Enzymology and Ecology of the Nitrogen Cycle
Enzymology under global change: organic
nitrogen turnover in alpine and sub-Arctic soils
James T. Weedon*1 , Rien Aerts*, George A. Kowalchuk*† and Peter M. van Bodegom*
*Department of Systems Ecology, Institute of Ecological Science, VU University Amsterdam, De Boelelaan 1085, 1081 HV Amsterdam, The Netherlands, and
†Department of Microbial Ecology, Netherlands Institute of Ecology, Boterhoeksestraat 48, 6666 GA Heteren, The Netherlands
Abstract
Understanding global change impacts on the globally important carbon storage in alpine, Arctic and sub-Arctic
soils requires knowledge of the mechanisms underlying the balance between plant primary productivity
and decomposition. Given that nitrogen availability limits both processes, understanding the response
of the soil nitrogen cycle to shifts in temperature and other global change factors is crucial for predicting
the fate of cold biome carbon stores. Measurements of soil enzyme activities at different positions of the
nitrogen cycling network are an important tool for this purpose. We review a selection of studies that
provide data on potential enzyme activities across natural, seasonal and experimental gradients in cold
biomes. Responses of enzyme activities to increased nitrogen availability and temperature are diverse
and seasonal dynamics are often larger than differences due to experimental treatments, suggesting that
enzyme expression is regulated by a combination of interacting factors reflecting both nutrient supply and
demand. The extrapolation from potential enzyme activities to prediction of elemental nitrogen fluxes under
field conditions remains challenging. Progress in molecular ‘-omics’ approaches may eventually facilitate
deeper understanding of the links between soil microbial community structure and biogeochemical fluxes. In
the meantime, accounting for effects of the soil spatial structure and in situ variations in pH and temperature,
better mapping of the network of enzymatic processes and the identification of rate-limiting steps under
different conditions should advance our ability to predict nitrogen fluxes.
Global change and the soil nitrogen cycle
It is predicted that global warming trends will continue to
be most severe in Arctic, sub-Arctic and alpine environments
[1]. Moreover, biological processes in these systems are often
temperature limited [2,3]. As soils are often close to the
freezing point, non-linear effects of temperature around
frequent freeze−thaw events can have large impacts [4,5].
Arctic and sub-Arctic biomes constitute a globally significant
carbon sink (∼30 % of the global soil carbon pool) in the form
of soil organic matter stored in peatlands and permafrost [6].
If changes to climate affect local biological processes in these
ecosystems and consequently modify elemental fluxes, there
is a potential for feedbacks to global biogeochemical cycles
[7−9]. Understanding the response of these important carbon
sinks to higher temperatures is therefore crucial to predicting
future biogeochemical cycles and climate.
Carbon storage in soil organic matter depends on the
balance between carbon assimilation via primary production,
and mineralization via decomposition. Although higher
temperatures are expected to increase the rates of both of
these processes in the short term, their long-term responses
will depend on interactions with other potentially limiting
factors such as soil moisture [3,9], oxygen availability [10]
and nutrient availability [11] and may also be affected by nonKey words: freeze−thaw cycle, nitrogen flux, organic nitrogen turnover, peatland, Q10 , soil
extracellular enzyme.
1
To whom correspondence should be addressed (email [email protected]).
Biochem. Soc. Trans. (2011) 39, 309–314; doi:10.1042/BST0390309
linear irreversible processes such as permafrost melting [12].
Nitrogen availability in particular is expected to constrain the
response of primary production and decomposition to global
change, given that both are potentially limited by nitrogen
availability, particularly in colder biomes [3,13]. Due to the
minimal inputs via atmospheric deposition and biological
fixation, increased nitrogen supply has been found to relate
closely to in situ decomposition rates of soil organic matter
in pristine Arctic and sub-Arctic habitats [3,14]. Although
plant species-specific factors can complicate models of litter
decomposition [15], the close links between carbon and
nitrogen cycling underscore the importance of understanding
the soil nitrogen cycle when attempting to predict the fate of
cold-biome carbon stores in a warming climate.
Plants and microbes, constituting the main sinks for soil
nitrogen, are both capable of assimilating low-molecularmass forms of organic nitrogen such as amino acids [16,17],
effectively short-circuiting the nitrogen cycle and leading to
minimal levels of complete mineralization of organic nitrogen
to ammonia [18]. For this reason, overall nitrogen cycling is
regulated by the process of depolymerization, defined as the
enzymatic release of labile low-molecular-mass nitrogenous
molecules (amino acids, amino sugars and peptides) from the
complex forms that make up soil organic matter [19,20].
In contrast to constructed nitrogen budgets, direct
measurements of the enzymatic processes that contribute
to the total flux provide information about the drivers
and modifiers of individual steps in a complex network of
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Figure 1 Simplified schematic diagram of the soil organic nitrogen cycle, including examples of assays available for the quantification
of potential rates of each process
interacting fluxes, information that is useful for gaining a
mechanistic and ultimately predictive understanding of soil
nitrogen cycling under global change. A range of standardized
soil enzyme assays for a large number of reaction substrates
has been developed [21,22], which allow the comparison
of soil enzymatic potentials across ecosystems [23]. In
particular, the use of substrates containing a fluorigenic
component have increased sensitivity and lowered detection
limits relative to colorimetry-based methods [24]. Figure 1
shows a selection of enzyme assays available for measuring
different steps in the pathway from polymeric soil organic
nitrogen to mineralization. Unfortunately, soil enzyme assays
typically involve incubations of homogenized soil slurries at
standardized temperature and buffer conditions with nonlimiting amounts of substrate for a specified period of time. As
a consequence, their relevance for estimating actual nitrogen
fluxes may at times be questionable. In the present paper,
we review briefly the experiments that have investigated the
effects of global change drivers on soil enzyme activities,
with a focus on alpine and (sub-)Arctic environments, so that
we can subsequently discuss the challenges for translating
enzyme assay data into predictions of soil nitrogen fluxes.
Global change effects on soil enzyme
activities in temperature-limited systems
Understanding the direct effects of higher temperatures on
soil nitrogen cycling requires knowledge of the kinetics
and stoichiometry of decomposition processes [25,26] and
their responses to temperature. One aspect of this response
is the temperature sensitivity of the reaction rate usually
expressed as the change in activity per 10◦ C increase in
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Authors Journal compilation temperature, Q10 . Although interpretation of Q10 values can
be influenced by the temperature range of their application
[27,28], they have proven useful in the study of the sensitivity
of biological processes to changes in temperature. A study
conducted in the Alaskan tundra suggests that carbon-cycle
enzymes are more temperature-sensitive than nitrogencycle enzymes [29]. This result is supported by experiments
with alpine soils that additionally found that enzymes related
to hydrolysing labile compounds are more temperaturesensitive than those associated with the breakdown of more
stable soil organic matter [30]. Given that many nitrogencontaining compounds are protected by carbon polymers,
the responses of soil enzymes associated with both cycles
need to be understood: if the differential response of carbon
and nitrogen cycles to warming is consistent and long
lasting, then non-linear shifts in the stoichiometric balance
of soil organic matter cycling, most likely towards enhanced
nitrogen limitation, would be expected.
In addition to directly affecting enzyme activities, global
warming may also increase nitrogen availability through
other pathways. Studies that manipulate temperature in
the field have the advantage of combining direct temperature effects on enzyme activities with a range of possible
indirect effects mediated by, e.g., longer-term changes in
vegetation composition and changes in nutrient supply via
litter and grazing. These indirect effects may be even stronger
than direct effects of global change drivers (temperature, CO2
and precipitation) [31], and it is therefore surprising that there
is a relative lack of enzyme data from this type of study from
Arctic and alpine studies, despite the large number of climate
manipulation experiments currently underway [32]. Several
studies have, however, investigated the effects of increased
mineral nitrogen inputs into soils on the dynamics of enzyme
Enzymology and Ecology of the Nitrogen Cycle
activities. Originally established to predict ecosystem impacts
of anthropogenic increases in nitrogen deposition [33], these
studies also provide important insights into the mechanisms
of enzymatic regulation of soil nitrogen cycling. In this
respect, it is still unclear whether measured soil enzyme activities reflect a response to nutrient deficiency or to availability,
in other words, whether enzyme production by the microbial
biomass is regulated by nutrient demand or supply. There
is evidence available to support both possibilities [22,34],
which might be due to the complex enzyme regulation of the
soil nitrogen cycle. Chronic nitrogen fertilization of alpine
tundra soils reduced leucine-aminopeptidase activities and
increased urease activities while not affecting other nitrogencycle enzymes [35], whereas in an ombrotrophic bog in
Scotland, nitrogen addition reduced potential activities of
chitinase and cellulase, and altered the patterns of carbon
substrate utilization [36]. Similar complex responses have
been found in other systems. Most strikingly, Enowashu
et al. [37] found that the activity of different types of
peptidases in German spruce forest soils showed opposite
responses to changes in mineral nitrogen input. Such
disparate responses among enzymes with presumably similar
functional roles point to a complex (and hard to predict)
regulation of enzyme expression.
Further evidence on the effects of both temperature and
nitrogen availability on enzyme activities is given by studies
that measured seasonal dynamics, as seasonality can be
understood as a driver that integrates simultaneous variance in
temperature, moisture, plant and microbial nutrient demand
and transport of nutrients into and out of the soil system.
Studies that measured seasonal variation in potential enzyme
activities have typically found large intra-annual differences
[29,34,36], up to 10-fold [36], with such differences often
being larger than those detected in response to experimental
manipulation of single factors (see above). In alpine, Arctic
and sub-Arctic environments, the highest enzyme activities
seem to coincide with the period of microbial and nutrient
turnover around the spring thaw, during which frequent
soil freeze−thaw cycles cause rapid drastic shifts in the soil
physicochemical conditions [4], with consequences for the
soil microbial community structure and associated functions
[38].
This implies that global change effects on enzyme activities
are: (i) likely to involve interactive (i.e. non-additive) effects
of changes to temperature and nutrient supply, and (ii) be
mediated through changes to nutrient demand and supply
both within the soil organic matter decomposing community,
as well as in the associated vegetation [39].
Extrapolating enzyme measurements to
flux predictions: the missing link
Soil enzyme activity measurements are useful only insofar
as they allow us to predict elemental fluxes and, e.g.,
their responses to global change. Despite this, studies that
explicitly link enzyme measurements to measurements of
fluxes in the same experimental units are rare (e.g. [40,41])
and, to our knowledge, non-existent in (sub-)Arctic and
alpine environments. To illustrate what this link may look
like, we present a synthesis of data from alpine [30] and
Arctic tundra [34,42] in Figure 2. The measured activities
of some enzymes were correlated with flux rates, i.e. nitrogen
mineralization with xylosidase (r2 = 0.58, P < 0.05) and βglucosidase (r2 = 0.52, P < 0.05), and carbon mineralization
with protease activity (r2 = 0.94, P < 0.05). However, not
all enzyme activities seem to translate into elemental fluxes,
as with nitrogen mineralization against protease activity
(Figure 2B) and carbon mineralization against β-glucosidase
and xylosidase in Figure 2(A) (i.e. none of these correlations
were significant). This latter result is all the more surprising
as β-glucosidase activity is traditionally considered to be a
reliable proxy of soil microbial activity [43].
Connecting potential enzyme activities, as reflected by
enzyme assays, to actual enzyme activities in situ and,
more crucially, realized elemental fluxes requires clarifying
the influence of some important complicating factors. For
instance, soil processes are spatially structured at multiple
scales [18]. Diffusion of enzymes and substrates within
and between microhabitats [44] could potentially limit soil
enzyme activities in ways that are not detectable by traditional
soil enzyme assays that incorporate a homogenization step,
particularly given the potentially important role of enzymes
stabilized on soil particles [21]. Furthermore, enzymatic
processes are sensitive to solution pH and temperature
conditions. Standardized assay conditions, although useful
for facilitating cross-system comparisons [23], may lead
to under- or over-estimates of in situ potential rates [24].
Moreover, given that temperature sensitivities have been
shown to vary considerably between enzymes and across
seasons [29,30], extrapolations from assay data collected at
a single temperature are potentially unreliable.
Probably the most serious factors complicating translation
of potential enzyme activities to fluxes are the two
(interrelated) problems of (i) the unclear role of substrate
availability, and (ii) the complex multi-step pathways of
enzymatic intermediate reactions, which ultimately lead to
elemental fluxes. As mentioned above, it remains uncertain
whether enzyme production is induced by nutrient deficiency
(demand driven) or by availability (supply driven) [22,34].
This makes using potential activities as a guide for flux
predictions problematic, as realized fluxes are a function of
the actual substrate supply rate, as well as potential activity.
If enzymes are produced in response to nutrient limitation,
then assays that measure potential activities will have an
inverse relationship with real fluxes in the field. Indeed,
experimental approaches give support for an ‘economic’ or
demand-driven model of enzyme regulation [45], and this
has also been incorporated into a modelling framework [46].
Further investigation into this problem across a range of
ecosystems will be an important step towards allowing us
to make well-informed links between enzyme measurements
and field-level nitrogen availability, particularly given the
interaction between the latter and other global change factors.
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Figure 2 Relationships between measured enzyme activities and carbon and nitrogen mineralization rates as reported in (A) Koch et al.
[30] and (B) Weintraub and Schimel [34,42]
Closed symbols and continuous lines, carbon mineralization (C min); open symbols and broken lines, nitrogen mineralization
(N min). For (A), each data point represents a season × soil combination (summer wet fen soils excluded from linear
trend line). Triangles and grey lines, xylosidase (Xylo) activity; squares and black lines, β-glucosidase (Beta-gluc) activity.
For (B), each point represents four separate soil types; protease activity was calculated as cumulative potential activity by
interpolation. See the text for further statistical information.
Similarly, the complex multi-step pathway from polymeric
organic nitrogen to mineral nitrogen (Figure 1) implies that
measurements of the activity of a simple step in a complex
network will not be sufficient for predicting total flux rates.
Indeed, multiple soil nitrogen-cycle networks are possible,
each with different dominant nitrogen forms and different
critical rate-limiting steps [18,19]. Given the multiple, indirect
effects of global change drivers, it is conceivable that they
can alter the relative importance of different nitrogen-cycle
pathways, and therefore the critical rate-limiting enzymatic
processes determining elemental flux rates. All this argues for
simultaneous measurements of enzymes in different positions
of the nitrogen-cycling network [37] (Figure 1) and further
research into how global change alters the different pathways
in such soil nitrogen flux networks [19].
Ultimately, the effects of global change on the soil
nitrogen economy will always be filtered through the soil
microbial community, the proximate driver of soil enzyme
pool sizes and elemental fluxes [21,22]. Whether this filtering
is best examined at the level of the composition of the
soil microbial community (as detectable via metagenomics
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their enzyme production (proteomics [49]) or through
soil enzyme assays remains an open question, although
a combination of approaches will probably be the most
fruitful approach. Molecular tools to predict enzyme
activities have therefore been strongly advocated [21,22].
Indeed, in the long run, molecular methods are likely
to offer considerable explanatory power in understanding
soil community function once it has been established to
what extent microbial communities are functionally and
kinetically redundant [50], and once bioinformatic tools are
sufficiently advanced to reliably predict functional characteristics of communities from environmental sequence data
[22,47].
Given the current state-of-the-art, we propose that a
greater focus on the direct effects of environmental conditions
and resource supply rates on elemental fluxes, and the enzyme
processes that underlie them, will help to provide important
information in the short term that should lead to considerable
advances in the understanding of the global change effects on
soil biogeochemical cycling.
Enzymology and Ecology of the Nitrogen Cycle
Funding
This study was supported financially by the Netherlands Organisation
for Scientific Research (NWO) [NWO-ALW grant number 816.01.012
(to R.A. and G.A.K.)].
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Received 15 September 2010
doi:10.1042/BST0390309