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Biogeochemistry (2007) 85:1–7 DOI 10.1007/s10533-007-9099-x

INTRODUCTION

Stabilization and destabilization of organic matter—a new focus

Phillip Sollins Æ Chris Swanston Æ Marc Kramer

Published online: 22 June 2007 Ó Springer Science+Business Media B.V. 2007

Interest in soil organic matter (SOM) is ramping specter of run-away seems to have up as concern mounts about steadily increasing now overtaken these other justifications. levels of atmospheric CO2. There are two reasons Much of the work on SOM triggered by climate for this. First, there is hope that improvements in change has involved measuring pools over large crop, forest, and soil management may allow areas and, especially, changes in those pools over significant amounts of CO2 to be removed from time (Smith 2004; Bellamy et al. 2005). Other the and sequestered in soil. Second is work has sought to measure changes in soil C and the possibility that increased soil respiration rates, N stores under elevated CO2 regimes (Lin et al. associated with climate change, will unleash a 1999; Six et al. 2001; Jastrow et al. 2005). But it is positive feedback in which temperatures rise even widely recognized that measuring such changes is faster than now expected. Other reasons have not enough. We have to understand the mecha- long existed for understanding SOM dynamics, nisms underlying soil organic matter stabilization such as SOM as the source of most of the non- if we are to predict the course of CO2 flux fertilizer N needed for plant growth, but the between atmosphere and soil under a changing climate and a steadily increasing demand for agricultural and forest products. & P. Sollins ( ) A 6-year project led by Prof. Ingrid Ko¨ gel- Forest Science Department, Oregon State University, Corvallis, OR 97331, USA Knabner ( as Source and Sink for e-mail: [email protected] CO2—Mechanisms and Regulation of Organic Matter Stabilization in Soils, funded by Deutsche C. Swanston Forschungsgemeinschaft) was arguably the first Lawrence Livermore National Laboratory, Center for Accelerator Mass Spectrometry, Livermore, CA, major formal effort in this direction. The project USA also hosted the First International Conference on Mechanisms of Soil Organic Matter Stabilization Present Address: as part of a mid-term project review. The confer- C. Swanston USDA Forest ServicNorthern Research Station, 410 ence (Munich, October 2003) was attended by MacInnes Drive, Houghton, MI 49931, USA about 140 people from 12 countries. Several American SOM scientists asked if a follow-up M. Kramer conference in the US was warranted. The Department of Earth and Planetary Sciences, University of California Santa Cruz, Santa Cruz, CA response was enthusiastic and funding was 95064, USA secured from US sources including the National

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Science Foundation (Ecosystems Cluster), USDA compounds that are still recognizable as plant NRI (Soil Biology Program), Lawrence Liver- and microbial metabolites. are thought more National Laboratory (Center for Accelera- to be involved in formation of humic substances tor Mass Spectrometry), Kearney Foundation of via reactions with , tannins and Soil Science, NASA (Applied Earth Science degradation products, but the resulting products Program, Carbon Management), and Oregon are not thought to play a major role in binding of State University (College of Forestry). The Sec- SOM to mineral surfaces. ond International Conference on Mechanisms of Kleber et al. (this volume), following on work Soil Organic Matter Stabilization was held at the by Wershaw et al. (1996), Piccolo (2001), and Asilomar Center, near Monterey, California in Sutton and Sposito (2005), offer an alternative October 2005, and was attended by about 120 view. Briefly, SOM is viewed as consisting of people from 13 countries. The papers presented organic molecular fragments of varying degrees in this special issue of Biogeochemistry derive of amphiphilicity in intimate contact with mineral from presentations made at this 2005 conference. surfaces of variable chemical reactivity and a Because of the success of the second conference, polar solvent (water). The second law of thermo- a third is scheduled for Adelaide, Australia, in dynamics then dictates that the organic fragments September 2007 to be hosted by Jan Skjemstad, and mineral surfaces will arrange themselves in Jeff Baldock, and Evelyn Krull, of the Australian structures that maximize entropy, which leads Commonwealth Scientific and Industrial Re- these authors to propose a layered structure for search Organization (CSIRO). The Adelaide mineral–organic associations. This layered struc- conference will specifically include both soils ture is fundamentally different from earlier and aquatic . ‘‘humic-substances’’ based concepts for organo– The Asilomar presentations, both oral and mineral interactions in that the organic molecular poster, covered topics ranging from soils to fragments are seen as degradation products riverine sediments, from kinetics of extracellular derived from the depolymerization and oxidation enzymes to mechanisms of OM sorption on of standard biomolecules, and not as large resyn- mineral surfaces, and from to microbial thesized polyaromatic structures as postulated by surface-active proteins. What follows highlights the various pathways of classical humification major scientific findings and questions that theory. emerged from the Asilomar conference, then The same work strongly emphasizes proteins considers scientific and logistical obstacles to as the organic compounds with the greatest further progress in this field and opportunities functional versatility. Unlike other organic moi- for addressing those obstacles. eties, proteins can bind to almost any kind of surface over a wide range of pH conditions. This is because of their multifunctional , that is, their ability to develop positive as well as negative charge as well as their ability to Conference themes and highlights gain entropy by conformational changes, which reinforces any electrostatic bonding to mineral One conference thread was the viability and surfaces. usefulness of the ‘‘humic’’ theory of SOM (e.g., The theme of the importance of soil N in Stevenson 1994; Essington 2004). The ‘‘humic’’ controlling soil C dynamics is taken up and paradigm holds that over time, plant debris is developed in more detail by Rillig et al. (this transformed into very large polyaromatic struc- volume) who review information on the nature tures, largely via abiotic condensation mecha- and amounts of soil , especially microbial nisms. In addition to ‘‘humic substances’’, SOM surface-active proteins. Despite controversy as to includes ‘‘non-humic substances’’: carbohydrates, precise amounts of such compounds in soil, and lignin, proteins, amino-sugars and other their role in aggregation, it is clear that they are

123 Biogeochemistry (2007) 85:1–7 3 ubiquitous in soil and exceptionally stable, which general, these synchrotron-based techniques (both is only reasonable since N is so often strongly NEXAFS and FTIR) offer unprecedented oppor- limiting to microbial activity in soils. After all, tunities for 2-d mapping of both elements and why would microbes have evolved attachment compounds across the soil microfabric. compounds that can be readily degraded? In fact, Much of the work presented at Asilomar refers recent work by Amelung et al. (2006) uses amino- to topsoil. This reflects in part the assumption that acid racemization rates to suggest that soil protein deep-soil SOM does not cycle or change as may have residence times measured in centuries rapidly as the topsoil SOM. An additional factor rather than decades. is simply the enormous work required for careful The paper by Rillig et al. (this volume) also deep-soil sampling. Baisden and Parfitt (this reinforces a second conference theme that the volume) go deeper and find that subsoil SOM in majority of the organic N atoms, and even to New Zealand is accumulating bomb carbon at a some extent the organic C atoms, are likely to substantial rate suggesting that it is more dynamic have undergone microbial processing since last than previously assumed. This idea that even having been part of plant tissue. Although virtu- SOM pools that yield long 14C mean residence ally all soil C derives ultimately from vascular- times (MRTs) may still be very dynamic fits well plant photosynthesis, a major tenet of the poly- with the multi-layer model of Kleber et al. (this phenol ‘‘humic’’ theory is that lignin-derived volume): The multi-layer model includes an outer aromatics provide the structural framework for kinetic zone in which molecules and even cell soil ‘‘humic’’ substances. The 13C-NMR evidence fragments can be bound rapidly but also exchange to date suggests, however, that aromatics account readily with the soil solution. Such rapid incor- only for a relatively small portion of SOM and poration of labeled material into an organo- that alkyl C, rather than aromatic C, accumulates mineral heavy fraction has also been noted by over the time scale of soil formation (e.g., Strickland et al. (1992) and Swanston et al. Baldock et al. 2004). This finding is supported (2005). by the spatial association of alkyl C with SOM fractionation procedures, and density- functional groups determined by synchrotron- based fractionation in particular, were used in based FTIR and the alkyl-rich coatings on min- many of the studies presented at Asilomar. Crow eral surfaces shown with X-ray spectroscopy et al. (this volume) review the development of the (Lehmann et al., this volume). Direct measure- density fractionation methodology and its limita- ment in soil of lignin monomers and their tions. They also include new experimental evi- degradation products further confirms a relatively dence that a large amount of C and N is mobilized rapid turnover for lignin compounds (e.g., Kiem in the fractionation medium (SPT). This SPT- and Ko¨ gel-Knabner 2003; Nierop and Filley 2006; solubilized fraction is discarded in most studies Sollins et al. 2006). and not typically reported or explicitly discussed. A fourth conference theme was the role of Moreover, the SPT-solubilized fraction is func- aggregation in stabilization of SOM. Johannes tionally distinct from both heavy and light frac- Lehmann et al. (this volume) use synchrotron- tion in ways that are not consistent across based spectroscopy to map not only element soils—clearly an important consideration and distributions, but even molecular speciation in intriguing opportunity for further work. individual microaggregates (< 5 lm) from a variety Lastly, the role of (char and soot) of soils. They found little systematic variation in C continues to receive attention, especially well- levels from the outside to inside of these aggre- deserved given the likelihood of increased wild- gates, suggesting that organic debris do not form a fire under a warming global climate. Knicker (this nucleus around which such microaggregates then volume) reviews the nature of black carbon and develop. Certain classes of organics, however, did possible modes of formation. She concludes that vary systematically from aggregate exterior to polyaromatics do form the core of these materials interior, in keeping with the multilayer theory but that molecular weights (number of benzene proposed here by Kleber et al. (this volume). In rings) are much less than previously assumed.

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This relatively small size raises interesting ultimately be even more important to global C questions about the recalcitrance of such materi- dynamics than stabilization processes, if the long- als and thus their potential to be degraded term net flux of C between soil and atmosphere microbially, especially under a warmer climate. turns out to be toward atmospheric CO2 rather Char research is also suggesting that most of the than soil C. heterocyclic N in soils is pyrogenic, although the Given the complexity of the soil, modeling extent to which some is inherited from organic- provides the only way to link mechanisms to future rich sedimentary parent materials has not yet fluxes. Unfortunately, little of the work presented been quantified. at the Asilomar conference is reflected in current models of SOM dynamics (Lu¨ tzow et al. 2006). One major class of SOM models focuses on Future SOM research needs substrate ‘‘quality’’ (A˚ gren and Bosatta 2002; Currie 2003) and assumes that the dynamics of C The Second Conference highlighted not just results and N in mineral soil and plant litter are identical. but also major gaps in both our knowledge and in Given that organic substrates as well as the our research efforts. Clearly, soil organic N microflora and the enzymes they produce all dynamics have received much less attention that interact with mineral surfaces in ways that greatly those of soil organic C. With the advent of 15N- affect their behavior, this assumption greatly limits NMR in the 1990s, it became clear that most of the the applicability of these models. A second class of organic N in soils is in amide form. Seemingly lost SOM models relegates soil organo–mineral inter- in this wave of NMR data, however, was a large actions to parameters that must be set empirically wet-chemistry literature on protein in soils and for sites of different . Moreover, most of sediments, some papers dating back to 1940s (see these models (e.g., Century, Trace, and Biome- Rillig et al. this volume). Moreover, clays have BGC) are built around pools that cannot be been used to remove protein in industrial applica- separated physically or chemically, or even quan- tions for decades (e.g., Kleber et al. this volume), tified directly (Kelly et al. 1997; Currie et al. 1999; and further review of this literature is needed. In Thornton and Rosenbloom 2005). A few ap- any case, it seems possible now that N dynamics in proaches do make use of pools that can be large part drive soil C stabilization, rather than the quantified. For example, several models distin- other way around, and that this occurs via at least guish between plant debris (either a light fraction two mechanisms, possibly interrelated: strong or a particulate organic matter pool) and mineral- sorption of proteins on mineral surfaces and associated OM (Hassink and Whitmore 1997; accumulation of recalcitrant surface-active pro- Skjemstad et al. 2004; Nadporozhskaya et al. teins in the soil. If true, this shift in thinking would 2006). A third group (e.g., GEM) assumes that have major implications, especially for attempts to ‘‘proximate analysis’’, an approach developed for model soil C and N dynamics. food and fiber and used for many years to model The Second Conference, like the first, empha- litter dynamics, is meaningful when applied to sized stabilization mechanisms over destabiliza- mineral soil (Rastetter et al. 1991; McKane et al. tion, which comprises processes that decrease 1997), but these again do not consider organo– stability and thus promote turnover and degrada- mineral interactions. tion (Sollins et al. 1996; Baldock and Skjemstad Unique perhaps is Terraflux (Neff and Asner 2000). Presenters, however, did discuss kinetics of 2001), which builds directly on Century but enzyme-mediated substrate degradation (J. Schi- includes a soluble C pool and allows sorption/ mel) and temperature dependence of microbial desorption reactions out of and into that pool. degradation processes (S. Frey). Less well covered The authors review the C sorption/desorption were processes of desorption of organics from literature in relation to soil mineralogy, especially mineral surfaces and of increases in substrate extractable Fe and Al, and subsume that infor- accessibility due to decreases in aggregation. mation into two parameters. Their appendix table Destabilization processes, however, may lists these parameter values for a wide range of

123 Biogeochemistry (2007) 85:1–7 5 soils, but the authors do not explore further how dispersed? Thus, meetings that focus on specific those values might relate to soil mineralogy or areas such as SOM and allow time for extended texture. Nonetheless, organo–mineral interac- discussion occupy a niche not filled by meetings of tions are widely recognized as of crucial impor- professional societies in that they bring together tance in SOM stabilization, and the modeling people from all the relevant fields and they do so community must begin to incorporate more of with much less distraction. This is not to in any this thinking into its work. Moreover, all SOM way denigrate the importance of professional models that include N use C:N ratios to link fluxes societies, their meetings and journals. They are of C and N. As already discussed, this assumption necessary but not sufficient. We sincerely hope may not apply if indeed nitrogenous and non- that funding agencies and societies worldwide will nitrogenous organics play fundamentally distinct join together to support the Third International roles in SOM stabilization. SOM Conference, which is now scheduled for Perhaps part of this reluctance to include Adelaide, Australia, as well as subsequent efforts. organo–mineral interactions in SOM models, The broad interdisciplinary nature of SOM stems from a disconnect between what might be research also affects funding. NSF Ecosystems termed ‘‘’’ and ‘‘SOM’’ research. Cluster increasingly funds landscape and global- ‘‘Decomposition’’ research, as the term is used level studies, not detailed process studies of the sort here, focuses on the breakdown of plant and needed to understand SOM dynamics. The USDA microbial substrates by microbes and higher NRI Soil Processes Program does fund this area trophic-level organisms. Perhaps because most but its budget is excruciatingly small. NASA’s of the research deals with organic horizons rather increased focus on space exploration has decreased than mineral soil horizons, such ‘‘decomposition’’ the funding available for earth-science research research tends to leave out the organo–mineral including all terrestrial process-level studies. The interactions entirely. A small group of people are DOE Office of Biological and Environmental studying microbial/mineral interactions directly Research, especially the Terrestrial Carbon Pro- (e.g., Omoike and Chorover 2006) but there cesses program, invests in carbon research at continue to be two highly disconnected literatures multiples scales, including studies of mechanisms and corresponding research communities: a ‘‘lit- of SOM stabilization. Yet even this DOE program ter decomposition community’’ (often forest eco- suffers from a static and increasingly strained system oriented) and an ‘‘SOM community’’ budget, with much of its yearly budget dedicated

(often agriculturally oriented). These groups need to infrastructure support of CO2 exchange and to interact more effectively if there is to be FACE experiments. In short, the possibilities for efficient progress on SOM dynamics. funding mechanistic SOM research, never exten- SOM science spans a huge array of disciplines, sive, are getting steadily smaller, at least in the US. perhaps even uniquely so. The authors of the If this trend continues we may slide into a major papers included in this issue cited papers in a 172 global crisis that we lack the information to even peer reviewed journals. Of these Soil Biology & fully understand, much less solve. Carbon cycle Biochemistry ranked first (54 citations), followed science in general and SOM research in particular by Soil Science Society of America Journal (48), must get higher priority than they do now if we are Organic Geochemistry (28), European Journal of to understand and mitigate the consequences of Soil Science (25), Soil Science (25), Geoderma fossil fuel emissions for the climate and ecosystems (24), and Global Biogeochemical Cycles (20). An of the Earth. additional 24 journals were cited between 6 and 19 times, while 135 journals were cited 5 times or fewer. An informal survey indicated that the References conference attendees hold membership in at least 10 professional societies, not counting general A˚ gren GI, Bosatta E (2002) Reconciling differences in science societies such as AAAS. Is there another predictions of temperature response of soil organic environmental-studies field that is so widely matter. Soil Biol Biochem 34:129–132

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Amelung W, Zhang X, Flach KW (2006) Amino acids in Lu¨ tzow Mv, Ko¨ gel-Knabner I, Ekschmitt K, Matzner E, grassland soils: climatic effects on concentrations and Guggenberger G, Marschner B, Flessa H (2006) Sta- chirality. Geoderma 130:207–217 bilization of organic matter in temperate soils: Baisden WT, Parfitt R. Bomb 14C enrichment indicates mechanisms and their relevance under different soil decadal C pool in deep soil. Biogeochemistry (this conditions—a review. Eur J Soil Sci 57:426–445 volume) McKane R, Rastetter E, Shaver G, Nadelhoffer K, Giblin Bellamy PH, Loveland PJ, Bradley RI, Lark RM, Kirk A, Laundre J, Chapin FS (1997) Climatic effects on GJD (2005) Carbon losses from all soils across Eng- tundra carbon storage inferred from experimental land and Wales 1978–2003. Nature 437:245–248 data and a model. 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