reduction of Fe (III) by dissolved organic substances and existence of Fe (II) in seawater during spring blooms. Mar Chem 37:15–27CrossRefGoogle Scholar
  136. Kustka AB, Sanudo-Wilhemy SA, Carpenter EJ, Capone D, Burns J, Sunda WG (2003) Iron requirements for dinitrogen- and ammonium-supported growth in cultures of Trichodesmium (IMS 101): comparison with nitrogen fixation rates and iron:carbon ratios of field populations. Limnol Oceanogr 48:1869–1884CrossRefGoogle Scholar
  137. Kustka AB, Allen AE, Morel FMM (2007) Sequence analysis and transcriptional regulation of iron acquisition genes in two marine diatoms. J Phycol 43:715–729CrossRefGoogle Scholar
  138. La Fontaine S, Quinn JM, Nakamoto SS, Page MD, Gohre V, Moseley JL, Kropat J, Merchant S (2002) Copper-dependent iron assimilation pathway in the model photosynthetic eukaryote Chlamydomonas reinhardtii. Eukaryot Cell 1:736–757PubMedPubMedCentralCrossRefGoogle Scholar
  139. La Roche J, Geider RJ, Graziano LM, Murray H, Lewis K (1993) Induction of specific proteins in eukaryotic algae grown under iron-deficient, phosphorus-deficient, or nitrogen-deficient conditions. J Phycol 29:767–777CrossRefGoogle Scholar
  140. La Roche J, Boyd P, McKay R, Geider R (1996) Flavodoxin as an in situ marker for iron stress in phytoplankton. Nature 382:802–805CrossRefGoogle Scholar
  141. Lane ES, Semeniuk DM, Strzepek RF, Cullen JT, Maldonado MT (2009) Effects of iron limitation on intracellular cadmium of cultured phytoplankton: implications for surface dissolved cadmium to phosphate ratios. Mar Chem 115:155–162CrossRefGoogle Scholar
  142. Lelong A, Bucciarelli E, Hagaret H, Soudant P (2013) Iron and copper limitations differently affect growth rates and photosynthetic and physiological parameters of the marine diatom Pseudo-nitzschia delicatissima. Limnol Oceanogr 58:613–623Google Scholar
  143. Lin W, Chai J, Love J, Fu D (2010) Selective electrodiffusion of zinc ions in a Zrt-, Irt-like protein, ZIPB. J Biol Chem 285:39013–39020PubMedPubMedCentralCrossRefGoogle Scholar
  144. Lin H, Rauschenberg S, Hexel CR, Shaw TJ, Twining BS (2011) Free-drifting icebergs as sources of iron to the Weddell Sea. Deep Sea Res II 58:1392–1406CrossRefGoogle Scholar
  145. Lis H, Shaked Y (2009) Probing the bioavailability of organically bound iron: a case study in the Synechococcus-rich waters of the Gulf of Aqaba. Aquat Microb Ecol 56:241–253CrossRefGoogle Scholar
  146. Lis H, Shaked Y, Kranzler C, Keren N, Morel FMM (2015) Iron bioavailability to phytoplankton: an empirical approach. ISME J 9:1003–1013PubMedCrossRefGoogle Scholar
  147. Liu XW, Theil EC (2005) Ferritins: dynamic management of biological iron and oxygen chemistry. Acc Chem Res 38:167–175PubMedCrossRefGoogle Scholar
  148. Lohan MC, Bruland KW (2008) Elevated Fe(II) and dissolved Fe in hypoxic shelf waters off Oregon and Washington: an enhanced source of iron to coastal upwelling regimes. Environ Sci Technol 42:6462–6468PubMedCrossRefGoogle Scholar
  149. Lommer M, Roy A, Schilhabel M, Schreiber S, Rosenstiel P, LaRoche J (2010) Recent transfer of an iron-regulated gene from the plastid to the nuclear genome in an oceanic diatom adapted to chronic iron limitation. BMC Genomics 11:718PubMedPubMedCentralCrossRefGoogle Scholar
  150. Lommer M, Specht M, Roy A-S, Kraemer L, Andreson R, Gutowska M, Wolf J, Bergner S, Schilhabel M, Klostermeier U, Beiko R, Rosenstiel P, Hippler M, LaRoche J (2012) Genome and low-iron response of an oceanic diatom adapted to chronic iron limitation. Genome Biol 13:R66PubMedPubMedCentralCrossRefGoogle Scholar
  151. Mahowald NM, Baker AR, Bergametti G, Brooks N, Duce RA, Jickells TD, Kubilay N, Prospero JM, Tegen I (2005) Atmospheric global dust cycle and iron inputs to the ocean. Glob Biogeochem Cycles 19:GB4025Google Scholar
  152. Maldonado MT, Price NM (1996) Influence of N substrate on Fe requirements of marine centric diatoms. Mar Ecol Prog Ser 141:161–172CrossRefGoogle Scholar
  153. Maldonado MT, Price NM (1999) Utilization of iron bound to strong organic ligands by plankton communities in the subarctic Pacific Ocean. Deep Sea Res II 46:2447–2473CrossRefGoogle Scholar
  154. Maldonado MT, Price NM (2000) Nitrate regulation of Fe reduction and transport by Fe-limited Thalassiosira oceanica. Limnol Oceanogr 45:814–826CrossRefGoogle Scholar
  155. Maldonado MT, Price NM (2001) Reduction and transport of organically bound iron by Thalassiosira oceanica (Bacillariophyceae). J Phycol 37:298–309CrossRefGoogle Scholar
  156. Maldonado MT, Boyd PW, Harrison PJ, Price NM (1999) Co-limitation of phytoplankton growth by light and Fe during winter in the NE subarctic Pacific Ocean. Deep Sea Res II 46:2475–2485CrossRefGoogle Scholar
  157. Maldonado MT, Boyd PW, LaRoche J, Strzepek R, Waite A, Bowie AR, Croot PL, Frew RD, Price NM (2001) Iron uptake and physiological response of phytoplankton during a mesoscale Southern Ocean iron enrichment. Limnol Oceanogr 46:1802–1808CrossRefGoogle Scholar
  158. Maldonado MT, Strzepek RF, Sander S, Boyd PW (2005) Acquisition of iron bound to strong organic complexes, with different Fe binding groups and photochemical reactivities, by plankton communities in Fe-limited subantarctic waters. Glob Biogeochem Cycles 19:GB4S23CrossRefGoogle Scholar
  159. Maldonado MT, Allen AE, Chong JS, Lin K, Leus D, Karpenko N, Harris SL (2006) Copper-dependent iron transport in coastal and oceanic diatoms. Limnol Oceanogr 51:1729–1743CrossRefGoogle Scholar
  160. Maranger R, Bird DF, Price NM (1998) Iron acquisition by photosynthetic marine phytoplankton from ingested bacteria. Nature 396:248–251CrossRefGoogle Scholar
  161. Marchetti A, Cassar N (2009) Diatom elemental and morphological changes in response to iron limitation: a brief review with potential paleoceanographic applications. Geobiology 7:419–431PubMedCrossRefGoogle Scholar
  162. Marchetti A, Harrison PJ (2007) Coupled changes in the cell morphology and the elemental (C, N and Si) composition of the pennate diatom Pseudo-nitzschia due to iron deficiency. Limnol Oceanogr 52:2270–2284CrossRefGoogle Scholar
  163. Marchetti A, Maldonado MT, Lane ES, Harrison PJ (2006) Iron requirements of the pennate diatom Pseudo-nitzschia: comparison of oceanic (HNLC) and coastal species. Limnol Oceanogr 51:2092–2101CrossRefGoogle Scholar
  164. Marchetti A, Lundholm N, Kotaki Y, Hubbard KA, Harrison PJ, Armbrust EV (2008) Identification and assessment of domoic acid production in oceanic Pseudo-nitzschia (Bacillariophyceae) from iron-limited waters in the NE Subarctic Pacific. J Phycol 44:650–661CrossRefGoogle Scholar
  165. Marchetti A, Parker MS, Moccia LP, Lin EO, Arrieta AL, Ribalet F, Murphy MEP, Maldonado MT, Armbrust EV (2009) Ferritin is used for iron storage in bloom-forming marine pennate diatoms. Nature 457:467–470PubMedCrossRefGoogle Scholar
  166. Marchetti A, Varela DE, Lance VP, Johnson Z, Palmucci M, Giordano M, Armbrust EV (2010) Iron and silicic acid effects on phytoplankton productivity, diversity, and chemical composition in the central equatorial Pacific Ocean. Limnol Oceanogr 55:11–29CrossRefGoogle Scholar
  167. Marchetti A, Schruth DM, Durkin CA, Parker MS, Kodner RB, Berthiaume CT, Morales R, Allen AE, Armbrust EV (2012) Comparative metatranscriptomics identifies molecular bases for the physiological responses of phytoplankton to varying iron availability. Proc Natl Acad Sci 109:E317–E325PubMedPubMedCentralCrossRefGoogle Scholar
  168. Marchetti A, Catlett D, Hopkinson BM, Ellis K, Cassar N (2015) Marine diatom proteorhodopsins and their potential role in coping with low iron availability. ISME J. doi: 10.1038/ismej.2015.74 PubMedGoogle Scholar
  169. Martin JH (1990) Glacial-interglacial CO2 change: the iron hypothesis. Paleoceanography 5:1–13CrossRefGoogle Scholar
  170. Martin JH, Fitzwater S (1988) Iron deficiency limits phytoplankton growth in the north-east Pacific subarctic. Nature 331:341–343CrossRefGoogle Scholar
  171. Martin JH, Gordon RM, Fitzwater S, Broenkow WW (1989) Vertex – phytoplankton iron studies in the Gulf of Alaska. Deep Sea Res I 36:649–680CrossRefGoogle Scholar
  172. Martinez JS, Carter-Franklin JN, Mann EL, Martin JD, Haygood MG, Butler A (2003) Structure and membrane affinity of a suite of amphiphilic siderophores produced by a marine bacterium. Proc Natl Acad Sci 100:3754–3759PubMedPubMedCentralCrossRefGoogle Scholar
  173. Matz CJ, Magnus RS, Walker CN, Fink MB, Treble RG, Weger HG (2006) Differences between two green algae in biological availability of iron bound to strong chelators. Can J Bot 84:400–411CrossRefGoogle Scholar
  174. Mawji E, Gledhill M, Milton JA, Tarran GA, Ussher S, Thompson A, Wolff GA, Worsfold PJ, Achterberg EP (2008) Hydroxamate siderophores: occurrence and importance in the Atlantic Ocean. Environ Sci Technol 42:8675–8680PubMedCrossRefGoogle Scholar
  175. McAllister CD, Parsons TR, Strickland JDH (1960) Primary productivity and fertility at Station P in the north-east Pacific Ocean. ICES J Mar Sci 25:240–259CrossRefGoogle Scholar
  176. Merchant SS, Allen MD, Kropat J, Moseley JL, Long JC, Tottey S, Terauchi AM (2006) Between a rock and a hard place: trace element nutrition in Chlamydomonas. Biochim Biophys Acta, Mol Cell Res 1763:578–594PubMedCrossRefGoogle Scholar
  177. Middlemiss JK, Anderson AM, Stratilo CW, Weger HG (2001) Oxygen consumption associated with ferric reductase activity and iron uptake by iron-limited cells of Chlorella kessleri (Chlorophyceae). J Phycol 37:393–399CrossRefGoogle Scholar
  178. Miethke M, Marahiel MA (2007) Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev 71:413–451PubMedPubMedCentralCrossRefGoogle Scholar
  179. Miller CB, Frost BW, Wheeler PA, Landry MR, Welschmeyer N, Powell TM (1991) Ecological dynamics in the subarctic Pacific, a possibly iron-limited ecosystem. Limnol Oceanogr 36:1600–1615CrossRefGoogle Scholar
  180. Millero FJ, Woosley R, DiTrolio BJW (2009) Effect of ocean acidification on the speciation of metals in seawater. Oceanography 22:72–85CrossRefGoogle Scholar
  181. Milligan AJ, Harrison PJ (2000) Effects of non-steady-state iron limitation on nitrogen assimilatory enzymes in the marine diatom Thalassiosira weissflogii (Bacillariophyceae). J Phycol 36:78–86CrossRefGoogle Scholar
  182. Mills MM, Ridame C, Davey M, La Roche J, Geider RJ (2004) Iron and phosphorus co-limit nitrogen fixation in the eastern tropical North Atlantic. Nature 429:292–294PubMedCrossRefGoogle Scholar
  183. Mirus O, Strauss S, Nicolaisen K, von Haeseler A, Schleiff E (2009) TonB-dependent transporters and their occurrence in cyanobacteria. BMC Biol 7:68PubMedPubMedCentralCrossRefGoogle Scholar
  184. Mitchell BG, Brody EA, Holm-Hansen O, McClain C, Bishop J (1991) Light limitation of phytoplankton biomass and macronutrient utilization in the Southern Ocean. Limnol Oceanogr 36:1662–1677CrossRefGoogle Scholar
  185. Mock T, Samanta MP, Iverson V, Berthiaume C, Robison M, Holtermann K, Durkin C, BonDurant SS, Richmond K, Rodesch M, Kallas T, Huttlin EL, Cerrina F, Sussmann MR, Armbrust EV (2008) Whole-genome expression profiling of the marine diatom Thalassiosira pseudonana identifies genes involved in silicon bioprocesses. Proc Natl Acad Sci U S A 105:1579–1584PubMedPubMedCentralCrossRefGoogle Scholar
  186. Monod J (1942) Recherches sur la croissance des Cultures Bactériennes. Hermann, ParisGoogle Scholar
  187. Monzyk B, Crumbliss AL (1982) Kinetics and mechanism of the stepwise dissociation of iron(III) from ferrioxamine B in aqueous acid. J Am Chem Soc 104:4921–4929CrossRefGoogle Scholar
  188. Moore JK, Braucher O (2008) Sedimentary and mineral dust sources of dissolved iron to the world ocean. Biogeosciences 5:631–656CrossRefGoogle Scholar
  189. Moore JK, Doney SC, Glover DM, Fung IY (2002) Iron cycling and nutrient-limitation patterns in surface waters of the World Ocean. Deep Sea Res II 49:463–507CrossRefGoogle Scholar
  190. Moore CM, Mills MM, Achterberg EP, Geider RJ, LaRoche J, Lucas MI, McDonagh EL, Pan X, Poulton AJ, Rijkenberg MJA, Suggett DJ, Ussher SJ, Woodward EMS (2009) Large-scale distribution of Atlantic nitrogen fixation controlled by iron availability. Nat Geosci 2:867–871CrossRefGoogle Scholar
  191. Morel FMM (1987) Kinetics of nutrient uptake and growth in phytoplankton. J Phycol 23:137–150CrossRefGoogle Scholar
  192. Morel FMM, Hudson R, Price N (1991) Limitation of productivity by trace metals in the sea. Limnol Oceanogr 36:1742–1755CrossRefGoogle Scholar
  193. Morrissey J, Bowler C (2012) Iron utilization in marine cyanobacteria and eukaryotic algae. Front Microbiol 3:43. doi: 10.3389/fmicb.2012.00043 PubMedPubMedCentralGoogle Scholar
  194. Morton SD, Lee TH (1974) Algal blooms. Possible effects of iron. Environ Sci Technol 8:673–674CrossRefGoogle Scholar
  195. Moseley JL, Allinger T, Herzog S, Hoerth P, Wehinger E, Merchant S, Hippler M (2002) Adaptation to Fe-deficiency requires remodeling of the photosynthetic apparatus. EMBO J 21:6709–6720PubMedPubMedCentralCrossRefGoogle Scholar
  196. Muggli DL, Harrison PJ (1996a) EDTA suppresses the growth of oceanic phytoplankton from the Northeast subarctic Pacific. J Exp Mar Biol Ecol 205:221–227CrossRefGoogle Scholar
  197. Muggli DL, Harrison PJ (1996b) Effects of nitrogen source on the physiology and metal nutrition of Emiliania huxleyi grown under different iron and light conditions. Mar Ecol Prog Ser 130:255–267CrossRefGoogle Scholar
  198. Muggli DL, Lecourt M, Harrison PJ (1996) Effects of iron and nitrogen source on the sinking rate, physiology and metal composition of an oceanic diatom from the subarctic Pacific. Mar Ecol Prog Ser 132:215–227CrossRefGoogle Scholar
  199. Neilands JB (1995) Siderophores: structure and function of microbial iron transport compounds. J Biol Chem 270:26723–26726PubMedCrossRefGoogle Scholar
  200. Nelson DM, Treguer P, Brzezinski MA, Leynaert A, Queguiner B (1995) Production and dissolution of biogenic silica in the ocean: revised global estimates, comparison with regional data and relationships to biogenic sedimentation. Glob Biogeochem Cycles 9:359–372CrossRefGoogle Scholar
  201. Nevo Y, Nelson N (2006) The NRAMP family of metal-ion transporters. Biochim Biophys Acta Mol Cell Res 1763:609–620CrossRefGoogle Scholar
  202. Nicolaisen K, Moslavac S, Samborski A, Valdebenito M, Hantke K, Maldener I, Muro-Pastor AM, Flores E, Schleiff E (2008) Alr0397 is an outer membrane transporter for the siderophore schizokinen in Anabaena sp. strain PCC 7120. J Bacteriol 190:7500–7507PubMedPubMedCentralCrossRefGoogle Scholar
  203. Nicolaisen K, Hahn A, Valdebenito M, Moslavac S, Samborski A, Maldener I, Wilken C, Valladares A, Flores E, Hantke K (2010) The interplay between siderophore secretion and coupled iron and copper transport in the heterocyst-forming cyanobacterium Anabaena sp. PCC 7120. Biochim Biophys Acta Biomembr 1798:2131–2140CrossRefGoogle Scholar
  204. Nishioka J, Takeda S (2000) Change in the concentrations of iron in different size fractions during growth of the oceanic diatom Chaetoceros sp.: importance of small colloidal iron. Mar Biol 137:231–238CrossRefGoogle Scholar
  205. Noinaj N, Guillier M, Barnard TJ, Buchanan SK (2010) TonB-dependent transporters: regulation, structure, and function. I Ann Rev Microbiol 64:43–60CrossRefGoogle Scholar
  206. North RL, Guildford SJ, Smith REH, Havens SM, Twiss MR (2007) Evidence for phosphorus, nitrogen, and iron colimitation of phytoplankton communities in Lake Erie. Limnol Oceanogr 52:315–328CrossRefGoogle Scholar
  207. Nouet C, Motte P, Hanikenne M (2011) Chloroplastic and mitochondrial metal homeostasis. Trends Plant Sci 16:395–404PubMedCrossRefGoogle Scholar
  208. Nuester J, Vogt S, Twining BS (2012) Localization of iron within centric diatoms of the genus Thalassiosira. J Phycol 48:626–634CrossRefGoogle Scholar
  209. Palenik B, Ren Q, Dupont CL, Myers GS, Heidelberg JF, Badger JH, Madupu R, Nelson WC, Brinkac LM, Dodson RJ (2006) Genome sequence of Synechococcus CC9311: insights into adaptation to a coastal environment. Proc Natl Acad Sci 103:13555–13559PubMedPubMedCentralCrossRefGoogle Scholar
  210. Palenik B, Grimwood J, Aerts A, Rouze P, Salamov A, Putnam N, Dupont C, Jorgensen R, Derelle E, Rombauts S, Zhou K, Otillar R, Merchant SS, Podell S, Gaasterland T, Napoli C, Gendler K, Manuell A, Tai V, Vallon O, Piganeau G, Sv J, Heijde M, Jabbari K, Bowler C, Lohr M, Robbens S, Werner G, Dubchak I, Pazour GJ, Ren Q, Paulsen I, Delwiche C, Schmutz J, Rokhsar D, Van de Peer Y, Moreau H, Grigoriev IV (2007) The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation. Proc Natl Acad Sci 104:7705–7710PubMedPubMedCentralCrossRefGoogle Scholar
  211. Pankowski A, McMinn A (2009) Iron availability regulates growth, photosynthesis, and production of ferredoxin and flavodoxin in Antarctic sea ice diatoms. Aquat Biol 4:273–288CrossRefGoogle Scholar
  212. Passy SI (2010) A distinct latitudinal gradient of diatom diversity is linked to resource supply. Ecology 91:36–41PubMedCrossRefGoogle Scholar
  213. Paz Y, Katz A, Pick U (2007a) Multicopper ferroxidase involved in iron binding to transferrins in Dunaliella salina plasma membranes. J Biol Chem 282:8658–8666PubMedCrossRefGoogle Scholar
  214. Paz Y, Shimoni E, Weiss M, Pick U (2007b) Effects of iron deficiency on iron binding and internalization into acidic vacuoles in Dunaliella salina. Plant Physiol 144:1407–1415PubMedPubMedCentralCrossRefGoogle Scholar
  215. Peers G, Price N (2006) Copper-containing plastocyanin used for electron transport by an oceanic diatom. Nature 441:341–344PubMedCrossRefGoogle Scholar
  216. Peers G, Quesnel SA, Price NM (2005) Copper requirements for iron acquisition and growth of coastal and oceanic diatoms. Limnol Oceanogr 50:1149–1158CrossRefGoogle Scholar
  217. Pollard RT, Salter I, Sanders RJ, Lucas MI, Moore CM, Mills RA, Statham PJ, Allen JT, Baker AR, Bakker DCE, Charette MA, Fielding S, Fones GR, French M, Hickman AE, Holland RJ, Hughes JA, Jickells TD, Lampitt RS, Morris PJ, Nedelec FH, Nielsdottir M, Planquette H, Popova EE, Poulton AJ, Read JF, Seeyave S, Smith T, Stinchcombe M, Taylor S, Thomalla S, Venables HJ, Williamson R, Zubkov MV (2009) Southern Ocean deep-water carbon export enhanced by natural iron fertilization. Nature 457:577–580PubMedCrossRefGoogle Scholar
  218. Pollingher U, Kaplan B, Berman T (1995) The impact of iron and chelators on Lake Kinneret phytoplankton. J Plankton Res 17:1977–1992CrossRefGoogle Scholar
  219. Pondaven P, Gallinari M, Chollet S, Bucciarelli E, Sarthou G, Schultes S, Jean F (2007) Grazing-induced changes in cell wall silicification in a marine diatom. Protist 158:21–28PubMedCrossRefGoogle Scholar
  220. Price NM (2005) The elemental stoichiometry and composition of an iron-limited diatom. Limnol Oceanogr 50:1159–1171CrossRefGoogle Scholar
  221. Price NM, Harrison GI, Hering JG, Hudson RJ, Nirel PMV, Palenik B, Morel FMM (1988/89) Preparation and chemistry of the artificial algal culture medium Aquil. Biol Oceanogr 6:443–461Google Scholar
  222. Price NM, Andersen LF, Morel FMM (1991) Iron and nitrogen nutrition of Equatorial Pacific plankton. Deep Sea Res II 38:1361–1378CrossRefGoogle Scholar
  223. Price NM, Ahner BA, Morel FMM (1994) The Equatorial Pacific Ocean – grazer-controlled phytoplankton populations in an iron-limited ecosystem. Limnol Oceanogr 39:520–534CrossRefGoogle Scholar
  224. Quigg A, Finkel ZV, Irwin AJ, Rosenthal Y, Ho TY, Reinfelder JR, Schofield O, Morel FMM, Falkowski PG (2003) The evolutionary inheritance of elemental stoichiometry in marine phytoplankton. Nature 425:291–294PubMedCrossRefGoogle Scholar
  225. Quigg A, Irwin AJ, Finkel ZV (2011) Evolutionary inheritance of elemental stoichiometry in phytoplankton. Proc Roy Soc B 278:526–534CrossRefGoogle Scholar
  226. Raiswell R, Benning L, Tranter M, Tulaczyk S (2008) Bioavailable iron in the Southern Ocean: the significance of the iceberg conveyor belt. Geochem Trans 9:7PubMedPubMedCentralCrossRefGoogle Scholar
  227. Raven JA (1988) The iron and molybdenum use efficiencies of plant growth with different energy, carbon and nitrogen sources. New Phytol 109:279–287CrossRefGoogle Scholar
  228. Raven JA (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 116:1–18CrossRefGoogle Scholar
  229. Raven JA, Waite A (2004) The evolution of silicification in diatoms: inescapable sinking and sinking as escape. New Phytol 162:45–65CrossRefGoogle Scholar
  230. Rose AL (2012) The influence of extracellular superoxide on iron redox chemistry and bioavailability to aquatic microorganisms. Front Microbiol 3:124. doi: 10.3389/fmicb.2012.00124 PubMedPubMedCentralGoogle Scholar
  231. Rue EL, Bruland KW (1995) 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 50:117–138CrossRefGoogle Scholar
  232. Rueter JG, Ades DR (1987) The role of iron nutrition in photosynthesis and nitrogen assimilation in Scenedesmus quadricauda (Chlorophyceae). J Phycol 23:452–457CrossRefGoogle Scholar
  233. Ryan-Keogh TJ, Macey AI, Cockshutt AM, Moore CM, Bibby TS (2012) The cyanobacterial chlorophyll-binding-protein isiA acts to increase the in vivo effective absorption cross-section of PSI under iron limitation. J Phycol 48:145–154CrossRefGoogle Scholar
  234. Saito MA, Rocap G, Moffett JW (2005) Production of cobalt binding ligands in a Synechococcus feature at the Costa Rica upwelling dome. Limnol Oceanogr 50:279–290CrossRefGoogle Scholar
  235. Saito MA, Goepfert TJ, Ritt JT (2008) Some thoughts on the concept of colimitation: three definitions and the importance of bioavailability. Limnol Oceanogr 53:276–290CrossRefGoogle Scholar
  236. Saito MA, Noble AE, Tagliabue A, Goepfert TJ, Lamborg CH, Jenkins WJ (2013) Slow-spreading submarine ridges in the South Atlantic as a significant oceanic iron source. Nat Geosci 6:775–779CrossRefGoogle Scholar
  237. Sandmann G, Reck H, Kessler E, Boger P (1983) Distribution of plastocyanin and soluble plastidic cytochrome c in various classes of algae. Arch Microbiol 134:23–27CrossRefGoogle Scholar
  238. Sandmann G, Peleato ML, Fillat MF, Lazaro MC, Gomez-Moreno C (1990) Consequences of the iron-dependent formation of ferredoxin and flavodoxin on photosynthesis and nitrogen fixation on Anabaena strains. Photosynth Res 26:119–125PubMedCrossRefGoogle Scholar
  239. Schauer K, Rodionov DA, de Reuse H (2008) New substrates for TonB-dependent transport: do we only see the “tip of the iceberg”? Trends Biochem Sci 33:330–338PubMedCrossRefGoogle Scholar
  240. Schenck RC, Tessier A, Campbell PGC (1988) The effect of pH on iron and manganese uptake by a green alga. Limnol Oceanogr 33:538–550CrossRefGoogle Scholar
  241. Sedwick PN, Garcia N, Riseman S, Marsay C, DiTullio G (2007) Evidence for high iron requirements of colonial Phaeocystis antarctica at low irradiance. Biogeochemistry 83:83–97CrossRefGoogle Scholar
  242. Shaked Y, Lis H (2012) Disassembling iron availability to phytoplankton. Front Microbiol 3:123. doi: 10.3389/fmicb.2012.00123 PubMedPubMedCentralGoogle Scholar
  243. Shaked Y, Kustka A, Morel F (2005) A general kinetic model for iron acquisition by eukaryotic phytoplankton. Limnol Oceanogr 50:872–882CrossRefGoogle Scholar
  244. Sherman DM, Sherman LA (1983) Effect of iron deficiency and iron restoration on ultrastructure of Anacystis nidulans. J Bacteriol 156:393–401PubMedPubMedCentralGoogle Scholar
  245. Shi D, Xu Y, Hopkinson BM, Morel FMM (2010) Effect of ocean acidification on iron availability to marine phytoplankton. Science 327:676–679PubMedCrossRefGoogle Scholar
  246. Shi D, Kranz SA, Kim J-M, Morel FMM (2012) Ocean acidification slows nitrogen fixation and growth in the dominant diazotroph Trichodesmium under low-iron conditions. Proc Natl Acad Sci 109:E3094–E3100PubMedPubMedCentralCrossRefGoogle Scholar
  247. Silva-Stenico ME, Silva CS, Lorenzi AS, Shishido TK, Etchegaray A, Lira SP, Moraes LA, Fiore MF (2011) Non-ribosomal peptides produced by Brazilian cyanobacterial isolates with antimicrobial activity. Microb Res 166:161–175CrossRefGoogle Scholar
  248. Simpson FB, Neilands JB (1976) Siderochromes in cyanophyceae: isolation and characterization of schizokinen from Anabaena sp. J Phycol 12:44–48Google Scholar
  249. Smayda TJ (1970) The suspension and sinking of phytoplankton in the sea. Oceanogr Mar Biol Ann Rev 8:353–414Google Scholar
  250. Smetacek V (1985) Role of sinking in diatom life history cycles: ecological, evolutionary and geological significance. Mar Biol 84:239–251CrossRefGoogle Scholar
  251. Smetacek V (1999) Diatoms and the ocean carbon cycle. Protist 150:25–32PubMedCrossRefGoogle Scholar
  252. Smetacek V, Assmy P, Henjes J (2004) The role of grazing in structuring Southern Ocean pelagic ecosystems and biogeochemical cycles. Antarct Sci 16:541–558CrossRefGoogle Scholar
  253. Smetacek V, Klaas C, Strass VH, Assmy P, Montresor M, Cisewski B, Savoye N, Webb A, d’Ovidio F, Arrieta JM, Bathmann U, Bellerby R, Berg GM, Croot P, Gonzalez S, Henjes J, Herndl GJ, Hoffmann LJ, Leach H, Losch M, Mills MM, Neill C, Peeken I, Rottgers R, Sachs O, Sauter E, Schmidt MM, Schwarz J, Terbruggen A, Wolf-Gladrow D (2012) Deep carbon export from a Southern Ocean iron-fertilized diatom bloom. Nature 487:313–319Google Scholar
  254. Smith K, Robison B, Helly J, Kaufmann R, Ruhl H, Shaw T, Twining B, Vernat M (2007) Free-drifting icebergs: hot spots of chemical and biological enrichment in the Weddell Sea. Science 317:478–483PubMedCrossRefGoogle Scholar
  255. Sohm JA, Webb EA, Capone DG (2011) Emerging patterns of marine nitrogen fixation. Nat Rev Microbiol 9:499–508PubMedCrossRefGoogle Scholar
  256. Soria-Dengg S, Horstmann U (1995) Ferroxiamines B and E as iron source for the marine diatom Phaeodactylum tricornutum. Mar Ecol Prog Ser 127:269–277CrossRefGoogle Scholar
  257. Stearman R, Yuan DS, Yamaguchi-Iwai Y, Klausner RD, Dancis A (1996) A permease-oxidase complex involved in high-affinity iron uptake in yeast. Science 271:1552–1557PubMedCrossRefGoogle Scholar
  258. Sterner RW, Smutka TM, McKay RM, Xiaoming Q, Brown ET, Sherrel R (2004) Phosphorus and trace metal limitation of algae and bacteria in Lake Superior. Limnol Oceanogr 49:495–507CrossRefGoogle Scholar
  259. Stevanovic M, Hahn A, Nicolaisen K, Mirus O, Schleiff E (2012) The components of the putative iron transport system in the cyanobacterium Anabaena sp. PCC 7120. Environ Microbiol 14:1655–1670PubMedCrossRefGoogle Scholar
  260. Straus N (2004) Iron deprivation: physiology and gene regulation. In: Bryant D (ed) The molecular biology of cyanobacteria, Book 1. Springer, Dordrecht, pp 731–750CrossRefGoogle Scholar
  261. Strong A, Chisholm S, Miller C, Cullen J (2009) Ocean fertilization: time to move on. Nature 461:347–348PubMedCrossRefGoogle Scholar
  262. Strzepek R, Harrison P (2004) Photosynthetic architecture differs in coastal and oceanic diatoms. Nature 431:689–692PubMedCrossRefGoogle Scholar
  263. Strzepek RF, Price NM (2000) Influence of irradiance and temperature on the iron content of the marine diatom Thalassiosira weissflogii (Bacillariophyceae). Mar Ecol Prog Ser 206:107–117CrossRefGoogle Scholar
  264. Strzepek RF, Maldonado MT, Hunter KAFDR, Boyd PW (2011) Adaptive strategies by Southern Ocean phytoplankton to lessen iron limitation: uptake of organically complexed iron and reduced cellular iron requirements. Limnol Oceanogr 56:1983–2002CrossRefGoogle Scholar
  265. Strzepek RF, Hunter KA, Frew RD, Harrison PJ, Boyd PW (2012) Iron-light interactions in Southern Ocean phytoplankton. Limnol Oceanogr 57:1182–1200CrossRefGoogle Scholar
  266. Sugie K, Yoshimura T (2013) Effects of pCO2 and iron on the elemental composition and cell geometry of the marine diatom Pseudo-nitzschia pseudodelicatissima (Bacillariophyceae). J Phycol 49:475–488CrossRefGoogle Scholar
  267. Sugie K, Endo H, Suzuki K, Nishioka J, Kiyosawa H, Yoshimura T (2013) Synergistic effects of pCO2 and iron availability on nutrient consumption ratio of the Bering Sea phytoplankton community. Biogeosciences 10:6309–6321CrossRefGoogle Scholar
  268. Sunda WG, Huntsman SA (1992) Feedback interactions between zinc and phytoplankton in seawater. Limnol Oceanogr 37:25–40CrossRefGoogle Scholar
  269. Sunda W, Huntsman SA (1995) Iron uptake and growth limitation in oceanic and coastal phytoplankton. Mar Chemy 50:189–206CrossRefGoogle Scholar
  270. Sunda WG, Huntsman SA (1997) Interrelated influence of iron, light and cell size on marine phytoplankton growth. Nature 390:389–392CrossRefGoogle Scholar
  271. Sunda W, Huntsman S (2003) Effect of pH, light, and temperature on Fe-EDTA chelation and Fe hydrolysis in seawater. Mar Chem 84:35–47CrossRefGoogle Scholar
  272. Sunda WG, Huntsman SA (2011) Interactive effects of light and temperature on iron limitation in a marine diatom: implications for marine productivity and carbon cycling. Limnol Oceanogr 56:1475–1488CrossRefGoogle Scholar
  273. Sunda WG, Huntsman SA (2015) High iron requirement for growth, photosynthesis, and low-light acclimation in the coastal cyanobacterium Synechococcus bacillaris. Front Microbiol 6:561PubMedPubMedCentralGoogle Scholar
  274. Sunda WG, Swift D, Huntsman S (1991) Low iron requirement for growth in oceanic phytoplankton. Nature 351:55–57CrossRefGoogle Scholar
  275. Sunda W, Kieber DJ, Kiene RP, Huntsman S (2002) An antioxidant function for DMSP and DMS in marine algae. Nature 418:317–320PubMedCrossRefGoogle Scholar
  276. Sunda WG, Price NM, Morel FMM (2005) Trace metal ion buffers and their use in culture studies. In: Anderson RA (ed) Algal culturing techniques. Elsevier Academic Press, London, pp 35–64Google Scholar
  277. Tagliabue A, Bopp L, Dutay J-C, Bowie AR, Chever F, Jean-Baptiste P, Bucciarelli E, Lannuzel D, Remenyi T, Sarthou G, Aumont O, Gehlen M, Jeandel C (2010) Hydrothermal contribution to the oceanic dissolved iron inventory. Nat Geosci 3:252–256CrossRefGoogle Scholar
  278. Takeda S (1998) Influence of iron availability on nutrient consumption ratio of diatoms in oceanic waters. Nature 393:774–777CrossRefGoogle Scholar
  279. Tang D, Morel FMM (2006) Distinguishing between cellular and Fe-oxide-associated trace elements in phytoplankton. Mar Chem 98:18–30CrossRefGoogle Scholar
  280. Taylor RL, Semeniuk DM, Payne CD, Zhou J, Tremblay J-E, Cullen JT, Maldonado MT (2013) Colimitation by light, nitrate, and iron in the Beaufort Sea in late summer. J Geophys Res 118:3260–3277CrossRefGoogle Scholar
  281. Tilzer M, Elbrachter M, Gieskes WWC, Beese B (1986) Light-temperature interactions in the control of photosynthesis in Antarctic phytoplankton. Polar Biol 5:105–112CrossRefGoogle Scholar
  282. Timmermans KR, Gerringa LJA, de Baar HJW, van der Wagt B, Veldhuis MJW, de Jong JTM, Croot PL, Boye M (2001) Growth rates of large and small Southern Ocean diatoms in relation to availability of iron in natural seawater. Limnol Oceanogr 46:260–266CrossRefGoogle Scholar
  283. Timmermans KR, van der Wagt B, de Baar HJW (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 49:2141–2151CrossRefGoogle Scholar
  284. Timmermans KR, van der Wagt B, Veldhuis MJW, Maatman A, de Baar HJW (2005) Physiological responses of three species of marine pico-phytoplankton to ammonium, phosphate, iron and light limitation. J Sea Res 53:109–120CrossRefGoogle Scholar
  285. Trick CG, Bill BD, Cochlan WP, Wells ML, Trainer VL, Pickell LD (2010) Iron enrichment stimulates toxic diatom production in high-nitrate, low-chlorophyll areas. Proc Natl Acad Sci 107:5887–5892PubMedPubMedCentralCrossRefGoogle Scholar
  286. Twining BS, Baines SB (2013) The trace metal composition of marine phytoplankton. Ann Rev Mar Sci 5:191–215PubMedCrossRefGoogle Scholar
  287. Twining BS, Baines SB, Fisher NS, Maserr J, Vogt S, Jacobsen C, Tovar-Sanchez A, Sañudo-Wilhelmy SA (2003) Quantifying trace elements in individual aquatic protist cells with a synchrotron X-ray fluorescence microprobe. Anal Chem 75:3806–3816PubMedCrossRefGoogle Scholar
  288. Twining BS, Baines SB, Fisher NS, Landry MR (2004) Cellular iron contents of plankton during the Southern Ocean Iron Experiment (SOFeX). Deep Sea Res I 51:1827–1850CrossRefGoogle Scholar
  289. Twining BS, Baines SB, Bozard JB, Vogt S, Walker EA, Nelson DM (2011) Metal quotas of plankton in the equatorial Pacific Ocean. Deep Sea Res II 58:325–341CrossRefGoogle Scholar
  290. Twiss MR, Auclair J-C, Charlton MN (2000) An investigation into iron-stimulated phytoplankton productivity in epipelagic Lake Erie during thermal stratification using trace metal clean techniques. Can J Fish Aquat Sci 57:86–95CrossRefGoogle Scholar
  291. Van Ho A, Ward DM, Kaplan J (2002) Transition metal transport in yeast. Annu Rev Microbiol 56:237–261PubMedCrossRefGoogle Scholar
  292. van Oijen T, van Leeuwe MA, Gieskes WWC, de Baar HJW (2004) Effects of iron limitation on photosynthesis and carbohydrate metabolism in the Antarctic diatom Chaetoceros brevis (Bacillariophyceae). Eur J Phycol 39:161–171CrossRefGoogle Scholar
  293. Varsano T, Wolf SG, Pick U (2006) A chlorophyll a/b-binding protein homolog that is induced by iron deficiency is associated with enlarged photosystem I units in the eucaryotic alga Dunaliella salina. J Biol Chem 281:10305–10315PubMedCrossRefGoogle Scholar
  294. Waite TD, Morel FMM (1984) Photoreductive dissolution of colloidal iron oxides in natural waters. Environ Sci Technol 18:860–868PubMedCrossRefGoogle Scholar
  295. Weger HG (1999) Ferric and cupric reductase activities in the green alga Chlamydomonas reinhardtii: experiments using iron-limited chemostats. Planta 207:377–384CrossRefGoogle Scholar
  296. Weger HG, Middlemiss JK, Petterson CD (2002) Ferric chelate reductase activity as affected by the iron- limited growth rate in four species of unicellular green algae (Chlorophyta). J Phycol 38:513–519CrossRefGoogle Scholar
  297. Wells ML, Goldberg ED (1994) The distribution of colloids in the North Atlantic and Southern Oceans. Limnol Oceanogr 39:286–302CrossRefGoogle Scholar
  298. Wells ML, Price NM, Bruland KW (1995) Iron chemistry in seawater and its relationship to phytoplankton – a workshop report. Mar Chem 48:157–182CrossRefGoogle Scholar
  299. Weng H-X, Sun X-W, Qin Y-C, Chen J-F (2007) Effect of irradiance on Fe and P uptake by Cryptomonas sp. Geochimica 4:008Google Scholar
  300. Wetz MS, Hales B, Chase Z, Wheeler PA, Whitney MM (2006) Riverine input of macronutrients, iron, and organic matter to the coastal ocean off Oregon, USA, during the winter. Limnol Oceanogr 51:2221–2231CrossRefGoogle Scholar
  301. Whitney L, Lins J, Hughes M, Wells M, Chappell P, Jenkins B (2011) Characterization of putative iron responsive genes as species-specific indicators of iron stress in Thalassiosiroid diatoms. Front Microbiol 2:234. doi: 10.3389/fmicb.2011.00234 PubMedPubMedCentralGoogle Scholar
  302. Wilhelm SW (1995) Ecology of iron-limited cyanobacteria: a review of physiological responses and implications for aquatic systems. Aquat Microb Ecol 9:295–303CrossRefGoogle Scholar
  303. Wolfe-Simon F, Grzebyk D, Schofield O, Falkowski PG (2005) The role and evolution of superoxide dismutases in algae. J Phycol 41:453–465CrossRefGoogle Scholar
  304. Zehr JP, Kudela RM (2009) Photosynthesis in the open ocean. Science 326:945–946PubMedCrossRefGoogle Scholar
  305. Zhao H, Eide D (1996a) The yeast ZRT1 gene encodes the zinc transporter protein of a high-affinity uptake system induced by zinc limitation. Proc Natl Acad Sci 93:2454–2458PubMedPubMedCentralCrossRefGoogle Scholar
  306. Zhao H, Eide D (1996b) The ZRT2 gene encodes the low affinity zinc transporter in Saccharomyces cerevisiae. J Biol Chem 271:23203–23210PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of Marine SciencesUniversity of North Carolina at Chapel HillChapel HillUSA
  2. 2.Department of Earth, Ocean and Atmospheric SciencesUniversity of British ColumbiaVancouverCanada

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