[Advances in Marine Biology] Aquatic Geomicrobiology Volume 48 || The Iron and Manganese Cycles

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  • Iron has a high abundance of 4.3% by mass in the continental crust (Wedepohl,

    1995). This, coupled with a variety of unique geochemical characteristics,1. INTRODUCTION1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 269

    2. Global Manganese and Iron Cycles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 270

    3. Environmental Geochemistry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 272

    4. Assimilation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 276

    4.1. Uptake . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 277

    4.2. Iron in the oceans . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 278

    5. Microbial Oxidation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 279

    5.1. Chemotrophic iron oxidation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 280

    5.2. Anoxygenic iron-oxidizing phototrophs and a note on evolution . . . . . . . . . . . . . . . . 286

    5.3. Microbial manganese oxidation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 288

    6. Microbial Reduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 290

    6.1. Diversity and phylogeny . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 291

    6.2. Metabolic diversity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 294

    6.3. Mechanisms of iron and manganese reduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 296

    6.4. Intracellular electron transport . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 298

    7. Microbial Manganese and Iron Reduction in Aquatic Environments . . . . . . . . . . . . . . . . . 299

    7.1. Environmentally important manganese and iron reducers . . . . . . . . . . . . . . . . . . . . . . 299

    7.2. Controls of microbial iron and manganese reduction . . . . . . . . . . . . . . . . . . . . . . . . . . . 300

    7.3. Quantification of microbial manganese and iron reduction . . . . . . . . . . . . . . . . . . . . . 303

    7.4. Kinetics. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 305

    7.5. Abiotic reduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 307

    7.6. Recycling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 308

    7.7. Role in benthic carbon mineralization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 310

    7.8. Manganese and iron reduction in water columns . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 311

    8. Stable Iron Isotopes and Iron Cycling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 312The Iron and Manganese CyclesChapter 8allows Fe to interact significantly with the cycles of a number of other

    biologically important elements such as carbon, sulfur, and phosphorus.

    Iron redox cycling has been active and globally important throughout

    ADVANCES IN MARINE BIOLOGY VOL 48 2005 Elsevier Inc.0-12-026147-2 All rights reserved

  • appropriate. Many of the microbes transforming iron and manganese also

    elements are not known to influence major biogeochemical cycles.

    270 CANFIELD ET AL.In addition to redox reactions with many other major elements, oxidized

    and reduced manganese and iron species adsorb and coprecipitate transition

    metals and other compounds of environmental significance. One such inter-

    action is the binding of phosphate to iron oxides (Chapter 11), which

    regulates the release of this nutrient from sediments, and which may have

    significantly limited primary production in the iron-rich Archean ocean

    (Bjerrum and Canfield, 2002).

    Both the oxidation and the reduction of iron and manganese in natural

    environments is, to a large extent, promoted by microbial catalysis, but

    abiotic transformations are often important too and may compete with the

    biological processes. In what follows we look at the processes regulating the

    transformations of iron and manganese in nature and the relationship be-

    tween the cycling of these and other biologically active elements. The story is

    part biological and part chemical, and the relative importance of, and inter-

    actions between, abiotic and microbial iron and manganese transformations

    are a central issue in this Chapter.

    2. GLOBAL MANGANESE AND IRON CYCLES

    Due to the very low solubility of oxidized manganese and iron, their global

    cycles are heavily influenced by physical processes. In the Earths crust the

    two elements are mainly found as minor components of rock-forming sili-

    cate minerals such as olivine, pyroxenes, and amphiboles (Table 8.1). Under

    oxic conditions and at near neutral pH, iron and manganese released during

    weathering are rapidly reprecipitated as oxides and hydroxides, as expressed

    here by the oxidative weathering of fayalite (Fe2SiO4) to goethite (FeOOH):

    Fe2SiO4s 0:5O23H2O ! 2FeOOHs H4SiO4aq 8:1catalyze the redox transformations of other rarer transition elements (Lovley,

    2000c; Lloyd, 2003), but this is not discussed in this Chapter because thoseEarths history as indicated by the massive deposition of iron-rich sediments,

    banded iron formations, during the Archean Eon (>2.5 billion years ago)and parts of the Proterozoic Eon (2.5 to 0.54 billion years ago). At a 50-fold

    lower crustal abundance than iron, manganese is the second most abundant

    redox-active metal (Wedepohl, 1995). However, manganese concentrates in

    certain environments, thereby enhancing its local biogeochemical signifi-

    cance. As there are many similarities between iron and manganese in terms

    of both geochemistry and microbiology, the two elements are discussed

    together in this Chapter, while important diVerences are emphasized when

  • THE IRON AND MANGANESE CYCLES 271Table 8.1 Representative iron- and manganese-containing mineralsa

    Silicates Olivines: fayalite, Fe(II)2SiO4Pyroxenes: augite, Ca(Mg,Fe(II))Si2O6Amphiboles: hornblende, (Ca,Na)23(Mg,Fe(II),Al)5(Al,Si)8O22(OH)2Garnets: almandine, Fe(II)3Al2(SiO4)3

    Sheetsilicates

    Micas: biotite, K2(Mg,Fe(II))64(Fe(III), Al,Ti)02(Si65Al23O20)(OH, F)4

    Smectites: nontronite, Na0.3Fe(III)2(Si,Al)4O10(OH)2nH2OOxides Ferrihydrite, Fe(III)5HO84H2O; lepidocrocite,

    -Fe(III)OOH; goethite, a-Fe(III)OOH; hematite, a-Fe(III)2O3;magnetite, Fe(II)Fe(III)2O4; ilmenite, Fe(III)2TiO4

    Green rusts E.g., [Fe(II)4Fe(III)2(OH)]12[(CO3,SO4)3H2O]Sulfides Mackinawite, Fe(II)S; greigite, Fe(II)3S4; pyrite, Fe(II)S2Carbonates Siderite, Fe(II)CO3Manganese

    silicatesb Rhodonite, (Mn(II),Fe(II),Ca,Mg)SiO3Oxides Birnessite, Mn(III)Mn(IV)6O135H2O; pyrolusite, -Mn(IV)O2;

    manganite, -Mn(III)OOH; hausmannite, Mn(II)Mn(III)2O4Carbonates Rhodocrosite, Mn(II)CO3

    aAfter Deer et al. (1966), Hurlbut and Klein (1977), Burns and Burns (1979), Cornell and

    Schwertmann (1996).bManganese-rich silicates are rare. Manganese occurs as a minor component in the same

    coordination sites as Fe(II).Most of the manganese and iron transported to the oceans is associated with

    river-borne particulates, while glaciers and wind-borne dust represent minor

    fluxes (Figure 8.1) (Poulton and Raiswell, 2002). Some 90% of the riverine

    inputs deposit on the continental shelves, and the atmosphere therefore is an

    important source of the metals to surface waters far oV shore (Duce andTindale, 1991), providing a potentially important source of iron for primary

    production (Section 4). In addition to the particulate fluxes, relatively small

    amounts of soluble iron and manganese are delivered to the ocean basins

    with hydrothermal fluids. Metals from this source are oxidized microbially or

    abiotically and may form copious precipitates around the vents.

    Once buried into anoxic sediments, manganese and iron may be mobilized

    through microbial respiration and abiotic reduction. However, soluble man-

    ganese and iron are eYciently trapped through oxidation in oxic surfacesediment layers only a few millimeters thick, and typically only a small frac-

    tion escapes to the bottom waters (e.g., Thamdrup et al., 1994b). Thus, there is

    an intensive redox cycling of manganese and iron around the oxicanoxic

    interface in many sediments (Canfield et al., 1993b). Still, some manganese

    can be lost from sediments with shallow oxygen penetration, leading to a

    redistribution toward locations with deeper oxic zones where manganese is

    retained (Sundby and Silverberg, 1981). A supply of soluble manganese from

    the water column is found in the deep sea where centimeter- to decimeter-size

  • 272 CANFIELD ET AL.nodules of manganese and iron oxides, manganese nodules, grow at the

    sediment surface by slow precipitation of metals from the bottom water

    (Glasby, 2000).

    Benthic iron fluxes, although very small relative to the rates of iron cycling

    within the sediment, may cover the iron requirements of primary production

    in shelf waters (Berelson et al., 2003). Far oV shore, however, soluble con-centrations of iron and manganese are below 1 nM (Landing and Bruland,

    1987; Johnson et al., 1997), and organisms in the surface waters may rely on

    scavenging of these trace metals from the particles that settle from the

    atmosphere. Under these conditions, solubilization is aided by organic che-

    lators produced by the plankton and may involve photochemical reduction

    (see below).

    3. ENVIRONMENTAL GEOCHEMISTRY

    In contrast to other elements discussed in this volume, which are mostly

    covalently bonded in well-defined molecules, iron and manganese in the

    environment are ions that interact with a wide variety of other species and

    Figure 8.1 The global iron cycle with fluxes in terragrams Fe per year (1012 g y1).Magnified circles illustrate biogeochemical cycling in pelagic waters and sediments.These are the main topic of this Chapter. After Poulton and Raiswell (2002).

  • are mainly found in solid phases (Table 8.1). The oxidized forms, Fe3,Mn3, and Mn4, have very low solubility at neutral pH and are precipitatedas hydroxides, oxyhydroxides or oxides, here collectively termed oxides.

    Chelation with organic compounds may keep Fe3 and Mn3 in solution,but their concentrations typically remain well below 1 mM in natural watersof near neutral pH. The reduced forms, Fe2 and Mn2, are more soluble,reaching concentrations in the millimolar range, but they also readily pre-

    cipitate, for example, with sulfides and carbonates (Table 8.1). In sediments,

    such precipitates are the most important sinks for these reduced ions.

    Thermodynamic calculations predict the existence of single, well-defined,

    mineral forms depending on the environmental conditions. For iron, exam-

    ples include goethite in the presence of oxygen, magnetite at intermediate

    redox potentials, and pyrite under sulfidic conditions (Stumm and Morgan,

    1981). Kinetic inhibition, however, allows the co-occurrence and frequent

    dominance of metastable phases that may be poorly crystalline and hard to

    define analytically. Additionally, a large fraction remains bound as a minor

    component in silicate minerals (Figure 8.2). While most of this is only

    reactive on geological timescales, iron in some sheet silicates is micro-

    THE IRON AND MANGANESE CYCLES 273bially reducible (Kostka et al., 1996). The kinetics of oxidation or reduction

    of iron and manganese, by both biological and abiotic mechanisms, depend

    on the mineral form, crystallinity, and grain size. In the reaction with

    sulfide, for example, the complex assembly of oxidized iron and manganese

    species found in sediments makes up a continuum of reactivities span-

    ning several orders of magnitude from highly reactive, poorly crystalline,

    Figure 8.2 Speciation of manganese and iron in river particulates. The poorlycrystalline oxide fraction corresponds roughly to the pool available to microbialreduction. After Canfield (1997); redrawn from Thamdrup (2000).

  • 274 CANFIELD ET AL.nanometer-sized oxides to silicate phases that are transformed only on

    million year timescales (Canfield et al., 1992).

    The reduction potentials of the Fe2/Fe3 and Mn2/Mn3/4 couplesdepend strongly on the speciation of both the reduced and oxidized metal

    species (Figure 8.3). Thus, the standard potential for the Fe3/Fe2 couple is0.77 V, but this potential is only relevant at low pH, where Fe3 is soluble.With poorly crystalline Fe oxide as the oxidant, the potential is around

    0.0 V, and with more crystalline oxides it may even become more negative

    than the H2S=SO24 couple, rendering sulfate the thermodynamically more

    favorable oxidant.

    Both oxidized and reduced forms of iron and manganese react spontane-

    ously with a range of compounds, and microbes that utilize manganese or

    iron metabolically will often have to compete for the metals with abiotic

    reactions (see also Chapter 9). Figure 8.4 gives an overview of the environ-

    mentally significant abiotic redox reactions involving iron and manganese,

    together with the microbially catalyzed pathways discussed in detail below.

    While Fe2 is rapidly oxidized by oxygen with a half-life on the order of

    Figure 8.3 Electrode potentials vs. standard hydrogen electrode of selectediron and manganese species, compared to other important redox couples. Potentialswere calculated for pH 7 and environmentally relevant concentrations of solutes(Thamdrup, 2000).

  • THE IRON AND MANGANESE CYCLES 275minutes, Mn2 in solution oxidizes much more slowly, with a half-life ofmonths or more (Stumm and Morgan, 1981). Abiotic manganese oxidation

    is accelerated by catalytic surfaces such as manganese and iron oxides

    (Davies and Morgan, 1989), but the overall slower oxidations kinetics result

    in a much larger mobility for manganese than for iron in aquatic environ-

    ments. Rapid abiotic oxidation of ferrous iron further occurs by reaction

    with manganese oxides (Postma, 1985), while iron oxidation with nitrate or

    nitrite, known as chemo-denitrification, is a relatively slow process, which is

    catalyzed by the surfaces of iron oxides and other minerals (Ottley et al.,

    Figure 8.4 Oxidants and reductants for manganese and iron in aquatic environ-ments. Thin lines indicate abiotic reactions; thick grey lines indicate microbiallycatalyzed reactions; stippled...

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