LLNL-CONF-750320

Deeply Rooted: Evaluating Plant Rooting

Depth as a Means for Enhanced Soil
Carbon Sequestration

J. Pett-Ridge, E. Nuccio, K. McFarlane

April 26, 2018

International Conference on Negative CO2 Emissions

Gothenburg, Sweden
May 21, 2018 through May 24, 2018
Disclaimer

This document was prepared as an account of work sponsored by an agency of the United States
government. Neither the United States government nor Lawrence Livermore National Security, LLC,
nor any of their employees makes any warranty, expressed or implied, or assumes any legal liability or
responsibility for the accuracy, completeness, or usefulness of any information, apparatus, product, or
process disclosed, or represents that its use would not infringe privately owned rights. Reference herein
to any specific commercial product, process, or service by trade name, trademark, manufacturer, or
otherwise does not necessarily constitute or imply its endorsement, recommendation, or favoring by the
United States government or Lawrence Livermore National Security, LLC. The views and opinions of
authors expressed herein do not necessarily state or reflect those of the United States government or
Lawrence Livermore National Security, LLC, and shall not be used for advertising or product
endorsement purposes.
 International Conference on Negative CO2 Emissions, May 22-24, 2018, Göteborg, Sweden

LLNL-CONF-750320

Deeply Rooted: Evaluating Plant Rooting Depth as a Means for

Enhanced Soil Carbon Sequestration
Jennifer Pett-Ridge1*#, Erin Nuccio1, Karis McFarlane1
1
Lawrence Livermore National Laboratory, Livermore CA, USA
*Corresponding Author, pettridge2@llnl.gov, #Presenting Author

Abstract – Soils store three times as much carbon (C) as the atmosphere, but are
not at capacity, and enhanced soil C storage is one of several strategies needed to
mitigate atmospheric C. Deep soil C is stored for centuries or millennia, in
contrast to C stored in vegetation, topsoils, or via other C sequestration strategies.
We hypothesize that the soil C sink could be enhanced (e.g. in marginal and
agricultural soils) via a greater emphasis on crops with deep rooting phenotypes.
Substantial evidence suggests that stabilized soil C is root carbon. Roots provide
30-40% of total soil organic C inputs, form a nexus for microbial transformations,
and are the primary source of C that becomes long-term stabilized. Agricultural
strategies that emphasize deep-rooted cultivars could simultaneously help to
achieve 'negative emissions' targets, while restoring soil C to native levels in
managed lands (increasing fertility, water holding capacity, lowering erosion
risk), improving plant drought tolerance, expanding C-neutral biomass of
bioenergy crops, and promoting microbial byproducts that help stabilize C on
mineral surfaces. However, the accrual, turnover and stabilization of C in subsoils
is a critical knowledge gap. Why some mineral-associated C persists and some
does not remains a central question in the field of soil C dynamics, and has
important implications for soil health and fertility and for microbial community
ecology. To address this concern, we propose a suite of advanced technologies,
that in combination can disentangle the complex interactions between soil mineral
surfaces, decomposing root-derived organic compounds and microbial catalysts.
We are currently testing this approach in two deep soil profiles in southern
Oklahoma where either deeply rooted perennials/crops (switchgrass, Panicum
virgatum) or shallow rooted crops have been cultivated for over a decade. In
combination, accelerator mass spectrometry 14C, soil C, and high-resolution
microbial community analyses can be used to measure soil carbon turnover time,
root characteristics, and microbial biomass, function and identity with depth.
Measurements of 14C on soil density fractions can be used to quantify soil C
distribution and turnover of particulate, aggregate occluded, and mineral-
associated C pools. Using the SoilR modeling approach, these data allow
quantification and forecasting of the future effects of deeper root inputs and
parameterization of vertically-resolved root inputs in earth-system land models.
This approach -- disentangling the complex interactions between root exudation,

1
 International Conference on Negative CO2 Emissions, May 22-24, 2018, Göteborg, Sweden

microbial communities, and soil minerals-- will advance our understanding of the
persistence of root-derived organic matter in deep soils, and help quantify the C
accrual possible with this negative CO2 strategy.

1 Introduction
The global terrestrial biosphere C sink is twice the atmospheric pool, and mostly stored as soil
organic matter (SOM) (Jobbagy and Jackson 2000). Globally, 65% of SOM in the top 3 m is
stored in the subsoil below 30 cm (Jobbagy and Jackson 2000). However, soils are currently
not at capacity, having lost 133 Pg C in the top 2 m due to the past century’s agricultural
practices (Sanderman et al. 2017). It is estimated that soils, already an important sink for
global C, could accommodate an even larger sink of up to 50t ha-1, (Jones and Donnelly 2004;
Lorenz and Lal 2005; Lal 2011), but empirical data is lacking, and the fundamental
mechanisms that regulate this vast pool (1500-1600 PgC in the top 1 m (Anderson-Teixeira et
al 2009) remain elusive (Schlesinger and Bernhart 2013). Overall, the amount of C stored in
soils is a function of biological, chemical, and physical parameters (Schmidt et al. 2011).
Patterns of soil C storage and cycling are determined by the balance between organic matter
inputs resulting from primary production (e.g., roots and root exudates), losses due largely to
microbial respiration during decomposition, and interactions between microbially derived
organic compounds and the soil mineral matrix (Cotrufo et al. 2013).
While fluxes of soil CO2, N2O and CH4 are the major contributor (37%) of agricultural
greenhouse gas (GHG) emissions, its thought that improved soil management and shifts
towards perennial crops could sequester C fixed by plants during photosynthesis while
simultaneously improving soil health, water holding capacity, nutrient capital, reducing
erosion and buffering against impacts of climate change (Paustian et al. 2016). A better
understanding of the mechanisms of deep soil C stabilization, and how this pool might be
augmented as a ‘negative C’ sink (e.g. through greater emphasis on deep-rooted agricultural
crops), requires a holistic analysis of the fate of deep soil C inputs, the role of soil microbial
communities, and the potential scale at which deep-rooted agricultural practices could be
implemented.

1.1 The fate of root carbon in deep soils

While not common knowledge in all circles, substantial evidence indicates that that stabilized
soil C is root carbon (Rasse et al. 2005; Schmidt et al., 2011; Clemmensen et al., 2013;
Jackson et al., 2017). Roots inputs account for up to 30-40% of total soil organic C (Grayston
et al. 1996), form a nexus for microbial transformations, and are the primary source of long-
term stabilized C (Kiem and Kogel-Knabner 2002). The organic carbon contributed by roots
enters soil as exudates, mucilage or decaying biomass, is taken up and transformed by nearby
rhizosphere microbes, and then either respired to the atmosphere (CO2, CH4), stored as SOM,
or leached away as dissolved organic matter (DOM). But what is the fate of root C in deep
soils? Below 30 cm, soil C is chiefly sorbed onto mineral surfaces or occluded within
aggregates, with multi-millenial 14C-calculated turnover times (Kiem and Kogel-Knabner
2002). The effect of deep roots on subsoil SOM accrual, turnover and stabilization is a critical

2
 International Conference on Negative CO2 Emissions, May 22-24, 2018, Göteborg, Sweden

knowledge gap, limiting our ability to predict future soil C sinks and evaluate land
management options (Rumpel and Kogel-Knabner 2011).

Despite the long turnover times typically associated with deep soil C, this pool is not ‘passive’
and plays an active role in the global C cycle (Rumpel and Kogel-Knabner 2011; Trumbore et
al., 1995; Veldkamp et al., 2003) and may be susceptible to environmental changes that could
shift the stability of soil C and soil C–climate change feedbacks (Pries et al. 2017). Recent
experimental results show that soil C at all depths may be vulnerable to loss, and deep soils
could lose the equivalent of ~3 % of current global ecosystem respiration (equal to 30% of
anthropogenic emissions) with 4 warming. Yet at the same time, elevated CO2 can change
the amount and depth of root inputs, thereby affecting microbial community composition and
function, and changing the carbon balance between soil and the atmosphere. Deep soils may
be particularly responsive to changes in root and rhizosphere volume (in comparison to
surface soils) because of their relative lack of substrate inputs; however, the direction of this
change is not well understood. There are two competing effects that could impact C storage at
depth due to increases in root biomass: increased C storage via incorporation and stabilization
of newly added C, and decreased C storage through priming of existing soil organic matter
decomposition. Deep soils may provide greater stabilization of new C inputs because of the
stronger effects of C stabilizing factors with depth, such as microaggregation and mineral-
surface interaction. In contrast, greater root C inputs may promote increased microbial
activity in the form of higher microbial respiration rates, as has been observed in many
elevated CO2 experiments. Thus, higher microbial respiration in deep soils may induce
priming losses of C already stored in deep soils (e.g., Fontaine et al. 2004). It is difficult to
compare the magnitude of these two effects on soil C storage because of the paucity of
information about changes to stabilization rates due to changes in root abundance. More
information is needed about the role of roots and new C in C stabilization in deep soils. Also,
the temporal extent of the priming effect (e.g., how long it can persist), and the state of the
carbon decomposed by the priming effect (e.g., whether priming can release otherwise stable
C, or C that is already microbially available) are needed to predict the net effect of elevated
CO2 on deep soil C storage.

1.2 Microbial function in deep soils

Most studies of soil microbiology tend to focus on surface soil horizons where root and
microbial biomass is highest. However, many microorganisms reside in subsurface soils
(Dodds et al., 1996, Fritze et al., 2000 and Blume et al., 2002; Fierer 2003) and are exposed to
SOM inputs from deep roots, dissolved organic carbon and the decaying necromass of other
microbial cells. In soil, microbial communities are critical to organic matter processing, and
are strongly influenced by environmental variables, such as temperature and moisture, which
modulate their activities. Many factors change with depth in soil profiles: temperature and
moisture conditions and their variability, roots impacts (their density, rhizosphere volume,
and exudates), the distance from surface inputs or weathering parent material, physical
properties (texture, aggregation, mineral surface area) and chemical properties (pH, redox,
oxygen availability, and mineral composition and reactivity). These factors interact to regulate

3
 International Conference on Negative CO2 Emissions, May 22-24, 2018, Göteborg, Sweden

soil’s biotic components, bacteria, fungi, archaea, viruses and fauna, whose metabolism
subsequently affects the transformation, mineralization, and stabilization of soil carbon.
Much of the approximately 2300 gigatons of carbon globally sequestered in soil has the
potential to be cycled by microbial activities, with important ramifications on fluxes of
greenhouse gases between the terrestrial ecosystem and the atmosphere (Jansson, 2011). It is
currently not known how climate change and land management practices impact the microbial
composition and functionality of deep soil ecosystems and the subsequent ability of these
microbial communities to bolster a positive vs negative soil C sink.

1.3 The potential for deep soil carbon sequestration

Aggressive soil C sequestration is considered a viable means to achieve GHG 'negative
emissions', drawing the equivalent of ~450 ppm CO 2 (eq) (Ciais et al. 2014) from the
atmosphere over 20-30 years (Smith et al. 2008; Paustian et al. 2016). On managed lands (e.g.
forestry, agriculture), an increased soil C sink could potentially occur at large scales with
relatively low cost, and simultaneously improve crop nutrient foraging and water acquisition
(Lynch and Wojciechowski 2015). Its estimated that a 25% increase in net C storage would
reduce the marginal abatement cost by 18%, relative to total mitigation costs of ~$500B (in
2012 dollars). Agricultural modeling suggests that better agricultural soil management,
including deep-rooted crops, could substantially mitigate greenhouse gas emissions (Smith et
al. 2008; Kell 2012; Paustian et al. 2016) (Fig. 1), and widespread planting of deep rooted
crops might add C equal to ~1 Pg CO2 yr−1 or more (Smith et al. 2008; Kell 2012; Paustian et
al. 2016). Improved soil management and shifts towards perennial crops could sequester C
fixed by plants while simultaneously improving soil health, water holding capacity, nutrient
capital, reducing erosion and buffering against impacts of climate change (Smith 2012;
Paustian et al. 2016).

Figure 1: Global potential for agricultural GHG mitigation practices, arranged according to
per hectare net GHG reduction rates and potential area of adoption From: Paustian, K. et
al. Climate-smart soils. Nature 532, 49-57 (2016).

4
 International Conference on Negative CO2 Emissions, May 22-24, 2018, Göteborg, Sweden

Typically, rooting depth is controlled largely by plant genetics and nutrition, and varies
widely. Experimental and breeding studies show that deep root architectural traits (e.g length,
angle and diameter of primary vs lateral roots; or cortical cell characteristics) enable more
optimal
water and N uptake in crops such as maize (Lynch 2018). In switchgrass, a native prairie
species and bioenergy crop, roots can extend to several meters depth. Logically, these deep
roots might also optimize soil C storage, and benefit marginal or degraded soils (Gelfand et al.
2013; Stoof et al. 2014). Because roots exist in close contact with soil bacterial and fungal
communities, and their biomass is a major precursor of stabilized SOM (Kallenbach et al.
2016), it may also be possible to select for plant cultivars that manipulate the soil–plant
microbiome in ways that additionally enhance rhizosphere C sequestration.
However, there are few estimates of the global C sink potential specifically for crop ‘root
enhancement’. Due to high analysis costs, few studies have directly measured C accrual
following shifts to deeply rooted plants (Ciais et al.; Smith et al. 2008), yet its well
understood that the C-rich soils that underlie much of the US Midwest were originally created
by long-term SOM additions derived from deep- rooted native prairie grasses (e.g.
switchgrass, Panicum virgatum). We hypothesize that a purposeful shift toward agricultural
species and improved plant cultivars with greater root mass and deep-rooting phenotypes will
cause C accumulation in deep soils where C turnover is slow—thereby significantly
increasing the terrestrial C sink (Kell 2012; Lynch and Wojciechowski 2015). This strategy
would be especially well-suited to marginal or degraded soils (fallow or low productivity
sites, ~12 million ha in the US Midwest), where cellulosic biofuel feedstocks could make up a
substantial proportion of future energy portfolios (Lynch 20130; Smith 2012) and would
simultaneously improve soil health, water holding capacity, nutrient capital, reduce erosion
and buffer against negative impacts of climate change (Smith 2012; Paustian et al 2016).

2 Approach
We propose that a purposeful shift towards perennial crops which allocate more C below-
ground, with higher productivity or C allocation to deeper roots will increase slow-turnover-
time deep soil C stocks. For example, establishment of deep-rooted grasses in savannas has
been reported to yield very high rates of C accrual (Fisher et al. 1994), although the
applicability of these results has not been widely confirmed (Conant et al. 2001). Focusing on
deeply-rooted bioenergy crops (e.g. switchgrass) would create a ‘double C benefit’, because
in addition to the deep soil C storage obtained from root biomass, CO2 released when the fuel
is burned is of recent atmospheric origin (via photosynthesis) and thus displaces CO2 which
otherwise would have come from fossil C. Currently, ~11% of the U.S. mainland is
comprised of 'marginal lands' and represent an untapped agronomic resource well-suited to
deep, extensive root growth architecture. Particularly in Oklahoma, and the classic 'Dust
Bowl' region, cultivation of perennial grasses such as switchgrass could represent a means to
provided ‘negative emissions’ via re-establishing soil organic carbon content (via root
biomass and rhizodeposition) (Fisher et al. 1994; Conant et al. 2001), preventing soil erosion
(Ciais et al. 2014), and restoring ecological services.

5
 International Conference on Negative CO2 Emissions, May 22-24, 2018, Göteborg, Sweden

To assess the accrual of soil C at depth, and the potential for increased SOM turnover time,
we propose a suite of multi-scale analyses (Fig. 2) to be used in concert at paired sites with
and without deeply-rooted plant phenotypes. These include measurements of SOM turnover
and microbial community function, SOM chemical characterization, and advanced multi-pool
modeling approaches.

Figure 2: Conceptual approach for multi-scale assessment of deep-rooted agricultural crop

impacts on soil carbon turnover time and stocks, and capacities of resident microorganisms.

2.1 Radiocarbon analysis

Radiocarbon (14C) measurements can be used to indicate the timescale and pathway of C as it
moves through the soil system, providing an extremely valuable metric for evaluating model
performance. 14C of density fractions (Sollins et al 2006) additionally enable quantification of
soil C distribution among different C pools and the turnover times of those pools. The ability
to use 14C as an isotopic tracer stems from changes in atmospheric 14CO2 over the last century
that resulted from atmospheric thermonuclear weapons testing in the late 1950’s and early
1960’s doubled the amount of 14C in the atmosphere (Hua et al., 2013). Following the
atmospheric nuclear weapons test ban in 1963, the amount of 14C in the atmosphere decreased
as “bomb” C was taken up by vegetation and oceans. Fossil fuel emissions contribute to the
sustained decline of atmospheric Δ14C values over recent decades (Graven et al., 2012).
Radiocarbon measurements consistently show that soil C is older than suggested by other
methods for calculating turnover times, such as dividing stocks by respiration rate (Trumbore
et al 2000; Torn et al., 2009). These results, supported by additional work using 14C to
quantify turnover times, demonstrate that soil organic matter is not homogenous with respect
to decomposition, rather it is made up of pools that cycle quickly (with turnover times of
years to decades) and pools that cycle slowly with turnover times of decades to millennia
(Trumbore et al., 1997; Gaudinski et al., 2000; McFarlane et al., 2013). Laboratory incubation
6
 International Conference on Negative CO2 Emissions, May 22-24, 2018, Göteborg, Sweden

and in situ 14C measurements of soil-respired CO2 demonstrate that quickly cycling pools
contribute disproportionately to soil respiration (Gaudinski et al., 2000; Phillips et al., 2013;
Phillips et al., 2015). Radiocarbon measurements of roots indicate that fine root biomass
consists of populations of roots that turnover on short timescales (≤ 1 year) and that are longer
lived (a decade or longer) rather than a single pool turning over annually (Gaudinski et al,
2001; Gaudinski et al, 2010).

2.2 IR based chemical characterization of SOM

Diffuse Reflectance Fourier Transformed Infrared (DRIFT) analyses enable measurements of
the chemical composition of soil organic matter (SOM) and can be used to compare SOM
profiles in soils with deep vs. shallow rooted plants (Ellerbrock et al. 1999; Kaiser and
Ellerbrock 2005; Diehl et al, 2009; Leue et al. 2010). DRIFT can detect and characterize
functional groups level differences in SOM across multiple soil depth profiles, identifying
carboxyl, carbonyl, alkyl groups that play different roles in terms of interactions between
organic and inorganic soil compounds by cation bridging (C=O groups) or ligand exchange
reactions (C=O, COOH and OH groups) (Ellerbrock et al. 1999; Kaiser and Ellerbrock 2005;
Leue et al. 2010).

2.3 Genome-resolved soil microbial metagenomes

Microorganisms have a broad range of traits that likely influence the persistence of soil C
(Keiluweit et al. 2012; Throckmorton et al. 2012; Kallenbach et al. 2016). For example, the
biochemical components of microbial cell walls and envelopes provide potentially important
precursors to persistent SOM (Keiluweit et al. 2012). Additionally, microorganisms also vary
widely in population dynamics and lifestyle traits (survivorship, growth rates, mortality),
which are directly related to C turnover. For example, carbon use efficiency dictates C
incorporation into biomass during microbial growth, and the fraction of C retained in soil
versus that respired can be related to microbial growth strategies (more rapidly growing
microorganisms have lower growth efficiency) (Roller et al. 2016). Many of the intrinsic and
adaptive microbial traits the regulate soil C stabilization can be identified at the genome scale
(Vieira-Silva and Rocha 2010; Fierer et al. 2014; Nayfach and Pollard 2015; Leff et al. 2015),
either directly as genome-inferred traits (e.g. maximum specific growth rate (Vieira-Silva and
Rocha 2010), cell wall type), or via gene or protein expression data (e.g. upregulation of stress
regulatory elements). However, until recently, it has not been possible to comprehensively
measure these traits in situ, with genomic resolution, making it impossible to test how they
relate to C persistence in heterogeneous matrices such as soil. Recent DNA sequencing and
bioinformatics advances (e.g. (Brown et al. 2016)), now make it possible to understand both
microbial functional potential, population dynamics, and biochemical composition of
individual populations. When used in concert with 18O quantitative stable isotope probing
(Hungate et al. 2015; Koch et al. 2018) (qSIP), these measurements become possible at the
individual or population genome scale. With this approach, one may connect C-persistence
traits from strain-resolved genomes to qSIP-derived population metrics, and thereby establish
robust mechanistic linkages between C cycling dynamics and soil microbial community
dynamics (Blazewicz et al. 2014).

7
 International Conference on Negative CO2 Emissions, May 22-24, 2018, Göteborg, Sweden

2.4 Soil C modeling

Earth System Models and the Land Surface Models within them consistently underestimate
carbon turnover time in soils (Todd-Brown et al., 2013; He et al., 2016). While adding
vertically resolved soil biogeochemistry data improves the Community Land Model’s (CLM)
ability to predict older soil carbon, the model output is sensitive to how vertically resolved
root inputs are parameterized and how to vertically resolve advection and diffusion (Koven et
al., 2013). To address these problems, we propose SoilR-- a modeling framework that allows
tracking of incorporation, transfer, and release of 14C in the soil system (Sierra et al., 2012;
Sierra et al., 2014). Soil C models constructed in SoilR can include any belowground carbon
pool (e.g., bulk soil, fractions, and roots) and flux (e.g., respiration, vertical transport of DOC,
and transfer between soil pools or fractions) and allows for time dependent input fluxes and
decomposition rates (i.e., it does not rely on steady state assumptions). SoilR also includes
functions to assess environmental drivers, including soil moisture, which can be used to
provide an additional test of the direct sensitivity of soil C turnover to moisture and
temperature in different soil types.

Using a combination of measurements and a reduced complexity model to constrain soil

carbon pool turnover times, SoilR can be used to assess the role of vertically-resolved root
inputs to the storage and longevity of soil C pools, and to predict the trajectory of soil carbon
stocks and turnover time with increased deep rooting. By combining soil carbon and 14C
profiles for roots and soil with other ecosystem C data (e.g. net primary productivity, litterfall,
belowground C stock size, soil respiration), a site-specific ecosystem soil carbon model can
be constructed in SoilR. Such models can be used to determined turnover times for root and
soil carbon pools with depth and for the entire soil system using on changes in atmospheric
14
CO2 over time. SoilR can also be used to quantify root inputs in plots with deep and shallow
rooting vegetation and predict the impact of those inputs on soil C storage and turnover to
2100.

3 Conclusion
A multi-site analysis using the approach described above would measure the magnitude and
rate of C storage in subsoils beneath deeply rooted vegetation, as well as the role of covarying
edaphic and biotic conditions (soil chemistry, microbiology). This detailed empirical data on
the accrual, turnover and stabilization of subsoil C would enable parameterization and
validation of mechanistic vertically-resolved models of soil C and a landscape-scale
evaluation of the effects of advancing deeply-rooted cultivars and their agricultural
management on SOM stocks.

8
 International Conference on Negative CO2 Emissions, May 22-24, 2018, Göteborg, Sweden

Acknowledgements

Work at LLNL was performed under the auspices of the U.S. Department of Energy under
Contract DE-AC52-07NA27344.

4 References
[1] Anderson-Teixeira, K. J., Davis, S. C., Masters, M. D. & DeLucia, E. H. (2009) Changes
in soil organic carbon under biofuel crops. Global Change Biology Bioenergy 1, pp. 75-
96.
[2] Blazewicz, S. J., Schwartz, E. & Firestone, M. K. (2014) Growth and death of bacteria
and fungi underlie rainfall-induced carbon dioxide pulses from seasonally dried soil.
Ecology 95, pp. 1162-1172.
[3] Blume, E., Bischoff, M., Reichert, J., Moorman, T., Konopka, A., Turco, R., (2002).
Surface and subsurface microbial biomass, community structure and metabolic activity as
a function of soil depth and season. Applied Soil Ecology 592, pp. 1–11.
[4] Ciais, P. et al. (2014) in Climate change 2013: The physical science basis. Contribution
of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on
Climate Change pp. 465-570 (Cambridge University Press).
[5] Clemmensen, K. E., Adam Bahr, O. Ovaskainen, A. Dahlberg, Alf Ekblad, Håkan
Wallander, J. Stenlid, R. D. Finlay, D. A. Wardle, and B. D. Lindahl. (2013) Roots and
associated fungi drive long-term carbon sequestration in boreal forest. Science 339 pp.
1615-1618.
[6] Conant, R. T., Paustian, K. & Elliott, E. T. (2001) Grassland management and conversion
into grassland: effects on soil carbon. Ecological Applications 11, pp. 343-355.
[7] Cotrufo, M. F., Wallenstein, M. D., Boot, C. M., Denef, K., & Paul, E. (2013). The
Microbial Efficiency Matrix Stabilization (MEMS) framework integrates plant litter
decomposition with soil organic matter stabilization: do labile plant inputs form stable
soil organic matter?. Global Change Biology, 19, 988-995.
[8] Diehl, D., Ellerbrock, R. H. & Schaumann, G. E. (2009) Influence of drying conditions
on wettability and DRIFT spectroscopic C–H band of soil samples. Eur. J. Soil Sci. 60,
pp. 557-566.
[9] Dodds, W.K., Banks, M.K., Clenan, C.S., Rice, C.W., Sotomayor, D., Strauss, E.A., Yu,
W., (1996). Biological properties of soil and subsurface sediments under abandoned
pasture and cropland. Soil Biology & Biochemistry 28, pp. 837–846.
[10] Ellerbrock, R. H., H, öhn, A. & Gerke, H. H. (1999) Characterization of soil organic
matter from a sandy soil in relation to management practice using FT-IR spectroscopy.
Plant and Soil 213, pp. 55–61.
[11] Fierer, N., Barberán, A. & Laughlin, D. C. (2014) Seeing the forest for the genes: using
metagenomics to infer the aggregated traits of microbial communities. Frontiers in
microbiology 5, pp. 614.
[12] Fierer, N., J.P. Schimel, and P.A. Holden, (2003) Variations in microbial community
composition through two soil depth profiles. Soil Biology & Biochemistry 35, pp. 167-
176.

9
 International Conference on Negative CO2 Emissions, May 22-24, 2018, Göteborg, Sweden

[13] Fisher MJ, Rao IM, Ayarza MA, et al. (1994). Carbon storage by introduced deep-rooted
grasses in the South American savannas. Nature 371: 236–238.
[14] Fisher, M. J., Rao, I. M., Ayarza, M. A., Lascano, C. E., Sanz, J. I., Thomas, R. J., &
Vera, R. R. (1994). Carbon storage by introduced deep-rooted grasses in the South
American savannas. Nature 371, pp. 236.
[15] Fontaine, S., Bardoux, G., Abbadie, L., & Mariotti, A. (2004). Carbon input to soil may
decrease soil carbon content. Ecology letters, 7 pp. 314-320.
[16] Fritze, H., Pietikainen, J., Pennanen, T., (2000). Distribution of microbial biomass and
phospholipid fatty acids in Podzol profiles under coniferous forest. European Journal of
Soil Science 51, pp. 565–573.
[17] Gaudinski, J.B., M.S. Torn, W.J. Riley, T.E. Dawson, J.D. Joslin, and H. Majdi, (2010)
Measuring and modeling the spectrum of fine-root turnover times in three forests using
isotopes, minirhizotrons, and the radix model. Global Biogeochemical Cycles 24, pp.
GB3029.
[18] Gaudinski, J.B., S.E. Trumbore, E.A. Davidson, A.C. Cook, D. Markewitz, and D.D.
Richter, (2001) The age of fine-root carbon in three forests of the eastern united states
measured by radiocarbon. Oecologia 129, pp. 420-429.
[19] Gaudinski, J.B., S.E. Trumbore, E.A. Davidson, and S. Zheng, (2000) Soil carbon
cycling in a temperate forest: radiocarbon-based estimates of residence times,
sequestration rates and partitioning fluxes. Biogeochemistry 51, pp. 33-69.
[20] Gelfand, I., Sahajpal, R., Zhang, X., Izaurralde, R. C., Gross, K. L., & Robertson, G. P.
(2013). Sustainable bioenergy production from marginal lands in the US Midwest.
Nature 493, pp. 514-517.
[21] Graven, H.D., T.P. Guilderson, and R.F. Keeling, (2012) Observations of radiocarbon in
CO2 at La Jolla, California, USA 1997-2007: Analysis of the long-term trend. J.
Geophys. Res. 117, pp. D02302.
[22] Grayston, S. J., Vaughan, D. & Jones, D. (1996) Rhizosphere carbon flow in trees, in
comparison with annual plants: the importance of root exudation and its impact on
microbial activity and nutrient availability. Appl. Soil Ecol. 5, pp. 29-56.
[23] He, Y., et al. (2016). Radiocarbon constraints imply reduced carbon uptake by soils
during the 21st century. Science 353, pp.1419-1424.
[24] Hua, Q., Barbetti, M., & Rakowski, A. Z. (2013). Atmospheric radiocarbon for the period
1950–2010. Radiocarbon, 55, pp. 2059-2072.
[25] Hungate, B. A., Mau, R. L., Schwartz, E., Caporaso, J. G., Dijkstra, P., Van Gestel, N.,
Koch, B. J., Liu, C. M., McHugh, T. A., Marks, J. C., Morrissey, E. & Price, L. B. (2015)
Quantitative microbial ecology through stable isotope probing. Appl. Environ. Microbiol.
81, pp. 7570-7581.
[26] Jackson RB, Lajtha K, Crow SE, Hugelius G, Kramer MG, Piñeiro G. (2017). The
ecology of soil carbon: pools, vulnerabilities, and biotic and abiotic controls. Annual
Review of Ecology, Evolution, and Systematics 48: pp. 419–445.
[27] Jansson, J., (2011) Towards “Tera-Terra”: Terabase Sequencing of Terrestrial
Metagenomes. ASM MIcrobe Magazine.
[28] Jobbagy, E.G. and R.B. Jackson, (2000) The vertical distribution of soil organic carbon
and its relation to climate and vegetation. Ecological Applications. 10: pp. 423-436.

10
 International Conference on Negative CO2 Emissions, May 22-24, 2018, Göteborg, Sweden

[29] Jones, M. & Donnelly, A. (2004) Carbon sequestration in temperate grassland

ecosystems and the influence of management, climate and elevated CO2. New
Phytologist 164, pp. 423-439.
[30] Kaiser, M. & Ellerbrock, R. H. (2005) Functional characterization of soil organic matter
fractions different in solubility originating from a long-term field experiment. Geoderma
127, pp. 196–206.
[31] Kallenbach, C. M., Frey, S. D. & Grandy, A. S. (2016) Direct evidence for microbial-
derived soil organic matter formation and its ecophysiological controls. Nature
Communications 7, pp. 13630.
[32] Keiluweit, M., Bougoure, J. J., Nico, P. S., Pett-Ridge, J., Weber, P. K. & Kleber, M.
(2012) Nano-scale investigation of the association of microbial nitrogen residues with
iron (hydr)oxides in a forest soil O-horizon. Geochimica et Cosmochimica Acta 95, pp.
213-226.
[33] Kell, D. B. (2012) Large-scale sequestration of atmospheric carbon via plant roots in
natural and agricultural ecosystems: why and how. Phil. Trans. R. Soc. B 367, pp. 1589-
1597.
[34] Kiem, R. & Kögel-Knabner, I. (2002) Refractory organic carbon in particle-size fractions
of arable soils II: organic carbon in relation to mineral surface area and iron oxides in
fractions< 6 μm. Organic Geochemistry 33, pp. 1699-1713.
[35] Koch, B. J., McHugh, T. A., Morrissey, E. M., Schwartz, E., van Gestel, N., Dijkstra, P.
& Hungate, B. A. (2018) Estimating taxon-specific bacterial growth rates in intact soil
communities. Ecosphere DOI:10.1002/ecs2.2090.
[36] Koven, C.D., W.J. Riley, Z.M. Subin, J.Y. Tang, M.S. Torn, W.D. Collins, G.B. Bonan,
D.M. Lawrence, and S.C. Swenson, (2013) The effect of vertically resolved soil
biogeochemistry and alternate soil C and N models on C dynamics of CLM4.
Biogeosciences, 10: pp. 7109-7131.
[37] Lal, R. (2011) Sequestering carbon in soils of agro-ecosystems. Food policy 36, pp. S33-
S39.
[38] Leff, J.W., Jones, S.E., Prober, S.M., Barberán, A., Borer, E.T., Firn, J.L., Harpole, W.S.,
Hobbie, S.E., Hofmockel, K.S., Knops, J.M. and McCulley, R.L., (2015). Consistent
responses of soil microbial communities to elevated nutrient inputs in grasslands across
the globe. Proceedings of the National Academy of Sciences, 112, pp.10967-10972.
[39] Leue, M., Ellerbrock, R. H. & Gerke, H. H. (2010) DRIFT mapping of organic matter
composition at intact soil aggregate surfaces. Vadose Zone Journal 9, pp. 317-324.
[40] Lorenz, K. & Lal, R. (2005) The depth distribution of soil organic carbon in relation to
land use and management and the potential of carbon sequestration in subsoil horizons.
Advances in agronomy 88, pp. 35-66.
[41] Lynch, J. P. & Wojciechowski, T. (2015) Opportunities and challenges in the subsoil:
pathways to deeper rooted crops. Journal of experimental botany 66, pp. 2199-2210.
[42] Lynch, J. P. (2013) Steep, cheap and deep: an ideotype to optimize water and N
acquisition by maize root systems. Annals of botany 112, pp. 347-357.
[43] McFarlane, K.J., M.S. Torn, P.J. Hanson, R.C. Porras, C.W. Swanston, M.A. Callaham,
Jr., and T.P. Guilderson, ( 2013) Comparison of soil organic matter dynamics at five
temperate deciduous forests with physical fractionation and radiocarbon measurements.
Biogeochemistry 112: pp. 457-476.
11
 International Conference on Negative CO2 Emissions, May 22-24, 2018, Göteborg, Sweden

[44] Nayfach, S. & Pollard, K. S. (2015) Average genome size estimation improves
comparative metagenomics and sheds light on the functional ecology of the human
microbiome. Genome biology 16, pp. 51.
[45] Paustian, K., Lehmann, J., Ogle, S., Reay, D., Robertson, G. P., & Smith, P. (2016).
Climate-smart soils. Nature 532, pp. 49.
[46] Phillips, C.L., K.J. McFarlane, B. LaFranchi, A.R. Desai, J.B. Miller, and S.J. Lehman,
(2015) Observations of 14CO2 in ecosystem respiration from a temperate deciduous forest
in northern wisconsin. Journal of Geophysical Research: Biogeosciences 120: pp. 600-
616.
[47] Phillips, C.L., K.J. McFarlane, D. Risk, and A.R. Desai, (2013) Biological and physical
influences on soil 14CO2 seasonal dynamics in a temperate hardwood forest.
Biogeosciences, 10: pp. 7999-8012.
[48] Pries, C. E. H., Castanha, C., Porras, R. C., & Torn, M. S. (2017). The whole-soil carbon
flux in response to warming. Science, 355, pp. 1420-1423
[49] Rasse, D. P., Rumpel, C. & Dignac, M. (2005) Is soil carbon mostly root carbon?
Mechanisms for a specific stabilisation. Plant and Soil 269, pp. 341-356.
[50] Roller, B. R., Stoddard, S. F. & Schmidt, T. M. (2016) Exploiting rRNA operon copy
number to investigate bacterial reproductive strategies. Nature Microbiology 1, pp.
16160.
[51] Rumpel, C. & Kögel-Knabner, I. (2011) Deep soil organic matter—a key but poorly
understood component of terrestrial C cycle. Plant and Soil 338, pp. 143-158.
[52] Schlesinger, W. H. & Bernhart, E. S. (2013) Biogeochemistry: An Analysis of Global
Change. (Academic Press/Elsevier).
[53] Schmidt MW, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M,
Kögel-Knabner I, Lehmann J, Manning DA, Nannipieri P. (2011) Persistence of soil
organic matter as an ecosystem property. Nature 478, pp. 49.
[54] Sierra, C., Muller, M. & Trumbore, S. (2012) Models of soil organic matter
decomposition: the SoilR package, version 1.0. Geoscientific Model Development 5, pp.
1045-1060.
[55] Sierra, C., Müller, M. & Trumbore, S. E. (2014) Modeling radiocarbon dynamics in soils:
SoilR version 1.1. Geoscientific Model Development 7, pp. 1919-1931.
[56] Smith, P. (2012) Soils and climate change. Current Opinion in Environmental
Sustainability 4, pp. 539-544.
[57] Smith, P., Martino, D., Cai, Z., Gwary, D., Janzen, H., Kumar, P., McCarl, B., Ogle, S.,
O'Mara, F., Rice, C. and Scholes, B., (2008) Greenhouse gas mitigation in agriculture.
Philosophical transactions of the royal Society B: Biological Sciences, 363, pp.789-813.
[58] Sollins, P., Swanston, C., Kleber, M., Filley, T., Kramer, M., Crow, S., Caldwell, B.A.,
Lajtha, K. and Bowden, R., (2006). Organic C and N stabilization in a forest soil:
evidence from sequential density fractionation. Soil Biology and Biochemistry, 38, pp.
3313-3324.
[59] Stoof, C.R., Richards, B.K., Woodbury, P.B., Fabio, E.S., Brumbach, A.R., Cherney, J.,
Das, S., Geohring, L., Hansen, J., Hornesky, J. and Mayton, H., (2015). Untapped
potential: opportunities and challenges for sustainable bioenergy production from
marginal lands in the Northeast USA. BioEnergy Research, 8, pp. 482-501.

12
 International Conference on Negative CO2 Emissions, May 22-24, 2018, Göteborg, Sweden

[60] Throckmorton, H. M., Bird, J. A., Dane, L., Firestone, M. K. & Horwath, W. R. (2012)
The source of microbial C has little impact on soil organic matter stabilisation in forest
ecosystems. Ecology Letters 15, pp. 1257-1265.
[61] Todd-Brown, K. E. O., et al. (2013). Causes of variation in soil carbon simulations from
CMIP5 Earth system models and comparison with observations. Biogeosciences 10, pp.
1717-1736.
[62] Torn, M.S., C.W. Swanston, C. Castanha, and S.E. Trumbore (2009) Storage and
Tunover of Organic Matter in Soil, in Biophysico-Chemical Processes Involving Natural
Nonliving Organic Matter in Environmental Systems, N. Senesi, B. Xing, and P.M.
Huang, Editors. John Wiley & Sons, Inc.: Hoboken, New Jersey. pp. 219-272.
[63] Trumbore, S. E., Davidson, E. A., Barbosa de Camargo, P., Nepstad, D. C., & Martinelli,
L. A. (1995). Belowground cycling of carbon in forests and pastures of Eastern
Amazonia. Global Biogeochemical Cycles, 9, pp. 515-528.
[64] Trumbore, S., (2000) Age of soil organic matter and soil respiration: radiocarbon
constraints on belowground C dynamics. Ecological Applications, 10, pp. 399-411.
[65] Trumbore, S.E. and J.W. Harden, (1997) Accumulation and turnover of carbon in organic
and mineral soils of the Boreas northern study area. Journal of Geophysical Research:
Atmospheres 102, pp. 28817-28830.
[66] Veldkamp, E., Becker, A., Schwendenmann, L., Clark, D. A., & Schulte Bisping, H.
(2003). Substantial labile carbon stocks and microbial activity in deeply weathered soils
below a tropical wet forest. Global Change Biology 9, pp. 1171-1184.
[67] Vieira-Silva, S. & Rocha, E. P. (2010) The systemic imprint of growth and its uses in
ecological (meta) genomics. PLoS genetics 6, pp. e1000808.

13