Abstract
The light-induced redox cycling of iron plays an important role for the formation of iron species that are available to phytoplankton. In aquatic ecosystems, siderophore-type ligands are likely to be involved in the formation of bioavailable iron via photolysis of both solution and surface Fe(III) complexes. Atmospheric waters are important “reactors” for the formation of potentially bioavailable iron. Atmospheric iron input is a significant external iron source to many oceanographic regions. Since iron is an essential micronutrient for phytoplankton, the presence of bioavailable iron in the euphotic zone of oceans is a prerequisite for the removal of atmospheric CO2 via the biological pump, particularly in high-nitrate, low-chlorophyll regions. Light-induced reduction of Fe(III) is accompanied by the oxidation of dissolved organic matter (DOM). DOM photooxidation results in the formation of CO2 and to a smaller extent CO. Also the photooxidation of colored dissolved organic matter (CDOM) may be catalyzed by iron and results in CDOM bleaching. CDOM photobleaching is particularly pronounced in stratified aquatic systems and negatively affects the biological pump since CDOM protects phytoplankton from the damaging solar UV-B radiation. Changes in continental hydrology due to climate and land-use change are expected to enhance the flux of terrigenous DOM and iron from terrestrial to aquatic ecosystems, possibly increasing the rate of CO2 formation via iron-catalyzed photooxidation of DOM. Hence, the light-induced redox cycling of iron may play an important role in climate-carbon cycle feedbacks.
Similar content being viewed by others
References
Armstrong E, Granger J, Mann EL, Price NM (2004) Outer-membrane siderophore receptors of heterotrophic oceanic bacteria. Limnol Oceanogr 49:579–587
Barbeau KA (2006) Photochemistry of organic iron(III) complexing ligands in oceanic systems. Photochem Photobiol 82:1505–1516
Barbeau KA, Rue EL, Bruland KW, Butler A (2001) Photochemical cycling of iron in the surface ocean mediated by microbial iron-binding ligands. Nature 413:409–413
Barbeau KA, Rue EL, Trick CG, Bruland KW, Butler A (2003) Photochemical reactivity of siderophores produced by marine heterotrophic bacteria and cyanobacteria based on characteristic Fe(III) binding groups. Limnol Oceanogr 48:1069–1078
Barry RC, Schnoor JL, Sulzberger B, Sigg L, Stumm W (1994) Iron oxidation kinetics in a Swiss alpine lake. Water Res 28:323–333
Behra P, Sigg L (1990) Evidence for redox cycling of iron in atmospheric water droplets. Nature 344:419–421
Behrenfeld MJ, Worthington K et al (2006) Controls on tropical Pacific Ocean productivity revealed through nutrient stress diagnostics. Nature 442:1025–1028
Blough NV, Zepp RG (1995) Reactive oxygen species in natural waters. In: Valentine JS, Foote CS (eds) Reactive Oxygen Species in Chemistry. Chapman and Hall, London, pp 280–333
Borer P, Hug SJ, Sulzberger B, Kraemer SM, Kretzschmar R (2007) Photolysis of citrate on the surface of lepidocrocite: an in situ attenuated total reflection infrared spectroscopy study. J Phys Chem C 111:10560–10569
Borer P, Hug SJ, Sulzberger B, Kraemer SM, Kretzschmar R (2009a) ATR-FTIR spectroscopic study of the adsorption of desferrioxamine B and aerobactin to the surface of lepidocrocite (γ-FeOOH). Geochim Cosmochim Acta 73:4661–4672
Borer P, Sulzberger B, Hug SJ, Kraemer SM, Kretzschmar R (2009b) Photoreductive dissolution of Fe(III) (hydr)oxides in the absence and presence of organic ligands: experimental studies and kinetic modeling. Environ Sci Technol 43:1864–1870
Borer P, Sulzberger B, Hug SJ, Kraemer SM, Kretzschmar R (2009c) Wavelength-dependence of photoreductive dissolution of lepidocrocite (γ-FeOOH) in the absence and presence of the siderophore DFOB. Environ Sci Technol 43:1871–1876
Boyce DG, Lewis MR, Worm B (2010) Global phytoplankton decline over the past century. Nature 466:591–596
Boyd PW, Watson AJ et al (2000) A mesoscale phytoplankton bloom in the Polar Southern Ocean simulated by iron fertilization. Nature 407:695–702
Buck KN, Moffett J, Barbeau KA, Bundy RM, Kondo Y, Wu J (2012) The organic complexation of iron and copper: an intercomparison of competitive ligand exchange-adsorptive cathodic stripping voltammetry (CLE-ACSV) techniques. Limnol Oceanogr Methods 10:496–515
Buesseler KO, Andrews JE et al (2005) Particle export during the Southern Ocean iron experiment (SOFeX). Limnol Oceanogr 50:311–327
Canadell JG, Le Quéré C et al (2007) Contributions to accelerating atmospheric CO2 growth from economic activity, carbon intensity, and efficiency of natural sinks. PNAS 104:18868–18870
Cassar N, Bender ML et al (2007) The Southern Ocean biological response to Aeolian iron deposition. Science 317:1067–1070
Del Vecchio R, Blough NV (2002) Photobleaching of chromophoric dissolved organic matter in natural waters: kinetics and modeling. Mar Chem 78:231–253
Del Vecchio R, Blough NV (2004) On the origin of the optical properties of humic substances. Environ Sci Technol 38:3885–3891
Dzombak DA, Morel FMM (1990) Surface complexation modeling hydrous ferric oxide. John Wiley & Sons, New York
Emmenegger L, King DW, Sigg L, Sulzberger B (1998) Oxidation kinetics of Fe(II) in a eutrophic Swiss lake. Environ Sci Technol 32:2990–2996
Emmenegger L, Schönenberger RR, Sigg L, Sulzberger B (2001) Light-induced redox cycling of iron in circumneutral lakes. Limnol Oceanogr 46(1):49–61
Erickson DJ III, Sulzberger B, Zepp RG, Austin AT (2015) Effects of stratospheric ozone depletion, solar UV radiation, and climate change on biogeochemical cycling: interactions and feedbacks. Photochem Photobiol Sci 14(1):127–148
Fichot CG, Benner R (2012) The spectral slope coefficient of chromophoric dissolved organic matter (S275-295) as a tracer of terrigenous dissolved organic carbon in river-influenced ocean margins. Limnol Oceanogr 57:1453–1466
Gaberell M, Chin YP, Hug SJ, Sulzberger B (2003) Role of dissolved organic matter composition on the photoreduction of Cr(VI) to Cr(III) in the presence of iron. Environ Sci Technol 37:4403–4409
Gledhill M, McCormack P, Ussher S, Achterberg EP, Mantoura RFC, Worsfold PJ (2004) Production of siderophore-type chelates by mixed bacterioplankton populations in nutrient enriched seawater incubations. Mar Chem 88:75–83
Gruber N (2011) Warming up, turning sour, losing breath: ocean biogeochemistry under global change. Philos Trans R Soc 369:1980–1996
Hopkinson BM, Morel FMM (2009) The roles of siderophores in iron acquisition by photosynthetic marine microorganisms. Biometals 22:659–669
Hopkinson BM, Mitchell G et al (2007) Iron limitation across chlorophyll gradients in the southern Drake Passage: phytoplankton responses to iron addition and photosynthetic indicators for iron stress. Limnol Oceanogr 52:2540–2554
Houghton RA (2007) Balancing the global carbon budget. Annu Rev Earth Planet Sci 35:313–347
Ibisamni E, Sander SG, Boyd PW, Bowie AR, Hunter KA (2011) Vertical distribution of iron(III) complexing ligands in the Southern Ocean. Deep-Sea Res 58:2113–2212
Jacquet SHM, Savoye N, Dehairs F, Strass VH, Cardinal D (2008) Mesopelagic carbon remineralization during the European iron fertilization experiment. Global Biogeochem Cycles 22. doi:10.1029/2006GB002902
Jickells TD, An ZS et al (2005) Global iron connection between desert dust, ocean biogeochemistry, and climate. Science 308:67–71
Jin X, Gruber N (2003) Offsetting the radiative benefit of ocean iron fertilization by enhancing N2O emissions. Geophys Res Lett. doi:10.1029/2003GL018458
Johnson CA, Sigg L (1985) Acidity of rain and fog: conceptual definitions and practical measurements of acidity. Chimia 39:59–61
Johnson KS, Riser SC, Karl DM (2010) Nitrate supply from deep to near-surface waters of the North Pacific subtropical gyre. Nature 465:1062–1065
Judd KE, Crump BC, King GW (2007) Bacterial responses in activity and community composition to photo-oxidation of dissolved organic matter from soil and surface waters. Aquat Sci 69:96–107
Kaiser E, Sulzberger B (2004) Phototransformation of riverine dissolved organic matter (DOM) in the presence of abundant iron: effect on DOM bioavailability. Limnol Oceanogr 49:540–554
Kaiser E, Simpson AJ, Dria KJ, Sulzberger B, Hatcher PG (2003) Solid-state and multidimensional solution-state NMR of solid phase extracted and ultrafiltered riverine dissolved organic matter. Environ Sci Technol 37:2929–2935
King AL, Barbeau KA (2007) Evidence for phytoplankton iron limitation in the southern California Current System. Mar Ecol Prog Ser 342:91–103
King AL, Barbeau KA (2011) Dissolve iron and macronutrient distributions in the southern California Current system. J Geophys Res 116:C03018. doi:10.1029/2010JC006324
King AL, Buck KN, Barbeau KA (2012) Quasi-Lagrangian drifter studies of iron speciation and cycling off Point Conception, California. Mar Chem 128:1–12
Laufkötter C, Vogt M, Gruber N (2013) Long-term trends in ocean plankton production and particle export between 1960–2006. Biogeosciences 10:7373–7393
Lelong A, Bucciarelli E, Hegaret 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 58:613–623
Lenton A, Codron F, Bopp L, Metzl N, Cadule P, Tagliabue A, Le Sommer J (2009) Stratospheric ozone depletion reduces ocean carbon uptake and enhances ocean acidification. Geophys Res Lett. doi:10.1029/2009GL038227
Lonborg C, Alvarez-Salgado XA, Davidson K, Martinez-Garcia S, Teira E (2010) Assessing the microbial bioavailability and degradation rate constants of dissolved organic matter by fluorescence spectroscopy in the coastal upwelling system of the Ria de Vigo. Mar Chem 119:121–129
Maldonado MT, Price NM (2001) Reduction and transport of organically bound iron by Thalassiosira oceanica (Bacillariophyceae). J Phycol 37:298–309
Martin JH, Gordon RM, Fitzwater SE (1990) Iron in Antarctic waters. Nature 345:156–158
Martinez-Carcia A, Sigman DM et al (2014) Iron fertilization in the Subantarctic Ocean during the last ice age. Science 343:1347–1350
Mawji E, Gledhill M, Milton JA, Zubkov MV, Thompson A, Wolff GA, Achterberg EP (2011) Production of siderophore type chelates in Atlantic Ocean waters enriched with different carbon and nitrogen sources. Mar Chem 124:90–99
Meunier L, Laubscher HU, Hug SJ, Sulzberger B (2005) Effects of size and origin of natural organic matter compounds on the redox cycling of iron in sunlit surface waters. Aquat Sci 67:292–307
Miller WL, Moran MA (1997) Interactions of photochemical and microbial processes in the degradation of refractory organic matter from a coastal marine environment. Limnol Oceanogr 42:1317–1324
Mingshun J, Barbeau KA et al (2013) The role of organic ligands in iron cycling and productivity in the Antarctic Peninsula: a modeling study. Deep-Sea Res 90:112–133
Moffett JW (2001) Transformations among different forms of iron in the ocean. In: Turner DR, Hunter KA (eds) The biogeochemistry of iron in seawater, JUPAC series on analytical and physical chemistry of environmental systems, vol 7. Wiley, New York, pp 343–372
Moore CN, Mills MM et al (2013) Processes and patterns of oceanic nutrient limitation. Nat Geosci 6:701–710
Morel FMM, Hering GH (1993) Principles and applications of aquatic chemistry. Wiley, New York
Morel FMM, Kustka AB, Shaked Y (2008) The role of unchelated Fe in the iron nutrition of phytoplankton. Limnol Oceanogr 53:400–404
Mundy CJ, Gosselin M, Starr M, Michel C (2010) Riverine export and the effects of circulation on dissolved organic carbon in the Hudson Bay system, Canada. Limnol Oceanogr 55:315–323
Nelson NB, Siegel DA (2013) The global distribution and dynamics of chromophoric dissolved organic matter. In: Carlson CA, Giovannoni, SJ (eds) Annual review of marine science, Annual Reviews, vol. 5, Palo Alto, pp 447–476
Obernosterer I, Benner R (2004) Competition between biological and photochemical processes in the mineralization of dissolved organic matter. Limnol Oeanogr 49:117–124
Para J, Charrière B, Matsuoka A, Miller WL, Rontani JF, Sempéré R (2013) UV/PAR radiation and DOM properties in surface coastal waters of the Canadian shelf of the Beaufort Sea during summer 2009. Biogeosciences 10:2761–2774
Pollard RT, Salter I et al (2009) Southern Ocean deep water carbon export enhanced by natural iron fertilization. Nature 457:577–581
Powell RT, Willson-Finelli A (2003) Photochemical degradation of organic iron complexing ligands in seawater. Aquat Sci 65:367–374
Reader HE, Miller WL (2012) Variability of carbon monoxide and carbon dioxide apparent quantum yield spectra in three coastal estuaries of the South Atlantic Bight. Biogeosciences 9:6927–6985
Regnier P, Friedlingstein P et al (2013) Anthropogenic perturbation of the carbon flux from land to ocean. Nat Geosci 6:597–607
Ribas-Ribas M, Gomez-Parra A, Forja JM (2011) Air-sea CO2 fluxes in the north-eastern shelf of the Gulf of Cadiz (southwest Iberian Peninsula). Mar Chem 123:56–66
Rijkenberg MJA, Powell CF et al (2008) Changes in iron speciation following a Saharan dust event in the tropical North Atlantic Ocean. Mar Chem 110:56–67
Rose AL, Waite TD (2005) Reduction of organically complexed ferric iron by superoxide in a simulated natural water. Environ Sci Technol 39:2645–2650
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 equilibrium adsorptive cathodic stripping voltammetric method. Mar Chem 50:117–138
Salawich RJ (2006) Atmospheric chemistry: biogenic bromine. Nature 439:275–277
Schlosser C, De La Rocha CL, Streu P, Croot PL (2012) Solubility of iron in the Southern Ocean. Limnol Oceanogr 57:684–697
Shadwick EH, Thomas H, Azetsu-Scott K, Greenan BJW, Head E, Horne E (2011) Seasonal variability of dissolved inorganic carbon and surface water pCO2 in the Scotian shelf region of the Northwestern Atlantic. Mar Chem 124:23–37
Shaked Y, Kustka AB, Morel FMM (2005) A general kinetic model for iron acquisition by eukaryotic phytoplankton. Limnol Oceanogr 50:872–882
Shank GC, Zepp RG, Vahatalo A, Lee R, Bartels E (2010) Photobleaching kinetics of chromophoric dissolved organic matter derived from mangrove leaf litter and floating Sargassum colonies. Mar Chem 119:162–171
Shen Y, Fichot CG, Benner R (2012) Floodplain influence on dissolved organic matter composition and export from the Mississippi-Atchafalaya River system to the Gulf of Mexico. Limnol Oceanogr 57:1149–1160
Shi D, Xu Y, Hopkinson BM, Morel FMM (2010) Effect of ocean acidification on iron bioavailability to marine phytoplankton. Science 327:676–679
Sigg L, Stumm W (1981) The interactions of anions and weak acids with the hydrous goethite (α-FeOOH) surface. Colloids Surf 2:101–117
Sigg L, Xue HB (1993) Metal speciation – Concepts, analysis and effects. In: Bidoglio G, Stumm W (eds) Chemistry of aquatic systems: local and global perspectives. 5: pp 153–181
Smetacek V, Klaas C et al (2012) Deep carbon export from a Southern Ocean iron-fertilized diatom bloom. Nature 487:313–319
Smith RM, Martell AE, Motekaitis RJ (2001) NIST standard reference database 46, version 6.0, Gaithersburg, MD, USA
Strzepek RF, Maldonado MP, Hunter KA, Frew RD, 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 56:1983–2002
Stubbins A, Spencer RGM et al (2010) Illuminated darkness: molecular signatures of Congo River dissolved organic matter and its photochemical alteration by ultrahigh precision mass spectrometry. Limnol Oceanogr 55:1467–1477
Stumm W, Wehrli B, Wieland E (1987) Surface complexation and its impact on geochemical kinetics. Croat Chem Acta 60:429–456
Sulzberger B, Durisch-Kaiser E (2009) Chemical characterization of dissolved organic matter (DOM): a prerequisite for understanding UV-induced changes of DOM absorption properties and bioavailability. Aquat Sci 71:104–126
Sulzberger B, Laubscher HU (1995a) Photochemical reductive dissolution of lepidocrocite: Effect of pH. In: Juang CP, O’Melia CR, Morgan JJ (eds) Aquatic chemistry: interfacial and interspecies processes., Adv Chem SerACS, Washington, DC, pp 279–290
Sulzberger B, Laubscher HU (1995b) Reactivity of various types of iron(III) (hydr)oxides towards light-induced dissolution. Mar Chem 50:103–115
Sulzberger B, Schnoor JL, Giovanoli R, Hering JG, Zobrist J (1990) Biogeochemistry of iron in an acidic lake. Aquat Sci 52:56–74
Sunda WG, Huntsman SA (2011) Interacting effects of light and temperature on iron limitation in a marine diatom: implications for marine productivity and carbon cycling. Limnol Oceanogr 56:1475–1488
Tamura H, Goto K, Nagayama M (1976) Effects of ferric hydroxide on the oxygenation of ferrous ions in neutral solutions. Corros Sci 16:197–207
Tranvik LJ, Bertillson S (2001) Contrasting effects of solar UV radiation on dissolved organic sources for bacterial growth. Ecol Lett 4:458–463
Trick CG, Bill BD, Cochlan WP, Wells ML, Trainer VL, Pickell LD (2010) Iron enrichment simulates toxic diatom production in high-nitrate, low chlorophyll areas. PNAS 107:5887–5892
Vahatalo AV, Wetzel RG (2008) Long-term photochemical and microbial decomposition of wetland-derived dissolved organic matter with alteration of C13:C12 mass ratio. Limnol Oceanogr 53:1387–1392
Velasquez I, Nunn BL, Ibisanmi E, Goodlett DR, Hunter KA, Sander SG (2011) Detection of hydroxamate siderophores in coastal and Sub-Antarctic waters off the South-Eastern coast of New Zealand. Mar Chem 126:97–107
Vermilyea AW, Voelker BM (2009) Photo-Fenton reaction at near neutral pH. Environ Sci Technol 43:6927–6933
Voelker BM, Sulzberger B (1996) Effects of fulvic acid on F(II) oxidation by hydrogen peroxide. Environ Sci Technol 30:1106–1114
Voelker BM, Morel FMM, Sulzberger B (1997) Iron redox cycling in surface waters: effects of humic substances and light. Environ Sci Technol 31:1004–1011
Vonk JE, Mann PJ et al (2013) Dissolved organic carbon loss from Yedoma permafrost amplified by ice wedge thaw. Environ Res Lett 8:035023. doi:10.1088/1748-9326/8/3/035023
Waugh DW, Primeau F, DeVries T, Holzer M (2013) Recent changes in the ventilation of the Southern Ocean. Science 339:568–570
Wehrli B (1990) Redox reactions of metal ions at mineral surfaces. In: Stumm W (ed) Aquatic chemical kinetics. Wiley, New York, pp 311–336
White EM, Kieber DJ, Sherrard J, Miller WL, Mopper K (2010) Carbon dioxide and carbon monoxide photoproduction quantum yields in the Delaware estuary. Mar Chem 118:11–21
Wu JF, Luther GW (1995) Complexation of Fe(III) by natural organic ligands in the northwest Atlantic Ocean by a competitive ligand equilibration method and a kinetic approach. Mar Chem 50:159–177
Zepp RG, Erickson DJ, Paul NG, Sulzberger B (2011) Effects of solar UV radiation and climate change on biogeochemical cycling: interactions and feedbacks. PPS 10:261–279
Zhang J, Hudson J et al (2010) Long-term patterns of dissolved organic carbon in lakes across eastern Canada: evidence of a pronounced climate effect. Limnol Oceanogr 55:30–42
Zurbruegg R, Suter S, Lehmann MF, Wehrli B, Senn DB (2013) Organic carbon and nitrogen export from a tropical dam-impacted floodplain system. Biogeosci 10:23–38
Acknowledgments
I enjoyed tremendously the collaboration with Laura Sigg in common research projects and learned a lot from her about metal cycling in aquatic systems. Unforgotten is the Lake Cristallina project as well as the research project on the light-induced redox cycling of iron in circumneutral Swiss lakes with Lukas Emmenegger as the Ph.D. student. Laura Sigg is not only an outstanding scientist but also a very fine colleague.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Sulzberger, B. Light-Induced Redox Cycling of Iron: Roles for CO2 Uptake and Release by Aquatic Ecosystems. Aquat Geochem 21, 65–80 (2015). https://doi.org/10.1007/s10498-015-9260-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10498-015-9260-4