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Appl Microbiol Biotechnol (2016) 100:3433– Appl Microbiol Biotechnol (2016) 100:3433–
344910.1007/s00253-016-7378-y
DOI 3449

MINI-REVIEW

Application of compost for effective bioremediation of organic

contaminants and pollutants in soil
1 1
Matthias Kästner & Anja Miltner

Received: 28 October 2015 / Revised: 1 February 2016 / Accepted: 3 February 2016 / Published online: 27 February 2016
# Springer-Verlag Berlin Heidelberg 2016
1
Abstract Soils contaminated with hazardous chemicals Department of Environmental Biotechnology, Helmholtz Centre
worldwide are awaiting remediation activities; for
Environmental Research – UFZ, Permoserstraße 15,
bioremediation is often considered as a cost-effective 04318 Leipzig, Germany
remediation approach. Potential bioapproaches are
biostimulation, e.g. by addition of nutrients, fertiliser and
organic substrates, and bioaugmenta- tion by addition of
compound-degrading microbes or of or- ganic amendments
containing active microorganisms, e.g. ac- tivated sludge or
compost. In most contaminated soils, the abundance of the
intrinsic metabolic potential is too low to be improved by
biostimulation alone, since the physical and chemical
conditions in these soils are not conducive to bio-
degradation. In the last few decades, compost or
farmyard manure addition as well as composting with
various organic supplements have been found to be very
efficient for soil bioremediation. In the present
minireview, we provide an overview of the composting
and compost addition ap- proaches as ‘stimulants’ of
natural attenuation. Laboratory degradation experiments
are often biased either by not con- sidering the abiotic
factors or by focusing solely on the elimination of the
chemicals without taking the biotic factors and processes
into account. Therefore, we first systemise the concepts of
composting and compost addition, then summa- rise the
relevant physical, chemical and biotic factors and
mechanisms for improved contaminant degradation
triggered by compost addition. These factors and
mechanisms are of particular interest, since they are more
relevant and easier to

* Matthias Kästner
matthias.kaestner@ufz.d
e
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Appl Microbiol Biotechnol (2016) 100:3433–
determine than the composition of the degrading
3449
communi- ty, which is also addressed in this review. Due
to the mostly empirical knowledge and the
nonstandardised biowaste or compost materials, the field
use of these approaches is high- ly challenging, but also
promising. Based on the huge met- abolic diversity of
microorganisms developing during the composting
processes, a highly complex metabolic diversity is
established as a ‘metabolic memory’ within developing
and mature compost materials. Compost addition can
thus be considered as a ‘super-bioaugmentation’ with a
complex natural mixture of degrading microorganisms,
combined with a ‘biostimulation’ by nutrient containing
readily to hardly degradable organic substrates. It also
improves the abiotic soil conditions, thus enhancing
microbial activity in general. Finally, this minireview also
aims at guiding poten- tial users towards full exploitation
of the potentials of this approach.
Appl Microbiol Biotechnol (2016)
. Composting 100:3433–
. Biodegradation
Keywords Soil amendment
3449
. Organic contaminants . Microbial communities .
Bioremediation processes . Fate of pollutants . Residual
concentrations . Metabolic cooperation . Functional
redundancy
Introduction
Starting from its beginning in 1962 with Rachel Carson’s
book ‘Silent Spring’, public and political awareness about
chemical contaminants in the environment has been
increas- ing and has resulted in improved legislation
concerning the approval and use of chemicals in Europe (EC
2006). There are many different ways by which pollutants
are introduced into the environment. Many chemicals are
entering the environ- ment via low-concentrated diffuse
sources, either by intended
use (e.g. pesticides, personal care products, etc.) or by ‘compost ap- plication’: sometimes the term composting is
unin- tended side effects of application processes, for considered to
example the exhaust emissions of combustion processes
from power plants, motor vehicles or comparable primary
sources. On the other hand, many pollutants enter the
environment via point sources after accidental events such
as oil spills, tank damages, ship collisions, leakages from
pipelines or oil dril- ling platforms, or simply by dumping
of waste materials, e.g. tar oils containing polycyclic
aromatic hydrocarbons (PAH) at historical manufactured
gas plant sites (Luthy et al. 1994; Wiesmann 1994) or
incompetent use and dumping in recent times. In addition,
military use of explosives has also led to widespread
contaminations, e.g. at World War II production,
ammunition storage and warfare sites (Certini et al. 2013).
Therefore, millions of sites contaminated with organic
pol- lutants exist worldwide and the numbers of
contaminated sites are strongly increasing, particularly in the
emerging nations as shown by the recent catastrophe in
Tianjin, China. With this explosion at a storage site for
hazardous substances in the harbour of Tianjin, several
hundred tons of cyanide were re- leased into the
environment (Xu and Webb 2015). As infor- mation on the
nature and the amount of hazardous substances stored in
the area is missing, it is unknown whether additional
pollution of soil and water in the region occurred. Many of
the contaminated sites need immediate active clean-up
measures in order to eliminate acute toxic impacts, but the
majority, in particular old contaminated sites with lower
impact or low pressure on reuse, are waiting for
remediation. For example, the costs for the assessment of
contaminated sites and the remediation measures in
Germany alone are estimated to be
500 million euros per year (UBA 2015). Thus, there is an
urgent need for cheap and effective remediation measures.
Bioremediation is considered as a potentially cost-
effective remediation approach (Kästner 2000; Michels et
al. 2000). The applicable processes are biostimulation, e.g.
by addition of nutrients and fertiliser and organic
substrates, and bioaug- mentation by addition of compound-
degrading microbes or of amendments containing active
microorganisms, such as acti- vated sludge or compost. In
particular, compost or farmyard manure addition is
considered to be very efficient for soil bioremediation
(Antizar-Ladislao et al. 2004; Chen et al.
2015; Loick et al. 2012; Semple et al.
2001).
Compost applications for biodegradation and
contaminant removal have been applied since the early
1980s, e.g. for remediation of chlorophenol-contaminated
soils (Häggblom and Valo 1985; Valo and Salkinoja-
Salonen 1986) and mainly used for the elimination of
mineral oils and PAH within tar oil or creosote
contaminations (for review, see Antizar-Ladislao et al.
2004). A comprehensive overview of such applications,
including pilot- and full-scale applications, is given in the
review of Loick et al. (2012). However, there is
widespread confusion regarding the terms ‘composting’ and
describe the incubation of contaminated soil with any
(waste-)biomaterials including bacteria (otherwise known
as
‘bioaugmentation’); however, other authors have used this
term for the amendment of contaminated soil with mature
composts, which clearly results in different processes.
Furthermore, the term is also used for the simple addition
of biogenic bulking agents (such as bark chips, straw or
garden clippings) or smart mixtures of them in order to
provide suf- ficient aeration and to adjust matrix conditions
such as water content, nutrients and pH. In general, two
major concepts are applied (Antizar-Ladislao et al. 2004;
Chen et al. 2015; Loick et al. 2012; Semple et al. 2001):
the addition of raw organic waste materials to
contaminated soils, called `composting´ in this review, and
the addition of mature composts after having performed the
full composting process, here called ‘compost addition’.
Higher degradation after amendment with mature composts
was observed, at least for PAH, by several authors (Kästner
and Mahro 1996; Loick et al. 2012); this may be due to the
lower oxygen demand and the supply of primary sub-
strates that are relatively low-concentrated and not easily
degradable.
Whether a bioremediation measure, e.g. composting or
compost addition, is regarded successful or not, often
depends on the defined target values; due to very low
targets in several European countries, it is often difficult to
meet the threshold values for unrestricted reuse of the soil
(Antizar-Ladislao et al.
2004). The residual contamination levels are mostly
accept- able for reuse of the soil material in landscape
building and management but not for settling, gardening,
and farming pur- poses. There is also a severe disadvantage
associated with the addition of organic materials to
contaminated soils: due to the high load of organic
materials, they can no longer be used as building ground. In
addition, mixing large amounts of organic additives to
contaminated soil requires excavation of the soil and ex
situ treatment resulting in higher effort and costs in
comparison to in situ treatments. This is certainly justified
for contaminated soils in urban areas, where the economic
pressure for reuse of the sites is high enough to make even
cost-intensive remediation measures economically feasible.
It is thus sometimes more reasonable to treat the
contaminated soil by soil-washing methods (Trellu et al.
2016) in order to separate the less contaminated mineral
fraction from the more contaminated organic materials and
to treat the latter fraction separately, e.g. by compost
treatments thereby substantially reducing the volume of
material to be treated.
Many examples of the successful application of
compost for enhanced bioremediation exist in the scientific
literature (for review, see Antizar-Ladislao et al. 2004; Loick
et al. 2012; Semple et al. 2001), mostly for the
bioremediation of hydro- carbons and PAH. However, there
are also many reports about the failure or low efficiency of
biostimulation measures at real contaminated sites.
Unfortunately, most of these reports are only published in
the ‘grey’ literature about remediation
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Appl Microbiol Biotechnol (2016) 100:3433– 343
Appl Microbiol Biotechnol (2016) 100:3433–
534
3449 3449 534
actions; nevertheless, some of them are also mentioned in organic waste in 2016 to 35 % of the 1995 level (EC
peer-reviewed literature (García-Delgado et al. 2015; 1999). This
Loick et al. 2012). The details of the biodegradation
processes, and particularly the reasons for the failures with
low elimination of the contaminants, mostly still remain
obscure.
The general mechanisms of the biodegradation
stimulation after the addition of compost or raw
biomaterials are only poorly understood, despite the fact
that a huge body of litera- ture on the composting process
in general is available (see below). The reviews on
compost application (Antizar- Ladislao et al. 2004; Chen
et al. 2015; Loick et al. 2012; Semple et al. 2001) and the
majority of the primary publica- tions in the field of
compost addition deal with the fate and turnover of
specific contaminants at contaminated sites, but barely with
the degradation mechanisms triggered by compost addition.
More generic considerations about the relevant processes
are provided by Chen et al. (2015) and Semple et al.
(2001), and general considerations according to all biore-
mediation processes by Megharaj et al. (2011). Several re-
views are available describing the principles of microbial
deg- radation of PAH with focus on bioremediation
(Bamforth and Singleton 2005; Johnsen et al. 2005; Juhasz
and Naidu 2000; Kanaly and Harayama 2010; Lu et al.
2011; Peng et al. 2008). Some of the primary publications
actually deal with fate modelling (Adam et al. 2015; Geng
et al. 2015; Rein et al.
2015; Zhang et al. 2014), but the residual contamination
values after bioremediation can still not adequately be
predict- ed and thus need to be evaluated in pilot studies
anyway.
The aim of the present review is to summarise the
scientific literature on bioremediation approaches using
composting or compost application as well as mechanistic
studies on organic pollutant biodegradation in order to
understand the reasons for success or failure of the
remediation approaches. Therefore, the focus of the review
is on the following: (i) presenting an overview about the
current knowledge on composting pro- cesses and on
compost-aided organic pollutant degradation in soils; (ii)
summarising it to understand effects of compost application
on the fate of various contaminants, including bio-
degradation; and (iii) relate the current expertise to the
reme- diation processes triggered by compost addition, in
particular to microbial degradation processes and the
related microbial communities. This knowledge will enable
further optimisation of the approach for a predictable
application of this biotech- nology, even if a considerable
number of questions still remain to be answered before this
biotechnology can be applied with truly predictable results.

Background: the processes of

composting

The EU legislation requires that the organic matter content

of landfills be decreased by limiting the percentage of
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Appl Microbiol Biotechnol (2016) 100:3433–
results in pressure to collect domestic organic waste
634
3449
separately and reuse it. One option for reuse of organic
wastes is composting. Composting is a managed
biooxidative process which converts solid heterogeneous
organic substrates into relatively stable organic-rich
material which can be used as soil amendment (Li et al.
2013; Loick et al. 2012). Potential input materials are not
only organic domestic or garden wastes but also industrial
organic wastes, farmyard manure, spent mushroom
substrates, and sewage sludge. The composting process
relies on the activity of a succession of complex mi-
crobial communities which colonise and emerge in the
organic material. The process runs dominantly under
aerobic condi- tions, comprises a wide variety of
metabolic processes, and yields ‘humus-like’ material
called mature compost as the final product.
The metabolic activity of the microorganisms during
composting generates heat, and a mass loss of about 50 %
is mainly released as CO2 and water. Depending on the
intensity of metabolism and heat production, three
phases of composting can be discerned: (1) the initial
mesophilic phase when the microbial community builds up
and adapts to the conditions, with moderate temperatures
up to 45 °C; (2) the thermophilic phase when metabolism is
most intense and tem- perature increases to a maximum
which can be as high as
70 °C; and (3) the curing phase when the readily available
organic substrates are exhausted and metabolism thus
slows down until the transformation of organic compounds
has de- creased to a minimum (Neher et al. 2013). The
changes in the Appl substrates available and343
Microbiol Biotechnol (2016) 100:3433–
organic
3449 634in
temperature result in a characteristic s uccession of
microorganisms during composting (Fogarty and
Tuovinen 1991; Steger et al.
2005). In particular, the high temperatures of up to 65–70
°C in the thermophilic phase result in sanitation of the
compost, because many living potential pathogens do not
survive these conditions (Ahmad et al. 2007). However,
residual DNA may still be detectable (De Gannes et al.
2013a). The chemical alteration and metabolic
processes occurring during composting are determining
the chemical composition and certain properties of the
resulting mature material; they de- pend both on the
composition of the organic input materials and on the
process conditions. In particular, sufficient aeration and
optimum moisture are crucial for optimum composting
results (Antizar-Ladislao et al. 2004) and, therefore, the
re- moval of surplus water formed by the metabolic activity
and the supply of sufficient oxygen are highly important.
A wide variety of microorganisms is involved in the
composting processes. More than 150 species and genera
have been found in culture-dependent studies (De Gannes
et al.
2013a; Ryckeboer et al. 2003). A much higher number of
taxa
can be found using culture-independent approaches such
as DNA extraction and sequencing (De Gannes et al. 2013a).
Not surprisingly, the communities derived from culture-
dependent and culture-independent studies can be very
different (Takaku
et al. 2006). As environmental conditions such as the
chemical composition of the organic materials and the
temperature change over time during composting, a
characteristic succes- sion of the microbial community can
be observed. For a set of seven composts from different
substrates, the C/N ratio, inor- ganic nitrogen, and
temperature have been identified as key parameters
controlling the composition and diversity of the microbial
community in the composts (Wang et al. 2015).
The initial phase of composting is particularly dynamic
as it is characterised by rapid changes in pH and
temperature as well as O2 and CO2 partial pressures, which
result in substan- tial shifts of the microbial community,
mainly associated with pH changes, as demonstrated in a
laboratory study with de- fined organic matter input and
under controlled environmental conditions (Schloss et al.
2003). During the initial mesophilic phase, bacterial
numbers increase largely due to the high sup- ply of easily
degradable compounds. In composts from ligno- cellulose
materials (rice straw, coffee hulls, sugar cane ba- gasse),
differences in the microbial community based on 454
sequencing were higher between compost phases than be-
tween starting materials (De Gannes et al. 2013a). In all
phases, Proteobacteria were the largest group detected.
They were more abundant in the mesophilic than in the
mature phase. In particular, the abundance of
Gammaproteobacteria, including Enterbacteriaceae,
was highest during the mesophilic phase and decreased
over time, resulting in a more even distribution between
Alphaproteobacteria- and Gammaproteobacteria in the
mature compost. Firmicutes (mainly Bacilli), in contrast,
were major community compo- nents in the mesophilic and
in particular in the thermophilic phase. Archaea were
almost absent in the starting materials, but their abundance
and diversity increased significantly dur- ing composting.
The mature compost products showed a rel- ative increase
in abundance of Bacteroidetes, Chloroflexi,
Planctomycetes, Bacteria and Archaea, as compared to the
mesophilic phase. Also, within specific microbial taxa, dis-
tinct shifts in community composition can be detected.
This has been also demonstrated for the Actinobacteria
communi- ties (Wang et al. 2014), but similar successions
can certainly be assumed for other taxa. In contrast to the
bacterial commu- nity, the composition of the fungal
community seems to de- pend rather on the starting material
than on the compost phase (De Gannes et al. 2013b),
although more species with a more even distribution was
found in the mature phase than before. The predominant
taxa were Ascomycota, in particular Sardomycetes. In
summary, each composting phase and mix- ture thus has its
characteristic bacterial and archaeal commu- nity, whereas
the fungal community seems to depend more on the
composition of the starting material.
At large scale, composting techniques designed to
acceler- ate and optimise the composting process can be
divided into three general categories: windrow composting,
static piles, and closed vessel approaches. The least
sophisticated
technique is windrow composting. For this, the organic
waste material is arranged in long, narrow piles. The
material is regularly turned in order to provide sufficient
aeration. In stat- ic piles, the material is piled up higher.
This requires enforced aeration by mechanical means. Often,
both oxygen supply and temperature are controlled by
blowers for optimum results. The most sophisticated
systems are the closed vessel systems. They optimise the
composting process by providing aeration, mixing and
temperature control; in addition, these systems avoid the
development of unpleasant odours. Closed systems are also
particularly suitable for composting food residues, which
may cause hygienic problems if composted in open
systems, in spite of the sanitation step mentioned above
(Antizar-Ladislao et al. 2004). The closed systems are,
how- ever, more expensive both in construction and in
maintenance. Therefore, composting in closed vessels is
often used to start composting, whereas the process is later
continued in wind- rows (Antizar-Ladislao et al. 2004).
However, composting does not exclusively involve
micro- bial activities. A number of animals, in particular
earthworms, are also important for the process. An
alternative technique therefore is vermicomposting, which
exploits the joint action of th e ea r th worms an d th e
m ic roorga nisms d uring composting, resulting in
enhanced transformation of the waste material into compost
(Lazcano et al. 2008). In contrast to normal composting
procedures, vermicomposting does not proceed through a
thermophilic phase due to differences in microbial
metabolism, and thus complete hygienisation can- not be
ensured although some pathogens may be suppressed
(Monroy et al. 2008). The end-product, vermicompost,
mainly consists of worm casts. It generally has higher
nutrient content than traditional compost (Dickerson 2001).
Independent of the exact technology for compost
produc- tion, the end-product compost is rich in nutrients
(N, P) and in organic matter, but only contains very limited
amounts of easily available compounds, as these were
utilised by the mi- croorganisms during composting. It
contains dark humic mat- ter and has a high porosity and
water-holding capacity. It also contains a high amount and a
large variety of microorganisms which were enriched
during the process of composting.
Compost application for degradation of specif
ic classes of (organic) contaminants
There are many reports about the addition of composts for
bioremediation of contaminated soils, either in laboratory-
or pilot-scale experiments (for details, see Antizar-Ladislao
et al.
2004; Loick et al. 2012). Often, these studies focus on
opera-
tional considerations related to the treatment of
contaminated sites rather than studying the underlying
processes. Nevertheless, they provide helpful information
on successful bioremediation approaches using compost
and we will use
them to learn about the relevant processes and effects that
are described in the next chapters. In the present chapter,
we will just review the general degradation performance of
classes of environmental chemicals treated by compost
application approaches.
Many applications of compost addition and composting
have been reported for soils contaminated with crude oil
or its refined hydrocarbon products, like, e.g. gasoline,
diesel fuel, heating oil, BTEX, etc. (for review, see Chen
et al.
2015; Megharaj et al. 2011; Semple et al. 2001). These ap-
proaches generally lead to considerable aerobic degradation
of these contaminants (60–90 %) with addition of organic
mate- rials in the range of 5–25 % and even with the
addition of slowly degradable bulking materials like bark
chips. For the degradation of these compounds, oxygen
supply is one of the key factors for optimal performance
of biodegradation. Several laboratory- and pilot-scale
applications addressed par- ticularly the degradation of
crude oils; some of the interesting technical-scale
applications were performed after the Iraqi in- vasion of
Kuwait. At that time, many oil spills occurred; after the
war, even the critical photo-oxidised, weathered and par-
tially combusted oil sludges were successfully subjected to
bioremediation measures using composting with fertiliser
ad- dition and with the addition of mature composts (Al-
Daher et al. 2001). After 8 months, both treatments resulted
in 60–
80 % elimination of the contaminants, including high-
molecular-weight (HMW) PAH. Interestingly, the final
prod- ucts showed good water-holding capacities and low
phytotox- icity indicating humification processes triggered
by the com- post addition.
The largest number of studies specifically addressed
deg- radation of PAH, which are also contained in crude
oils in varying amounts depending on the geographic origin
(for re- view, see Antizar-Ladislao et al. 2004; Loick et
al. 2012). Contaminations by these compounds occur as
major compo- nents of tar oils and creosote for specific use
(e.g. timber wood and railway slipper preservation) or as by-
products of produc- tion at manufactured gas plant sites
(Johnsen et al. 2005; Kästner 2000). Similar to the
hydrocarbon and monoaromatic compounds, the low-
molecular-weight (LMW) compounds in tar oils are well
degraded (up to 90 %) in aerobic processes with compost
addition. However, the HMW PAH in these mixtures were
degraded to a much lower extent due to mass transfer
limitations that are known from pure culture experi- ments
(Juhasz and Naidu 2000; Kanaly and Harayama 2010).
These limitations and the reduced bioavailability resulting
from nonaqueous-phase liquids (NAPLs) and black carbon
materials are of critical concern for PAH degradation in
gen- eral (see physical and chemical processes). Beside
of monooxygenase reactions, limited information about the
in- tracellular HMW PAH metabolism in degrading
microorgan- isms is available; information on the variability
of the contam- inated sites and the contribution of
bacteria and fungi to
contaminant degradation is provided by Juhasz and Naidu
(2000). An overview of pilot-scale applications is provided
by Loick et al. (2012). HMW PAH in tar oil mixtures were
sometimes better degraded after addition of surfactants: in
particular, alcohol ethoxylates and glycoside-based surfac-
tants (Madsen and Kristensen 1997; Megharaj et al. 2011),
or organic solvents such as acetone (Grotenhuis et al.
1999; Rein et al. 2015). Compost addition results in
increased DOC concentration; this DOC may contain
natural surfactants re- ducing mass transfer limitations and
thus an increased biodeg- radation of PAH. Fungi with their
exoenzymes may be better in targeting HMW PAH and can
be stimulated by addition of lignocellulose materials to the
composting process. Therefore, mushroom substrates and
spent mushroom composts (SMCs) resulted in good PAH
degradation, especially for LMW PAH (Covino et al. 2015;
Eggen 1999; Loick et al. 2012; Sasek et al. 2003; Scelza et
al. 2008). However, HMW PAH were found to be better
degraded with SMC from Agaricus bisporus (García-
Delgado et al. 2015). Horse manure was also successfully
used for these applications, ensuring a better sup- ply with
ligninolytic fungi for oil sludges containing PAH
(Kirchmann and Ewnetu 1998).
Much fewer reports are available for the compost-aided
biodegradation of pesticides in general. Several studies
have provided evidence for substantial degradation (>85
%) of chlorophenol biocides and related wood preservation
agents using aerobic composting approaches with bark chips
and also with specific chlorophenol degraders (Häggblom
and Valo
1985; Valo and Salkinoja-Salonen 1986). Other authors
com- pared the addition of bark chips and nutrients with
compost addition and found nearly similar degradation
of the chlorophenols; samples of these pilot-scale
experiments showed mineralisation up to 60 % of
radiolabelled pentachlo- rophenol (Barriuso et al. 1997;
Laine et al. 1997b; Laine and Jörgensen 1997a). Using
farmyard manure addition, also re- ductive dechlorination
of these compounds was observed (Jaspers et al. 2002).
Presumably, this process is located in anaerobic
microenvironments forming after amendment with high
amounts of organic matter. Chlorophenol related bio- cides
are generally highly toxic to microorganisms and the
addition of bark chips may help here to reduce the toxicity
(Valo and Salkinoja-Salonen 1986). In addition,
chlorophenol biocides contain also minor amounts of other
highly chlori- nated compounds like oligomers,
chlorophenoxyphenols, dibenzodioxins and –furans, which
often remain recalcitrant after composting. This indicated
that composting may not be the appropriate approach for
treating other polychlorinated compounds like PCB.
However, only poorly enhanced and highly variable
aero- bic degradation of higher concentrations (160–186
mg/kg soil) of several pesticides in agricultural use was
observed after addition of various organic amendments at
amounts of
0.5 and 5 % to agricultural soil. After 245 days of
incubation,
30 % of atrazine, 33 % of metolachlor and 44 % of
trifluralin was degraded in nonamended soil; atrazine
degradation was enhanced (>50 %) by composting with
0.5 % manure, 5 % peat and 5 % cornstalk in comparison
to nonamended soils. Metolachlor degradation was only
enhanced by 5 % sawdust, manure, corn fermentation
product, and cornstalk amend- ments and not at 0.5 %
amendments. Trifluralin degradation was not enhanced by
any of the amendments (Moorman et al.
2001). There are also results (Alvey and Crowley 1995;
Barriuso et al. 1997) indicating a reduced mineralisation
of triazine pesticides, such as atrazine, after compost
addition with increased microbial formation of so-called
bound or nonextractable residues (NERs). DDT has been
found to be degraded after addition of spent mushroom
composts (Purnomo et al. 2010). Pesticide degradation
obviously de- pends on the soil, the conditions, the
concentrations and the specific properties of the respective
pesticide. In particular, the increased supply of organic
matter after compost amendment has the potential to
increase microbial activity in general due to enhanced
substrate supply, but also to sorb contaminants (in particular
at low concentrations), resulting in lower availabil- ity for
degrading microorganisms.
Some reports are also available about the compost-aided
biodegradation of explosives, e.g. 2,4,6-trinitrotoluene
(TNT) and related compounds (Breitung et al. 1996;
Bruns-Nagel et al. 1998; Weiss et al. 2004b; Williams et
al. 1992). However, no mineralisation of TNT was
observed in these processes, since they were performed
under thermophilic con- ditions with high nutrient loads
resulting in partly anaerobic or even alternating conditions.
These conditions led to sequential reduction of the amino
groups with humification of these com- pounds, which
means the coupling of the metabolites to the organic
matter, finally resulting in complete detoxification. Othe r
aero bic co mpo s ting app r oa ches usin g s pent-
15
mushroom-compost showed a partial mineralisation of N
14
labelled TNT but not of C TNT with full incorporation
of the label into the soil organic matter and the conversion
of a certain amount of the 15N label into microbial biomass
(Weiss et al. 2004b; Weiss et al. 2004a). TNT and other
cyclic nitramine explosives like Royal Demolition
Explosive (RDX) are used as sole sources of nitrogen for
growth of bacteria and fungi; sometimes RDX is being
used concomi- tantly as sole source of carbon and energy
(Crocker et al.
2006; Esteve-Nunez et al. 2001). For these compounds,
the addition of compost triggers biological conversion
which al- lows subsequent chemical bonding of the
metabolites to nat- ural organic matter.
There are also many reports about compost-aided
complex- ation and immobilisation of heavy metals such as
Cd, Cu, Pb, Zn, Cr and Ni; however, elimination is not
possible without transfer to other environmental
compartments (Farrell and Jones 2010; Pérez et al. 2007).
Therefore, the processes of heavy-metal elimination are not
within the focus of the present
work. The effects are mostly based on immobilisation and
coprecipitation with organic compounds (van Herwijnen
et al. 2007); they are much stronger in acidic soils than in
neutral soils (for review, see Chen et al. 2015) and lead to
reduced phytotoxicity. However, Cu mobilisation due to
chelatisation by humic acids and dissolved organic matter
was often observed (van Herwijnen et al. 2007). In
contrast, Mn mobility often remained unchanged
(Alburquerque et al.
2011) and may lead to remaining phytotoxicity. Technical
applications are reviewed by Chen et al. (2015).
Factors and mechanisms of improved
contaminant degradation triggered by compost
addition
It has long been known from gardening that amendment of
compost to soils improves the soil properties in terms of
or- ganic carbon content, nutrient availability, pH, water
retention and soil texture. This improvement is generally
considered for plant growth promotion but in principle is
similarly valid for microbial activity. Since mature
compost consists of about
30–50 % organic C (Alburquerque et al. 2011), compost
ad- dition to soils even in low percentage quantities has a
consid- erable effect on the organic matter content of the
soil (SOM), which is typically in the range of 0.1 to 5 %
depending on land use, vegetation and contamination. The
addition of organic matter leads to a significant shift in
microbial activity based on combined effects of changing
the soil properties as well as substrate and nutrient
availability. However, the compost or- ganic matter is a
matrix which is not really defined in a chem- ical sense,
and consists of humic compounds, derived from plant and
microbial biomass residues in various stages of de- cay.
This matrix seems to be essential for improving the phys-
ical and chemical properties which enable the degradation
of organic contaminants even at low concentrations.
The organic matrix of compost was found to be
essential for enhancing microbial degradation of PAH and
tar oils (Kästner and Mahro 1996): the decrease of soil
PAH concen- trations after compost addition was caused
not only by (i) sorption of the contaminants to the newly
introduced organic matter, but also by (ii) diminishing the
sorption in the parent contaminated soil due to displacement
of the PAH from sorp- tive sites by humic compounds. The
fact that parts of the solid organic matter of the waste
materials or the compost matrix can be biodegraded results
in a considerable mass loss (Zhang et al. 2011) and makes
the PAHs and tar oils (and presumably also other
compounds) more bioavailable for degradation by the
associated microbial communities (Loick et al. 2012).
Another important aspect is the high diversity of the
com- post microorganisms, resulting in a reinforcement of
the over- all microbial activity both by high physiological
redundancy and abundance of metabolic potentials in
various different microorganisms (Abraham et al. 2002;
Freilich et al. 2011).
Metabolic cooperation and cross-feeding may also There is a huge body of literature available on the
enhance the fitness and survival of particular organisms in sorption behaviour and processes of single organic
ecosystems (Pande et al. 2014). Functional redundancy compounds to soil
(Allison and Martiny 2008) in such systems is also of high
ecological im- portance; it was recently shown, for various
sterile artificial soil mixtures supplemented with sterilised
farmyard manure and inoculated by a microorganism extract
of a Cambisol, that the carbon mineralisation kinetics were
similar for all the dif- ferent mineral compositions (Pronk et
al. 2013). However, the similar mineralisation kinetics were
performed by completely different microbial communities
(Ding et al. 2013).
However, compost addition may also be of
disadvantage, since the mineralisation of some compounds,
like, e.g. triazine pesticides, may be suppressed by the
addition of composts (Alvey and Crowley 1995; Barriuso
et al. 1997). In the latter study, which evaluated overall
eight pesticides, the addition of increasing amounts of
mature composts to pesticide-spiked soil resulted in a
decrease of the relatively high mineralisation rates of the
nonamended soil. At the same time, the amounts of polar
nonidentified metabolites and NER increased, which was
considered by the authors to be as a result of microbial
activity. However, the conditions of the soil-compost
experi- ments (very high water contents of 95 % of the
max. water- holding capacity of the mixtures and the
relatively low oxygen content in the incubation vessels
may have impacted these results. In addition, the
degradation of pesticides, in particular for highly oxidised
N-containing triazo-compounds such as triazines, may also
depend on their use as nitrogen sources and thus on the
nitrogen and carbon substrate availability in general
(Abdelhafid et al. 2000). The nitrogen availability is highly
elevated in most of the composts and may repress the
degradation of such compounds; this may be an important
issue if compost application is considered as a remediation
measure.

Physical and chemical

mechanisms

The addition of particulate organic matter from composts

to soils has important effects on relatively low-concentrated
con- taminants in soils. The most important process is
sorption to organic and mineral surfaces, which generally
leads to de- creasing toxicity towards plants and
microbes (Antizar- Ladislao et al. 2004). In the long run,
sorption processes lead to ageing and sequestration of the
compounds in the organic matrix, resulting in
immobilisation and reduced bioavailabili- ty (Hatzinger
1995) or the formation of NERs (for review, see Kästner et
al. 2014). These processes depend on the properties of the
contaminants and the soil matrix; they may be caused by
several mechanisms, such as hydrogen or ion bonding, van
der Waals forces, hydrophobic interactions, entrapment in
or- ganic matter voids, etc. (Pignatello and Xing 1996).
organic matter and humic compounds (Chefetz and Xing
2009; Pignatello and Xing 1996). However, apart from the
work of Luthy and colleagues (Luthy et al. 1994; Luthy
et al. 1993) on PAH in tar oils in the last few decades,
there are much fewer references available on the behaviour
of mix-
ture-associated contaminants. For example, PAH are
never introduced into the environment as pure compounds
but rather as complex mixtures associated to soot particles
from com- bustion or as tar oils from coal gasification
processes (Johnsen et al. 2005; Kästner 2000). Luthy et al.
(1993) impressively showed that the transfer of PAH from
tar oils to the water phase (and thus also to the microbes)
may be highly restricted by solidified interfaces of non-
aqueous-phase-liquids (NAPL) such as tar oils. In
addition, according to Raoult’s law, the
chemical activit y of each single compound within the
NAPL, which may be significantly lower than that of the
pure compounds, is the driving force for the transfer to the
water phase (Eberhardt and Grathwohl 2002; Ghoshal et
al. 1996; Kästner 2000; Lee et al. 1992; Luthy et al. 1994;
Wehrer et al.
2013). Due to the hydrophobic conditions in the NAPL, the
phases also extract the surrounding water phase and solid
mat- ter from lipophilic and amphiphilic biomolecules
such as waxes, resins fatty acids and also proteins to some
extent. The enrichment with these molecules and the
association of polar tar oil compounds towards water
molecules in the NAPL decreases the viscosity of the NAPL
interface and thus reduces the mass transfer to the water
phase and the bioavailability. In addition, volatilisation,
oxidation processes and/or biodegradation or of easily
degradable LMW compounds from the tar oil also lead to
resinified aggregates in the interfacial layer with increased
vis- cosity. At many contaminated sites, PAH solubilised in
tar oils are also present associated to coal and coke particles
due to the history of waste dumping at manufactured gas
plant sites (Luthy et al. 1994; Rein et al. 2015; Wiesmann
1994). These associations considerably diminish the
bioavailability of PAH and the tar oil NAPL and may cause
the failure of several remediation measures at historic
manufactured gas plant sites. This also explains why
contaminants in soils at sites of wood preservation and
creosote applying facilities are often more bioavailable than
at former gas plant sites with much higher contents of
particulate black carbon materials. Such kinds of interaction
of complex contaminant mixtures are also relevant for other
compound classes, e.g. crude oils or explosives, in
particular if solid production wastes were dumped into the
soil.
In turn, the presence of water-soluble compounds such
as humic or fulvic acids as well as small biomolecules such
as peptides and fatty acids may cause desorption,
solubilisation and/or complexation of organic
contaminants, leading to in- creased mobility of the
compounds with increasing (phyto)- toxicity, and may
result in leaching towards the groundwater (Mayer et al.
2007; Mayer et al. 2005; Pignatello et al. 2006; Smith et al.
2009; Smith et al. 2011; Vacca et al. 2005). This process
also leads to increased bioavailability and accelerated
biodegradation (Haderlein et al. 2001; Ortega-Calvo and presence of potentially active microbes having access to the
Saiz- Jimenez 1998; Puglisi et al. 2007). It needs to be contaminant,
controlled in bioremediation measures: the concentration of
the contami- nant must be kept low enough to avoid
toxicity but high enough to support degradation
(Puglisi et al. 2007). Therefore, compost may be a perfect
agent for the modulation of the balance between sorption to
organic compounds and biodegradation in contaminated
soils.
An often overlooked biological phenomenon is linked to
physical and chemical processes. In comparison to other
groups of bacteria, certain groups of bacteria (mostly
nocardioformic Actinobacteria from the genera Nocardia,
Gordona, Rhodococci and Mycobacteria) show highly
elevat- ed sorptive potentials to PAH and hydrophobic
compounds (Stringfellow and Alvarez-Cohen 1999). This
is presumably due to highly hydrophobic cell envelope
structures; it results in improved bioavailability and
degradation by PAH- degrading organisms mostly found
in these groups of bacteria. However, it may also result in
decreased bioavailability due to accumulation of cells at the
NAPL interfacial surface areas, thus decreasing the overall
mass transfer to the aqueous bulk solution, in particular if
the enriched organisms do not degrade the respective
compounds. Sorption processes of contami- nants were
also found for pesticides and chlorophenols, in particular
to fungal mycelia (Benoit et al. 1998).

Biological mechanisms

Microbial (primary) oxidation processes of organic

contami- nants are based on three different principles
(Kästner 2000): (i) complete mineralisation and
metabolisation, which is most- ly intracellular and leads to
the formation of microbial bio- mass by use as carbon and
energy source, whereby CO2, H2O and biomass are the
main products and theoretically no me- tabolites
accumulate; (ii) cometabolism, which occurs mainly
intracellularly but also extracellularly and results in
partial oxidation, e.g. by monooxygenases, with the
accumulation of transformation products but without
formation of biomass or energy gain for the organisms; and
(iii) nonspecific radical
oxidation, which occurs extracellularly with initial
oxidation by one-electron abstraction and radical formation.
Secondary reactions of the primary oxidation products, with
reaction cas- cades all the way to CO2 (enzymatic
combustion), are possible as is known from wood-decaying
fungi (Hofrichter 2002). In particular, due to the nonspecific
radical oxidation, the process of oxidative coupling of the
metabolites to SOM may occur by radical scavenging
reactions resulting in covalently bound
nonextractable or bound residues, which are almost
impossi- ble to remobilise (Kästner et al. 2014).
There are also several biological mechanisms and
condi- tions that need to be considered in order to initiate
and main- tain microbial degradation activity. Beside the
one of the most important but often overlooked facts is that
a the contaminated soil (see physical and chemical
minimum concentration is needed in order to cover
energy needs for maintenance of the cell integrity of
organisms degrading the respective compounds and to
enable motility, allowing the concurrence of the compound
and the degrading microbe (Adam et al. 2014; Rein et al.
2015; Semple et al.
2001). As a consequence, nondegraded residual concentra-
tions may be encountered.
The minimum concentration in general is not based on
‘actual’ concentration but on ‘steady-state’ concentrations
of the compounds in terms of matter flux from sorption
sites or NAPLs to the respective degrading
microorganisms, since microbial activity depends on
substrate flux and not on con- centration. This is
particularly valid for the degradation of water-insoluble
hydrophobic compounds such as crude or tar oils and all
related organic compounds, for which the biodeg- radation
is usually limited by the mass transfer (Adam et al.
2014; Bosma et al. 1997; Marchal et al. 2013a; Marchal et
al.
2013b; Rein et al. 2015; Volkering et al. 1992; Wick et
al.
2001). The compost matrix, consisting of particulate and
slowly biodegradable organic substrates, and the presence
of humic acids and other amphiphilic biomolecules
obviously provides an appropriate system to improve the
mass transfer.
In addition, mixing of the contaminated soil with
compost may also contribute to improved mass transfer by
introducing energy, e.g. shear forces and elevated
temperatures for break- ing up or softening the mass-
transfer-resistant interfacial sur- faces of aged NAPLs in
processes). The destruction of these interfaces by mixing
and addition of organic matter results in higher
bioavailability and thus much faster degradation of
organic contaminants.
In the case of cometabolic degradation, the mass-
transfer limitation applies to the entire system, which needs
to provide amounts of nutrients and primary substrates
sufficient for maintaining the energy needs of the
degrading microbes. This may not always be the case in
contaminated soils, but biowaste additives, compost or
farmyard manure addition (Alburquerque et al. 2009; Chen
et al. 2015; Gandolfi et al.
2010; Megharaj et al. 2011) normally provide sufficient
amounts of primary substrates. The most generally
considered effect of compost addition to contaminated soils
is the provi-
sion of nutrients in terms of nitrogen and phosphorus
(Antizar-
Ladislao et al. 2004; Chen et al. 2015). However, compost
supplementation also acts as organic conditioner and
bulking
agent, which improves the overall structure by increasing
the
pore volume, gas space and water-holding capacity of the
soil. Both conditions are needed in order to enable
sufficient oxy- gen transfer to (and CO2 transport from) the
microbes and to provide sufficient chemical activity of
water needed for gen- eral microbial activity (Potts 1994).
The improved gas con- ductivity in the soil compost
mixtures and the resulting micro- bial activity also alters the
self-heating thermal properties of
the mixture. This is particularly of interest in technical- formed during deg- radation may improve the growth
scale soil heaps for the treatment of contaminated soils. In conditions of the microor- ganisms. The degradation
addition, due to its buffering capacities, compost addition in processes mostly lead to growth
many cases also acts as pH adjustor of the soil compost
mixtures towards more neutral conditions (Gandolfi et al.
2010; Zhang et al.
2011). The positive effect of compost addition on the
activity and abundance of microbial biomass has been
shown to per- sist for more than 5 years in long-term
studies (Hernandez et al. 2015).
The overall aim of the compost addition to
contaminated soils is to improve or enable microbial
degradation of the contaminants (Kästner et al. 1998;
Kästner and Mahro
1996). Therefore, it is generally considered that compost
ad- dition provides sufficient microbial biomass and
inoculum of potent microbes for the degradation of organic
contaminants; this has mostly been analysed in terms of
colony forming units (cfu) and/or phospholipid fatty acids
(PLFA) (Adam et al.
2015; Covino et al. 2015; Gandolfi et al. 2010; Puglisi et
al.
2007). However, it has been shown that the addition of
com- post sterilised by three consecutive sterilisation
procedures also enabled (slightly delayed) biodegradation
of certain PAH that were not degraded in the soil without
compost ad- dition (Kästner and Mahro 1996). Obviously,
the organic par- ticulate matrix and the physical and
chemical conditions of the compost enable microbes from
the soil to (re-)colonise the
‘niches’ of the former compost microbes. These results
indi- cate that the effect of the inoculum provided by the
compost may be overestimated in comparison to the ‘
matrix effect’. This may be explained by the provision of
primary substrates for support of degradation of low
concentrated compounds as well as solubilising and
bioavailability-enhancing agents such as humic acids and
small biomolecules (Haderlein et al. 2001; Marchal et al.
2013a; Marchal et al. 2013b; Mayer et al. 2005; Ortega-
Calvo and Saiz-Jimenez 1998; Puglisi et al. 2007; Smith
et al. 2011). In addition, the matrix effect may also be
expected if the compost addition leads to desorption of the
contaminants from the contaminated soil material with
subse- quent sorption to biodegradable solid organic matter
from the compost. In order to maintain this effect, it is
important to have a certain mixing ratio of around 10–50 %
(mostly 20 to
25 %) based on fresh weight and to keep the moisture and
oxygen contents at an appropriate level (Antizar-Ladislao
et al. 2004; Li et al. 2010; Megharaj et al. 2011).
Microbial degradation in general leads to metabolites
and to the additional mineralisation products CO2 and H2O,
which is often not considered but may be relevant in soil
with limited water supply (Kästner 2000). For example,
during the composting process the excess of process water,
which is sub- stantial due to the high loss of organic matter
during the pro- cess, must be removed in order to keep the
system oxygenat- ed. In dry systems, in contrast, the water
and biomass formation by the microbes, which after cell
death contribute to the formation of SOM from their nec
roma ss (Miltner et al. 2012). However, in the case of
cometabolic degradation without growth, only metabolites
may occur, which may lead to the formation of toxic
transformation prod- ucts from the parent compounds
(Semple et al. 2001). In par- ticular, the formation of NER
can be observed in studies using isotope-labelled tracer
compounds. The NER can only be analysed by means of
the isotope label; they may consist of entrapped or
sequestered parent compounds, metabolites or even the
necromass residues after conversion of the carbon or
nitrogen isotope into the microbial biomass (Kästner et al.
2014).
Microbial communities
After going through the described composting processes,
composts contain a wide variety of archaea, bacteria
(includ- ing Actinomycetes) and fungi. Many organisms are
described to be involved in the process of composting
(see section Background: process of composting); the
composts are thus considered to introduce large and
diverse microbial commu- nities and the related
degradation potentials into contaminated soil (Dees and
Ghiorse 2001; Loick et al. 2012; Thummes et al. 2007).
These potentials are normally not or only barely present in
most contaminated soils; compost amendment leads to a
significant increase of the total numbers of active micro-
organisms in soil-compost mixtures, including potential
con- taminant degraders. The mixture of soil with
composts also mobilises the activity of specific microbes
from both compart- ments, resulting in the degradation of
other organic materials that would not be degraded without
the amendments. Such processes related to SOM in
general are known from soils and are called priming
effects (Kuzyakov et al. 2000).
There are many frequently modified and improved lists
of specific bacteria and fungi, in particular for PAH
degradation (Antizar-Ladislao et al. 2004; Cerniglia 1984;
Cerniglia 1992; Cerniglia and Heitkamp 1989; Cerniglia and
Sutherland 2010; Juhasz and Naidu 2000; Loick et al. 2012;
Lu et al. 2011; Peng et al. 2008), showing the biodiversity
of these degradation potentials. These reviews were often
dedicated to microbial degradation in general or to the
degradation pathways; only some of them also deal with
environmental conditions (Aitken et al. 1998; Bamforth and
Singleton 2005; Johnsen et al. 2005) but only very few are
really devoted to bioremediation in soil (Megharaj et al.
2011). Chen et al. (2015) stated general trends after compost
addition to contaminated soils, with shifts from Alphap
rote obac te ria an d Ga mmap roteoba cte r ia to
Bacteroidetes and Firmicutes as well as with shifts of main
genera from Actinobacteria to certain Betaproteobacteria
and Acidobacteria. However, this review is also not
focussed on the processes and the specific degrading
microbial communi- ties relevant in compost-aided
bioremediatio n of
contaminated soils. Therefore, a thorough evaluation of microbial commu- nities of noncontaminated and
the development of microbial populations during contaminated soil.
remediation measures after mixing of contaminated soil
and composts is still missing (Megharaj et al. 2011; Vila et
al. 2015).
Only a few reports about the development of microbial
communities after soil compost mixing are available,
mainly focusing on hydrocarbon and PAH degradation.
Gandolfi et al. (2010) analysed the bioremediation process
of diesel–fuel- and PAH-contaminated soil after compost
addition (15 % w/ w) over a period of 180 days. The
authors showed that com- post addition significantly
increased both the elimination per- formance and the
numbers of cultivable heterotrophic bacte- ria. Based on
16S rRNA gene analyses, the diesel–fuel-con- taminated
soil showed microbial communities dominated by
Alphaproteobacteria and Actinobacteria, which were intro-
duced by the compost ad dition w ith Fi r mi c
ute s , Betaproteobacteria and Deltaproteobacteria.
However, dur- ing t h e biod egra dation , Alphap ro
te oba cteria an d Actinobacteria again began to increase
in proportion. In con- trast, the initial communities in the
PAH-contaminated soil w e r e d o m i n a t e d b y A l p h
a p r o t e o b a c t e r i a a n d Gammaproteobacteria, mainly
Bacteroidetes and Firmicutes
( a n d t o a s m a l l e r e xt en t b y Ac t i no ba c t e r i a an d
Alphaproteobacteria), all of which were added with the
com- post. After the biodegradation process, the
community was dominated by Bacteroidetes (Gandolfi et
al. 2010). The im- pact of the compost community on the
total community was higher in the PAH-contaminated soil
than in the hydrocarbon- contaminated soil; the authors
stated that this effect may de- pend on the low diversity
and abundance of the initial com- munities in the
contaminated soils: the higher the diversity and abundance
of the contaminated soil, the lower may be the impact of
the inoculum by compost addition.
Ros et al. (2010) reported about the bioremediation of
re- finery sludge by land farming with addition of
activated sludge and composted activated sludge (180 t/ha,
equivalent to estimated 7 % w/w). In these experiments,
the activated sludge performed better since more active
biomass was pres- ent in the fresh sludge. The microbial
community of both composted activated sludge and
noncomposted activated sludge dominated that of the
contaminated soil. This domi- nance, however, was
maintained in the composted-sludge- amended soil,
whereas in the activated-sludge-amended soil, the impact of
the initial activated sludge was lost. This again indicates a
higher impact of the microbial communities of the mature
composts on the communities of the contaminated soils.
The d o min a ting phyla i n a ll treatments w ere
Actinobacteria consisting of a variety of Actinomycetales
in- cluding Arthrobacter, Nocardia, Microbacterium
and Mycobacterium species. The most abundant fungal
phylum observed was Ascomycota (Ros et al. 2010). The
authors ob- served a significant difference between the
 Bastida et al. (2015) studied the bioremediation of
semiarid soils contaminated with 2 % crude oil (w/w) by
amendment with 5 % mature compost from garden waste
in a 50-day incubation experiment. Using PLFA and, for
the first time in this field, metaproteomic approaches, they
also found a sig- nificant increase in active biomass and
turnover performance after compost addition. The crude oil
increased the detectable proteobacterial proteins but
lowered those of the Rhizobiales in comparison to the
noncontaminated soil. Only 0.55 % of the metaproteome of
the compost-soil mixture could be asso- ciated to the
degradation of alkanes and aromatic compounds including
PAH, although up to 88 % of the contaminants were
degraded, in contrast to negligible degradation in the soil
with- out addition. Sphingomonadales and uncultured
bacteria showed the highest increase of catabolic enzymes
related to dioxygenase-mediated degradation pathways of
catechols (Bastida et al. 2015). Proteobacteria and
Actinobacteria ini- tially dominated the compost-treated
soil finally being domi- nated by Actinomycetales.
However, no key metabolic pro- teins related to alkane
degradation were observed. A very interesting additional
result is that the relative abundance of Gram-negative
bacterial proteins was increased by the con- tamination
with crude oil but decreased after the incubation with
compost. This is contradictive to the results from PLFA
analyses showing that the response of Gram-negative
bacteria may be based on membrane modifications, but
was not reflected by the abundance of proteins.
Peng et al. (2013) analysed soil from a rye-grass-planted
13
site artificially contaminated with 100 mg/kg C4-labelled
pyrene and added leaves, saw dust and green vegetables
ground to <2 mm particles at an extremely high final total
carbon content of 44 %. During composting at elevated
tem- peratures (38, 55 and 70 °C) for up to 60 days, the
authors extracted DNA samples and performed density
gradient cen- trifugation in order to separate the C-
13
labelled heavy DNA from the nonlabelled lighter ones
(DNA-SIP method). In their search for specific pyrene
degraders, they applied terminal restriction length
polymorphism analysis (T-RFLP) to the dif- ferent density
gradient fractions of the DNA from the incuba- tion with
13
nonlabelled and C-labelled pyrene. In all temper- ature
13
incubations with C-pyrene, they found a slight increase of
several TRFs in the heavier fractions of the gradients in
comparison to those from the nonlabelled experiment, care-
fully interpreting them as a ‘tendency’ to increase due to
pyrene consumption (Peng et al. 2013). They found these
TRFs to be representative for Alpha proteo bac teria
, Betapr oteoba cte r ia , Ga mmapr oteo bacteria
a n d Actinobacteria at 38 °C. Streptomyces appeared to
dominate a t 5 5 ° C w h e r e a s B e t a p r o t e o
bacteria a n d Gammaproteobacteria plus
Actinobacteria dominated at
70 °C. However, these results also indicate that instead of
a specific key degrader, more complex communities may
be involved during degradation of pyrene.
 13 Sometimes, in particular, when the degradation of
Applying 100 mg/kg C6-labelled pyrene, Adam et al.
(2015, 2016, submitted) described the effect of compost hardly degradable compounds such as PAH, phenols,
amendment (20 % w/w) and long-term fertilisation with explosives and
farm- yard manure on the turnover of the PAH in an
agricultural soil. Both treatments resulted in the complete
metabolisation of pyrene, whereas around 50 % were still
recovered in the nonsupplemented soil after 160 days. The
degradation was slightly delayed with the farmyard-
manure-fertilised soil due to much lower overall biomass
content (measured by PLFA analysis), but finally
performed similarly to the compost- amended soil. PLFA
indicative for Gram-negative bacteria and for
Actinomycetales finally increased during the incuba- tions
of the mixtures. However, statistical analysis showed that
soil-compost, soil-farmyard-manure and native soil clus-
tered clearly separated from each other. At the end of the
13
experiments, the C incorporation into PLFA derived
from pyrene was observed in nearly all PLFA for both
treatments, indicating a spread of the labelled carbon
within the entire microbial food web (Adam et al. 2015).
There was also no indication of specific labelling of PLFA
during the most in- tense degradation of pyrene, i.e. the
expected label uptake by
‘key degraders’ was not observed. This conclusion was
also supported by the analysis based on RNA and DNA
from these experiments. The overall incorporation into the
nucleic acids was too low for separation of the labelled
ones by density gradient centrifugation; attempts to
identify the label within proteins have also failed so far.
Therefore, the bacterial genera abundance data based on
total RNA and DNA extracted from the soil mixture
samples was statistically evaluated (Adam et al.,
submitted). The analysis revealed complex pyrene-
degrading communities with low abundances of individual
degraders, rather than the expected single or few key
players. This result was consistent with the PLFA analysis.
Pyrene treatments did not differ significantly from
controls, both in general and for the respective incubation
time. Similar find- ings were observed for the
farmyard-manure mixture. However, genera indicative
for PAH degradation were found to be highly different for
the two organic amendments, being comprised of six
genera and one unclassified OTU for the soil-compost
mixture and of 16 genera and three unclassified OTUs for
the soil-farmyard-mixture, although both amend- ments
showed similar degradation kinetics (Adam et al.
2015). In addition, the enrichment of pyrene-mineralising
bac- teria from the mixtures by cultivation did not result in
pure or mixed cultures of organisms dominating the
amended soils, according to the molecular analyses.
Although applying sim- ilar pyrene concentrations, the
higher label enrichment of the DNA observed by Peng et
al. (2013) may be due to the ele- vated temperatures applied
and the provision of green waste as real growth substrates
during the composting experiments, rather than adding
mature compost or farmyard manure.
pesticides was intended, the so-called sp ent m u s
hro om
composts or spent mushroom substrates (SMC or SMS)
were applied as additives to contaminated soils (Antizar-
Ladislao et al. 2004; Hawari et al. 2000; Phan and
Sabaratnam 2012; Sasek et al. 2003). These materials are
regular substrates ap- plied for the industrial growth of
mushrooms for food supply. After harvesting the fruit
bodies of mushrooms such as Pleurotus ostreatus,
Lentinus edodes or Agaricus bisporus, the SMC provide a
‘perfect’ industrially available waste prod- uct containing a
source of active mycelia of the respective fungi and the
related composted substrates, including the as- sociated
microflora. The substrates for growing the
ligninolytic fungi are usually composed of a mixture of
wood sawdust or similar materials, nitrogen-rich materials
(fibrous materials such as straw or hay mixed with horse
or pig ma- nure) and gypsum (Covino et al. 2015; Phan and
Sabaratnam
2012). The application of white rot fungi and other wood-
decaying fungi for soil bioremediation may be of
advantage, based on the unspecific radical oxidation
processes of various kinds of peroxidases and laccases that
are considered to be relevant in the metabolisation of
highly recalcitrant com- pounds (Harms et al. 2011; Kues
2015; Steffen et al. 2002). For example, Mn-peroxidase
may lead to unspecific enzymat- ic radical f ormation,
fina lly resulting i n a parti a l mineralisation of
organic compounds known as ‘enzymatic combustion’
(Hofrichter 2002), whereas in soil systems, rad- ical
scavenging reactions may result in oxidative coupling
reactions to SOM (see physical and chemical processes).
However, some authors found that the PAH degradation in
contaminated soils is not directly correlated to detectable
ligninolytic enzyme activities (Eggen 1999). Only laccase
ac- tivity could be detected in extracts of SMC from several
fungi (Li et al. 2010); the activity against HMW PAH
such as benzo(a)pyrene could be enhanced by radical
mediating agents such as 2,2-azino-bis-(3-
ethylbenzothiazoline-6-sul- fonic acid) (ABTS). In any
case, the synergistic metabolic cooperation by the
microflora associated to the SMC and the respective fungi
must also be considered (Ahlawat et al. 2010; García-
Delgado et al. 2015), since the primary oxidation prod- ucts
of these enzymes need to be further metabolised. In ad-
dition, such processes may need to be investigated
carefully, since it is argued that peroxidases may produce
traces of toxic metabolites (such as PCDD/PCDF from
chlorophenols) from chloroaromatic compounds under
certain conditions (Laine et al. 1997b; Morimoto and
Tatsumi 1997; Öberg et al.
1990). This risk needs to be reasonably balanced against
the elimination of sometimes high amounts of toxic
compounds in the contaminated soils.
Related to the wood-decaying fungi, there is also an inter-
esting recent study by Covino et al. (2015) regarding
remedi- ation of PAH-/tar-oil-contaminated railway sleepers
biotreated by cocomposting with fresh grass cuttings or
fresh mushroom cultivation substrate consisting of
chopped wheat straw,
chicken manure and gypsum, similar to the substrates for
the commercial cultivation of mushrooms. The amendments
were used in a 1:1 ratio with ground railway sleepers; the
mixtures were incubated for 240 days in aerated
composting devices. Interestingly, a higher elimination of
PAH (far above the assessed bioavailable concentrations,
even for the high- molecular-weight PAH) was observed
for the grass cuttings (97 %) in comparison to the
mushroom substrate (81 %). Based on next-generation
sequencing of 16S rRNA genes, the impact of the
microbial community of the mushroom sub- strate on the
mixture was found to be much higher in compar- ison to the
grass cutting. PLFA concentrations were continu- ously
increasing, accompanied by a relatively stable compo-
sition of all bacterial phyla of Proteobacteria, Firmicutes
and Bacteroidetes, and were finally dominated by fungi,
namely Ascomycota and putatively Glomeromycota. In
contrast, the impact of the grass cuttings was relatively
short, with contin- uously decreasing PLFA concentrations
and stable bacteria- to-fungi ratios but with a significantly
changing bacterial com- munity. The initial community
shifted from Firmicutes and Ac t i no ba c t e r i a t o a m
o r e c om pl e x o n e w i t h al l Proteobacteria classes and
a constantly high proportion of Firmicutes.
In general, the identification of the relevant microbes
for degradation is highly difficult, due to the high amount
and diversity of potentially active microbes. In addition, the
mate- rials are not standardised and the compost products
are highly different, depending on the fresh waste
materials used, e.g. general organic waste of different
origins, garden, park or graveyard waste, various kinds of
manure, spent mushroom composts, sewage sludge or
comparable organic materials.
Fig. 1 Summarised processes
relevant for the fate of organic
contaminants in soil-compost
mixtures (modified from Semple
et al. 2001). Italics = processes,
blue lines = triggered processes;
boxes left side = soil particles;
rounded boxes = system parts
embedded within the soil matrix;
boxes right side = potential
effects
The addition of bulking agents such as pine bark-chips may
also alter the composition of the microbial communities of
composts and may increase ligninolytic fungi. Severe gaps
of knowledge thus exist in identifying the microbial
commu- nities relevant for processes in real complex
environmental or technical systems, as recently stated for
the processes of PAH degradation, even though these are
in principle well- understood (Vila et al. 2015). This is
particularly relevant for PAH/tar-oil contaminations, since
PAH degradation was found in many distant genera. There
are also upcoming de- bates as to whether specific
degradation processes in complex terrestrial systems are
primarily due to k ey deg ra de rs or com-
plex communitie s with high physiological redundancies
(Adam et al., submitted; Peng et al. 2013). Therefore, the
evidence-based assignment of the microbes to specific
turn- over processes requires sophisticated methods: it is
normally only possible by application of isotope-labelled
compounds, applying the stable-isotope-probing (SIP)
approaches, PLFA- SIP, DNA or RNA SIP (Boschker and
Middelburg 2002; Dumont and Murrell 2005; Jones et al.
2011; Neufeld et al.
2007) alone or combined with the recently highly
improved protein SIP, which can identify organisms actively
degrading a
13
C-labelled substrate by analysing the label incorporation
into proteins (Seifert et al. 2013; von Bergen et al. 2013).
However, recent results of comparison of PLFA and
proteo- mic analyses of cyanate-metabolising archaea
showed that significant shifts of PLFA patterns and
contents may not be reflected by similar changes of the
protein inventory (Bastida et al. 2015; Palatinszky et al.
2015). Therefore, proteomic analyses of the compost
addition processes will provide much deeper insight in
future. For such purposes, the application of
the full set of ‘omics’ approaches, including next- an appropriate mea- sure, since the physical and chemical
generation sequencing approaches which were reviewed conditions in a given
recently for their application in wastewater (Rodriguez et al.
2015) may also be needed for soil compost systems. In
particular, linking the current metagenomics and
transcriptomics with metabolomic and proteomic
approaches, while considering the limitations (Prosser
2015), may provide additional process-related infor- mation
beyond enumerating the degradation-related microor-
ganisms. These approaches enable linking individual mem-
bers of the microbial community with activities related to
contaminant degradation. They therefore allow identifying
the actors and their interaction for contaminant
degradation and analysing their responses to
environmental conditions. This will be the scientific basis
for optimisation of remediation strategies including
compost application to soil. The relevant processes and
factors influencing the turnover and degrada- tion of
organic contaminants in soil-compost mixtures are
summarised and combined in Fig. 1.

Summary: applicability of compost

addition

Composting and compost addition can be powerful tools

for establishing and enhancing microbial activity and
degradation of organic chemicals in contaminated soil.
Due to the huge metabolic diversity of microorganisms
developing in succes- sion during the composting
processes, a highly complex met- abolic diversity can be
expected, constituting a ‘metabolic memory’ in
developing and mature compost materials. Compost
addition can thus be considered as a kind of ‘su- per-
bioaugmentation’ of contaminated soils with a complex
natural mixture of degrading microorganisms with highly
di- verse metabolic potential, high functional redundancy
and a wide range of potential metabolic cooperations. This
is com- bined with a ‘biostimulation’ by the nutrients and
the diverse additional organic substrates contained in the
compost mate- rial as well as by the positive effects on
physical soil proper- ties, mainly on water retention and
availability. It may thus be much more important to
identify the relevant metabolic po- tentials rather than
trying to identify the often expected key degrading
organism.
Compost or farmyard manure addition provides effects
similar to pre-exposure and adaption of soils to the
degrada- tion of specific contaminants suc h as
chlorin ated dibenzodioxins/furans and PAH
(Haderlein et al. 2001; Megharaj et al. 2002) or triazine
pesticides (Abdelhafid et al.
2000). For microbial adaptation, the exposure histories of
a site and the compound mixtures as well as the physical
and chemical conditions are also of importance. However, in
most contaminated soils, the intrinsic metabolic potential is
too low to be improved by biostimulation alone.
Bioaugmentation with single organisms is usually also not
contaminated soil are mostly not appropriate for these
organisms.
For all contaminants with mass-transfer limitations to
the degrading microorganisms, or for HMW compounds,
the ap- plication of mushroom cultivation substrates or
SMC is more appropriate, since SMC is known to provide
many extracellu- lar enzymes of the lignocellulose-
degrading fungal colonisers for primary attack of the
contaminants. However, the compost or SMC amendment
may be of disadvantage in particular for C- and N-
containing compounds with highly oxidised carbon, which
are preferably used by microorganisms as a nitrogen
source. The relatively high supply of primary substrates
and nutrients by composts and farmyard manure may
inhibit deg- radation of such compounds.
Beside the provision of nutrients and substrates, abi-
otic factors are also relevant for the degradation-
stimulating effect of compost addition. An important
abiotic effect is pH adjustment of the frequently slightly
acidic contaminated soils towards a more neutral pH
value due to the slightly alkaline pH of mature com-
posts. In addition, the fine-grained organic materials of
mature composts or farmyard manure act as bulking
agents, in particular for highly binding clay-containing
soil materials. Due to the high water-holding capacities
of the compost materials, the water retention is in-
creased and thus gas exchange and water availability
for microbial activity are enhanced. Dissolved humic
substances from the composts may improve bioavailabil-
ity. In addition, these compounds may compete for sorp-
tion sites in the contaminated soil and may thus lead to
desorption of the contaminants. In contrast, slowly de-
gradable particulate organic matter of composts may act
as resorbing agents, enabling slow release during degra-
dation of the entire particle. Energy introduction, for
example in technical mixing devices, may accelerate
sorption and desorption.
Overall, soil amendment with compost can enhance
contaminant degradation in many cases and thus is a highly
promising and potentially cost-effective technology.
However, substantial improvement in terms of understand-
ing the microbial ecology of contaminant degradation, in
particular related to the abiotic factors and the matrix ef-
fect, is needed in order to enable tight control over the
microbial processes. In particular, more information is
needed on the microbial actors in the remediation process,
their in situ activities and metabolic networks. We also
need to know how the processes and actors involved in
contaminant degradation are affected by specific environ-
mental conditions, and how we can draw advantage of the
functional redundancy for successful remediation under a
variety of environmental conditions. This would allow
optimising bioremediation measures and to predict failure
or success in reaching target values.
Acknowledgments This work was performed in the framework of directions. J Chem Technol Biotechnol 80(7):723–736.
the European Union project BMolecular Approaches and doi:10.1002/jctb.1276
MetaGenomic Investigations for optimizing Clean-up of PAH
contaminated sites (MAGICPAH)^ within the seventh framework
programme (FP7- KBBE, #245226) and by general funding of the
Helmholtz-Association.

Compliance with ethical

standards

Conflict of interest The authors declare that they have no conflict

of interest.

Ethical approval This article does not contain any studies with
human participants or animals performed by any of the authors.

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