Interactions and Self-Organization in the

Soil-Microbe Complex
I. M. Young, et al.
Science 304, 1634 (2004);
DOI: 10.1126/science.1097394

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 SOILS—THE FINAL FRONTIER
SPECIAL SECTION
REVIEW

Interactions and Self-Organization in the

Soil-Microbe Complex
I. M. Young* and J. W. Crawford

Soil is the most complicated biomaterial on the planet. As with any material, the across all measured scales, from nm to km
physical habitat is of prime importance in determining and regulating biological (4 ). The geometrical complexity of the pore
activity. However, until recently the opaque nature of soil has meant that any pathways determines the biochemical pro-
interrogation of its interior architecture has been relatively rudimentary, restricted cesses that govern life on Earth, such as plant
to simple qualitative expressions of the physical heterogeneity that fail to relate to productivity (5 ), water retention (6), and
any specific function. However, new techniques and insights into the biophysical and greenhouse gas emissions (7), and offer an
biochemical processes of this inner space are leading to the developments of unrivaled buffering capacity against potential
theoretical frameworks and experimental approaches that will allow us to sustain- pollutants entering the waterways (8, 9). A
ably manage Earth’s most important resource. We introduce the concept that the key distinction between older geological fea-
soil-microbe system is self-organized and suggest new priorities for research based

Downloaded from www.sciencemag.org on June 9, 2009

on an integrative approach that combines biochemistry and biophysics.
The Mars Rover is looking for evidence that life
existed in martian soil. This is perhaps the only
extraterrestrial foothold for life we will be able
to directly observe for generations to come. If
signs of life are indeed discovered, it promises
to be one of the most notable scientific findings
of all time. It is appropriate that soil is afforded
this special status, underpinning as it does all
forms of life on our own planet. Given its
importance, it is surprising how little we know
about our most important natural resource. In-
deed, much about soil remains a mystery, yet it
probably presents us with the most important
clues as to how complex ecosystems become
capable of self-organization and sustaining
functionality. Pick up a handful of soil and ask
the question “what is in it?” and an exciting
new journey into inner space begins.
Biological Diversity
In fertile garden or organic soil, there will be
more individual organisms than the total num-
ber of human beings that have ever lived: 1012
bacteria, 104 protozoa, 104 nematodes, 25 km
of fungi, and countless other species. Depend-
ing on clay composition and amount, the soil’s
total surface area could cover a full-sized foot-
ball pitch. So, although the soil is teeming with
life, the fraction of the surface area covered by
soil microbes is only about 10– 6 %, which,
coincidentally, is the same percentage of land
area on Earth that humans cover. The important
point here is not the absolute coverage, which
can vary with clay content, moisture, and sub-
strate availability, but the fact that it is consid-
erably less than 1%, even with the most opti-
mistic balance of inputs.
Scottish Informatics, Mathematics, Biology, and Sta-
tistics (SIMBIOS) Centre, University of Abertay, Bell
Street, Dundee, DD1 1HG Scotland, UK.
*To whom correspondence should be addressed. E-
mail: imy@tay.ac.uk
The soil-microbe complex is particularly
important with regard to the services it provides
for agriculture, waste management, and the wa-
ter industry, as well as the natural and semi-
natural environment (1). There is now a large
body of evidence showing that heterogeneity at
these scales is highly ordered, and the resulting
spatial clustering of the matrix gives soil its
characteristic aggregated structure (2). This ag-
gregated state gives rise to a broad range in pore
sizes that permits the coexistence of air and
water essential to the biological functioning of
soil. This structure determines the ease with
which plants may extract water, the rate of flow
in unsaturated conditions, and the rate of diffu-
sion of compounds and gases into and out of the
soil matrix. Small changes in soil moisture can
change the associated rate coefficients by or-
ders of magnitude, sensitively dependent on the
fine-scale structure.
The processes governing the survivability
and functioning of above-ground communities
are the same as those below ground. We now
know that an understanding of ecosystem func-
tion requires an integration of both biotic and
abiotic factors (3). Nowhere is ecosystem func-
tioning more important to sustaining life than in
soil. Here, however, although much work has
concentrated on developing techniques that are
able to measure the diversity of soil biology,
little effort has been spent in connecting
these measures with habitat and then func-
tion. This is despite the fact that the phys-
ical structure of soil is likely to have a
major impact on the diversity of biophysi-
cal microenvironments for soil microbes. A
major impediment to progress is the structural
complexity of soil that presents major challenges
in understanding its role as a habitat.
Diversity in Microenvironments
The physical habitat of soil is characterized
by physical and temporal heterogeneities
tures, such as sandstone and granite, and
younger soil systems is that the latter exhibit
pore structures that are defined not only by
the chemical nature of the material but by life
itself and thus experience significant bio-
physical and biochemical changes over rela-
tively short spatial and temporal scales. This
distinction appears to dominate all fertile
soils and is possibly a key diagnostic for the
health of soil ecosystems because it repre-
sents an important functional bridge between
the physics and biology of soil (Fig. 1).
Quantifying the physical habitat of soil
systems has been an area of intense research
with relatively little reward. Most of the tech-
niques at large (m) and small (␮m to mm)
scales have revealed a staggering variability
in pore structures but have failed to relate
such variability to function in any meaningful
way (2). Over the past decade, research has
moved from highly qualitative descriptors
of pore shape to more quantitative mea-
sures of pore connectivity and tortuosity.
More importantly, increasing emphasis has
been given to understanding the conse-
quences of structure for the physical and
chemical properties of soil with a range of
modeling techniques (6 ).
The capacity of soil to sorb chemicals
from solution (the cation exchange capacity)
regulates the movement of pollutants to the
atmosphere and waterways. It controls the
sorptive properties of nutrients through inter-
action between cations and clay particles,
which tend to have net negative charges, and
thus the productivity of the soil in terms of
plant biomass and the activity of organisms
and movement of viruses through the soil.
The techniques used to measure this involve
the homogenization of the soil below a spe-
cific particle size range, which is then satu-
rated. Under such circumstances accessibility
of reactive sites to any chemical in solution is
maximized. This test is in widespread use
throughout the world, the results of which
may bear little relation to what is really hap-

1634 11 JUNE 2004 VOL 304 SCIENCE www.sciencemag.org

 SOILS—THE FINAL FRONTIER

pening. The accessibility of the reactive sites
and retention time of solution near an ex-
change site is dictated by the fine-scale struc-
ture and the hydraulic connectivity and
conductivity of the habitat. Comparisons
between cation exchange capacities in ho-
mogenized and structured soils show that the
amount of exchangeable cations of the struc-
tured soil is reduced by 10% in the structured
system, where mass flow dominates. Where
diffusion processes becomes more important, over
longer time scales and/or under desaturated con-
ditions, the reduction is over 50% (10). In other
areas such as designing porous catalysts for chem-
ical reactors, the links between reactive surfaces
and exchange processes have been explained in
terms of fractal processes (11, 12), an approach
that has had a growing following in application
to soil (13) and in some of our recent work on
bilities including resolutions of 1 ␮m, dual
energy facilities to decouple solid, water, and
pore, as well as (in the higher specification
systems) a facility to quantify the 3D distri-
bution of some organics and minerals (Fig.
2). However, technical difficulties associated
with distinguishing microbes will have to be
overcome before the technique can be used to
investigate structure-microbe interactions in
situ (Movie S2).
In parallel with the development of these
imaging techniques, sophisticated modeling
tools have been developed with the aim of
understanding the consequences of soil struc-
ture and microbial distribution for various func-
tions of the soil-microbe complex. Perhaps the
most important of the generic approaches is the
use of fractals as models of structure. These
have provided a sufficiently simple
SPECIAL SECTION
physical structure of soil. These on their own
cannot be regarded as proof that the structure
is fractal, and indeed the measurement of the
fractal properties of soil is fraught with dif-
ficulties (22). Further evidence is required,
and this relates to the origins of the underly-
ing power-law structural correlations. There-
fore progress requires that we move from the
static picture of soil structure that has pre-
dominated in the literature to one that em-
braces the dynamic properties. Interestingly,
this picture points to the fundamental impor-
tance of the interaction between the physical
and biological processes in soil.
System Dynamics
The prevailing understanding of the origin of
soil structure emphasizes the different forces

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the impact of irregular surfaces in predator-prey
dynamics in soils (14).
An important step toward integrating the
biology and physics of the soil ecosystem has
been the development of techniques that allow
the microbes to be observed in their natural
physical habitat. Foster, with the use of ultrathin
sections, investigated the organization of soil
organic matter and minerals in the context of
bacteria (15) and suggested that the polar na-
ture of some organisms allows physical adhe-
sion between organisms and charged clay plate-
lets (Fig. 1). More recent advances in sample
preparation, image processing, and analysis
have now allowed us to physically fix the lo-
cation of fungi and bacteria and investigate
their spatial distribution in the context of a
spatially heterogeneous habitat (16). The use of
such techniques in combination with powerful
geostatistical analysis reveals a hitherto un-
known variability in microbial populations.
Some of our recent work has shown that,
whereas the distribution of individual bacterial
cells was organized at two separate scales in the
subsoil, within the topsoil the distribution was
random (17). Other work examining whole-
community DNA and amplified fragment
length polymorphism DNA fingerprinting
showed that, even within a habitat deemed ho-
mogeneous at the plot scale, bacterial distribu-
tions were highly structured, with individual
microbial communities being aggregated in
specific ways in response to the spatial hetero-
geneity imposed by the habitat (18). The im-
portance of such aggregation in terms of func-
tion and how we understand our environment is
summarized in an excellent paper by Ettema
and Wardle (19) (Movie S1).
Any technique based on sectioning is lim-
ited by the difficulty in inferring the proper-
ties of the original three-dimensional (3D)
structure. Some of these limitations will be
overcome by the advancements in computer-
aided tomography, pioneered in soils re-
search by Crestana et al. (20). New desktop
systems promise advanced tomography capa-
representation to allow some poten-
tially important generalizations to be
drawn. First, with the use of these
models it has been shown that as-
sumptions behind the traditional
measures of soil structure, such as
the particle size distribution and the
water retention characteristic, are in-
valid and that these measures on
their own are unreliable. It has also
been possible to show that the
fractal-like structure of soil means
that coefficients determining diffu-
sion and convection rates will be
scale-dependent over the length
scales where the models are appro-
priate. These length scales are of
importance to microbial processes,
and, as we shall see, scale dependen-
cy in the rate coefficients might play
a defining role in the organization of
the soil-microbe complex and the
sustainability of soil function. Sec-
ond, fractal models have shown how
natural length scales can emerge
from the interaction between biolog-
ical and physical processes in soil.
With the use of the distribution of
oxygen in soil as an example, Rap-
poldt and Crawford (21) have
shown that simple models for deni-
trification that model the geometry
of soil as a packing of aggregates
obeying a log-normal size distribu- Fig. 1. (A and B) Two soil thin sections taken from the same
tion require an artificial (and arbi- core. Note the high degree of spatial variability within one
trary) cutoff in upper aggregate size undisturbed soil sample. Each thin section is ⬃30 ␮m thick
and 2 cm in length. To visualize the pore space, we cap-
to perform well. A fractal model pro- tured images on a high-resolution digital camera first under
duces the same result, but the rarity of transmitted light (left-hand images) and then with the use
large-scale structures emerges natural- of cross polar light. The latter allows us to distinguish pores
ly as a consequence of the interaction from quartz grain. A binary image is then made of the solid
between biological activity and phys- (black) and the pore (white) space (right-hand images). (C)
ical complexity of soil (Fig. 3). High-resolution biological thin section (⬃30 ␮m thick and
600 ␮m in length). Illumination under ultraviolet light
Perhaps the most important reveals the location of fluorescently labeled microbes,
lesson from fractal models is the which can be segmented with the use of a series of image
emphasis on the power-law corre- processing steps to reveal their location relative to the
lations that are observed in the structure (yellow spots on right-hand image).

www.sciencemag.org SCIENCE VOL 304 11 JUNE 2004 1635

 SOILS—THE FINAL FRONTIER
SPECIAL SECTION

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Fig. 2. A 3D visualization of a repacked dried soil core (3.5 cm by 1 Fig. 3. The predicted distribution of oxygen in structured soil modeled as
cm), with a resolution of 42 ␮m Voxel. Computer tomography a fractal and its dependence on microbial respiration rate. Each box
reconstruction produced by X-Tek System Limited (Tring, England) for represents a 2D layer of soil open to the atmosphere at the upper and
SIMBIOS Centre. The range in photon densities of the inorganic and lower boundary. The structure in each box is the same, whereas the
organic materials in many soils systems means that strict image- potential respiration rate per unit volume decreases from a maximum
capture protocols and sophisticated image analysis must be used to (top) to a minimum (bottom). Red denotes low oxygen concentration,
resolve the pore space from the surrounding components. New yellow denotes atmospheric concentration, and light blue is the soil
generation machines will be able to distinguish water from pore and matrix. The pore-scale spatial complexity and diversity of oxygen envi-
identify specific mineral components in three dimensions. ronments is obvious in all boxes, as is the spatial proximity of high and
low oxygen concentration regimes. Even where potential microbial res-
piration is low, regions of low oxygen concentration prevail. [See (21) for
that dominate at different scales. At the molec- activity in affecting further details. Images courtesy of K. Rappoldt.]
ular scale, aggregated structures such as clay structural characteris-
platelets are dominated by electrostatic and van tics (28). This model
der Waal forces. At progressively larger scales, incorporated the impact of microbial activity on quence of the interaction between the physi-
aggregation is dominated by soil microbes, structural genesis as a scale-dependent binding cal and biological processes as mediated by
such as fungi and bacteria either exuding glue- probability representing the relative weakness the structure of soil. The soil-microbe com-
like substances or acting as reinforcement rods and smaller probability of microbially mediated plex can be viewed as a self-organizing sys-
through the soil matrix, or roots acting to bind binding at larger scale. Fractal-like power-law tem capable of adapting to prevailing condi-
soil aggregates and particles together. This view correlations in the aggregated structure were tions (29, 30). Therefore, by ignoring the
formed the conceptual model of Tisdall and predicted. The results showed that, whereas interaction between physical and biological
Oades (23) and has been consistently misinter- mechanical restructuring and the particle size processes in soil, we might be missing its
preted as providing evidence for the existence distribution of the primary particles are major most essential feature.
of discreet, experimentally manipulative aggre- determinants of soil structure as measured by
gates rather than as a qualitative description of the fractal dimension, microbial activity affect- Conclusions
the aggregated hierarchical nature of the soil ed only the range over which fractal-like Soil is the most diverse and important ecosys-
system in terms of the linkages between the power-law correlations in structure emerged. tem on the planet. Myriad biophysical and bio-
architecture of the habitat and biological func- This, combined with the scale dependency in chemical processes persist in parallel that are
tioning. Over the past decade, this conceptual the rate coefficients that is predicted by fractal required to sustain all of the other trophic levels
model has been used as an excuse to develop a models for soil structure, means that increased in the biosphere. A key to this is the physical
wide variety of tests that purport to quantify the microbial activity would lead to changes in soil complexity of the soil physical structure that
stability of soil ecosystems (24, 25) but in structure that would increase local oxygen dif- provides the habitat for soil organisms and the
reality tell us little about the functioning of soil fusion rates. Thus changes in the environmental conduit for essential resources.
and more about the tests used (26). Neverthe- context that act to increase local microbial activity Although ecologists studying above-
less it does implicate microbial activity in the (e.g., the arrival of a biologically available solute) ground systems are beginning to realize the
genesis of soil structure and provides us with a will result in a reorganization of the soil-microbe important role of interactions between biotic
basis of a conceptual model for the dynamics of complex that facilitates further exploitation (Fig. and abiotic factors, soil science is still pro-
the soil-microbe complex. 4). Structure continues to build up in this way until gressing with soil biology, soil chemistry,
Aggregation processes have been studied in the context is changed (e.g., the resource is used and soil physics as largely independent fields.
a wide range of contexts in physics, chemistry, up), whereupon the structure changes to one with This is doomed to failure, because no one
and biology (27). These approaches have been correspondingly lower diffusion rates. discipline will be able to understand the most
exploited in a simple model for soil aggregation In this picture, the functionality and dy- complex biomaterial on the planet. There is
and in particular to study the role of microbial namical behavior of soil emerges as a conse- mounting evidence that the essential features

1636 11 JUNE 2004 VOL 304 SCIENCE www.sciencemag.org


types in soil and de-
termine the rate and
consequences of gene
flow. A 3D dynami-
cal model of soil
structural genesis is
also absent but is
likely to be needed to
study the potential
for self-organization
in soil.
The representation
of the diversity of
microenvironments
in soil depends on an
ability to model the
distribution of water,
unsaturated solute
Fig. 4. Conceptual model for self-organization in the soil-microbe com- flow, and diffusion in
plex. Substrate arrives at a location in soil, and the potential microbial porous media. Tech-
respiration rate increases, leading to local depletion of oxygen (left-hand niques for some of
image, with oxygen concentration represented as in Fig. 3). Increased these are relatively
microbial activity changes the local structure, creating a more open well advanced, but
aggregated state. This leads to enhanced rates of oxygen supply (right-
hand image). As substrate is used up, activity declines and the structure the modeling of mul-
collapses to a more closed state. The open and closed states may tiphase flow is still
represent optimal configurations for oxygen supply in a high potential problematic. An inte-
activity regime (open) and protection from desiccation and predation in grated approach to
a low potential activity regime (closed). studying soil with
emphasis on the in-
of soil will emerge only when the relevant teractions between physical and biological
physical and biochemical approaches are in-
processes is required to bring the science up
tegrated. Some progress has been made, but to comparable levels with above-ground ecol-
there remains much to be done. For example, ogy. This would greatly benefit from contri-
a theory linking microbial population dynam- butions by scientists working in related topics
ics to biodiversity and function in terms of in application areas outside soil. Not only
the soil microenvironment is more or less will soil science benefit, but, by having func-
absent. This presents a major challenge and tionality, ecosystem dynamics, and evolution
will require molecular biologists, microbiol- at its core, soil could become the paradigm
ogists, soil physicists, and theoreticians to system for exercising our understanding of
work closely together. A means of function- sustainable ecological processes and reveal
ally classifying microbes in terms of essential insights into how the inner space of a wide
traits that relate growth and competition to range of materials impacts function.
environmental conditions will be required.
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Supporting Online Material
www.sciencemag.org/cgi/content/full/304/5677/1634/
DC1
Movies S1 and S2
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