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Biogeochemistry (2007) 85:9–24
DOI 10.1007/s10533-007-9103-5ORIGINAL PAPER
A conceptual model of organo-mineral interactions in soils: self-assembly of organic molecular fragments into zonal structures on mineral surfaces
M. Kleber · P. Sollins · R. Sutton
Received: 11 March 2006 / Accepted: 27 November 2006 / Published online: 15 June 2007© Springer Science+Business Media B.V. 2007
Abstract In this paper, we propose a structurefor organo-mineral associations in soils based onrecent insights concerning the molecular struc-ture of soil organic matter (SOM), and on exten-sive published evidence from empirical studies oforgano-mineral interfaces. Our conceptualmodel assumes that SOM consists of a heteroge-neous mixture of compounds that display a rangeof amphiphilic or surfactant-like properties, andare capable of self-organization in aqueous solu-tion. An extension of this self-organizationalbehavior in solution, we suggest that SOM sorbsto mineral surfaces in a discrete zonal sequence.In the contact zone, the formation of particularlystrong organo-mineral associations appears to befavored by situations where either (i) polarorganic functional groups of amphiphiles interactvia ligand exchange with singly coordinated mineral
hydroxyls, forming stable inner-sphere com-plexes, or (ii) proteinaceous materials unfoldupon adsorption, thus increasing adhesivestrength by adding hydrophobic interactions toelectrostatic binding. Entropic considerationsdictate that exposed hydrophobic portions ofamphiphilic molecules adsorbed directly to min-eral surfaces be shielded from the polar aqueousphase through association with hydrophobic moi-eties of other amphiphilic molecules. This pro-cess can create a membrane-like bilayercontaining a hydrophobic zone, whose compo-nents may exchange more easily with the sur-rounding soil solution than those in the contactzone, but which are still retained with consider-able force. Sorbed to the hydrophilic exterior ofhemimicellar coatings, or to adsorbed proteins,are organic molecules forming an outer region,or kinetic zone, that is loosely retained by cationbridging, hydrogen bonding, and other interac-tions. Organic material in the kinetic zone mayexperience high exchange rates with the sur-rounding soil solution, leading to short residencetimes for individual molecular fragments. Thethickness of this outer region would depend moreon input than on the availability of binding sites,and would largely be controlled by exchangekinetics. Movement of organics into and out ofthis outer region can thus be viewed as similar toa phase-partitioning process. The zonal conceptof organo-mineral interactions presented here
M. Kleber (&)Earth Sciences Division, Lawrence Berkeley National Laboratory, One Cyclotron Road, Berkeley, CA, 94720, USAe-mail: [email protected]
P. SollinsDepartment of Forest Science, Oregon State University, Corvallis, OR, 97331, USA
R. SuttonDepartment of Environmental Science, Policy and Management, University of California, #3114 Mulford Hall, Berkeley, CA, 94720-3114, USA
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oVers a new basis for understanding and predictingthe retention of organic compounds, includingcontaminants, in soils and sediments.
Keywords Multilayer · Adsorption · Soil organic matter · Nitrogen · Protein · Amphiphilic · Organo-mineral · Micelle · Humic
Introduction
Decades ago, earth scientists acknowledged theability of mineral particles to protect soil organicmatter (SOM) from biological attack (Jung 1943;Allison et al. 1949). In temperate, cultivated soils,50–75% of SOM exists within clay-sized organo-mineral particles (Christensen 2001), and numer-ous researchers have reported positive correla-tions between the contents of Wne mineralparticles and carbon in soils (Körschens 1980;Nichols 1984; Burke et al. 1989; Mayer and Xing2001). As a consequence, it is widely assumed thatthe inhibiting eVect of soil minerals on decompo-sition can inXuence strongly the turnover of SOM(Martin and Haider 1986; Theng et al. 1992;Hsieh 1996; ParWtt et al. 1997). It follows thatunderstanding SOM stabilization requires knowl-edge of the processes operating at the organo-mineral interface. Of particular importance butgreat complexity are the questions of howstrongly SOM may bind to mineral surfaces, howsuch bonds form and eventually break, and howthe mechanisms of attachment of SOM to mineralsurfaces aVect its residence time in soils.
While the characteristics of mineral surfacesare reasonably well known, the chemical proper-ties of SOM continue to be the subject of muchdebate. After all, while minerals crystallizetowards or dissolve from a deWned and compara-tively simple crystal structure, SOM encompassesorganic molecules representing both compoundsreleased from living plant and microbial cells(e.g., extracellular enzymes, surface-active pro-teins, chelating compounds, and many others)and complex plant, microbial and animal residuesin various stages of alteration due to both bioticand abiotic processes (Baldock and Skjemstad2000). Considerable spectroscopic evidence(Chien et al. 1997; Engebretson and von
Wandruszka 1997, 1998; von Wandruszka 1998;von Wandruszka et al. 1999; Ferreria et al. 2001;Martin-Neto et al. 2001; von Wandruszka andEngebretson 2001; Nanny and Kontas 2002) indi-cates that soluble mixtures of organic moleculesrepresenting a signiWcant fraction of SOM canform organized structures called micelles withinaqueous solution, structures that consist of hydro-philic exterior regions that shield hydrophobicinteriors from contact with water molecules (vonWandruszka 1998). Because amphiphilic mole-cules are requisite to the formation of micelles,the ability of SOM components to form thesestructures suggests that many of these moleculesare amphiphilic. SigniWcant to this insight, Wer-shaw (1993) previously developed a bilayer modelof organo-mineral interactions (Fig. 1) thatsharply contrasted with the traditional view oforgano-mineral interactions (Stevenson 1985),which were visualized as associations of large,multifunctional polymers with mineral surfacesvia a broad range of bonding mechanisms (Ste-venson 1985; Leinweber and Schulten 1998). Fur-ther, Wershaw and Pinckney (1980) postulatedthat decayed organic materials are often bound toclay surfaces by amino acids or proteins, based onthe observation that deamination of organo-min-eral complexes with nitrous acid released organicmaterials from the clay.
It is our intention to develop this earlier workinto a generally applicable concept of the zonalstructure of organo-mineral associations (Fig. 2),based on the amphiphilicity of SOM fragments,and the intimate involvement of proteinaceouscompounds in stable organo-mineral associations.As deWned here, a zonal structure is formed whenthe organic matter attached to a mineral surface issegregated into more than one layer or zone ofmolecules, such that not all adsorbed moleculesare in contact with the mineral surface. Assumingsuch a zonal structure, we are able to accountsimultaneously for a number of phenomenaobserved in soils and sediments, including:
a) The decrease of C/N ratio with decreasingparticle size (Hedges and Keil 1995; Aufdenk-ampe et al. 2001);
b) The decrease of C/N ratio with increasingparticle density (Sollins et al. 2006);
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Biogeochemistry (2007) 85:9–24 11
c) The decrease of 14C content with decreasingC content in heavy fractions (Sollins et al.2006);
d) The preferential sorption of large, hydropho-bic organic compounds in sorption experi-ments with soils (Jardine et al. 1989; Guo andChorover 2003) and in marine/estuarine sedi-ments (Zhou et al. 1994);
e) The existence of at least two diVerent C andN pools in heavy fractions: an older, more sta-ble pool of C and N, and a more recent, fastcycling pool of C and N (Trumbore et al.1989; Strickland et al. 1992; Swanston et al.2005);
f) The observation that mineral-associatedorganic matter accumulates in A horizonsbeyond levels consistent with monolayer cov-erage (Eusterhues et al. 2005);
g) The correlation of concentrations of poorlycrystalline mineral phases with amounts ofoxidation-resistant SOM (Kleber et al.2005);
h) Seasonal changes in water repellency in soils(Horne and McIntosh 2000).
To support the concept of zonal structure oforgano-mineral complexes, we Wrst discuss theidea of SOM as consisting of associations oforganic molecules capable of micellar self-organi-zation in aqueous solution. Given this importantconcept, it is appropriate to view a signiWcant por-tion of SOM as consisting of a mixture of diversebut typically amphiphilic molecules. We will pres-ent empirical evidence that supports the idea of azonal structure of organic accretions on mineralsurfaces, demonstrate the special importance ofproteinaceous compounds for the architecture ofthis structure, and show that the assumption ofdiVerent zones of sorption implies diVerentialexchange kinetics for organic fragments movinginto and out of individual zones.
Amphiphilic molecules and the micellar association model of soil organic matter
Critical insights regarding organo-mineral com-plexes arose from studies probing the behavior of
Fig. 1 The “Wershaw bilayer model” of organo-mineralinteractions (Wershaw et al. 1996a). Figure adapted from Es-sington (2003). Accumulation of amphiphilic fragments onsoil surfaces is initiated by electrostatic interactions between
hydrophilic organic moieties and surface oxygens or hydrox-ylated surface-metal cations. The hydrophobic portions ofthese surface molecules are shielded from the polar aqueousphase by a second layer of amphiphiles, forming a bilayer
Hydroxylatedmineralsurface
Electrostatic interactionwith soluble ions
Direct bond with surface metal cation
O
Al
O
Al
O
Al
O
O
Al
O
Al
O
Al
CH 3O
P
OO
OH
CH 3
O
O
CH 3
O
O
CH 3
O
O-
CH 3
O
O-
CH 3
O
O-
CH 3NH 3
+Ca
2+
Mg2+
Ca2+
Mg2+
OH
O
H
H
O
H
H
O
H
H
O
H
H
O
H
H
O
H
H
O
Hydrophobicstructures
Hydrophilicfunctional groups
Na+
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12 Biogeochemistry (2007) 85:9–24
natural organic fractions in aqueous solution. Toexamine and manipulate the behavior of thesecomplex organic materials within a controlledlaboratory environment, alkaline extraction isoften used to solubilize a large portion of SOM,producing an operationally deWned humic frac-tion. That alkaline extraction eVectively removesbetween 50% (Rice 2001) and 80% (ScheVer andSchachtschabel 2002) of the organic material insoil samples indicates that while the humicfraction represents only a portion of SOM, it is a
signiWcant portion of this organic material, and itcontains many reactive polar or charged moietiesthat respond to pH. In addition, behavior consis-tent with micellar organization, observed using adiverse array of spectroscopic techniques includ-ing Xuorescence (Engebretson and von Wan-druszka 1997, 1998; von Wandruszka 1998; vonWandruszka et al. 1999; von Wandruszka andEngebretson 2001; Nanny and Kontas 2002), elec-tron spin resonance (Ferreria et al. 2001; Martin-Neto et al. 2001), and nuclear magnetic resonance
Fig. 2 The zonal model of organo-mineral interactions.The variety of surface types in soils is represented by a low-charge smectite, a hydroxylated Fe-oxide coating, and ahydrophobic kaolinite siloxane surface. This selection ismeant to illustrate major bonding mechanisms, and is notintended to represent the full range of mineral surfacetypes that may be encountered in soils. In the contact zone,amphiphilic fragments accumulate on charged surfacesthrough electrostatic interactions, directing hydrophobicportions outwards toward the polar aqueous solution. Pro-teins serve as a surface conditioner that adds polar func-tionality to low-charge siloxane surfaces. Somehydrophobic organic compounds may also associate withnoncharged mineral surfaces. The zone of hydrophobicinteractions is equivalent to the hydrophobic region formedas part of the Wershaw bilayer model, and results from theentropically driven shielding of the hydrophobic portions
of adsorbed organic molecules from the polar aqueousphase by a second layer of amphiphilic molecules. Thehydrophobic zone is thought to be discontinuous, as someproteins directly adsorbed to mineral surfaces may well ex-pose ionized or polar functional groups towards the soilsolution. In the outer region or kinetic zone, further accu-mulation of organic molecular fragments is possible, prob-ably largely mediated by the presence of multivalentcations. Depending on stereochemical orientation, degreeof amphiphilicity, cation content of the soil solution, pH,temperature, and perhaps several other controlling factors,a variety of modes of attachment of organic molecular frag-ments to the intermediate region appears to be possible.The thickness of the outer zone is likely to depend on inputof organic materials and thus to be largely be controlled byexchange kinetics
CH3
O
O-
OHO
P
OOH
OFe
OH
O
OFe
O-
OOH
CH3
O
O-
low charge2:1 mineral(smectite)
with proteinconditioning
2:1mineral
withcoating
ofhydrous
ironoxide
uncharged1:1
siloxane(kaolinite)
Fe
OH
Fe
Fe
OH
Fe
contactzone
kinetic zone(outer region)
= octahedral charge
= tetrahedral charge
O
H
H
zone of hydrophobicinteractions
O-
O-
CH 3
O
O-
O
CH3
O
O-
O
CH 3
CH3
O
O-
OH
O-
O
CH 3
CH3
O
O-
OH
O
O-
O
O-
CH 3
CH 3
OH
O
O
O
OH
Fe
M2+
M2+
M2+
M2+
M2+
M2+
M2+
M2+
M2+
M2+
M2+ = metal cation
O
H
H
M2+
NHOH
O-
O
O-
O
CH3
O-
O
O
O- OH
NH3+
NH
NH
NH
R
O
O
O
R
SH 2+
O-
O
R
R
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Biogeochemistry (2007) 85:9–24 13
(Chien et al. 1997), suggests that nonpolar moie-ties are also present within humic fractions. Afterall, it is the presence of hydrophobic functionalgroups within amphiphilic molecules that triggersentropically-driven self-organization to shieldthese nonpolar moieties from the polar aqueousmedium through formation of a micelle. Thus, theobservation of micellar structure within humicextracts representing a major portion of SOMindicates that a signiWcant fraction of the mole-cules making up this complex organic material areamphiphilic in nature.
The components of decomposing SOM displaya range of functional qualities based on chemicaland structural composition (Sutton and Sposito2005). We suggest that these chemical propertiesrepresent a continuum of amphiphilicity thatranges from molecules that are solely nonpolarand hydrophobic, to those that are predomi-nantly amphiphilic because they also containhydrophilic, highly polar or charged functionalgroups. Nonpolar, hydrophobic compounds arecomposed predominantly of alkyl and aromaticfunctional groups, and may derive from sourcessuch as plant waxes and cutins. Occupying themid-range of this chemical continuum are mildlypolar materials, such as many carbohydrates andtheir derivatives, which feature functional groupslike alcohols or ethers that do not ionize undertypical soil and water pH conditions. In additionto hydrophobic functional groups, the amphi-philic compounds that populate the otherextreme of this chemical spectrum contain morereactive functional groups like carboxyls andamines, which can develop charge under typicalsoil and water pH conditions. The dominant roleof amphiphilic molecules in the behavior of com-plex organic mixtures within aqueous environ-ments cannot be ignored when considering themechanisms by which SOM adsorbs to mineralsurfaces.
Experimental evidence in support of a zonal structure of organic accretions on mineral surfaces
While mounting experimental evidence (Chienet al. 1997; Engebretson and von Wandruszka
1997, 1998; von Wandruszka 1998; von Wan-druszka et al. 1999; Ferreria et al. 2001; Martin-Neto et al. 2001; von Wandruszka and Engebret-son 2001; Nanny and Kontas 2002) supports theability of complex natural organic substances toself-assemble into associations featuring regionswith diVerent chemical properties, similar behav-ior is not typically ascribed to SOM adsorbed tomineral surfaces. However, starting with the pre-viously mentioned work by Wershaw and col-leagues (Wershaw and Pinckney 1980; Wershaw1986; Wershaw 1993), information from a broadrange of scientiWc Welds has provided numerousclues suggesting that SOM sorbs to minerals inlayers or zones that may have diVerent chemicalor functional properties. In the following sectionswe use (i) the fate of organic pollutants in soils,sediments, and aquifers, (ii) the distribution oforganic matter over mineral surfaces in naturalsystems, (iii) information from density fraction-ation experiments, (iv) evidence from the study ofwater repellency in soils, and Wnally, (v) dataobtained through laboratory synthesis of layeredorgano-mineral structures, to draw inferencessuggesting that organic accretions on mineralsconsist of multiple zones of self-assembling mate-rials.
Sorption of organic compounds to organic coat-ings on mineral surfaces as a model of zonal org-ano-mineral architecture
The idea that organic matter covers mineral sur-faces in a layered or zonal fashion (Fig. 2) is notnew (Chassin 1979), with most early concepts oforganics sorbing to mineral surfaces in two ormore layers resulting from a wealth of studies onthe fate of organic pollutants in soils, sediments,and aquifers. A review of this early work ledVoice and Weber (1983) to conclude that,although hydrophobic bonding was a major sorp-tion mechanism for hydrophobic compounds, nosingle sorption mechanism adequately explainedall experimental observations. Instead, Weberet al. (1983) state that “the organic carbon contentof a solid appears to be the major factor in deter-mining its sorptive capacity.”
A step forward in advancing mechanisticknowledge about zonal arrangements of organic
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14 Biogeochemistry (2007) 85:9–24
molecules on mineral surfaces was taken by Mur-phy et al. (1990), who, following up on the workof Hunter and Liss (1982) among others, foundthat hydrophilic mineral particles exposed tohumic fractions developed hydrophobic surfaces,rendering them more capable of sorbing hydro-phobic organic compounds. Hydrophobic interac-tions bind the outer layer hydrophobiccompounds to the inner layer organics becausethe total hydrocarbon surface that is exposed towater is reduced, and entropy maximized, whenhydrophobic entities organize to reduce the non-polar surface area exposed to water molecules.Jardine et al. (1989) provided additional supportfor the importance of hydrophobic interactions toadsorption of organic materials by comparing thesorption of dissolved organic carbon solutionsthat had been fractionated into operationally deW-ned hydrophobic and hydrophilic organic por-tions. Hydrophobic organic solutes werepreferentially adsorbed by soils relative to hydro-philic organic solutes, leading the authors to con-clude that hydrophobic interactions driven byfavorable entropy changes represent the primarymechanism of adsorption for these organic sol-utes. Murphy et al. (1990) further showed that thenature of the mineral surface, particularly theconcentration and spatial distribution of hydroxylsites, inXuenced the amount of hydrophobicorganic C adsorbed to organic coatings. Thechemical properties of the humic fraction used tocoat the mineral particles inXuenced the amountof hydrophobic compounds adsorbed, with themost aromatic humic material being the strongestsorbent for hydrophobic material.
Patchy organic matter distributions on mineral surfaces indicate zonal architecture of sorbed materials
Further evidence for the zonal or layered sorp-tion of organic matter to mineral surfaces comesfrom the examination of natural organo-mineralcomplexes taken from soil and marine systems.Both speciWc surface area (SSA) determinationsand microscopic analyses indicate that thedistribution of organic materials on the mineralsurfaces of soils (Mayer and Xing 2001; Kahle
et al. 2002) and marine sediments (Ransom et al.1998; Mayer 1999) is typically discontinuous.While organic matter loadings on sedimentarymineral surfaces are often on the order of the so-called monolayer equivalent of 0.5–1.0 mgorganic C m¡2 (Keil et al. 1994; Mayer 1994), thefact that organic material is not distributedevenly over the available mineral surface indi-cates that the material must instead be clusteredin small patches with some vertical extension.Aluminosilicate sediments with low to moderateloadings of organic matter (<3 mgorganic C m¡2) generally have less than 15% oftheir surfaces coated, with organic materialsexisting in discrete spots on the mineral surfaces(Arnarson and Keil 2001).
Speculations about a layered architecture ofthese patches have been voiced by Kaiser andGuggenberger (2003), who found that thereduction of SSA following sorption of increas-ing amounts of DOC was not uniform: thedecrease in SSA was larger at smaller organicmatter loadings than at larger ones. Amongother potential explanations, they hypothesizedthat “with increasing surface loading an increas-ing portion of the sorbing molecules did notattach to mineral surfaces but formed organicmultilayers as a result of hydrophobic interac-tions or bridging by polyvalent cations betweenorganic ligands of sorbed and soluted mole-cules.” This interpretation was subsequentlysupported by the work of Wang and Xing(2005), who found that, even under diVerentorganic matter loading levels, mineral surfacecoverage remained nearly constant, indicatingthat “the coating must have increased in thick-ness while retaining practically the same surfacecoverage at a higher loading. In such a multilayerarrangement, the Wrst several molecular layersclose to the mineral surface may take a morecompacted form due to the attractive forces of themineral surface.” In addition, ocean sedimentstudies show a direct relationship betweenorganic matter content and mineral surface areaat organic loadings 2–5 times that of a mono-layer equivalent (Hedges and Keil 1995), furthersupporting the existence of minerals coated withmultiple layers of organic molecules.
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Biogeochemistry (2007) 85:9–24 15
Organo-mineral associations isolated through density fractionation may also suggest a zonal architecture of sorbed materials
In addition to the ocean sediments describedabove (Hedges and Keil 1995), soil particles iso-lated through density fractionation have also pro-vided evidence indicating that organic material issorbed to minerals through both direct and indi-rect interactions with mineral surfaces. Euster-hues et al. (2005) found that organic matterloadings in heavy fractions (>2 g cm¡3) from aseries of topsoils were greater than could beexplained solely by direct attachment to the avail-able mineral surfaces area in a monolayer fashion.They hypothesized that interactions betweenorganic molecules leading to greater than mono-layer coverage would be necessary to explain thelarge amounts of sorbed organic material (Eus-terhues et al. 2005).
Organic C in the heavy fraction of soils is com-monly seen as being closely associated with min-erals and typically more depleted in 14C thanlight-fraction material, which is not intimatelybound to minerals (Trumbore and Zheng 1996).However, when Swanston et al. (2005) traced anatmospheric 14C pulse into a forest ecosystem,they noticed that the elevated 14C signal appearednot only in the light fraction, but also in thestrongly mineral-associated dense fraction. Theyinterpreted this observation as indicating the exis-tence of at least two diVerent C pools in the org-ano-mineral fraction: an older, more stable poolof C, and a younger, fast cycling C pool. Strick-land et al. (1992) found similarly that 15N-labeledinorganic N was incorporated rapidly into dense(organo-mineral) fractions of Wve soils of greatlydiVering mineralogy, then released as both inor-ganic and organic N during a subsequent incuba-tion. The existence of rapidly cycling C and N inthe dense or mineral-associated fraction can satis-factorily be explained by a zonal structure oforganic accretions on mineral surfaces. While theorganic materials directly adsorbed to the mineralsurface are likely to be tightly bound and wellprotected from microbial degradation, the materi-als sorbed in outer regions of the organo-mineralcomplex, and lacking direct interaction with themineral surface, are presumably more loosely
bound and more readily desorbed or decom-posed. That only part of the mineral-bound car-bon is protected from oxidation is corroboratedby experiments that subject subsoils to chemicaloxidation. The resulting C solubilization and min-eral dissolution show that most of the organicmatter in subsoils is associated with mineral sur-faces (Eusterhues et al. 2003; Mikutta et al. 2006).Thus mild chemical oxidation leaves an organicresidue with a mass that correlates signiWcantlywith mineral surface F- reactivity, and a �14Cvalue lower than that of the original organic mat-ter pool (Kleber et al. 2005).
Seasonal water repellency explained through presence of organic material sorbed to mineral surfaces in a zonal fashion
Seasonal changes in soil water repellency mayalso be explained by alterations to the zonalarchitecture of sorbed organic matter induced byseasonal changes in the soil environment. Non-seasonal water repellency in soils has often beenattributed to the presence of hydrophobic moie-ties such as those found in long-chain fatty acids(Ma’shum et al. 1988). The presence of hydropho-bic compounds alone, however, does not explainseasonal changes in water repellency. Using the‘molarity of ethanol droplet’ method to measurerepellency, combined with a set of organic extrac-tions, Horne and McIntosh (2000) attributed sea-sonal changes in soil wettability to the existenceof multiple, functionally diVerent layers oforganic matter on sandy grains. In their model, aninner layer of more hydrophobic compounds iscovered by a layer of amphiphilic compounds.When the soil is wettable, the hydrophobic mate-rial is eVectively screened, especially if the outersurface is well hydrated. Repellence occurs whenthe hydrophobic compounds making up the innerlayer are more exposed. This can be linked to sea-sonal moisture diVerences through a combinationof factors: during the wet season, the outer layerwill be well hydrated, amphiphilic compounds willbe arranged in such a fashion as to have theirpolar portions oriented outwards, the carboxylateanion will predominate, and hydrophobic groupswill be eVectively screened by more hydrophilicgroups. With the onset of the dry season, a more
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16 Biogeochemistry (2007) 85:9–24
hydrophobic outer surface develops as the amphi-philic compounds change in orientation, the car-boxylate groups are protonated, and contractionof the amphiphilic ‘surface screen’ exposes theinterior hydrophobic layer.
Laboratory and industrial synthesis of multilayer organic assemblages
Multilayered organo-mineral structures are rou-tinely manufactured and studied in the labora-tory, mainly for biomedical (Galeska et al. 2001)and biotechnical purposes (Halthur et al. 2004).Because these artiWcial organo-mineral struc-tures likely form as a result of some of the sameadsorption mechanisms active in soils, they maybe viewed as potential analogs of natural organo-mineral complexes. In one such study of artiWcialorgano-mineral assemblages, Spaeth et al. (1997)sorbed protein multilayers to hydrophobic silan-ized silicon wafers using alternating incubationswith poly-streptavidin and bovine serum albumin.They found that the thickness of the organic lay-ers increased 18.75 nm per incubation, yielding aWnal protein multilayer thickness of 350 nm.
Galeska et al. (2001) sorbed layers of the Ald-rich commercial humic fraction onto siliconwafers, noting that the expansion of the organicWlm could be signiWcantly altered by the incorpo-ration of salt, with the charge screening eVect con-tributing to thicker Wlm deposition irrespective ofpH. Further experimentation indicated that thepermeability of simple carbohydrates through thehumic coating was a function of the number ofself-assembled layers of organic material. Thatthe probe glucose penetrated thick Wlms com-posed of many layers of organic matter morereadily than thin Wlms made up of few layers sug-gests that organic molecules, including both SOMand xenobiotic substances, may not be tightlybound to outer regions of organo-mineral com-plexes.
Alkylated silicon oxide surfaces were used bySchmidt et al. (1990) in studies of protein adsorp-tion on hydrophobic surfaces. They found that amodel with at least three classes of adsorbed mol-ecules was necessary to adequately describe theirexperimental results. A Wrst layer was formed bythe molecules that adsorbed within a short time
after the beginning of the incubation. These mole-cules made up approximately 65% of the Wnalcoverage. They were irreversibly adsorbed anddid not measurably exchange with bulk solutionmolecules. A second layer reached equilibriumafter several hours of incubation and showed apronounced and temperature-dependentexchange with bulk molecules. A third layer con-sisted of molecules that exchanged rapidly withthe bulk solution, but comprised only about 10%of the total coverage. An important implication ofthis work is that a protein-based multilayer struc-ture allows occurrence of both hydrophobicadsorption on a stable inner layer, as well asphase-partitioning into a dynamic outer layer,thus explaining experimental results suggestingthe coexistence of both kinds of sorption mecha-nisms in the same system.
Reconciling the evidence for zonal structures on mineral surfaces
The evidence compiled above suggests thatSOM may attach to mineral surfaces in a zonalor layered fashion. In conjunction with the workof Wershaw et al. (1995; 1996a; b) on adsorptionof compost leachates to aluminum oxide, studiesof the amounts or spatial distributions of organicmaterials bound to mineral particles, and of vari-ations in C turnover time and seasonal waterrepellency, have provided a wealth of direct andindirect information supporting the concept ofan organized, zonal architecture for SOM sorbedto mineral surfaces. Experiments and observa-tions in the laboratory prove that organic multi-layers on mineral surfaces can even bemanufactured to serve speciWc purposes. Eco-logically speaking, the work of Schmidt et al.(1990) is especially signiWcant, as it assigns diVer-ent exchange kinetics to molecules making updiVerent parts of the organo-mineral complex,with molecules of the inner zone being the moststable, and molecules of the outermost zone hav-ing the fastest exchange with the soil solution.Such diVerential, zone-dependent kinetics couldexplain why organo-mineral isolates from soilscan contain C and N pools with diVerent turn-over times (Trumbore et al. 1989; Stricklandet al. 1992; Swanston et al. 2005).
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Biogeochemistry (2007) 85:9–24 17
The role of proteins in organo-mineral associations
Mineral-associated SOM exhibits C/N ratios of 7–14, whereas water-extracted SOM has C/N ratiosof 26–55 (Aufdenkampe et al. 2001), indicating Nenrichment of adsorbed organic materials.Numerous observations, made in both soils andmarine/freshwater environments (Aufdenkampeet al. 2001), similarly suggest that the adsorptionof nitrogenous compounds to mineral surfacesmay be a broadly relevant ecological process.Thus, a model of organo-mineral associationsshould account for the body of evidence suggest-ing preferential adsorption of N-containing moie-ties over other organic compounds to mineralsurfaces (Omoike and Chorover 2006; Hedgesand Oades 1997).
Certainly, the relatively high strength of pro-tein adsorption to mineral surfaces (Theng 1979;Chevallier et al. 2003; Wershaw 2004) is a long-established (Ensminger and Gieseking 1942)—and often technologically exploited (Gougeonet al. 2003)—chemical phenomenon, and one thathas proved relevant to the laboratory synthesis ofmultilayer organo-mineral complexes, as dis-cussed previously (Schmidt et al. 1990). We sug-gest that proteinaceous materials play aprominent role in the formation and structure oforgano-mineral complexes due to both the rela-tively high abundance of such compounds in soils,and the ability of these materials to adsorb irre-versibly to mineral surfaces.
Protein availability at soil mineral surfaces—15N-NMR analysis has demonstrated that a signiWcantamount of soil nitrogen is present in amide form
(Almendros et al. 1991 Knicker et al. 1995;Knicker and Lüdemann 1995; Knicker 2000, 2002;Leinweber and Schulten 2000; Mahieu et al. 2000,2002; Mathers et al. 2000; Zang et al. 2000), andthus most likely in the form of proteins or proteinresidues. Tremblay and Brenner (2006) showed ina 4-year decomposition experiment that on aver-age 60–75% of the N in highly decomposed detri-tus was derived from heterotrophic bacteria, ratherthan plant tissues. As the smallest organisms in thesoil, bacteria and fungi are able to enter small, con-Wned pore spaces and die and decompose there,and also contain far more N than vascular plantmaterials or surface litter (Table 1). In fact, bacte-ria are known to actively use proteins to attach tosurfaces (Bashan and Levanony 1988; Dufreneet al. 1999). Mycelial fungi also secrete a broadclass of surface-active glycoproteins (Wright andUpadhaya 1996). Abundant evidence indicatesthat microbial products accumulate in Wne clayfractions of soils (Leinweber and Schulten 1995;Kleber et al. 2004; Mertz et al. 2005), further cor-roborating the supposition that the more proteina-ceous microbial residues are likely to make initialcontact with mineral surfaces, rather than the lessproteinaceous plant residues.
Protein polyfunctionality and adsorption tomineral surfaces—Proteins are a special class ofamphiphilic molecules with a strong tendency tobind to surfaces and to resist desorption (Hladyand Buijs 1996). They consist of chains of aminoacids with both apolar and polar (either neutral orcharged) side chains, folded into a conformationin which as many apolar residues as possible arepacked into the interior, leaving mainly polar andcharged residues at the surface.
Table 1 Relative composition of vascular plants, algae, bacteria, and fungi, compiled using data from Knicker (2004) and White (1997)
Vascular plants Algae Bacteria Fungi
% Dry matter
Lignin 5–30Cellulose 15–60Hemicellulose 10–30
N-containing compounds 2–15 24–50 50–60 14–52Lipids 2–10 10–35 1–42Carbohydrates 40 4–32 8–60
Ratio
C:N ratio 20–50 (tree leaves) 6 5–8 t1025–80 (herbaceous plants)
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Given the diversity of functional groups mak-ing up proteins, no single process dominates pro-tein adsorption to mineral surfaces. Instead, threesubprocesses drive adsorption behavior: (i) struc-tural rearrangement of the protein molecule; (ii)dehydration of parts of the sorbent and proteinsurfaces; and (iii) redistribution of charged groupsat the organo-mineral interface (Haynes andNorde 1994). Numerous electrostatic bonds canform between reactive mineral sites and organicamide and other polar or charged functionalgroups during the adsorption process (Brash andHorbett 1995). Due to their large size and coiledstructure, proteins gain considerable conforma-tional energy by unfolding at the solid/liquidinterface, an entropically driven rearrangementthat produces numerous organo-mineral interac-tions and distinguishes protein adsorption fromthat of other available biomolecules (Haynes andNorde 1994). With adsorption to a mineral, pro-teins may increase the number of reactive sites onthe newly coated surface by exposing their abun-dant polar functional groups to the soil solution.This eVect is known as support preconditioning(Dufrene et al. 1996), and is considered a routinestep preceding the adhesion of microorganisms tomineral surfaces (Bos et al. 1999; Bakker et al.2004). The surface charge densities of both pro-tein and surface can vary with pH, and adsorptionis typically greatest at the isoelectric point of theprotein (Ramsden 1995).
Proteinaceous compounds can bind especiallystably to mineral surfaces over long time periods,as illustrated by the fruitless attempts of archaeol-ogists to remove protein from archaeological arti-facts for further study (Craig and Collins 2002).Amelung et al. (2006) used changes in chirality ofaspartic acid and lysine to show that some soilproteins achieve residence times of centuries.Sorption experiments (Hedges and Hare 1987;Wang and Lee 1993) as well as observational datafrom marine sediments and riverine particles(Hedges and Hare 1987; Wang and Lee 1993;Mayer et al. 1995; Arnarson and Keil 2001; Auf-denkampe et al. 2001) also indicate strong andstable binding of amino acids to clay minerals.Glycoproteins secreted by arbuscular mycorrhizalfungi (Wright and Upadhaya 1996) stabilize soilaggregates (Baveye 2006), likely due to their
ability to bind to both hydrophilic and hydropho-bic mineral surfaces. Strong adsorption of deWnedproteins on clean clays is well documented in thelaboratory, with the amount of adsorbed materialvarying over nearly Wve orders of magnitude withthe nature of the sorbate, sorbent, and experi-mental conditions (Theng 1979; Burchill et al.1981; Wang and Lee 1993; De Cristofaro and Vio-lante 2001; Ding and Henrichs 2002).
N-containing biomolecules as contact materials within a zonal organo-mineral complex
The proposed special role of proteins in the org-ano-mineral contact zone has implications for theattachment of additional organic compounds, orthe zonal architecture of organic materialsadsorbed to mineral surfaces. Organo-mineralcomplexes featuring multiple layers of proteinshave been synthesized using a variety of experi-mental methods (Schmidt et al. 1990; Spaeth et al.1997; Halthur et al. 2004). The amounts of pro-teins that may eventually sorb to mineral surfacescan be large, approaching 1 g protein g¡1 clay forclean clays (e.g., Burchill et al. 1981; De Cristof-aro and Violante 2001) and buried ceramics(Craig and Collins 2002), with record values of2.4 g g¡1 (Greenland 1965) on montmorillonite,implying a soil C concentration greater than thatallowed for a mineral soil horizon according toSoil Taxonomy (Soil Survey StaV 1999).
However, observations from natural systemsprovide more compelling evidence regarding thecritical role proteins play within soil organo-min-eral complexes. Physical fractionation data ledSollins et al. (2006) to postulate that sorption ofproteins might create a basal layer to which otheramphiphilic molecular fragments would adsorbmore strongly than they would to clean clay sur-faces, creating a zonal eVect, with N-rich com-pounds more abundant near mineral surfaces, andC-rich compounds more abundant farther fromthe surface. Physical fractionation reveals the ten-dency for the C/N ratio to decrease with increas-ing particle density (Turchenek and Oades 1979;Young and Spycher 1979). Lighter fractions(<1.8 g cm¡3) have high C/N ratios because theyare rich in plant structures high in lignin and cel-lulose. The continued downward trend in C/N
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Biogeochemistry (2007) 85:9–24 19
ratios at densities beyond 2.2 and even 2.4 g cm¡3
has previously been attributed to the accumula-tion of proteinaceous material (Oades 1988), andis consistent with our suggestion that N-rich com-pounds have a high probability of remainingsorbed to mineral surfaces.
Sollins et al. (2006) further suggested thatsequential density fractionation combined with14C analysis might oVer a way to assess the role ofN-rich compounds in the formation of organo-mineral complexes. They pointed out that varia-tion in particle density correlated well with thepercentage of C in the particles, and thus that Cloadings decreased with increasing particle den-sity, suggesting thinner coatings of organics, andin turn a more protein-rich inner layer. Assumingthese thin inner coatings were more stable, 14Cage should increase with particle density. Thisproved to be true for an Andic forest soil theyexamined. However, large diVerences in mineral-ogy of the density separates from this soil pre-cluded ascribing the increase in 14C age solely tocoating thinness.
The zonal structure of organo-mineral complexes: a hypothesis
Recent spectroscopic evidence suggests that thedecomposing organic residues in soils can beviewed as a mixture of largely amphiphilic frag-ments (Chien et al. 1997; Engebretson and vonWandruszka 1997, 1998; von Wandruszka 1998;von Wandruszka et al. 1999; Ferreria et al. 2001;Martin-Neto et al. 2001; von Wandruszka andEngebretson 2001; Nanny and Kontas 2002). Theamphiphilicity of many of these molecular frag-ments, and the polarity of the aqueous soil solu-tion in which they are contained, cause them toself-assemble into micellar associations when sus-pended at high concentrations, and into layeredor zonal structures when in contact with mineralsurfaces. Based on the evidence presented above,we propose that the self-assembly of SOM onmineral surfaces creates a layered or zonal struc-ture with regular features (Fig. 2).
The contact zone—When brought into contactwith a mineral surface, amphiphilic SOM com-pounds form a contact zone whose structural
properties depend mainly on the type, density,and chemical reactivity of the mineral functionalgroups, and on the pH of the soil solution.Organic fragments directly attached to mineralsurfaces are protected against decomposition anddo not participate in signiWcant exchange withorganic compounds in the soil solution. This canbe explained in part by the strong, ligand-exchange bonding of charged or polar heads ofamphiphilic molecules to hydroxylated mineralsurfaces (Tiberg et al. 1999). Proteins, a specialclass of amphiphilic molecules, can bind particu-larly strongly to mineral surfaces because theyreinforce the initial organo-mineral bonds thatform with entropically favorable conformationalchanges that produce further opportunities formore numerous adsorption interactions (Haynesand Norde 1994).
The hydrophobic zone—Amphiphilic mole-cules adsorbed directly to mineral surfaces tendto mask the physicochemical properties of thesesurfaces (Bos et al. 1999), to the extent that anoutwardly oriented region of high hydrophobicitymay be created, especially when the underlyingmineral surface has high densities of reactive, sin-gly coordinated hydroxyls (Murphy et al. 1990).The hydrophobic zone thus formed provides asuitable region for sorption of hydrophobic moie-ties, including the hydrophobic portions of amphi-philic molecules in the soil solution, leading toformation of a bilayer structure on the surface ofthe mineral. In contrast, the direct adsorption ofproteins to a mineral surface may lead to anincrease in the number of reactive surface sites,rather than hydrophobic sites. Direct adsorptionof proteins may not result in formation of ahydrophobic zone or a bilayer structure, butinstead enable the attachment of SOM compo-nents through electrostatic interactions. Thus, thehydrophobic zone must not be considered anessential and continuous layer present within allorgano-mineral associations, but rather a zonelikely to be found to varying degrees in many ofthese associations.
The kinetic zone—Depending on stereochemi-cal orientation, degree of amphiphilicity, cationcontent of the soil solution, pH, temperature, andperhaps several other controlling factors, a vari-ety of modes of attachment of further organic
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20 Biogeochemistry (2007) 85:9–24
molecules appears to be possible. No commonprinciple governing these associations is apparent.However, there is reason to assume that theorganic compounds trapped in this outer regionare partitioned rather than sorbed, and that theirresidence times within the outer region areshorter than the residence times of compounds inthe intermediate or inner regions. Because“Crowded conditions promote selfassembly”(Goodsell 2004), the thickness of the outer layeris likely to depend more on input of organic mate-rials than on the availability of binding sites, andto be largely be controlled by exchange kinetics.This suggests that more material will be sorbed tokinetic zones in topsoil A horizons than in subsur-face B and C horizons. Movement of organics intoand out of this outer region may thus resemble aphase-partitioning process, rather than classicaladsorption.
Conclusions
With the proposed zonal model, we attempt toreconcile information from diVerent natural andartiWcial systems and from various scientiWc Weldsinto an integrated view of the organo-mineralcomplex and its most important properties. Ourmodel encompasses interdependent hypothesesregarding (i) the formation of organo-mineralassociations, (ii) the speciWc architecture of thezones of adsorbed organic matter, and (iii) theexchange kinetics of these organic materials withthe surrounding soil solution.
We suggest a zonal structure for organic matteraccretions on mineral surfaces by recognizing thatSOM consists largely of amphiphilic molecularfragments with the thermodynamic impetus toself-assemble into micellar structures on mineralparticle surfaces suspended in a polar liquid(Fig. 2). We further propose that microbial pro-teins are better able to bind to mineral surfaces,as well more likely to arrive at these surfaces,than are residues of vascular plants, thus explain-ing the proposed existence of a particularly stablybound, N-rich inner layer of organic material.Hydrophobic portions of these surface-boundmolecules can be protected from contact withaqueous solution by the additional accumulation
of amphiphiles arranged such that the polar por-tions point towards the aqueous phase, creating abilayer structure with a discrete hydrophobiczone. Empirical evidence for organic surfaceloadings of 2–5 times the monolayer equivalent(Hedges and Keil 1995) suggests that furtherattachment of organics in a third region or kineticzone is possible, although for this outer zone orregion, exchange rates of organic compounds withthe soil solution are likely high, and residencetimes brief.
The arguments in support of the zonal hypoth-esis of organo-mineral complexes are indirect innature. We invite the scientiWc community to joinus in future attempts to challenge the zonal con-cept and to help us further elucidate the structureand dynamics of organo-mineral associations. Ifexperimentally and empirically validated, thezonal model for organo-mineral associations innatural systems should not only open up a newroad towards improved understanding of organicC and N dynamics in soils and sediments, but alsofacilitate the modeling of the fate and transport ofcontaminants.
Acknowledgements We thank M.S. Torn, T. Filley, C.Swanston, M. Kramer, G. Sposito and especially B. Caldwellfor discussions and helpful comments on earlier drafts of themanuscript. The comments of J. Chorover were particularlyvaluable and are gratefully appreciated. The contribution ofMK results from previous support through the German Sci-ence Foundation (DFG) priority program SPP 1090 andfrom current Wnancial support by the Climate Change Re-search Division, OYce of Science, U.S. Department of En-ergy under Contract No. DE-AC03-76SF00098. Partialfunding was provided by NSF SGER and USDA CSRIgrants to PS and MK and by the Andrews LTER program.
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