Soil Biology & Biochemistry 105 (2017) 45e48

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Soil Biology & Biochemistry

journal homepage: www.elsevier.com/locate/soilbio

Points of View

Dinner in the dark: Illuminating drivers of soil organic matter

decomposition
Annemieke van der Wal a, *, Wietse de Boer a, b
a
Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, 6708 PB, The Netherlands
b
Department of Soil Quality, Wageningen University, Wageningen, 6708 PB, The Netherlands

a r t i c l e i n f o a b s t r a c t

Article history: Soil organic matter (SOM) dynamics plays a crucial role in soil ecosystem functioning and global
Received 21 April 2016 warming. SOM is normally degraded slowly, but its decomposition rate can change substantially after
Received in revised form addition of easily decomposable C sources. This process, known as “the priming effect”, has already been
2 November 2016
described in 1926 but is still poorly understood. Priming can be positive (extra decomposition of SOM) or
Accepted 4 November 2016
Available online 12 November 2016
negative (reduction of SOM decomposition), depending on the amount and physicochemical charac-
teristics of added compounds, the composition of SOM and the metabolic abilities of responding mi-
croorganisms. We propose that the understanding of priming effects can be greatly advanced by
Keywords:
Priming effects
investigating the level of convergence between the chemical characteristics of the added compound and
Functional potential of microbial SOM fractions, and the functional potential of microbial communities. This can be achieved by combining
communities two different disciplines-microbial ecology and biogeochemistry. Such knowledge will deliver infor-
Decomposition mation under which conditions sequestration of soil carbon can be expected and provide possibilities to
Physicochemical properties steer soil carbon dynamics in sustainable agricultural systems.
Soil organic matter © 2016 Elsevier Ltd. All rights reserved.
Home-field advantage

1. Introduction matter to protective mineral surfaces and the intrinsic biochemical

In terrestrial ecosystems, large quantities of carbon (1500 Gt in
the first meter) are held in soil organic matter (SOM) (Jobba
gy and
Jackson, 2000). Its turnover plays a crucial role in soil ecosystem
functioning and global warming. SOM is critical to the stabilization
of soil structure, retention of plant nutrients and maintenance of
water-holding capacity. Furthermore, the decomposition of SOM
releases mineral nutrients thereby making them available for plant
growth (Johnston et al., 2009). SOM formation results from mi-
crobial and geochemical processes that convert carbon (C) mainly
comprised of plant litter and microbial biomass into stabilized,
potentially long-lived materials (Ko € gel-Knabner, 2002). Whereas
SOM is often thought to be mainly composed of degraded plant
litter, microbial exudates and -necromass are themselves also
important components of SOM (Clemmensen et al., 2013; Liang and
Balser, 2011). Long turnover times of organic compounds are not
only explained by anaerobic conditions such as in peats, but also by
incorporation into aggregates after the attachment of organic
* Corresponding author.
E-mail addresses: a.vanderwal@nioo.knaw.nl (A. van der Wal), w.deboer@nioo.
knaw.nl (W. de Boer).
properties of SOM (Lehmann and Kleber, 2015; Schmidt et al.,
2011). This physical and chemical stabilization of SOM hinders
microbial decomposition via restricted mobility of microbes,
diffusion of water, enzymes and oxygen (von Lützow et al., 2007). In
addition, it requires a broad range of microbial enzymes to degrade
the insoluble macromolecules that comprise SOM (Wallenstein and
Weintraub, 2008). SOM stabilization can thus provide a possibility
for long-term storage of carbon. However, intensive soil manage-
ment practices can disrupt soil aggregation and soil organisms that
contribute to aggregation, thereby enhancing release of carbon to
the atmosphere (Powlson et al., 2011). Recently, the French gov-
ernment proposed ahead of COP21 (Conference of Parties on
climate change) to sequester annually an additional 0.4% of the
current soil carbon stock to combat global warming, and sustain-
able agricultural practices are seen as valuable options to reach this
target.
One of the crucial processes in ecosystem carbon balances is the
“priming effect” on SOM decomposition. This effect is defined as
the increase in decomposition of soil carbon stocks as a result of
addition of easily degradable compounds (Bingeman et al., 1953).
However, negative priming, e.g. a decrease in SOM decomposition,
can also occur. Priming is not yet considered in current carbon-

http://dx.doi.org/10.1016/j.soilbio.2016.11.006
0038-0717/© 2016 Elsevier Ltd. All rights reserved.
46 A. van der Wal, W. de Boer / Soil Biology & Biochemistry 105 (2017) 45e48
cycle-climate models (Perveen et al., 2014) as the underlying
mechanisms are not well understood (Heimann and Reichstein,
2008; Zhu et al., 2014). Yet, priming effects can have dramatic im-
pacts on ecosystem carbon budgets. For instance, exudation of
carbon compounds by living roots can suppress 50% or stimulate up
to 400% of SOM decomposition (Zhu et al., 2014).
2. Current view
To date, the most widely held explanation for positive priming
effects is the theory of co-metabolism, i.e. the addition of easily
degradable organic compounds serves as an energy source for
microorganisms to synthesize extracellular enzymes capable of
degrading SOM. Direct and indirect co-metabolism have been
suggested to be responsible for the priming effect. It has been
shown that the addition of labile C first stimulates the growth of
pioneering micro-organisms (Kuzyakov, 2010). After a slight lag
phase, these opportunistic responders are followed by bacteria and
fungi that utilize more recalcitrant C (e.g. the necromass of the
pioneers) and increase their enzyme activity leading to a co-
metabolic decomposition of SOM (Fontaine et al., 2003;
Blagodatskaya et al., 2014). Direct co-metabolism has also been
shown; addition of ryegrass induced a priming effect whereas
glucose did not (Wu et al., 1993). It was suggested that the enzymes
produced by the microorganisms degrading the ryegrass, were also
capable of decomposing fractions of SOM. However, supply of car-
bon compounds to soil resulted in a huge variation of priming ef-
fects, ranging from large e and small positive, to no or even
negative priming effects (Hamer and Marschner, 2002; Kuzyakov
et al., 2007; Blagodatskaya et al., 2007; Rousk et al., 2015). Nitro-
gen (N) limitation has also been proposed as an additional factor
regulating priming effects by stimulating microbes that mine for N
in SOM (Fontaine et al., 2011). Negative priming effects occur less
often than positive priming effects (Kuzyakov et al., 2000), and are
often explained by the result of “preferential substrate utilization”.
After addition of easily degradable compounds, soil microorgan-
isms prefer to utilize the added substrate to SOM (Fontaine et al.,
2004a). This leads to a temporary decrease of SOM decomposi-
tion. In spite of all publications on priming effects, a clear mecha-
nism remains elusive. We propose to combine two important
disciplines -microbial ecology and biogeochemistry-to unravel the
mechanisms driving priming effects with the purpose to provide
possibilities to steer soil carbon dynamics.
3. Perspectives and implications
Major observations that may lie at the basis of understanding
priming effects are:
1. The supply of different carbon compounds to soils induces
priming effects that vary greatly in direction and magnitude
(Dalenberg and Jager, 1989; Wu et al., 1993; Shen and Bartha,
1997).
2. The extent and direction of priming is influenced by the amount
of added carbon compounds (Blagodatskaya and Kuzyakov,
2008; Guenet et al., 2010).
3. Similar carbon compounds can trigger different priming effects
in different soils (Hamer and Marschner, 2005).
Thus, priming effects depend on the amount and physico-
chemical characteristics of the added substrate and the properties
of the receiving soil. The latter could involve both the composition
of SOM and that of the responding micro-organisms. Fontaine et al.
(2003) suggested that the degree of physicochemical similarity
between the added carbon substrate and SOM is an important
factor explaining the extent of the priming effect. If added com-
pounds trigger the production of extracellular enzymes by mi-
crobes, then these enzymes will also decompose fractions of SOM
resembling the added compounds. For example, it has been shown
that cellulose addition can stimulate two types of microbes: soil C
decomposing microbes that also use cellulose, and specialized
microbes that exclusively decompose cellulose (Fontaine et al.,
2004b). However, the link between physicochemical properties of
SOM and added substrates, and the extent of the priming effect has
not yet been investigated.
Elaborating on the suggestion by Fontaine et al. (2003), we
propose that the understanding of priming effects can be greatly
advanced by investigating the level of convergence between the
components involved, namely the physicochemical characteristics
of the 1) added compound and 2) SOM fractions, and 3) the func-
tional potential of microbial communities (Fig. 1). The functional
potential of microbial communities can be grouped based on spe-
cific characteristics, such as extracellular enzyme profiles or ability
to decompose hydrophobic compounds (Allison, 2012; Krasowska
and Sigler, 2014). We hypothesize that a high degree of physico-
chemical similarity between added compounds and SOM fractions
will result in a positive priming effect provided that indigenous soil
microbes adapted to decompose SOM are well represented (Fig. 1A,
hypothesis A). Adding a substrate that is chemically similar to SOM
fractions, but with immediate access for microorganisms since it is
not occluded in SOM aggregates (Lützow et al., 2006), will provide
an extra source of energy to spark decomposition of SOM. Alter-
natively, a high degree of physicochemical dissimilarity between
added compounds and SOM fractions will stimulate groups of mi-
crobes that decompose the added substrate without affecting SOM
(“preferential substrate utilization” theory). This results in no or
even negative priming effects (Fig. 1B, hypothesis B). An alternative
explanation for this scenario is that microbes decomposing the
added compounds have antagonistic effects against the SOM-
degrading microbes resulting in decreased SOM decomposition.
For instance, bacteria that grow on easily degradable compounds
do often have antifungal activities to prevent fungi from using these
substrates, including production of antibiotics, lytic enzymes and
volatiles (De Boer et al., 2015). In addition, it has been shown that
opportunistic fungi can delay the growth of specialized lignin-
degrading fungi (Greaves, 1971; Van der Wal et al., 2007). A third
possibility is that during negative priming, microorganisms grow
on the added C (preferential substrate utilization), and their exu-
dates increase SOM protection via greater reactivity towards min-
eral surfaces and incorporation into aggregates (Lehmann and
Kleber, 2015). No or negative priming effects can also be expected
when substrates are added that resemble fractions of the SOM but
without the presence of microbial communities that are able to
degrade these substrates and/or SOM fractions. This can for
instance be the case in soils that have been contaminated with
organic pollutants (Fig. 1C, hypothesis C). Biostimulation of mi-
crobes by addition of compounds that chemically resemble the
pollutant may only lead to increased pollutant degradation after
the microbial communities have adapted to decompose the organic
pollutants in the soil (Kowalchuk, 2012).
We expect that hypotheses A and B will be especially applicable
to soils where microbial communities are strongly adapted to
breakdown of plant-specific compounds that are preserved in SOM
fractions, such as cutin, suberin, lignin-derived molecules and
tannins (Spielvogel et al., 2010; Kononova, 1966). It has been shown
that saprophytic fungal communities are, to a certain degree,
specialized on different litter - and wood types (Osono, 2007;Van
der Wal et al., 2013). Since plant litter provides the primary
source of SOM formation, it is likely that SOM-degrading microbes
are, to some extent, also specialized on their substrate. This idea
 A. van der Wal, W. de Boer / Soil Biology & Biochemistry 105 (2017) 45e48
Fig. 1. The level of convergence between the physicochemical characteristics of the 1) added compound, 2) soil organic matter fractions, and 3) the functional potential of microbial
communities will determine the extent and direction of the priming effect (PE). A: A high degree of physicochemical similarity between the added compound (1) and SOM fractions
(2) on the one hand, and the metabolic abilities of soil microbial communities (3) on the other hand, will result in a positive priming effect (PE). B: A high degree of physicochemical
dissimilarity between the added compound (1) and SOM fractions (2), will mainly stimulate groups of microbes that decompose the added substrate without affecting SOM,
resulting in no or even negative priming effects. C: A high degree of physicochemical similarity between the added compound (1) and that of SOM fractions (2) will result in no or
negative priming effects when microbial communities are not specialized to break down those substrates and/or SOM fractions. This could occur in recently contaminated soils
when a compound is added that chemically resembles the pollutant.
relates to the phenomenon of “home-field advantage” (HFA), which
refers to the fact that decomposition of litter is faster than expected
in the vicinity of the plant from which it originates than at some
distance away from that plant (Austin et al., 2014). According to the
HFA theory, microbial communities are functionally different and
specialized to break down litter from plants with which they are
associated. The more chemically similar the added compound
(added litter in case of HFA) is to the chemical composition of SOM
(litter originated from their “own” vegetation in case of HFA), the
higher the priming effect should be.
It will be challenging to determine the strength of the link be-
tween physicochemical characteristics of SOM and SOM-degrading
potential of soil microbial communities. Extracellular enzymes
produced by microbial communities are the major drivers of
decomposition processes (Wallenstein and Weintraub, 2008).
Therefore, we suggest determining enzyme activity profiles as be-
ing the most important functional potential of microbial commu-
nities for priming effects of SOM decomposition (Sinsabaugh et al.,
2005; Baldrian et al., 2011). Plant litter and microbial biomass are
the main inputs for SOM formation. Their major organic com-
pounds include cellulose, hemicellulose, lignin, proteins, poly-
saccharides, tannins, lipids, cutin, suberin, chitin and acids (Ko€ gel-
Knabner, 2002). To identify these C compounds in SOM, detailed
physicochemical analyses will be needed (Yassir and Buurman,
2012). The spectrum of enzyme activities and the composition of
SOM will provide data to detect the strength of the relationship
between functional potential of microbial communities and SOM
compounds. Soils that show a strong relationship between these
components are expected to exhibit higher priming effects on SOM
decomposition (Fig. 1A).
In conclusion, unraveling the mechanism of the priming effects
requires a thorough understanding of the interactions between the
physicochemical properties of SOM fractions, the added com-
pounds and the metabolic capacities of microbial communities. An
interdisciplinary approach integrating microbial ecology and
biogeochemistry is needed to improve understanding of the
observed variation in priming effects in different soil ecosystems.
The obtained knowledge will be essential to the development of
soil management practices that lead to increased carbon seques-
tration in agricultural soils.
Acknowledgements
We thank George Kowalchuk and Petr Baldrian for reading
previous versions of this manuscript and for providing helpful
comments. Funding was provided by the Netherlands Organisation
47
for Scientific Research in the form of a personal Veni grant to A. van
der Wal. This is publication number 6193 of the NIOO-KNAW
Netherlands Institute of Ecology.
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