Biogeochemistry of Trace Metals and MettaloidsC Gilmour and G Riedel, Smithsonian Environmental Research Center, Edgewater, MD, USA

ã 2009 Elsevier Inc. All rights reserved.

Introduction

Trace elements are simply elements that are present inlow concentrations in the environment. Trace ele-ment concentrations in inland surface waters canrange from a few parts per million (iron concentra-tions in some highly enriched systems), down to partsper trillion or less (e.g., Cd and Hg). Accurate mea-surement of these low concentrations has been anongoing challenge in trace metal biogeochemistry.Many trace elements are essential micronutrients(i.e., Fe, Mn, Cu, Ni, Mo, Se, and Zn), acting ascatalysts in enzyme systems. Others, like Hg and Pb,serve no known physiological function in organisms.However, all of these elements exert toxic effects onorganisms as concentrations increase. Trace elementsmay impact ecosystem productivity and communitystructure either as limiting nutrients or as toxicants.This article focuses on the biogeochemistry of trace

metals and metalloids that are toxic at relatively lowconcentrations and are common contaminants ofinland aquatic ecosystems. Trace elements are ubiq-uitously, if unevenly, distributed in the Earth’s crust.The more abundant, like Fe, may occur at percentageconcentrations, while a large number, including Znand Cu generally occur at part per million (ppm)concentrations, and a few, like Hg and Ag, occur atpart per billion (ppb) or even lower levels.The chemical properties of each trace element are

unique, although patterns of similarities exist acrossand down the periodic table, causing each to partitiondifferently in the environment, and to interact differ-ently with organisms. Furthermore, organisms sub-stantially influence the redox status and complexationof trace metals, and therefore their fate and transportin the environment. The level of complexity is suchthat we cannot comprehensively cover the subject oftrace element biogeochemistry in inland waters here,but we hope to highlight the importance and the widevariety of these interactions.

Essential and Nonessential TraceElements

Trace elements can be roughly divided into twogroups based on their biological requirements. Essen-tial elements are necessary for the metabolism oforganisms.

Examples include Fe, Cu, Mn, and Zn, which virtu-ally all organisms use in the active sites of a significantnumber of important enzymes and other active pro-teins. Some elements, for example Se, Co, and Crhave a few specific uses in most if not all organisms;others like Cr, Ni, Mo, and W, seem to have specificessential roles for a limited class of organisms. Forexample, Co is essentially universally used in vitaminB12 and similar compounds while Ni functions innitrogen metabolism in some microorganisms andplants. Nonessential elements include common con-taminants such as Ag, Pb, and Hg. These elementsare often toxic at lower concentrations than theessential elements. The physiological role of a numberof trace elements (e.g., Bo, Sb, and V) remains opento conjecture.

Low concentrations of essential trace elementsmay limit algal growth (primary production) insome inland waters; however, trace metal limitationis generally less severe in freshwaters than in the moredilute oceans. The need for organisms to take upessential trace elements and to detoxify others leadsto significant changes in the speciation and complex-ation of trace metals in natural waters.

Sources of Trace Elements

Geological Sources

Erosion and dissolution of rock and soils release traceelements into aquatic environments. Natural oresrelease metals when exposed to water and oxygen.In most cases, the natural concentrations of tracemetals in natural waters are low and well tolerated,or even limiting for biological growth, but in someinstances, geologic background levels can be toxic. Inthe American west, for example, rocks and soils ofthe Colorado Plateau leach high concentrationsof Se, which threaten native fish.

Trace metal concentrations are generally elevated ingeothermal areas. Microorganisms in these areasdevelop resistance to toxic trace metals and someare uniquely adapted to utilize trace metals in che-molithotrophic energy-generating processes. Thepassage of groundwater through aquifers and soilsprior to surfacing can also bring trace elementsinto surface waters. For example, in many regions ofthe world, aquifers used as drinking water containarsenic at levels that can adversely affect human health.

7

8 Inorganic Chemicals _ Biogeochemistry of Trace Metals and Mettaloids

Human activity can exacerbate the mobility andtoxicity of trace metals with natural geologic sources.For example, acid deposition increases aluminumleaching from soils, leading to fish toxicity in streams.Evapo-concentration of Se in agricultural drainagewaters in California has caused significant toxicityto breeding birds. In Bangladesh, wide scale fertiliza-tion of soil has led to anaerobic conditions, resultingin As solubilization into groundwater used fordrinking.

Anthropogenic Sources

Human activities have mobilized trace elements fromgeologic reservoirs into the surface environment forthousands of years. Some of the first polluted sitesknown are prehistorical Cu mining and refining sites,which date back at least 7000 years. Trace metal pol-lution sources may be localized or diffuse, and mayrelease metals to aquatic ecosystems, to land, or to theatmosphere. Metals emitted to the atmosphere areredeposited to watersheds. Efforts to control, assess,and monitor metal contaminants have been on therise in the developed world for at least two decades.Sediment and ice cores, which provide an historicalrecord of metal contamination, suggest that the high-est levels of metal contamination in Europe andNorth America occurred in the mid-to-late twentiethcentury, and that metal releases have generallydeclined since that time. Progress has been slowerfor the developing world, where metal pollution con-tinues to increase in many countries.

Point source pollution Releasesfromisolatedsourcesare known as ‘point source pollution.’ Point sourcereleases from mining, smelting, refining, and otherindustry have contaminated harbors and industrialareas worldwide, resulting in some of the most acuteincidents of tracemetal toxicity in natural waters. Con-tamination from mining includes contaminated spoilheaps, abandoned mines, and contaminated flood-plain sediments.Most urban harbors contain substan-tially elevated levels of metals in sediments, makingrelocationof dredge spoils problematic.

Nonpoint source pollution Metal pollution fromdiffuse sources to natural waters is more difficult tocontrol than metals from point-sources. The wide-spread use of metals in construction materials, bat-teries, vehicles, personal care products, clothing, andmany other materials leads to moderate contamina-tion of watersheds in populated and industrializedareas. Wastewater treatment effluent, combined seweroverflows, and urban runoff all contain elevated

concentrations of metals that are very difficult to con-trol. Control of metals in an upstream manufacturingprocess can reduce metals loads effluent.

Common diffuse sources of metal contaminationinclude lead-based paints; lead pipes; CCA (Cu, Crand As)-treated lumber; batteries (Zn, Pb, and for-merly Hg); Cd in phosphate fertilizers; Hg fromswitches, thermometers, and dentistry; Cu and tribu-tyl tin from antifouling paints; and Cu in biocides.Rubber tires and brake pads contain substantialquantities of zinc, which wears off over time asparticulates. Galvanized (Zn) or Cd-coated steelslowly weathers releasing Zn or Cd. Copper roofsand guttering also oxidize and slowly erode. The useof Ag in dentistry and black and white photographyhas lead to widespread Ag contamination of munici-pal waste water with Ag (not to mention cleaningGrandma’s silver).

Sources to the atmosphere Metals may be releasedto the atmosphere as gases, aerosols, or particulates,and subsequently deposited to natural waters andwatersheds. Ice cores provide a record of trace metalsemissions and deposition through time. They suggestat least one order of magnitude increases in emissionsof Cd, Cu, Zn, Bi, Cu, and Hg in industrial regionsrelative to preindustrial times. Sources of metals tothe atmosphere include ore smelting, industrial metalprocessing, combustion source such as coal-burningpower plants, vehicles, refuse incineration, andcement manufacture; and road and soil dust. Mercuryand Pb are two metals for which significant atmos-pheric emissions have led to global contamination ofsoils and sediments. Tetraethyl lead added to gasolinewas a widespread airborne pollutant, until it wasphased out in many countries in the 1970s and1980s. A large fraction of Hg is emitted to the atmos-phere during combustion. Many nations are nowimplementing control technologies to reduce Hgemissions from combustion processes.

Biogeochemistry of Trace Metals inFreshwaters

The basic chemical properties of the elements controltheir interactions with the biological, geological,and chemical environment and determine the struc-ture of their biogeochemical cycles. Trace elementsare present in the environment in a plethora of forms,including different oxidation states, and a wide vari-ety of organic and inorganic complexes in the dis-solved, colloidal, and solid phases. These forms arepartitioned among phases in natural waters, includ-ing solid, aqueous, and colloidal phases.

Mx+

M

Mx+Mx+

MLn

MSnMx+

S2–

Mx – y

M

MM

+

Mx+

M

M

Adsorptiondesorption

Settlingresuspension

Uptakedepuration

Diffusionadvection

+nL–

Complexation

Settling andbenthic feeding

Abiotic ormicrobial reduction

Bottom feedingand excretion

Anaerobic sediment

Aerobic sediment

Burial and mixing

Wet and drydeposition

Trophictransfer

M(x ± y)

Oxidationor

reductionParticlesLower trophic levelsHigher trophic levels

Sulfide complexation

M

Mx – y

Abiotic ormicrobial oxidation

Inflow andoutflow

Figure 1 Some of the major processes affecting the behavior of trace element cycling between water, sediments, and organisms.

Inorganic Chemicals _ Biogeochemistry of Trace Metals and Mettaloids 9

Figure 1 shows the major types of reactions inthe biogeochemical cycle of a hypothetical metal.All metals do not go through all of the reactions inthis theoretical cycle. Microorganisms may partici-pate in all of these reactions. The major reactionsinclude:

. aqueous complexation – which influences bioavail-ability, toxicity, transport, and partitioning behavior

. adsorption/desorption – which determines the lossof metals to sediments, and affects bioavailabilityand toxicity

. reduction and oxidation – which affects solubility,partitioning, and toxicity, and for Hg, remission tothe atmosphere

. biotic uptake

. methylation and demethylation – for a subset ofmetals and metalloids, either via addition of amethyl group directly to a metal cation or to ametalloid oxyanion.

The following sections discuss each of these aspects oftrace metal biogeochemistry.

Aqueous Complexation

Metals bind reversibly to a wide variety of com-pounds present in natural waters, called ligands.The equilibrium reaction between a generic free

metal cation (M) and a simple anionic ligand (L) canbe written as

MðxþÞ þ nLð�Þ $ MLðþx�nÞn

where the number of ligand molecules in the com-plex, and x is the charges of metal and cation.

The strength of the interaction can be defined viathe equilibrium association constant

Ka ¼ ½MLn�=½M�½L�n

where Ka is the equilibrium association constant, [M]is the free molar concentration of the trace element,[L] is the free molar concentration of the ligand, and[MLn] is the molar concentration of the trace metalligand complex. It is important to note thatmetals andligands are often not at equilibrium in natural waters.

Metals and metalloids form complexes with inor-ganic and organic ligands. Equilibrium constants formost common metals cations with common inorganicanions (e.g., Cl�, SO4

2�, Br2�, CO32�) are well-defined,

as are the equilibrium coefficients for anionic metal-loids with the abundant dissolved inorganic cations(e.g., Kþ, Naþ, Ca2þ and Mg2þ). If the concentrationsof metals and ligands, including pH, are known, theequilibrium concentrations of their complexes can becalculated by solving all of the equilibrium equationssimultaneously. A number of commonly-used equilib-rium speciation software programs (e.g., MINEQL,

10 Inorganic Chemicals _ Biogeochemistry of Trace Metals and Mettaloids

MINETAQ, and PHREQC) provide numerical solu-tions, and help to automate the calculation.However, the dominant metal complexes in natural

waters are often complexes with natural organic mat-ter (NOM). Complexation of metals and metalloidswith organic ligands significantly complicates the cal-culation of metal speciation. Metal complexationwith organic ligands ranges from ionic interac-tions with small dissolved ligands to complex inter-actions with colloidal organic matter. The interactionbetween metals and organic matter is a particularlyactive research area. Filter passing NOM, often calleddissolved organic matter (DOM), is composed of rel-atively high-molecular weight organic compounds,such as humic and fulvic acids, the exact compositionof which is difficult to determine. DOM interacts witha variety of dissolved metals and metal complexes,and with major cations (like Ca2þ) that compete forbinding sites with metals, to form complex colloids.Metals interact in a number of ways with DOM,

including ligand interactions, hydrophobic and electro-static interactions with metal ions, and interactionswith neutrally-charged metal complexes. Weakerligands, such as those dominant in humic and fulvicacid, are largely carboxylate sites. NOM also containsstrong metal ligands at lower concentrations. Thesestrong ligands are poorly defined, but likely includethiol, amine, phenol, pyrrole, or pyridine moieties, allof which are used by cells internally to complexmetals.Complexing agents may have single or multiple activesites on a single molecule. For example, ethylenediami-netetraacetic acid (EDTA), a common synthetic com-plexing agent, contains two amine complexing sitesand four carboxylate sites in a single molecule. Com-plexing agents with more than one active site are oftencalled ‘chelators’ from the Greekword ‘chela’ for claw.In natural waters, with relatively low metal concen-trations, nearly all of the filterable metal pool maybe bound up in these ligands, making metals largelyunreactive and unavailable to cells. Exceptions aremolecules specifically excreted by organisms to captureand aid in the transport of essential trace elements intocells (e.g., siderophores, compounds excreted by fungiand bacteria to promote dissolution and uptake ofiron). Weaker binding sites on DOM are filled afterthe strong sites are saturated. Electrostatic interactionsaremore difficult tomodel; however, numericalmodels(e.g., the Windermere humic aqueous model WHAM)have been specifically designed to model theseinteractions.

Phase Partitioning

Complexation or other interactions with the solidphase is often called partitioning. All trace metals

are particle reactive to some extent, meaning theyreadily bind to organic colloids and suspended parti-cles in natural waters, and are removed via particlesettling. This means that most metals are highly con-centrated in sediments and wetland soils relative tosurface waters. Particle reactivity is highly variableamong metals, and depends on nature and strength ofthe interaction. This tendency of trace elements toadsorb to particles is commonly measured as a ‘dis-tribution coefficient’ or kd

kd ¼ Cs=Cw

whereCs is the concentration of the element in the solidphase and Cw is the concentration of the element dis-solved in the water, in the same units. Partition coeffi-cients range from on the order of 105 to 106 for Hg andPb, to as little as 102 or even less for chromate, selenate,and selenite. Partition coefficients also depend stronglyon the water quality, particularly pH, and the concen-trations of other competing ions. Theoretically, thepartition coefficient for a metal in an unsaturated sys-tem should be concentration independent. In practice,this is not always the case.

Oxidation, Reduction, and Speciation

Trace metals may undergo reduction and oxidationvia photochemical, microbial, and geochemical pro-cesses. In the oxidizing environment of most surfacewaters, a relatively oxidized valence state is often themost thermodynamically stable; however, biologicalprocesses and slow oxidation kinetics sometimesresult in significant concentrations of reduced forms.In sediments and anoxic waters, microbial respirationcan produce highly reducing conditions through oxy-gen depletion and by the production of reduced end-products like sulfide, hydrogen, and methane. Inreducing, sulfidic environments, many divalent metals(i.e., Fe, Zn, Cd, and Cu) can form relatively insolublecomplexes with sulfides and precipitate, while othermetals are themselves reduced. For some metals andmetalloids, reduction increases solubility while theopposite is true for others. Dredging, eutrophication,and other anthropogenic influences can change theredox status of sediments, soils, and surface waters,and thus alter the mobility of trace metals.

Iron and chromium are examples of metals thatchange oxidation states between oxic surface watersand anoxic sediments. Under oxic conditions, iron isgenerally found as ferric iron, Fe(III),which forms insol-uble hydroxyl complexes (essentially rust). However,dissolved and colloidal organic matter may hold Fe(III)in the aqueous phase. Under reducing conditions inanoxic water or sediments, Fe(III) is reduced to ferrousiron Fe(II), which is much more soluble and mobile.

Inorganic Chemicals _ Biogeochemistry of Trace Metals and Mettaloids 11

Chromium, a common pollutant metal, is anotherexample of a metal that readily changes valence. Innatural waters, Cr is present in two oxidation states,Cr(VI), generally as soluble CrO4

2� (chromate) orCr2O7

2� (dichromate) depending on pH, or Cr(III),which forms insoluble hydroxides. In oxygenatedwater, Cr(VI) should be favored, while in reducingenvironments, Cr(III) should be favored. However,the kinetics of the reactions between these two formsis very slow, and oxygenated surface waters can con-tain both. The two valences of Cr also have strikinglydifferent biological effects. Cr(III) has relatively lowtoxicity, probably because Cr3þ is relatively poor atpenetrating biological tissue. Cr(VI) species are highlytoxic, because the anionic forms are readily taken upby cells, possibly by sulfate transporters.

Microbial Metal Reduction and Oxidation

Most microbes (and indeed, all nonphotosyntheticorganisms) obtain their energy by facilitating reac-tions that are thermodynamically favored, but kineti-cally slow, and capturing a part of that energy.Indeed, respiration is merely the facilitation of thenatural (but very slow) oxidation of organic matterby atmospheric oxygen. Some bacteria can use tracemetals and metalloids as electron acceptors in placeof oxygen in respiration, coupling metal reduction toorganic matter oxidation for energy generation. Ironand manganese reduction are the best studied of theseprocesses, but uranium, chromium, technetium, sele-nium, arsenic, gold, and others can also be used.Microbial metal reduction may serve as a remediationroute for metals that are more mobile in their oxi-dized forms, like Cr and U. Metals may be reducedvia electron-shuttling compounds excreted outside ofcells, or by uptake and reduction within cells. Most ofthe bacteria that can use metals as electron acceptorsin metabolism are found in among the iron-reducingbacteria and the sulfate- or sulfur-reducing bacteria.Nonmetabolic metal reduction can also occur, amonga wider range of microorganisms. These reductionprocesses may have evolved as metal or metalloidresistance mechanisms.Chemolithotrophic (‘rock eating’) bacteria can use

the zero-valent (metallic) or reduced forms of tracemetals as electron donors in energy generation, oftencoupled to the reduction of inorganic anions likenitrate, selenate, or arsenate. These types of organ-isms are common in acid-mine drainage and in metalcorrosion environments. Acid-mine drainage occurswhen mine wastes with high concentrations of sulfideare exposed to oxygenated water. Sulfide is oxidizedto sulfate with microbial help, making sulfuric acid,and metals are solubilized in the resulting acid

solution. Iron is probably the most important metal inthis behavior, because it is the most common, but otherelements can be used as well, including Mn, As, Se.Similar, if less marked, bacterial action occurs whenreduced sediments or soils are exposed to oxygen.

Biological Uptake, Accumulation, andTransformation of Metals

Uptake of trace elements by algae and bacteria isgenerally the first step in metal accumulation intohigher trophic levels. Microorganisms use active cat-ion transport systems to take up most essential traceelements. These usually operate by binding the metalat the cell surface with strong ligands on the transportprotein and then spending energy in some form (ATP,NADP, proton gradient, etc.) to transport the elementinto the cell. Although dedicated transport systemshave evolved for some trace elements, others may betransported via major cation transport systems.

Metal uptake by algae and bacteria also plays acritical role in the cycling and transport of trace ele-ments in the inland waters. Fixed metals may betransferred through food webs, released back intothe aqueous phase in a variety of forms as cellsdecay, or sequestered in sediments following deposi-tion. A number of microbial uptake pathways haveevolved for acquisition of essential metals. Pathwayshave also evolved for protection against toxic metals,including a variety of redox, speciation, and phasetransformations. These include enzyme systems thatproduce less reactive or more volatile forms of toxicelements (i.e., Se, Hg, As), systems that sequestermetals (metallothioneines, phytochelatins, and min-eral granule precipitates are examples), and excretionsystems. Only a small fraction of the dissolved pool ofany trace metal is generally available for uptake.Early models for metal toxicity and uptake assumedthe entire dissolved metal pool was available.

Over time, models for bioavailability have evolvedto reflect the idea that only certain metal complexesare available for uptake. The free metal ion activitymodel is one paradigm for metal uptake by bacteriaand algae. It postulates that metal uptake is a functionof free (uncomplexed) metal activity in bulk solution.To apply the free ion activity model, equilibriumgeochemical models are used to calculate the concen-tration of free metals cations in the milieu of ligandsand competing cations in natural waters.

The Biotic Ligand Model (BLM) is a commonly-used mathematical framework for determining thebioavailability and toxicity of metals in naturalwaters. It is an extension of the free ion activitymodel, based on the idea that metal transport pro-teins on the surfaces of cells act as competing ligands

12 Inorganic Chemicals _ Biogeochemistry of Trace Metals and Mettaloids

for free metal cations, so that metal uptake can bemodeled using geochemical equilibrium models. TheBLM was derived from models for metal uptake byfish gills, and is often used to generate site-specificambient water quality criteria for metals.However, some metal uptake mechanisms are not

captured by the free ion activity and biotic ligandmodels. These include uptake mechanisms that usean extracellular complexing agent to capture metalsfor transport (e.g., siderophores or biofilms). Cellsmay also take up metals via diffusion of neutrally-charged complexes (Hg, Ni, and Ag are examples) orthrough the uptake of metals bound to amino acids(e.g., Se). Metalloids are dominantly found as oxy-anions in surface waters, and are taken up in thatform. They can be taken up via transport systems foranalogs like phosphate (arsenate) or sulfate (selenate),or through metalloid-specific transport systems.Therefore, metalloid bioavailability is determined bythe concentration of metalloid oxyanions, competingoxyanions, and the nutrient status of organisms.

Metal Resistance Mechanisms

A wide variety of metal-resistant mechanisms haveevolved inmicroorganisms. In bacteria, themost com-mon metal resistance mechanism is removal fromcells through energy-dependant efflux mechanisms.Metals present as divalent cations (Ag, Cd, Co, Cu,Ni, and Zn) are often detoxified in this way. Lesscommonly, enzymatic reduction, oxidation, chelation(oftenwithmetallothioneins), or sequestration are usedfor metal detoxification. Metalloid oxyanions (i.e.,arsenate, selenite) can be detoxified by methylationto produce less toxic and/or more volatile forms.Long-term exposure of microbial populations tohigh-metal environments selects for resistant strains.Metal resistance genes may be specific to one metalor a group of similar metals, and are often carriedon mobile genetic elements with antibiotic resis-tance genes. Human use of metals may enhance thenumber and type of metal- and antibiotic-resistantmicroorganisms.

Example: Arsenic and Selenium

Arsenic and selenium speciation, transport, andtoxicity in natural waters are strongly affected bymicrooganisms. Arsenic is present in the surfacewaters in at least two valences, As(V) (primarily asarsenate) and As(III) (as arsenite), and a variety oforganic arsenic compounds, nominally As(�III).Oxic waters favor As(V), and sufficiently reducingconditions favor As(III) (Figure 2). However, in oxicfresh and marine waters, high concentrations of

arsenite and monomethyl and dimethyl arsine areoften observed in conjunction with phytoplanktonblooms. Phytoplanktons take up arsenate (AsO4

3�)as a phosphate (PO4

3�) analog, especially under con-ditions where phosphate limits phytoplankton growth.Many algae and bacteria have developed chemicalpathways to reduce arsenate to arsenite and/or volatilemethylated arsenic compounds, and excrete these com-pounds. In bacteria, the ars operon (one of the mostwidely distributed operon systems) confers arsenicresistance. It commonly includes a regulator gene andan efflux pump.Other arsenic oxidation and reductionsystems also exist in bacteria, both for detoxificationand arsenate respiration.

Selenium is taken up by plants, including algae, asa required nutrient. Selenium is a partial sulfurmimic, and forms seleno-amino acids in cells.Seleno-cysteine is an essential part of the active sitesof a few important enzymes. Cells release a poorlydefined group of organic selenium compounds, whichcan constitute a significant fraction of the total Se insurface waters. Selenium can be accumulated throughfood webs in amino acid complexes. Algae and bac-teria can produce volatile methylated Se compounds,dimethylselenide and dimethyldiselenide (similar toAs compounds), which can be lost from surfacewaters. Some anaerobic bacteria can also reduce sele-nate and selenite to elemental selenium, coupling Sereduction to energy generation, in process analogousto microbial sulfate reduction. This can be a major Sedetoxification mechanism in sediments and wetlandsoils. Bacterial and algal Se reduction can also occurthrough processes that do not generate energy, andmay confer resistance.

Example: Mercury

Mercury is an example of a metal whose toxicityand bioaccumulation in natural waters is largelycontrolled by microbial transformation to methyl-mercury. The biogeochemistry of Hg is elaborateand contributes greatly to its role as a contaminant(Figure 3). It is the only metal found as a liquid atroom temperature, has a high vapor pressure andsignificant cycling in the atmosphere. It is readilyreduced and oxidized, so that microbial, chemical,and photochemical redox processes play importantroles in its cycling.

A small percentage of the inorganic Hg in the envi-ronment is converted to the highly toxic and highlybioaccumulated monomethyl mercury (MeHg).Worldwide, MeHg contamination of fisheries hasresulted in more consumption advisories than anyother contaminant. For humans, concern has centered

AsO32− AsO4

3−Organic As

AsO32−(CH3)2 AsO2

+(CH3)AsO

32+

AsAs

AsAsAs

AsAsAs

As

As

Settlingresuspension

Diffusionadvection

Settlingbenthic feeding

Oxidation

Excretion ofdimethyl As

Bottom feedingdeath and decay

Sulfidic sediment

Trophictransfer

(CH3)2AsO2+

AsO43−

AsO32−

AsS(s)

Organic As

(CH3)2AsC2O2H Excretion ofarsenite

Aerobic sediment

Suboxic sediment

Excretionhigher trophic levels

Monomethyl arsenicArseniteDimethyl arsenic

Arsenate

AsO43−

Arsenobetaine

Adsorptiondesorption

Phytoplankton

Fe(OH)3(s) MnO2(s)

Fe2+ Mn2+

FeS(s) MnS(s)

Microbially mediatedoxidation and reduction

Figure 2 A diagram showing many of the specific forms and major processes known to affect the cycling and speciation of arsenic

in aquatic ecosystems.

Inorganic Chemicals _ Biogeochemistry of Trace Metals and Mettaloids 13

on developmental effects, particularly reductions in IQ,which have constituted the basis for risk assessmentsand public health policies. However, there are healthhazards associatedwith exposure toMeHg throughoutthe lifespan, including potential cardiovascular andendocrine impacts. In wildlife, MeHg has significantimpacts on the reproductive success of a numberof species at concentrations commonly found in atmos-pherically-contaminated ecosystems.

MeHg Production

The sensitivity of an aquatic ecosystem to mercuryis determined by the ability of that ecosystem totransform inorganic Hg load into MeHg in biota.For Hg to impact an aquatic ecosystem, mercurymust be transported from sites of deposition to sitesof methylation, it must undergo methylation, andthe MeHg produced must be accumulated in foodwebs. Transport of Hg through watersheds is com-plex, and retention of Hg is watersheds may bevery long (decades to centuries). Key controllingfactors include watershed size, with decreasingHg yields as watershed size increases, and land

development and disturbance, which enhance Hgtransport downstream.

Methylmercury production is a microbial process,occurring mainly under the anoxic conditions foundin aquatic sediments, wetlands, and other hydricsoils. It appears to be a inadvertent side reaction ofnormal metabolism. Methylation is not a detoxifica-tion mechanism nor does it confer Hg resistance.Although a strong link to microbial sulfur cycling isclear, the pathways and distribution of Hg-methylatingorganisms have not been well characterized. Dis-similatory sulfate-reducing bacteria (DSRB) areimportant mediators of MeHg production in aquaticecosystems. Sulfate stimulation of methylation hasbeen demonstrated in studies that range from purebacterial culture to field amendments to lakes andwetlands. Control of sulfur sources to freshwaterecosystems – including control of sulfur emissionsand control of sulfur in agricultural runoff – can bean effective strategy to reduceMeHg risk. A few otherbacterial groups that produce MeHg have been iden-tified, particularly iron-reducing bacteria, and therole of these organisms in methylation in naturalsystems is being investigated.

Emission and transportOxidation

Volatilization

Wet and drydeposition

Methylation

Runoffand inflow

Settling/resuspdiffusion

Burial

Bioaccumulation

Hg(0)

Hg(0)

Hg(II)

Hg(II)

Hg(II)

MeHg

MeHg

Oxidation

ReductionPhotodegradation

Demethylation Methylation

Figure 3 Mercury cycling in a lake and its watershed. Mercury emissions are transported long distances, primarily as gaseous

elemental mercury [Hg(0)], oxidized in the atmosphere to reactive gaseous mercury [Hg(II)], and deposited in precipitation and bysurface contact (dry deposition). Anaerobic bacteria convert a small portion of the incoming Hg(II) to methylmercury (MeHg), which is

then bioconcentrated in the aquatic food chain. Various biotic and abiotic reactions interconvert the different forms of Hg, affecting

uptake, burial, and evasion back to the atmosphere. From Engstrom D (2007) Fish respond when mercury rises. PNAS 104:

16394–16395. www.pnas.org/cgi/doi/10.1073/pnas.0708273104.

14 Inorganic Chemicals _ Biogeochemistry of Trace Metals and Mettaloids

MeHg Demethylation and Hg Reduction

Demethylation of MeHg is largely a microbial processin sediments and soils, although photo-demethylationis important in lighted surface waters. Mechanisms todetoxify Hg and MeHg via reduction and demethyl-ation are common among bacterial communities, andthe genetics and distributions of these systems arefairly well understood. In bacteria, demethylation andreduction often proceed via the highly specific andevolved mer operon system, although other, less well-characterizedpathwaysexist.

Temporal and Spatial Controls on Net Hg

Methylation

Wetlands can be particularly active zones of MeHgproduction, although highly dependant on flow pathsthat govern the location and extent of zones of micro-bial activity. Reservoir formation, soil drying, andrewetting cycles (including seasonal cycles in wet-lands) can increase net MeHg production becauseof increased decomposition rates, sulfur oxidationduring drying, and development of anoxia afterrewetting. In freshwater aquatic ecosystems, warm,shallow sediments and the anoxic bottom waters ofstratified lakes and estuaries are important zones ofnet methylation. Estuarine and coastal sediments arealso significant net producers of MeHg.

MeHg Accumulation in Food Webs

Methylmercury concentrations increase by roughly afactor of 10 at each step through a food chain, andMeHg fish tissue concentrations increase substan-tially with age. Of the ‘persistent bioaccumulativepollutants,’ only PCBs exhibit comparable bioconcen-tration factors. Although field and experimental evi-dence clearly indicate that Hg loading rates affect fishHg concentrations, MeHg concentrations in fish canvary by an order of magnitude or more in regions withsimilar atmospheric Hg deposition rates as a result ofthe factors that control production and accumulationof MeHg. Comparisons of MeHg bioaccumulationacross water bodies must include consideration ofspecies, food web structure, and fish size.

Solving the Mercury Problem

Fortunately, Hg availability for methylation andbioaccumulation decreases as it ages in place in sedi-ments and soils. This means that recently depositedmercury contributes disproportionately to currentMeHg levels in fish, and that Hg emissions controlshould help reduce MeHg levels in fish in the near-term, despite 150 years’ of accumulated mercury inour watersheds.

Recently, the United States and other developedcountries have begun to implement direct emissions

Inorganic Chemicals _ Biogeochemistry of Trace Metals and Mettaloids 15

controls on coal-fired utilities. Most new Hg emis-sions worldwide come from combustion processes:coal burning, trash burning, and cement production.Controls on major point sources of Hg have beenin place for some time in developed nations. Effortsto reduce Hg emissions in North America and Europemay be overshadowed by the growing energydemands of the developing nations. Controls on dif-fuse sources of Hg – such as batteries, switches,and thermometers – have also been implemented.Fluorescent light bulbs contain small amounts of Hgthat are difficult to contain because of lack of recy-cling programs. Their increased use must be balancedagainst Hg emission reductions that result frommore efficient lighting. Metallic mercury use in goldmining in developing nations remains a direct humanhealth risk.The complexity of the atmospheric and biogeo-

chemical cycles of this element, and the widespreadimpact of Hg on people and ecosystems, necessitatesthe development of carefully designed Hg monitoringprograms to assess the effectiveness of our regulatoryactions.

Further Reading

Andren AWand Bober TW (eds.) (2002) Silver in the Environment:Transport, Fate, And Effects, pp. 192. Pensacola, FL, USA: Soci-ety of Environmental Toxicology and Chemistry (SETAC).

Campbell PCG (1995) Interactions between trace metals andaquatic organisms: A critique of the free-ion activity model. In:

Tessier A and Turner DZ (eds.) Metal Speciation and Bioavail-ability in Aquatic Systems. IUPAC Series on Analytical andPhysical Chemistry of Environmental Systems, pp. 45–102.Chichester: Wiley.

Fasfous II, Yapici T, Murimboh J, et al. (2004) Kinetics of trace

metal competition in the freshwater environment: Some funda-mental characteristics. Environmental Science and Technology38: 4979–4986.

Lindberg S, Bullock R, Ebinghaus R, et al. (2007) A synthesis of

progress and uncertainties in attributing the sources of mercuryin deposition. Ambio 36: 19–33.

Lloyd JR (2003) Microbial reduction of metals and radionuclides.

FEMS Microbiology Reviews 27: 411–425.

Mason RP, Abbott ML, Bodaly RA Jr, et al. (2005) Monitoring the

response to changing mercury. Environmental Science and Tech-nology 39: 14A–22A.

Meyer JS, Clearwater SJ, Doser TA, Rogaczewski MJ, and Hansen

JA (eds.) (2007) Effects of Water Chemistry on Bioavailabilityand Toxicity of Waterborne Cadmium, Copper, Nickel, Lead,and Zinc to Freshwater Organisms, pp. 352. Pensacola, FL,

USA: Society of Environmental Toxicology and Chemistry

(SETAC).

Monastersky R (1996) Ancient metal mines sullied global skies.Science News 149: 230.

Munthe J, Bodaly R, Branfireun B, et al. (2007) Recovery of mer-

cury-contaminated fisheries. Ambio 36: 33–44.

Nelson WO and Campbell PGC (1991) The effects of acidificationon the geochemistry of Al, Cd, Pb and Hg in fresh-water envir-

onments – A literature-review. Environmental Pollution 71:

91–130.Oremland RS, Stolz JF, and Hollibaugh JT (2004) The microbial

arsenic cycle in Mono Lake, California. Fems MicrobiologyEcology 48: 15–27.

Riedel GF, Williams SA, Riedel GS, Gilmour CC, and Sanders JG(2000) Temporal and spatial patterns of trace elements in the

Patuxent River: A whole watershed approach. Estuaries 23:

521–535.

Santschi PH, Lenhart JJ, and Honeyman BD (1997) Heterogeneousprocesses affecting trace contamination distribution in estuaries:

the role of natural organic matter.Marine Chemistry 58: 99–125.Scheuhammer AM, Meyer MW, Sandheinrich MB, and Murray

MW (2007) Effects of environmental methylmercury on the

health of wild birds, mammals, and fish. Ambio 36: 12–19.

Stolz JE, Basu P, Santini JM, and Oremland RS (2006) Arsenic and

selenium in microbial metabolism. Annual Review of Microbiol-ogy 60: 107–130.

Stumm W and Morgan JJ (1996) Aquatic Chemistry, 3rd. edn.

New York: John Wiley and Sons.

Relevant Websites

http://www.webelements.com/ – WebElements.

http://www.atsdr.cdc.gov/toxfaq.html – ASTDR ToxFAQs.

http://www.dartmouth.edu/~toxmetal/TX.shtml – Dartmouth ToxicMetals Program.

http://nadp.sws.uiuc.edu/mdn/ – Mercury Deposition Network.

http://www.chem.unep.ch/chemicals/default.htm – UNEP Chemi-

cals Programme.http://www.epa.gov/mercury/ – EPA Mercury homepage.

http://www.epa.gov/waterscience/criteria/ – EPA Water Quality

Criteria.