Opinion TRENDS in Biotechnology
1 January 2006
Life in earth: the impact of GM
plants on soil ecology?
Andrew K. Lilley1, Mark J. Bailey1, Colin Cartwright2, Sarah L. Turner1
and Penny R. Hirsch3
1
Centre for Ecology and Hydrology, Oxford, Mansfield Road, Oxford, UK, OX1 3SR
2
Atkins Environment, Woodcote Grove, Ashley Road, Epsom, Surrey UK, KT18 5BW
3
Plant Pathogen Interactions Division, Rothamsted Research, Harpenden, Herts, UK, AL5 2JQ
The impact of changes incurred by agricultural biotech-
nology has led to concern regarding soil ecosystems
and, rightly or wrongly, this has focused on the
introduction of genetically modified (GM) crops. Soils
are key resources, with essential roles in supporting
ecosystems and maintaining environmental quality and
productivity. The complexity of soils presents difficulties
to their inclusion in the risk assessment process
conducted for all GM plants. However, a combined
approach, informed by both soil ecology and soil quality
perspectives, that considers the impacts of GM crops in
the context of conventional agricultural practices can
provide a regulatory framework to ensure the protection
of soils without being overly restrictive.
Introduction
The development of GM crops has spurred concerns
regarding the sustainability of soil ecosystems (ecological
communities and their environment, functioning as a
unit). GM plants contain genetic material that is not
normally present in, or that has been modified artificially
outside, the plant. This article considers GM plants and
their impacts on farming and natural ecosystems;
however, we should stress that most of the issues raised
equally apply to the introduction of new cultivars and
novel crops (GM or non-GM) and any attendant changes in
agricultural practice, such as mechanization, ploughing
regimes, planting times and pest control. Indeed, there is
a need for improved scientific means to assess the impact
of many of these conventional changes on soil ecosystems.
Plants are the major drivers of the soil ecosystem,
which provides fundamental services to the functions of
local and global ecosystems. In addition to supporting
plant growth, these services include: the regulation of
water quality and quantity; nutrient cycling; carbon
sequestration; and the bioremediation of wastes. The
close relationship between plants and soil ecosystem
function causes concern that GM-associated changes in
crops and agronomic practices will affect soil systems.
If GM crops do affect highly complex soil-ecosystems,
how can these impacts – beneficial or deleterious – be
assessed and compared with the effects of conventional
Corresponding author: Bailey, M.J. (mbailey@ceh.ac.uk).
Available online 22 November 2005
www.sciencedirect.com 0167-7799/$ - see front matter Q 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.tibtech.2005.11.005
Vol.24 No.
agriculture? In this article, we propose that the appro-
priate science and criteria for risk assessment and post-
release monitoring of GM plants requires (i) both broad
and specific assessments of soil systems, and (ii) that these
assessments should benefit from the contrasting perspec-
tives of soil ecology (soil organisms and soil processes) and
soil quality (capacity to provide and sustain defined
functions). Improvements in soil science and biomolecular
methods ensure that a substantial amount of bioinfor-
matic and functional data can be collected at either the
community level or the more specific population level. The
continued improvement in these methods generates new
challenges to align data from nucleic-acid signature,
microarray, metagenomic and other technologies with
existing knowledge of the response of soil ecosystems to
conventional agricultural practices.
Unlike conventional breeding, the genetic manipu-
lation of plants is expected to herald an increasing number
of novel applications for agribiotech, including the
production of fuels, pharmaceuticals and compound
syntheses [1]. In adopting the usual case-by-case
approach, novel assays will be called for, but the key to
assessing the impacts of GM plants on soil systems will
continue to be our understanding of soil functions, soil
ecology, and how we define harm. Some crops will be
modified deliberately to affect soil factors, including
nutrient uptake and drought and disease resistance.
These innovations will place increasing pressure on us to
improve risk assessments and monitoring of the potential
effects of these novel plants. Such evaluations are
important because the application of the precautionary
principle requires a serious effort to identify possible
harmful effects and make scientific evaluations that are
proportionate to the desired level of protection [2].
Because our understanding of soil ecology is imperfect, it
is important that this principle should not be interpreted
as aiming for zero risk; otherwise, we might fail to benefit
fully from the GM technologies that could potentially
improve the efficiency of agriculture, reduce the pressure
on land, advance food quality and increase the sustain-
ability of production [3].
Soil systems and the influence of plants
Soils are home to a diverse range of life. The microbial
components (bacteria, fungi, protists and nematodes) are
10 Opinion TRENDS in Biotechnology Vol.24 No.1 January 2006

dominant, although their diversity is not well classified
(Figure 1). The interactions between these organisms take
place within the soil matrix, an environment where micro-
scale (mm) changes in distance can mean changes in the
bioavailability of key factors, such as water, oxygen and
nutrients, thereby conferring selection pressure on a
range of substantially different microbes. This
heterogeneity helps to explain why soils are the most
diverse habitats on the planet and why competition does
not exclude more species [4].
Plants and microorganisms are greatly affected by the
soil, and vice versa. Plants influence soils through
rhizodeposition (root exudates, sloughing of root cells
and root turnover) [5], plant litter, and water, gas and
nutrient exchanges. The most intimate effects of plant
roots on the soil microbiota are known collectively as the
‘rhizosphere effect’ and occur in the rhizosphere – the area
directly around a root. The rhizosphere is profoundly
influenced by the root, resulting in a distinct microbial
population that is larger and more active than that found
in the surrounding bulk-soil zone, which is not
immediately adjacent to roots [6–8]. Plants, as the major
source of organic carbon, are the drivers of microbial
growth and activity in soil and changes to plants can affect
the structure of the soil community and its functions
[9,10].
The activity and diversity of soil communities are known
to be directly affected by common variables of agricultural
practice, including: change of plant species [11,12]; water
stress [13]; fertilization [14]; field management [15]; tillage
[16]; fungal disease [17]; plants and field management [18];
grassland improvement [19]; nitrification [20]; and soil
depth [21]. It is therefore expected that GM crops will have
some effects on soils, and the challenge is to formulate
realistic criteria for the assessment and monitoring of the
effects of the genetic modification of these plants on the
soil communities.
Assessing the impacts of GM crops on the soil
ecosystems
A recent and comprehensive review [22] of research into
the effects of GM plants on soil systems considered the

Microbiota (1 – 100 µm) Mesofanna (100 µm – 2 mm) Macrofauna (2 – 20 mm) Megafauna (>20 mm)
Primary producers, Detritovores and/or shredders Shredders and detrivores Herbivores, predators
herbivores, detritovores, bacterial and fungal feeders herbivores, predators Arthropods
predators
Tardigrades 0.1 – 1 mm Enchytraeid worms
Molluscs
Nematodes: 50 – 1000 µm
Collembola 0.2 – 6 mm Arthropods Mammals

Predatory Mites 0.5 – 2 mm Molluscs Birds

Bacteria and/or fungus Earthworms
Plant feeders

Protists 5 – 500µm

Fungi 5 – 50 µm

Bacteria 0.5 – 5 µm

1st Trophic level

(primary producers)
plants, autotrophic bacteria

detritus

2nd Trophic level

decomposers and/or detritovores,
mutualists, pathogens, parastites,
root feeders

3rd Trophic level

shredders,grazers, predators

4th Trophic level

higher predators
5th Trophic level
higher predators
TRENDS in Biotechnology

Figure 1. Soil food web showing an outline classification of the soil biota based on type, body size and trophic level. These components have a variety of interactions ranging
from the competitive or predatorial to the cooperative and symbiotic. Size class is based on the width of the organism according to Swift [38].

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 Opinion TRENDS in Biotechnology
Box 1. The effects of GM plants on soil systems
A recent comprehensive review [22] has been made of studies of the
effects of GM plants on soil systems (http://www.defra.gov.uk/
environment/gm/research/epg-1-5-214.htm). This highlights 25 peer-
reviewed studies involving nine plant species (alfalfa, bird’s-foot
trefoil, black nightshade, potato, rice, maize, cotton, tobacco and
oilseed rape) genetically modified in ten distinct ways for the
expression of: a-amylase; lignin peroxidase; an organic acid (malate
dehydrogenase); T4-lysozyme (anti-pathogenic); cecropin b (an
antibacterial lytic peptide); Bt toxin; insect resistance (proteinase
inhibitor I); herbicide tolerance; opines; and lignin production. Effects
on the soil community or soil system were noted in 16 of the studies.
Although these effects were generally transient, they included effects
on bacterial diversity, number and activity; fungal counts; effects on
numbers of protozoa, nematodes and collembola; diversity of
nematodes; and woodlice mortality. Most of these studies were
limited to a single growth-season; although some post-experiment
monitoring was reported and two- and three-year studies were
reported in transgenic herbicide tolerant canola [39] and T4-lysozyme
expressing potato [25,40]. The conclusions of this review [22] were as
follows:
† Considerations of the transgene product, its activity, site of
expression and persistence are important guides to developing, on a
approaches used to assess the risks to, and the resulting
changes observed in, one or more components of the soil
ecosystem (Box 1). As part of the regulation process for
new GM plants, risk assessments proceed on a case-by-
case basis. The nature of the novel trait and the probable
impact of the modified plant on the environment are both
considered; however, the importance of plants in the soil
ecosystem means that the case-by-case approach needs to
be grounded in soil ecology to ensure a suitable choice of
criteria and methods for risk assessment and monitoring.
Because it is not feasible to monitor all components of a
soil ecosystem for their response to a GM crop, the use of
keystone indicators is advocated. These focus the moni-
toring process on organisms whose demise is expected to
result in the loss of a particular soil function and are
therefore indicative of any negative effects exerted on the
soil ecosystem [23,24]. Keystone indicators are chosen for
their agronomic relevance, ecological significance and
responsiveness to perturbations, plus the availability of
practical assay methods.
Some keystone indicators have been particularly
advocated [22,23]. These include arbuscular mycorrhizal
fungi, plant growth-promoting rhizobacteria (PGPR),
wood lignin-decomposing fungi and nitrogen fixing and
nitrifying bacteria [24,25]. In some cases, the type of GM
plant will influence the choice towards more specific
keystone indicators (i.e. those likely to be affected by the
introduced trait) [26–28]: when monitoring a crop produ-
cing transgenic opine, for example, the opine-utilizing
agrobacteria populations were assayed [29]. Although
keystone indicator organisms specific to the GM crop are
often identified in risk assessments, the general keystone
indicators listed above have, so far, usually been ignored
in the assessment and monitoring process. This is
unfortunate, because it is only through their application
in a range of soils and crops that more general criteria can
be established. It could also be the case that field-grown
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Vol.24 No.1 January 2006 11
case-by-case basis, lines of investigation into probable and/or
important potential effects.
† Most transgenic plants have detectable effects on the soil system,
which are relatively minor compared with differences between
cultivars or those associated with weather and season. Assays of the
natural variation in the system provide valuable baseline references.
† The response of soil systems when transgenic plants are removed
provides an important measure of impact. Studies generally find a
quick return of many soil parameters to match those of the
control soils.
† Many apparent losses of taxa observed in field monitoring are
probably changes in the relative numbers of different groups in
the community.
† Regular sampling is important because changes in community
structures, through the season and plant development, confer an
added level of complexity to comparing transgenic–non-transgenic
effects. Many of these effects are context-dependent and not
systematic in character through the season.
† Arising from the case-by-case approach, specific targets for
monitoring are established, which have intrinsic and clear definitions
of damage; however, there is a lack of monitoring activity, which is
linked to a concept of damage to the system.
GM crops have not had the kind of impact on soils that
would result in the loss, or serious decline, of an important
functional group.
Assays of GM plant impacts on soil ecosystem activity
and diversity
It is recognized that, in addition to the use of keystone
indicators, there is a need for broader analyses of the
impacts on the soil microbial and faunal communities to
improve sensitivity and, importantly, to improve detection
of unforeseen effects. Such monitoring requires a combi-
nation of measures, each responding to different types of
change, for example monitoring the biomass, activity and
diversity of the microbial and faunal communities, to
improve the detection of any impacts.
Population size and activities
There is no simple correlation between plant productivity
and the size of the soil microbial biomass. Fluctuations in
the microbial biomass are not a sensitive indicator of any
GM crop effects, although a consistent long-term decline
might indicate significant changes. Predators can reduce
the numbers of soil bacteria [30], thereby making it
difficult to use bacterial numbers or biomass to assess the
impact of GM plants directly. Because fungi tend to be
regulated by fungal competition and interactions [4,31],
fungal biomass might not reflect changes in plant inputs
to soil. Similarly, the varied responses of soil fauna
populations to increases in plant productivity [4,32–36]
limit their use as indictors of the effects of GM plants.
Thus, population size and activity of soil bacteria, fungi
and fauna are complex and, consequently, insensitive as
ecosystem measures. Despite this, their use remains
popular because they provide basic ecological data and
any changes, compared with controls, can indicate
interesting or important effects.
12 Opinion TRENDS in Biotechnology
Box 2. Diversity and soil function
Diversity refers to both the species present and the community
structure. It is an important issue when addressing the impact of
plants on a soil ecosystem but distinctions must be made between
an impact on soil diversity (the range of organisms the soil
contains) and one on soil function (what the soil does): a
reduction in soil diversity might not necessarily cause a decrease
in soil function.
Studies investigating the links between diversity and function have
reported both a strong role for diversity in soil function [41], and also
that function can be maintained with just a relatively small number of
species present [42]. The general consensus among researchers is that
there is ‘no predictable relationship between diversity and function’
and that species richness is not an important factor in the overall
function of soils [43,44].
Although biodiversity is not viewed as an important factor, it is
understood that a minimum number of species is required to ensure
that the functioning of soil system is maintained. Compared with soils
Biodiversity
The role of biodiversity in the function of the soil
ecosystem is controversial and there is little support for
a direct diversity–function relationship (Box 2). Despite
this, assays of biodiversity are commonly used to detect
impacts on soil systems. This is, in part, because these
assays have proven to be sensitive to perturbation. They
provide a useful indicator of changes arising from a
variety of causes. This is important because our inability
to define and monitor the whole system requires the use of
indicators that are sensitive to a wide range of pertur-
bations. One problem is that the methods might be too
sensitive and every plant cultivar could cause different
responses in soil biodiversity making the overall
significance of any changes, for example when comparing
GM plants with parental lines, difficult to assess.
Diversity of soil microbes
The microbial community is often chosen for assay
because of the central importance of the bacterial and
fungal populations to nutrient cycling and soil quality.
This attribute has frequently made soil microbes the
dominant focus of monitoring and risk assessment.
Because soil microbes are the primary consumers of
plant exudates and plant material, their diversity has
been proven to be sensitive to change. Suitable methods
Box 3. Outstanding questions
Many monitored changes in community diversity are structural
(relative proportions) and are evaluated using richness measures or
indices. These measures provide a convenient way of comparing soils
but there is a paucity of data relating their magnitude to
ecosystem measures.
† What is the relationship between biodiversity and soil resistance
and resilience?
† What is the significance of diversity for suppressive soils?
Two research areas in soil ecology – soil food web interactions and soil
spatial heterogeneity – can be identified as having the most potential
to improve both our understanding of soil ecology and our
assessment and monitoring of GM plants.
† Food-web structure is considered a key determinant of ecosystem
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Vol.24 No.1 January 2006
in stable conditions, more disturbed soils require a larger number of
species to maintain soil function. The lack of a clear relationship
between soil diversity and soil function is a consequence, in part, of
the level of functional redundancy present within the soil ecosystem.
Significant functional redundancy exists within all soil ecosystems,
both as a whole and within specific groups of organisms, including
bacteria [45], nematodes [46], b-proteobacterial ammonia-oxidising
bacteria [47], and in the microarthropod communities [48]. Where a
single soil-function is conducted by, for example, three different soil
species, two of those species could be lost from soil without a
concomitant loss of the soil function but only if they are all active
between a similar range of environmental variables. Soil functions
carried out by a large number of species are, therefore, more resilient
to changes in conditions than those conducted by only one or two
species. Hence, the resilience of the soil ecosystem is another soil
characteristic linked to diversity, and is viewed by some researchers as
a valuable characteristic that should be conserved.
are available for large-scale sampling and assay of
microbial taxonomic and functional diversity.
The analysis of bacterial and fungal community
structures, using DNA technologies that target ribosomal
RNA (rRNA) sequences, can profile whole communities
and detect microbes absent from the limited populations
isolated using traditional culturing methods [22,24].
Microbial functional diversity is assayed using a variety
of methods, notably community level physiological
profiling (CLPP). Here, soil samples are assayed for the
use of several carbon sources by the bacteria or fungi.
Transgenic and non-transgenic alfalfa have shown a clear
separation of the untransformed and transgenic rhizo-
spheres [37] with the rhizosphere bacteria of the
transgenic alfalfa using significantly more substrates
and having a greater functional diversity than bacteria
from the untransformed control. CLPP is a popular
technique in soil ecology and it frequently provides
information that can be related to changes in the soil
habitat, although it is unclear whether this information
can indicate changes in soil function. Both traditional and
molecular techniques can detect many of the pertur-
bations in the rhizosphere soil community caused by GM
plants; however, there is no direct relationship between
these perturbations and the detection of negative effects.
Furthermore, the issue of an improved definition of harm
in soils needs to be addressed in the near future.
productivity. There is evidence that soil ecosystem function is
resolved primarily by dominant species and the complex interactions
of soil food-webs [49,50]. Improved analytical methods, including the
use of stable isotopes, show promise for the analysis of food web
interactions in soil [51].
† Improved understanding of spatial soil ecology is needed to
provide insights into the regulation of soil-biodiversity, soil-coex-
istence and the effects of soil communities on plant growth and plant
diversity [52].
† Research is needed to address issues of the use of soil-quality
measures in GM risk assessment [53], to investigate the relationship
between soil quality and ecosystem functions and integrate soil-
quality indicators with soil biological and physical indicators.
 Opinion TRENDS in Biotechnology
Beyond soil ecology
To qualify the effects associated with GM plants in assays
of community structure, or of keystone indicators, they
must be related to functional changes in soil systems, but
there is insufficient knowledge in most cases. To overcome
this, many studies compare the scale of direct and residual
effects of any GM plant with the variation associated with
normal changes, such as crop type and season. [22] (Box
1). Farmers and growers continually monitor their soil in
terms of nutritional status and pH, structure (i.e. does it
become waterlogged or compacted), and function (do crop
residues fail to decompose, are there problems with pests
and pathogens). These practical observations are related
to wider issues of soil quality and provide a set of workable
indicators related to essential services.
Slowly accumulating effects, effects that become
apparent when land-use conditions change, and effects
detected only at commercial scales make it important that
long-term monitoring is undertaken and data collected,
both of which can improve the science of risk assessment.
Long-term studies and post-commercialization monitoring
might not, however, be best served by using the standard
approach of comparison with non-transgenic controls but
will instead require a different choice of keystone
indicators and soil parameters. A more useful approach
is to monitor the quality of the soil, which will assess the
provision of ecosystem services and refocus attention on
agricultural practice in general.
Concluding remarks
Although it is currently not possible to make exhaustive
assays of soil diversity and relate these directly to soil
health, substantial components of the soil community can be
monitored for perturbations. New methods in soil science
will provide substantially more detailed data on community
structure and function and support the design of better risk
assessments (Box 3). A combined approach, informed by
both soil ecology and soil-quality perspectives, can provide a
regulatory framework that detects important changes and
provides a framework for the efficient use of soil resources,
but is not overly restrictive.
The GM controversy seems likely to continue to
rekindle questions and research into the impact of
agriculture and other human activities on soil ecology –
a serious but neglected topic, albeit of fundamental
importance to life on, and in, Earth.
Acknowledgements
A.K.L. was supported by the Department for Environment, Food and
Rural Affairs (DEFRA) and the Natural Environment Research Council
(NERC). M.J.B. and S.L.T. were supported by NERC. C.C. was supported
by DEFRA. Rothamsted Research. P.R.H. receives grant-aided support
from the Biotechnology and Biological Sciences Research Council
(BBSRC) of the UK.
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Endeavour
the quarterly magazine for the history
and philosophy of science

You can access Endeavour online via

ScienceDirect, where you’ll find a
collection of beautifully illustrated
articles on the history of science, book
reviews and editorial comment.

featuring

Selling the silver: country house libraries and the history of science by Roger Gaskell and Patricia Fara
Carl Schmidt – a chemical tourist in Victorian Britain by R. Stefan Ross
The rise, fall and resurrection of group selection by M.E. Borello
Mary Anning: the fossilist as exegete by T.W. Goodhue
Caroline Herschel: ‘the unquiet heart’ by M. Hoskin
Science in the 19th-century zoo by Oliver Hochadel
The melancholy of anatomy by P. Fara
and coming soon
Etienne Geoffroy St-Hillaire, Napoleon’s Egyptian campaign and a theory of everything by P. Humphries
Losing it in New Guinea: The voyage of HMS Rattlesnake by J. Goodman
The accidental conservationist by M.A. Andrei
Powering the porter brewery by J. Sumner
Female scientists in films by B.A. Jones
and much, much more . . .
Locate Endeavour on ScienceDirect (http://www.sciencedirect.com)

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