trends in plant science
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Are microorganisms more
effective than plants at
competing for nitrogen?
Angela Hodge, David Robinson and Alastair Fitter
Plant scientists have long debated whether plants or microorganisms are the
superior competitor for nitrogen in terrestrial ecosystems. Microorganisms have
traditionally been viewed as the victors but recent evidence that plants can take
up organic nitrogen compounds intact and can successfully acquire N from
organic patches in soil raises the question anew. We argue that the key
determinants of ‘success’ in nitrogen competition are spatial differences in
nitrogen availability and in root and microbial distributions, together with
temporal differences in microbial and root turnover. Consequently, it is not
possible to discuss plant–microorganism competition without taking into
account this spatiotemporal context.
N
itrogen (N) is the primary limiting
nutrient in most terrestrial ecosystems1. Competition between plants
and microorganisms for this nutrient is
believed to be intense2,3. Traditionally, it was
assumed that plants can access only the inorganic forms of N made available via the mineralization of soil organic matter. It was also
assumed that microorganisms are the superior
competitors for this N (Ref. 4) because of their
major role in the mineralization process, large
surface-area:volume ratios and rapid growth
rates compared with plant roots. Some mineral N will also be released by eukaryotic
organisms and by the action of exoenzymatic
activities but the rhizosphere (the volume of
soil surrounding and influenced by the plant
root) is densely populated with microorganisms and so there will be competition for
this mineral N also.
However, some plants can also take up
organic N compounds directly via their roots5,6
or when in association with some types of
mycorrhizal fungi7–9, therefore bypassing the
dependency on microbial mineralization. This
can only be a partial bypass because microorganisms can also use organic N sources and
therefore will compete with plants for these,
too. Consequently, the widespread importance
of this mechanism to the N supply of plants
remains debatable.
Inorganic nitrogen
Production and pools
Inorganic N is made available by the mineralization of organic N to ammonium (NH41) and
subsequent nitrification (mainly autotrophic)
to nitrate (NO32) (Fig. 1). Additionally, NO32
can be produced from organic N by certain heterotrophic bacteria and fungi, mainly in acid
soils, thereby avoiding the ammonification
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July 2000, Vol. 5, No. 7
step10 (Fig. 1). Microbial mineralization and
nitrification are generally thought to be the
rate-limiting steps in the N cycle and it has
thus been assumed that microorganisms are
able to acquire inorganic N before plants.
It is difficult to assess direct competition
between plants and microorganisms for soil N
because (1) there are multiple loops and pathways through which N cycles at variable rates
and in varying amounts between different
pools (Fig. 1), and (2) some plants and some
fungi in any ecosystem will be in a mycorrhizal symbiosis, providing an additional pathway for N movement.
The use of 15N-pool-dilution techniques has
helped to resolve many uncertainties about
N-pool fluxes. For example, 15N-labelling of
the NH41 and NO32 pools of a grassland soil
revealed that, even though the NH41 pool was
always moderately large, it was extremely
dynamic and had a turnover time of ~1 day.
The NO32 ‘pool’ was even more dynamic,
being consumed as rapidly as it was produced2. Similarly, the mean residence time
of small amounts of NO32 in undisturbed
coniferous forests was only ~15 h (Ref. 11),
indicating intense microbial activity. On a
longer timescale, pulses of NH41 in an acid
woodland soil were short-lived persisting for
a few weeks12.
Influence of the C:N ratios of soil
organic matter
Most soil microorganisms are usually limited
by the supply of easily decomposed carbon (C)
in soil. However, most soil N transformations
are carried out by microbial heterotrophs that
depend on the supply of available organic C.
The chemoautotrophic nitrifiers Nitrosomonas
and Nitrobacter are notable exceptions, using
inorganic C as their C source and obtaining
their energy from the oxidation of inorganic
N compounds. Therefore the N and C cycles
cannot be considered in isolation. This point
is highlighted particularly by the influence of
C:N ratios on the balance between N mineralization and immobilization.
The rate of mineralization of organic N
depends first on the C:N ratio of the substrate
being decomposed and second on the decomposer community’s need for N relative to its
need for C. Fungi generally assimilate substrate more efficiently than bacteria, which
have a smaller C:N ratio and consequently a
larger N demand per unit C (Ref. 10; Fig. 2).
If the C:N ratio of the substrate being decomposed exceeds that of the decomposers (after
taking account of respired CO2) then those
microorganisms will not release inorganic N
during decomposition and might supplement
their N requirements from the soil’s inorganic
N pool, reducing the availability of that pool
to plants by the act of immobilization.
Conversely, if the C:N ratio of the substrate
being decomposed is less than that of the
decomposers (after taking account of respired
CO2) then those microorganisms will liberate
excess N, often as NH41, adding to the soil’s
inorganic N by the process of mineralization.
Thus, at C:N ratios less than about 12:5, neither fungi nor bacteria will require additional
N, and net N release (mineralization) will
occur. At C:N ratios greater than about 30:1,
both fungi and bacteria will require additional
N and net immobilization will occur (Fig. 2).
Under natural conditions, the situation is
more complex. The heterogeneous nature of
soil organic matter and the presence of a range
of decomposers in soil ensure that N mineralization and immobilization occur simultaneously; net mineralization will occur typically
at soil-organic-matter C:N ratios below ~25:1
(Ref. 13). Net N immobilization after the addition of organic residues to soil can reduce plant
growth, an effect that can be reversed by
adding available N (Ref. 14). The rate of plant
N capture generally increases as the C:N ratio
of the substrate decreases (Table 1)
Plant–microorganism competition
and spatiotemporal variations
There is abundant evidence that plants use N
that is left over from microbial metabolism, at
least in non-agricultural soils. For example,
24 h after the injection of 15NH41 and 15NO32
into a grassland soil, most of the 15N label was
recovered in the microbial biomass2 (Table 1).
Because the labelled N was added as an external source rather than produced via microbial
processes, true competition between microorganisms and plants for the available N
source would have been expected, rather than
roots simply accessing N that had been discarded
by the microorganisms. This study2 shows that,
on a short timescale, soil microorganisms do
1360 - 1385/00/$ – see front matter © 2000 Elsevier Science Ltd. All rights reserved. PII: S1360-1385(00)01656-3
trends in plant science
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NH3 volatilization
Denitrification
losses
Litter inputs
Root
turnover and
exudation
Root or
mycorrhizal
uptake
Soil
Plant or mycorrhizal
uptake
Heterotrophic
nitrification
Mineralization
+
NH4
Biomass N
Organic N
Immobilization
Autotrophic
nitrification
-
NO3
Leaching
losses
Trends in Plant Science
Fig. 1. The main pools (boxes) and fluxes between pools (arrows) of nitrogen (N) in terrestrial ecosystems, excluding both animals and inputs
via nitrogen fixation. The solid arrows indicate a high flux; the broken lines for litter inputs and mineralization indicate the fluxes that are most
likely to be limiting steps.
compete better than plants for the added N,
particularly for NH41: its uptake by microorganisms was five times faster than that by
plants. The NO32 uptake rate by microorganisms was double that of plants.
By marked contrast, after 12 d, plants in an
alpine ecosystem acquired 93–96% of an
(15NH4)2SO4 solution applied, compared with
4–7% recovered in the microbial biomass15.
However, in this study15, the N supplied was
sprayed directly onto the plots and it is possible that roots absorbed the labelled surface
solution before it could penetrate into the soil;
however, direct adsorption by the foliage was
ruled out15. Although microorganisms are better short-term competitors for N, it has been
suggested that plants will win out in the longer
term2. Microbial cells turn over more rapidly
than plant roots do, therefore releasing N back
into the soil, whereas plants are able to retain
captured N to a greater extent.
There is much evidence to support this view.
For example, 49 d after the addition of discrete
patches of organic material of low C:N ratio
(i.e. ,4) to Lolium perenne swards, about half
of the added N (45–54%) was found in the
plants16, compared with ,10% in the microbial biomass (Table 1). Furthermore, the
organic material added was labelled with both
15
N and 13C, and, although 15N enrichments
were detected in the plant tissues, plant 13C was
never enriched. This implies that microbial
decomposition of these patches occurred first
and that the plants took up N in inorganic form
rather than as intact organic compounds.
However, plants captured only 11% of the N
from a patch with a higher C:N ratio (i.e. 21:1),
a comparable amount to the microbial biomass
(Table 1), and most of this patch remained
undecomposed. These quantities of N in the
microbial biomass are similar to the 6–15%
reported from long-term field studies (1.9–27.0
months) after the addition of either urea or
NH41 (reviewed in Ref. 17).
After an initially rapid N capture and the
assimilation of inorganic N by soil microorganisms, as short-term studies indicate
(Table 1), the microbial biomass appears to
reach a steady state. One possible explanation
is that the microbial biomass again becomes
limited by C rather than by N. As the microbial biomass turns over, there is insufficient
C to maintain its fast initial growth rates and
therefore N is released into the soil, there
becoming available to plants. The relative
turnover times of roots and microorganisms
are therefore likely to be a key determinant of
competitive success: it is the rapid turnover of
microbial biomass that gives the roots an
opportunity to capture released N through
microbial cell lysis. However, there can be
large differences between microbial populations in turnover time: mycelial structures
(fungi and actinomycetes) can recycle N internally and their N turnover therefore can be
much slower than for bacteria. Similarly,
perennial plants also recycle N internally by
remobilizing N from senescing tissues, thus
reducing N losses to the external environment
relative to those from annuals.
Freeze–thaw and drying–rewetting events
disrupt microbial cells18,19, thus reducing
microbial populations. Such events might provide the plant with a competitive opportunity
because roots both compete with a decreased
microbial population and have additional N
available via microbial-cell lysis. Most of this
N will be organic, especially, in prokaryotes,
whose production of proline and glutamate
generally increases with osmotic stress10.
Plants such as the arctic sedge (Kobresia
myosuroides), which is common in systems
prone to freeze–thaw and dry–rewet events,
can take up amino acids directly6.
The pronounced heterogeneity of soils profoundly affects all plant–microorganism interactions. The organic matter from which NH41
and NO32 are produced is patchily distributed
throughout the soil in both space and time, and
its decomposition creates nutrient-rich patches.
July 2000, Vol. 5, No. 7
305
trends in plant science
Perspectives
100 Units
of carbon
(a)
short term, the relative length density of the
root systems and hence root production are
crucial when they compete with the roots of
other plants. This is particularly true in complex organic patches, in which microbial
decomposition continually produces inorganic
N throughout the patch; consequently, the spatial placement of roots becomes much more
important. The greater the root-length density
maintained by a plant within the patch, the
more likely roots are to be present when and
where mineralized N is released. Thus, localized root proliferation has two ecologically
relevant functions: it enhances N capture for
the plant that has produced the most roots; and
it reduces N capture by competitors.
100 Units
of carbon
Fungi
(C:N ratio 15:1)
Bacteria
(C:N ratio 5:1)
50 C units respired
60 C units respired
100 C - 50 C = 50 C
100 C - 60 C = 40 C
C:N ratio = 15:1
C:N ratio = 5:1
N requirement equals:
50 C = 3.3
15
Substrate C:N ratio:
100 C = 30.3 C:N
3.3
N requirement equals:
40 C = 8
5
Substrate C:N ratio:
100 C = 12.5 C:N
8
Organic nitrogen
(b)
Decreasing N availability for plant uptake
N released by
both fungi and
bacteria
10
N released by fungi but
sequestered by bacteria
12.5
N sequestered from soil
by both fungi and
bacteria
Substrate C:N ratio
20
30.3
40
Substrate C:N ratio
e.g. urea, amino acids
e.g. cereal straw
Trends in Plant Science
Fig. 2. (a) Influence of the type of decomposer (bacterial or fungal) on the minimum (or ‘critical’)
carbon:nitrogen (C:N) ratio for the decomposition of organic material at which net N mineralization is zero. Fungi have a greater substrate-assimilation efficiency than bacteria. Figure redrawn
from Ref. 10. (b) Consequences of the relationships in (a) on plant nitrogen availability.
Many plant species proliferate their roots
within such patches (Fig. 3). However, this
proliferation can take a long time to establish
(e.g. ~35 d for a range of grass species20), during which the microbial biomass might have
turned over many times and decomposition
thus be complete. Nevertheless, plants can
acquire a large fraction of N from an organic
patch relatively quickly, simply because the
slower turnover of roots and the potential for
internal recycling makes the plant N pool an
effectively self-absorbing sink.
The important point here is that not only do
plants capture N from the turnover of older soil
organic matter but they can also capture substantial amounts from the turnover of morerecent additions, in spite of the microorganisms
apparently getting the N first. Why then do
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July 2000, Vol. 5, No. 7
plants proliferate roots in N-rich patches at all?
Inorganic N (particularly NO32, which is more
mobile in soil than NH41) will diffuse readily
through the soil to the root surface and the speed
at which new roots can be produced will never
match that of the turnover rates of microbial
cells. Indeed, in plant monoculture, the extent
of root proliferation is unrelated to plant N capture from decomposing complex physical and
chemical organic patches (e.g. L. perenne shoot
material) in the soil20.
However, more recent evidence21 has
shown that, when plants are grown in competition with other plant species, there is a direct
relationship between root proliferation and N
capture. Thus, although roots might not be
produced quickly enough to compete directly
with microorganisms for inorganic N in the
In some ecosystems (e.g. tundra, boreal and
temperate forests, and heathlands), the rate of N
mineralization is insufficient to meet the known
rate of N uptake by the vegetation. This might
reflect a simple underestimate of N mineralization or the existence of N-acquisition mechanisms that allow direct uptake by plants of
unmineralized (i.e. organic) N (Refs 5,6; Fig. 1).
Much emphasis has been placed on the ability
of roots to take up organic N compounds
directly, so reducing plants’ dependency on
mineralization. However, many studies of this
phenomenon have been at unrealistic temperatures, with unlikely nutrient enrichments and in
the absence of microorganisms. The amino acid
glycine, commonly used as a putative organic N
source for plants5–7, is a relatively poor substrate
for microbial growth22. This, in itself, does not
argue against the uptake of organic N by roots
(indeed, it might be that a capacity to take up
this amino acid has evolved in roots for this very
reason) but it does question whether true
microorganism–plant competition is occurring.
There is also evidence that many plants might
in practice be unable to take up organic N
compounds in competition with microorganisms16,20,21, as shown by the lack of detectable 13C enrichments in the plant tissues
when 15N–13C-labelled substrates have been
applied. However, it is possible that small
amounts of 13C might have been absorbed and
then lost via catabolism over the experimental
period in these studies. Furthermore, if only
small amounts of 13C were present then they
might have been below detectable limits. Alternatively, amino acid influx into roots has been
proposed as a mechanism by which roots could
control the availability of nutrient supplies and
hence regulate the size and activity of their associated rhizosphere microbial population23. The
true ecological significance of the phenomenon
of organic N uptake currently remains obscure.
Role of mycorrhiza
Most plants are colonized by mycorrhizal
fungi under natural conditions. Although the
trends in plant science
Perspectives
Table 1. Plant and microbial partitioning of added 15N substrates
Material added
Substrate
C:N ratio
Plant species
Duration
% N captured
Plants
Ref.
Microbial biomass
Lolium perenne shoots
Lolium perenne shoots
Lolium perenne shoots
Lolium perenne shoots
Lolium perenne shoots
31.0:1.0
31.0:1.0
31.0:1.0
31.0:1.0
31.0:1.0
Festuca arundinacea
Phleum pratense
Poa pratensis
Dactylis glomerata
Lolium perenne
39 d
39 d
39 d
39 d
39 d
3.6
3.5
3.2
4.8
5.0
ND
ND
ND
ND
ND
20
Lolium perenne shoots
Algal amino acids
Algal cells
L-lysine
Urea
21.0:1.0
3.1:1.0
3.2:1.0
2.4:1.0
0.4:1.0
Lolium perenne sward
Lolium perenne sward
Lolium perenne sward
Lolium perenne sward
Lolium perenne sward
49 d
49 d
49 d
49 d
49 d
11.0
54.0
45.0
46.0
53.0
12a
9a
9a
9a
7a
16
NA
NA
CA, USA grassland (field study)
CA, USA grassland (field study)
1d
1d
9.0–11.0
20.0–26.0
46–61
38–50
2
NA
Alpine moist meadow,
CO, USA (field study)
12 d
93.0–96.0
4–7
15
NH41
NO32
15
15
(15NH4)2SO4
a
N in microbial biomass not measured directly but indirectly using protozoan biomass values
Abbreviations: ND, not determined; NA 5 not applicable.
main benefit that plants derive from mycorrhiza
is usually considered to be enhanced phosphorus uptake, other benefits include pathogen and
drought resistance. Certain mycorrhizal associations, notably the ecto- and ericoid mycorrhiza, definitely do improve plant N nutrition
by accessing organic N that is inaccessible to
roots alone8,9,24. These fungi might capture N
from organic sources by producing proteolytic
and chitinolytic enzymes that degrade large
organic N polymers or by the direct uptake of
simple organic molecules such as amino
acids8,9.
The arbuscular mycorrhiza association is the
most common type, and the role of these fungi
in accessing organic N for plants is the most
controversial. Direct uptake of glycine by ecto,
ericoid and arbuscular mycorrhizal plants has
been shown in the field, although most (.60%)
of the amino acid remained in the soil7. There
is also some evidence from laboratory experiments that roots colonized by arbuscular
mycorrhizal fungi showed enhanced uptake of
intact serine compared with uncolonized
controls25. However, other microorganisms
were excluded in this study, preventing any
direct competition for the substrate between
plants and microorganisms or between microorganisms; in addition, serine, like glycine, is a
poor substrate for microbial growth compared
with many other amino acids22.
When a more-complex substrate (L. perenne
shoots) was added to soil containing either an
indigenous arbuscular mycorrhiza inoculum
or an indigenous and an additional inoculum
(Glomus mosseae), there was no direct uptake
of intact organic N (Ref. 26). Nitrogen capture
from the mineralized organic material was,
however, related to the proportion of vesicles
(fungal storage organs) in the roots.
Arbuscular mycorrhizal fungi might enhance
plant N capture from inorganic sources27, presumably by being more effective than roots as
competitors with soil microorganisms for
mineralized N. Evidence that arbuscular
mycorrhizal fungi contribute to the direct
uptake of intact N from organic sources that
are also potential substrates for other microorganisms remains equivocal. Perhaps this is
not surprising: both fungal and plant partners
in the arbuscular mycorrhizal association have
generally coevolved in soils deficient in available phosphorus but not N, unlike the partners
in the ectomycorrhizal and the ericoid associations28. Therefore, for most plant species that
form arbuscular mycorrhizal associations, it is
unlikely that fungal N capture is an important
factor in root–microorganism competition.
Concluding remarks
Superficially it might seem that plants are the
inferior competitors for N, particularly inorganic N and especially in the short term.
However, data from longer-term studies that
have followed N capture from discrete patches
imply that plants do eventually capture most
Fig. 3. Root growth into an N-rich
organic patch composed of lyophilized
algal cells viewed using a minirhizotron
tube and a borescope camera. Each image
is ~7 mm in diameter. (a) 21 days after the
patch has been added, a single root is seen
growing into the nitrogen-rich zone. (b)
The same image four days later shows
increased root production and root-hair
development in the nitrogen-rich zone.
July 2000, Vol. 5, No. 7
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Perspectives
of this N. When N is in the form of discrete
patches of low C:N ratio, these longer periods
might be only a few days16, apparently because
of the longer lifespan of root systems compared with most soil microorganisms. For most
plant species, both the direct uptake of simple
organic compounds and arbuscular mycorrhizal assistance appear to be unimportant in N
capture. The principal weapon that plants possess is their ability to sequester N for much
longer periods than most microorganisms.
Root-proliferation responses are more important to understanding plant–plant than plant–
microorganism competitive interactions.
We still know little about the precise factors
regulating the expansion, activity and diversity
of the microbial biomass in the rhizosphere,
which are responsible for the localized transformations of complex N substrates into plantavailable forms. In addition, we do not yet have
sufficient information about the contributions
of specific components of the microbial biomass to particular N transformations. Recent
advances have revealed important new information about gene expression in certain Ntransforming microorganisms29, in signalling
between plants and rhizosphere microorganisms30, and between external NO32 and
roots31. These suggest that tools are now available to approach the ecologically important
question of plant–microorganism competition
for N at molecular scales.
Acknowledgements
We thank three anonymous reviewers for their
perceptive comments. A.H. is funded by a
fellowship awarded by the Biotechnology
and Biological Sciences Research Council
(BBSRC), UK.
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Angela Hodge* and Alastair Fitter are at the
Dept of Biology, PO Box 373, University of
York, York, UK YO10 5YW; David Robinson
is at the Dept of Plant and Soil Science,
University of Aberdeen, Aberdeen, UK
AB24 3UU.
*Author for correspondence
(tel 144 1904 432878; fax 144 1904 432860;
e-mail [email protected]).
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