Selected persistent organic pollutants (POPs) in the rhizosphere of sewage sludge-treated soil: Implications for the biodegradability of POPs

Abstract

The impact of regular application of sewage sludge or farmyard manure on the organic contaminant loads in soil was assessed in a model rhizobox experiment. Two soils originating from a long-term field crop rotation and fertilizer experiment running since 1996 were used. The total polychlorinated biphenyls (PCBs), polycyclic aromatic hydrocarbons (PAHs), organochlorinated pesticides (OCPs), polybrominated diphenyl ethers (PBDEs), perfluorooctanoic acid (PFOA), and perfluorooctane sulfonate (PFOS) contents were determined in the rhizosphere and bulk soil. The results showed low but still detectable contents of PCBs and OCPs in the soil, substances which were banned a few decades ago. Among the OCPs, dichlorodiphenyltrichloroethane (DDT) and its metabolites reaching up to 18.2 µg kg⁻¹ of the soil even exceeded the preventive levels for these compounds in agricultural soils, i.e. 7.5 µg kg⁻¹ of soil. For PBDEs, PFOA, and PFOS, their contents in the soil significantly increased with sewage sludge application. The enhancement of the potential biodegradability of the POPs in the rhizosphere was confirmed only for hexachlorocyclohexane (γ-HCH), where, the level of γ-HCH increased significantly in the rhizosphere soil compared to bulk soil. Thus, natural attenuation of POPs in the soil-plant system seems to be insufficient for most of the investigated compounds.

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Archives of Agronomy and Soil Science
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Selected persistent organic pollutants (POPs) in
the rhizosphere of sewage sludge-treated soil:
implications for the biodegradability of POPs
Jiřina Száková, Jana Pulkrabová, Jindřich Černý, Filip Mercl, Andrea Švarcová,
Tomáš Gramblička, Jana Najmanová, Pavel Tlustoš & Jiří Balík
To cite this article: Jiřina Száková, Jana Pulkrabová, Jindřich Černý, Filip Mercl, Andrea Švarcová,
Tomáš Gramblička, Jana Najmanová, Pavel Tlustoš & Jiří Balík (2019) Selected persistent
organic pollutants (POPs) in the rhizosphere of sewage sludge-treated soil: implications for
the biodegradability of POPs, Archives of Agronomy and Soil Science, 65:7, 994-1009, DOI:
10.1080/03650340.2018.1543945
To link to this article: https://doi.org/10.1080/03650340.2018.1543945
Accepted author version posted online: 31
Oct 2018.
Published online: 10 Nov 2018.
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Selected persistent organic pollutants (POPs) in the rhizosphere
of sewage sludge-treated soil: implications for the
biodegradability of POPs
Jiřina Száková
a
, Jana Pulkrabová
b
, Jindřich Černý
a
, Filip Mercl
a
, Andrea Švarcová
b
,
TomášGramblička
b
, Jana Najmanová
a
, Pavel Tlustoš
a
and Jiří Balík
a
a
Department of Agroenvironmental Chemistry and Plant Nutrition, Czech University of Life Sciences, Prague,
Czech Republic;
b
Department of Food Analysis and Nutrition, Faculty of Food and Biochemical Technology,
University of Chemistry and Technology, Prague, Czech Republic
ABSTRACT
The impact of regular application of sewage sludge or farmyard manure
on the organic contaminant loads in soil was assessed in a model rhizo-
box experiment. Two soils originating from a long-term field crop rota-
tion and fertilizer experiment running since 1996 were used. The total
polychlorinated biphenyls (PCBs), polycyclic aromatic hydrocarbons
(PAHs), organochlorinated pesticides (OCPs), polybrominated diphenyl
ethers (PBDEs), perfluorooctanoic acid (PFOA), and perfluorooctane sul-
fonate (PFOS) contents were determined in the rhizosphere and bulk soil.
The results showed low but still detectable contents of PCBs and OCPs in
the soil, substances which were banned a few decades ago. Among the
OCPs, dichlorodiphenyltrichloroethane (DDT) and its metabolites reach-
ing up to 18.2 µg kg
−1
of the soil even exceeded the preventive levels for
these compounds in agricultural soils, i.e. 7.5 µg kg
−1
of soil. For PBDEs,
PFOA, and PFOS, their contents in the soil significantly increased with
sewage sludge application. The enhancement of the potential biode-
gradability of the POPs in the rhizosphere was confirmed only for hexa-
chlorocyclohexane (γ-HCH), where, the level of γ-HCH increased
significantly in the rhizosphere soil compared to bulk soil. Thus, natural
attenuation of POPs in the soil-plant system seems to be insufficient for
most of the investigated compounds.
ARTICLE HISTORY
Received 13 June 2018
Accepted 29 October 2018
KEYWORDS
Organic fertilizers; organic
contaminants; rhizobox;
long-term experiments;
microbial degradation
Introduction
Land application of sewage sludge is becoming more popular due to the possibility of recycling
valuable components such as organic matter and plant nutrients (Singh and Agrawal 2008).
However, land application of sewage sludge could be hampered by the environmental risk
connected with the different amounts of various inorganic and organic contaminants contained,
according to its origin. In the Czech Republic, the maximum PAH, PCB, and OCP levels permissible
in agricultural soils are determined by public notice No. 153/2016 (Ministry of Environment of the
Czech Republic 2016). Thus, the levels of a wide spectra of other organic pollutants connected with
anthropogenic activity which might be transferred into sludge remain unknown. Jones et al. (2014)
surveyed 28 wastewater treatment plants in Great Britain over a period of 12 months and, except
for contaminants such as risk elements, pharmaceuticals, and PAHs, low contents of PBDEs were
CONTACT Jiřina Száková szakova@af.czu.cz Department of Agroenvironmental Chemistry and Plant Nutrition, Czech
University of Life Sciences, Kamýcká 129, CZ-165 21, Prague 6, Czech Republic
ARCHIVES OF AGRONOMY AND SOIL SCIENCE
2019, VOL. 65, NO. 7, 994–1009
https://doi.org/10.1080/03650340.2018.1543945
© 2018 Informa UK Limited, trading as Taylor & Francis Group

detected. Moreover, Clarke and Smith (2011) identified perfluoroalkylated substances (PFASs) in
sewage sludge as the chemicals of primary concern.
Serious soil contamination by PCBs still exists in the areas of former PCB production plants, such
as Serpukhov City (Russia), where recent PCB concentrations have been found to reach up to
1169 mg kg
−1
of dry matter depending on the distance from the pollution source (Malina and
Mazlova 2017). In the Czech Republic, PCBs have still been recently detected in soils (Křesinová
et al. 2014).
The massive application of OCPs during the 20th century can result in long-term contamination
of soil. Egorova et al. (2017) determined that the concentration of DDT reached up to 25 mg kg
−1
in
soil 45 years after the last application of the insecticide. Residues of OCPs were identified in
agricultural soils in the Czech Republic as well (Shegunova et al. 2007).
The long-term persistence of chlorinated, brominated, and perfluorinated organic compounds
in soil indicates a limited ability of soil microorganisms to degrade these substances, and the
regular application of sewage sludge can result in an ongoing supply of these substances to the
soil. In organic matter degradation processes, the role of the plant rhizosphere seems to be
important because of the specific soil physico-chemical parameters within this zone and the
specific pattern of soil microorganisms in contact with the root exudates; the root exudates can
modify the soil physico-chemical properties in the plant rhizosphere (Kim et al. 2010).
Xie et al. (2012) and Guo et al. (2017) observed the degradation rate of PAHs in the individual
zones of the rhizosphere soil and suggested differences in the soil microbiome within the rhizo-
sphere soil zones as well as the substantial role of the plant roots. More intensive degradation of
the dioxin-like PCB CB-77 in the rhizosphere compared to the bulk soil was reported by Tu et al.
(2017). Enhanced microbial activities in the rhizosphere of Lolium multiflorum plants growing in soil
contaminated with PCBs was observed by Ding et al. (2011), who indicated that rhizospheric
microorganisms had a high tolerance for pollutants and therefore a great potential to degrade
these compounds. The role of root exudates in the potential enhancement of the biodegradation
rate of PCBs in the rhizosphere was highlighted (Toussaint et al. 2012; Pino et al. 2016).
Seasonal changes as well as the effect of crop rotation on the contents of PBDEs in soil were
published by Jiao et al. (2016), indicating the potential role of the plant rhizosphere. The sub-
stantial effect of the root exudate components on the potential degradability of PBDEs was
observed by Huang et al. (2016). The long-term effect of sewage sludge land application on the
contents of PBDEs in soil was investigated by Xia et al. (2010) who found 658 μgkg
−1
of ΣPBDEs in
the upper layer (0-15 cm) of soil treated annually with sewage sludge for 33 years, documenting
slow degradation of these substances in the soil.
Among the PFASs, PFOA and PFOS are the two most commonly studied representatives
receiving attention due to their ubiquity in the environment. The plant-availability of PFOS and
PFOA was observed in recent investigations by Zabaleta et al. (2018) and Zhao et al. (2018).
However, Venkatesan and Halden (2014) and Sepulvado et al. (2011) showed a long-term stability
of sludge-derived long-chain PFASs in soil. Tight sorption of PFOA and PFOS on soil organic matter
was observed by Miao et al. (2017) and Qian et al. (2017), whereas perfluoroalkylated phosphonates
(PFPAs) showed high mobility in environmental systems (Lee and Mabury 2017). Thus, the behavior
of the individual PFASs in soil will depend on the particular compound and/or the soil physico-
chemical parameters. Moreover, PFOA and PFOS in soil can result from microbial degradation of
PFASs in soil (Liu and Avendano 2013). If PFOA was present in the soil, Liou et al. (2010) observed
no microbiological degradation of this compound.
The findings mentioned document that chlorinated, brominated, and fluorinated organic com-
pounds could be present in soils in appreciable concentrations and land application of sewage
sludge belongs to the group of potential sources of these compounds in soil. However, low
biodegradability of these contaminants in soil is evident, though rhizosphere processes indicate
a possibility for enhancement of the potential biodegradability rate. Thus, the main objectives of
this study were established as follows: i) to assess the potential impact of long-term regular
ARCHIVES OF AGRONOMY AND SOIL SCIENCE 995

application of sewage sludge on the organic contaminant loads in soil as compared to the
untreated variant and/or farmyard manure application, where the soils originating from the long-
term field experiment crop rotation/fertilizer experiment with regular application of sewage sludge
were used, ii) to evaluate the potential alterations of organic contaminants in the rhizosphere as
a function of the distance from the roots, and iii) because the long-term field experiment the soils
for this study are derived from is based on the rates of organic fertilizer application to achieve
comparable nitrogen rates in the treated variants, to evaluate the activities of soil enzymes
connected predominantly with the N-cycle in the rhizosphere of the soils. To achieve the stated
objectives, a model rhizobox experiment was conducted in which the soils originating from the
long-term crop rotation/fertilizer experiment running since 1996 at two sites in the Czech Republic
(Lukavec –Soil A, Prague-Suchdol –Soil B) with different soil and climate characteristics were
investigated.
Material and methods
Experimental soils and rhizobox experiment design
The model experiment was based on two soils originating from the long-term fertilizer experiment.
The field experiment was designed to simulate common agricultural practices as much as possible.
Potatoes (Solanum tuberosum L.), winter wheat (Triticum aestivum L.), and spring barley (Hordeum
vulgare L.) were grown in a three-year rotation, which enabled investigation of the direct as well as
subsequent effects of different treatments. For the rhizobox experiment, three treatments were
chosen as follows: i) sewage sludge applied at a rate corresponding to 330 kg N ha
−1
, ii) farmyard
manure applied at a rate corresponding to 330 kg N ha
−1
, and iii) untreated control. The application
rate of the organic fertilizers was always calculated on the basis of their nitrogen content. The
organic fertilizers (sewage sludge, farmyard manure) were applied only before potatoes were
planted, i.e., once in a three-year period. Identical anaerobically treated sewage sludge originating
from the same wastewater treatment plant was used at all experimental sites, whereas farmyard
manure originated from local farmers. The application of the organic fertilizers resulted in slight
(insignificant) changes in the soil properties, with pH values of 4.45, 4.58, and 4.73 in the control,
sewage sludge, and farmyard manure treated soil A and 6.93, 7.01, and 7.09 in the control, sewage
sludge, and farmyard manure treated soil B, respectively. The levels of the cation exchange capacity
(CEC) were 45, 46, and 51 mmol kg
−1
in the control, sewage sludge, and farmyard manure treated
soil A and 262, 259, and 254 mmol kg
−1
in the control, sewage sludge, and farmyard manure
treated soil B, respectively. The oxidizable carbon (Cox) levels were 1.1, 1.2, and 1.3% in the control,
sewage sludge, and farmyard manure treated soil A and 1.8, 1.5, and 1.5% in the control, sewage
sludge, and farmyard manure treated soil B, respectively. The whole design of the experimental
tool and procedure as well as and the main characteristics of the experimental sites and soils are
described in detail elsewhere (Kulhánek et al. 2014;Vašák et al. 2015). The detailed description of
the loads of the wide spectrum of the organic contaminants at the individual experimental fields
was presented elsewhere, as well (Pulkrabová, personal communication).
The upper layer (0-25 cm) of the soils was sampled at the individual experimental fields, and the
samples were air-dried, sieved through a 2 mm diameter mesh, and thoroughly homogenized.
Before the start of the experiment, soil moisture was set at 60% of the maximum water holding
capacity (MWHC) using deionized water and kept at this level for the whole experiment. No
sterilization of the soil was provided to keep the natural microbial community intact, and no
additional fertilizer was applied. Specially designed rhizoboxes (Wenzel et al. 2001) allowing
sampling of the soil rhizosphere vertical profile were used in six repetitions, and spring wheat
(T. aestivum) was cultivated in the soil–plant compartment (10 plants per pot). The duration of the
experiment was 90 days. The experiment was carried out in a greenhouse under controlled
conditions at 20°C. At the end of the experiment, the soil was cut without freezing into root-
996 J. SZÁKOVÁ ET AL.

parallel sections according to the distance from the plant roots using a specially designed slicing
device (Fitz et al. 2003); the 0-3 mm, 3-6 mm, and bulk soil sections were separated, freeze-dried,
and homogenized.
Determination of persistent organic pollutants (POPs)
Analytical methods
PCBs, OCPs, PAHs. Soil samples (10 g) were mixed with anhydrous sodium sulfate and extracted
for 7 hours in dichlormethane. After pre-concentration, the extract was purified using gel permea-
tion chromatography (GPC) on a Bio Beads S-X3 column, and a mixture of cyclohexane:ethyl-
acetate (1:1, v/v) was employed as the mobile phase. A purified extract was also evaporated to
dryness, re-dissolved in isooctane, and analyzed using an Agilent gas chromatograph 7890A
equipped with an electronically controlled multimode injection port coupled to an Agilent 7000B
triple quadrupole mass selective detector operated in electron ionization with a DB5-MS (30 m ×
250 μm × 0.25 μm) capillary column for PCBs and OCPs. For the determination of PBDEs, a DB-XLB
(15 m × 180 μm × 0.07 μm) capillary column and negative chemical ionization were employed.
In the case of PAHs, high performance liquid chromatography with a fluorescence detector
(HPLC-FLD) was performed on an HP 1200 Series liquid chromatograph equipped with the HP 1200
FLD G1321A fluorescent light detector (Agilent Technologies) on a SUPELCOSILTM LC-PAH C18
analytical column (100 mm × 2.1 mm × 1.7 μm). For each compound, specific excitation and
emission wavelengths were set and monitored.
PFASs. Soil samples (5 g) were mixed with 10 mL of acetonitrile and 10 mL of deionized water and
shaken for 1 min. After the addition of 1.5 g of NaCl and 6 g of MgSO
4
, the extract was shaken once
again and then centrifuged for 5 min. Then 5 mL of extract was concentrated, re-dissolved in
methanol, and analyzed by an Agilent 1290 Infinity II liquid chromatograph interfaced with an
Agilent 6795 LC/MS triple quadrupole mass selective detector (Agilent Technologies) operated in
electrospray ionization in negative mode, multiple reaction monitoring (MRM) mode and with an
Acquity UPLC BEH C18 (100 mm × 2.1 mm × 1.7 μm) column (Waters).
Soil microbial activities
ß-glucosaminidase (EC 3.2.1.30) activity was assessed following the method described by Parham
and Deng (2000). Protease activity (EC 3.4.2.21-24) was determined according to the method
described by Ladd and Butler (1972), and arylamidase (EC 3.4.11.2) was determined by the method
published by Acosta-Martinez and Tabatabai (2000).
Data analysis
All statistical analyses were performed using Statistica 12.0 software (www.StatSoft.com). The effect
of the treatment and distance from the roots was analyzed by factorial analysis of variance, ANOVA
(p < 0.05), and Tukey’s honestly significant difference (HSD) post-hoc test was used to determine
significant differences between the individual variables.
Results and discussion
The contents of POPs in the rhizosphere soils
The different soil treatments resulted in differing yields of wheat biomass; the aboveground
biomass dry matter reached 5.27 ± 1.32 g for soil A and 4.60 ± 2.87 g for soil B in untreated
soils. In the sewage sludge treated soils, the biomass dry matter was 8.33 ± 0.74 g for soil A and
ARCHIVES OF AGRONOMY AND SOIL SCIENCE 997

7.37 ± 1.48 g for soil B, and in the case of farmyard manure treatment it was 6.57 ± 0.25 g for soil
A and 5.87 ± 0.75 g for soil B. Therefore, the results indicated a better fertilizing effect for the
sewage sludge compared to farmyard manure, but the differences in plant growth and develop-
ment do not allow us to predict any differences in the root development and, subsequently, the
quality and quantity of the root exudates.
Table 1 shows the results of the multivariate statistical evaluation of the analytical data, in which the
predominant role of the soil and treatment was confirmed in most of the cases, including the interactions
of these two variables. On the contrary, except for γ-HCH representing the OCPs, the effect of the
rhizosphere was negligible, and the potential interactions of the effect of distance from the roots with the
soil/treatment effects remained insignificant as well.
The contents of PAHs in the rhizosphere soil are summarized in Table 2,where∑12 PAHs represents
the sum of anthracene (AN), benz[a]anthracene (BaA), benzo[a]pyrene (BaP), benzo[b]fluoranthene
(BbFA), benzo[k]fluoranthene (BkFA), benzo[ghi]perylene (BghiP), dibenz[a,h]anthracene (DBahA), fluor-
anthene (FA), chrysene (CHR), indeno[1,2,3-cd]pyrene (IP), phenanthrene (PHE), and pyrene (PY), and ∑8
PAHs represents the compounds with morearomaticrings,i.e.,BaA,BaP,BbFA,BkFA,BghiP,DbahA,CHR,
and IP. According to the public notice characterizing the conditions for the protection of agricultural soil
quality in the Czech Republic (Ministry of Environment of the Czech Republic 2016), the preventive value
of ∑12 PAHs in the soil is 1 mg kg
−1
. Hildebrandt et al. (2009) detected levels of PAHs in soil samples from
the Ebro River basin (NE Spain) up to 465 µg kg
−1
. Thus, the levels of PAHs are far below the Czech limits
as well as the cited findings.
The most abundant compounds in the soils were benz[a]anthracene, benzo[a]pyrene, benzo[b]
fluoranthene, and chrysene, regardless of the soil and treatment, i.e., compounds characterized by
their low water solubility (Bamforth and Singleton 2005) and, therefore, higher long-term stability
in soils. Tables 1 and 2illustrate that there were no significant differences in the PAH content
among the individual treatments as well as no effect of the distance from the roots, but there was
a significant (p < 0.05) effect of the soil (in the case of ∑8 PAHs). This indicates i) no impact of the
treatments on the PAHs loads in the soils and ii) no effect of the rhizosphere environment on the
potential degradation of these mostly stable, low solubility, and low degradability compounds. As
observed by Pulkrabová (personal communication), the results indicate long-term soil contamina-
tion, most probably originating from the past before the establishment of the long-term experi-
ment. Thus, according to Bamforth and Singleton (2005), biodegradability of PAHs in soil can be
significantly reduced with time of ageing. Moreover, Bourceret et al. (2017) stated that the shifts in
the bacterial communities in rhizospheric soil contaminated by PAHs are affected by the root depth
gradients and not by the PAHs contamination level. Thus, the degradability of the PAHs residues in
soils seems to be unaffected by the rhizosphere conditions in this case.
The levels of OCPs are summarized in Table 3,confirming that the residues of these substances are
still present in these agricultural soils even several decades after their use was banned. In the Czech
Republic (Ministry of Environment of the Czech Republic 2016), the preventive value of ∑DDTs is
7.5 µg kg
−1
, and for HCB and HCH it is 20 µg kg
−1
and 10 µg kg
−1
, respectively. Thus, HCB and HCH levels
were far below these limits. On the contrary, the sum of DDT+DDD+DDE varied between 5.1 and
18.2 µg kg
−1
in soil A and between 0.95 and 11.8 µg kg
−1
in soil B, with numerous measurements
exceeding the given preventive values. However, these data did not reach the value which can directly
threaten human and animal health, i.e., 8 mg kg
−1
(Ministry of Environment of the Czech Republic
2016). Soils from the Ebro River basin (NE Spain) showed a prevalence of DDT and DDE, where the
detectable contents found in 53% and 88% of the soil samples varied between 0.13 and 58 µg kg
−1
(Hildebrandt et al. 2009), showing values similar to this experiment. Lu and Liu (2015) also found DDT
and DDE to be the dominant OCPs in soils in Guanzhong Basin, China. Higher average values were
observed in these soils compared to soil B, indicating either different application rates of these
compounds in the past (over more than 20 years), or different degradation abilities of both soils.
Although no significant differences were observed among the OCP levels at different distances from
the roots, significant differences were recorded for the individual treatments (except for the γ-HCH levels
998 J. SZÁKOVÁ ET AL.

with no significant differences). Moreover, an effect of the rhizosphere on the γ-HCH levels was observed
(Table 1). For HCB and DDT, significantly (p < 0.05) higher values were determined for the sewage sludge
treatment in both soils. For DDE and DDD, a different pattern of these compounds in the different soils
was observed: in soil A, significantly (p < 0.05) higher DDE and DDD values were observed for the
farmyard manure treatment compared to the remaining variants, whereas in soil B the highest (p < 0.05)
DDE value occurred in the sewage sludge treated variant. For DDE, the farmyard manure treatment
showed a lower (p < 0.05) level of DDD compared to the control and sewage sludge treatments in soil
B. The uncontaminated sewage sludge application can be helpful for the enhancement of DDT and HCH
biodegradation in contaminated soil due to the increasing organic matter content and introduction of
efficient degradation microbes into the soil (Liang et al. 2014). In this case, however, the results indicated
potential loads of OCPs via the sewage sludge application. Abhilash and Singh (2009) reported decreased
contents of γ-HCH in the rhizosphere soil compared to bulk soil, where the mean concentrations of the
total HCH in bulk soil and rhizospheric soil samples were found in the range of 39 to 104 mg kg
−1
and 8.4
to 26 mg kg
−1
, respectively. The biodegradation ability of HCH in the plant rhizosphere was described
also by other authors (Boltner et al. 2008).
Similar to OCPs, PCBs are still detectable long after they were banned in the 1980s (Table 4). The
preventive value of ∑7 PCB in agricultural soils is 20 µg kg
−1
(Ministry of Environment of the Czech
Republic 2016), and therefore, all the values determined in this study are below these limits.
Among the individual detected congeners, the hexa- and heptachlorinated ones (i.e., especially
the congeners 138, 153, and 180) were the predominant compounds, with higher values found in
soil B compared to soil A, and no differences among the soil rhizosphere segments. The concen-
trations of tri-, tetra-, and pentachlorinated congeners were close to the detection limits.
Comparing the treatments, no differences among the variants were observed in soil B, and
enhanced levels of penta-, hexa-, and heptachlorinated PCBs were observed for the treated variants
compared to the control in soil A with the sewage sludge treated variants showing significant
enhancements (p < 0.05). Malina and Mazlova (2017) identified heptachlorinated biphenyls as the
predominant PCBs in soil in the vicinity of a former production plant. In this experiment, the
Table 1. Summary of 3-way ANOVA of the effects of soil, treatment and distance from root on the contents of POPs in soil.
Source of variation
Pollutant
Soil
type Treatment
Distance
from
roots Soilxtreatment Soilxdistance Treatmentxdistance Soilxtreatmentxdistance
∑12 PAH ns ns ns ns ns ns ns
∑8 PAH 4.74* ns ns ns ns ns ns
HCB 49.1*** 8.51*** ns ns ns ns ns
γ-HCH 9.54** ns 3.17* ns ns ns ns
DDE 264*** 16.2*** ns 31.2*** ns ns ns
DDD 227*** 5.07** ns 27.4*** ns ns ns
DDT 170*** 7.73*** ns 6.37** ns ns ns
∑tri-PCB 24.2*** 4.92** ns 6.14** ns ns ns
∑tetra-PCB 4.70* ns ns ns ns ns ns
∑penta-PCB 8.80** 3.5* ns ns ns ns ns
∑hexa-PCB 58.7*** 3.14* ns ns ns ns ns
∑hepta-PCB 42.6*** ns ns ns ns ns ns
∑tetra-BDE 15.0*** 12.4*** ns 3.55* ns ns ns
∑penta-BDE 7.95** 98.2*** ns ns ns ns ns
∑hepta-BDE ns ns ns ns ns ns ns
∑okta-BDE ns ns ns ns ns ns ns
∑nona-BDE ns ns ns ns ns ns ns
Deka-BDE ns ns ns ns ns ns ns
PFOA ns 98.8*** ns ns ns ns ns
Br-PFOS ns 116*** ns ns ns ns ns
L-PFOS 12.7*** 354*** ns ns ns ns ns
Values shown represent F-value of 3-way ANOVA. ns not significant; * p < 0.05; ** p < 0.01; *** p < 0.001
ARCHIVES OF AGRONOMY AND SOIL SCIENCE 999

dominance of these congeners was expected because these compounds were frequently produced
and applied in the former Czechoslovakia. On the contrary, lower chlorinated PCBs were generally
detected more frequently and at higher concentrations than higher chlorinated PCBs in agricultural
soils in Guanzhong Basin, China (Lu and Liu 2015), indicating a different source of PCBs in this area.
Table 5 shows the detectable contents of the individual PBDEs, whereas tri- and hexabromi-
nated congeners (i.e., BDE-28, −153, and −154) were below the method detection limits (varying
between 0.03 and 0.08 μgkg
−1
, according to the individual compounds). McGrath et al. (2016)
found that the sum of eight congeners of PBDEs of environmental concern (BDE-28, −47, −99,
−100, −153, −154, −183, and −209) in a set of urban soil samples reached up to 13.2 μgkg
−1
, with
the highest values identified at waste disposal sites. In this experiment, the sum of these congeners
varied between 0.2 and 8.3 μgkg
−1
, demonstrating low PBDE loads in agricultural soils compared
to urban areas. Li et al. (2015) found that BDE-99 was the congener most frequently determined in
sewage sludge amended soils. In this experiment, however, high proportions of nona- and
decabrominated congeners (i.e., BDE-206, −207, and −209) were recorded.
No significant differences between the PBDE contents in soils A and B, as well as among the rhizo-
sphere sections, were determined. Enrichment of the rhizosphere soil with PBDEs compared to the bulk
soil was observed by Wang et al. (2016), indicating the key role of soil organic matter in the behavior of
PBDEs in the soil. Moreover, Mueller et al. (2006) indicated that plants can enhance the bioaccessibility of
PBDEsinsoil.Theseaspectswerenotconfirmed by this experiment. On the contrary, the soil BDE
contents were affected by treatments, with significantly (p < 0.05) higher contents of tetra-, penta-, hepta-
,anddecabrominatedBDEcongenersobservedinthesewagesludgetreatedvariants,confirming the
anthropogenic origin of the brominated compounds. The low potential bioaccessibility of the sewage
sludge-derived PBDEs was already described. Meng et al. (2015) showed that the bioaccessible propor-
tion of PBDEs in sewage sludge was around 5%, and differences among the sludges of different origins
and compositions were observed. Possible groundwater contamination by PBDEs after land application
of sewage sludge was observed by Gottschall et al. (2017). However, significant reductions (>90%) of
sludge-derived PBDEs within one-year post-application were observed by these authors. This experiment
Table 2. The contents of PAHs in the rhizosphere and bulk soils (µg kg
−1
of dry weight) according
to the individual soils and treatments; data are presented as mean ± standard deviation, n = 6.
∑12 PAHs*
< 3mm > 3-6 <mm Bulk soil
Soil A
Control 123 ± 30 179 ± 99 198 ± 89
Farmyard manure 218 ± 61 196 ± 92 201 ± 83
Sewage sludge 170 ± 86 232 ± 90 159 ± 42
Soil B
Control 187 ± 65 172 ± 17 255 ± 86
Farmyard manure 227 ± 71 248 ± 72 295 ± 98
Sewage sludge 215 ± 60 189 ± 67 224 ± 60
∑8 PAHs*
< 3mm > 3-6 <mm Bulk soil
Soil A
Control 127 ± 56 111 ± 51 83.9 ± 7.5
Farmyard manure 154 ± 99 122 ± 55 145 ± 72
Sewage sludge 104 ± 72 151 ± 74 147 ± 84
Soil B
Control 153 ± 74 162 ± 98 188 ± 94
Farmyard manure 149 ± 72 163 ± 82 194 ± 71
Sewage sludge 137 ± 36 136 ± 35 164 ± 13
*∑12 PAHs represents sum of AN, BaA, BaP, BbFA, BkFA, BghiP, DBahA, FA, CHR, IP, PHE, and PY, ∑8
PAHs represent sum of BaA, BaP, BbFA, BkFA, BghiP, DbahA, CHR, and IP.
1000 J. SZÁKOVÁ ET AL.

Table 3. The contents of OCPs in the rhizosphere and bulk soils (µg kg
−1
of dry weight) according to the
individual soils and treatments; data are presented as mean ± standard deviation, n = 6.
HCB
< 3 mm > 3-6 < mm Bulk soil
Soil A
Control 0.49 ± 0.25 0.58 ± 0.29 0.67 ± 0.20
Farmyard manure 0.60 ± 0.19 0.48 ± 0.17 0.63 ± 0.07
Sewage sludge 0.77 ± 0.37 0.78 ± 0.41 0.95 ± 0.29
Soil B
Control 0.34 ± 0.16 0.41 ± 0.16 0.27 ± 0.13
Farmyard manure 0.33 ± 0.11 0.28 ± 0.10 0.26 ± 0.07
Sewage sludge 0.41 ± 0.09 0.43 ± 0.15 0.54 ± 0.33
γ-HCH
< 3 mm > 3-6 < mm Bulk soil
Soil A
Control 0.18 ± 0.14 0.31 ± 0.25 0.27 ± 0.22
Farmyard manure 0.18 ± 0.13 0.26 ± 0.10 0.21 ± 0.09
Sewage sludge 0.17 ± 0.10 0.24 ± 0.12 0.23 ± 0.18
Soil B
Control 0.13 ± 0.11 0.17 ± 0.12 0.24 ± 0.15
Farmyard manure 0.04 ± 0.02 0.14 ± 0.12 0.13 ± 0.07
Sewage sludge 0.09 ± 0.06 0.15 ± 0.07 0.15 ± 0.09
DDEs
< 3 mm > 3-6 < mm Bulk soil
Soil A
Control 2.38 ± 0.21 2.90 ± 0.94 2.51 ± 0.18
Farmyard manure 4.90 ± 1.33 5.23 ± 1.53 5.16 ± 1.23
Sewage sludge 3.33 ± 0.41 3.56 ± 0.78 3.24 ± 0.47
Soil B
Control 0.94 ± 0.07 1.06 ± 0.10 0.90 ± 0.13
Farmyard manure 0.69 ± 0.11 0.77 ± 0.12 0.59 ± 0.08
Sewage sludge 1.30 ± 0.19 1.48 ± 0.36 1.94 ± 0.50
DDDs
< 3 mm > 3-6 < mm Bulk soil
Soil A
Control 0.57 ± 0.13 0.80 ± 0.30 0.66 ± 0.07
Farmyard manure 1.10 ± 0.17 1.16 ± 0.32 1.29 ± 0.38
Sewage sludge 0.80 ± 0.20 0.78 ± 0.20 0.85 ± 0.33
Soil B
Control 0.29 ± 0.09 0.44 ± 0.32 0.30 ± 0.09
Farmyard manure 0.17 ± 0.07 0.16 ± 0.05 0.13 ± 0.02
Sewage sludge 0.28 ± 0.08 0.34 ± 0.14 0.39 ± 0.26
DDTs
< 3 mm > 3-6 < mm Bulk soil
Soil A
Control 3.50 ± 1.10 3.72 ± 1.10 3.96 ± 1.30
Farmyard manure 5.95 ± 1.52 6.05 ± 2.72 5.75 ± 3.34
Sewage sludge 6.29 ± 2.22 4.94 ± 1.18 5.89 ± 2.19
Soil B
Control 1.02 ± 0.61 1.35 ± 0.83 0.88 ± 0.65
Farmyard manure 0.58 ± 0.29 0.90 ± 0.18 0.59 ± 0.31
Sewage sludge 1.63 ± 0.39 1.85 ± 0.55 2.36 ± 0.76
ARCHIVES OF AGRONOMY AND SOIL SCIENCE 1001

Table 4. The contents of PCBs in the rhizosphere and bulk soils (µg kg
−1
of dry weight) according to the
individual soils and treatments; data are presented as mean ± standard deviation, n = 6.
∑tri-PCBs
< 3 mm > 3-6 < mm Bulk soil
Soil A
Control 0.03 ± 0.01 < 0.03 < 0.03
Farmyard manure < 0.03 0.03 ± 0.01 0.04 ± 0.03
Sewage sludge < 0.03 < 0.03 < 0.03
Soil B
Control 0.04 ± 0.01 0.05 ± 0.00 < 0.03
Farmyard manure 0.07 ± 0.00 0.06 ± 0.01 0.05 ± 0.03
Sewage sludge 0.08 ± 0.00 0.14 ± 0.00 0.07 ± 0.00
∑tetra-PCBs
< 3 mm > 3-6 < mm Bulk soil
Soil A
Control < 0.03 < 0.03 < 0.03
Farmyard manure < 0.03 < 0.03 0.03 ± 0.02
Sewage sludge < 0.03 < 0.03 < 0.03
Soil B
Control < 0.03 < 0.03 < 0.03
Farmyard manure 0.04 ± 0.00 < 0.03 0.03 ± 0.02
Sewage sludge 0.04 ± 0.00 0.12 ± 0.00 0.04 ± 0.00
∑penta-PCBs
< 3 mm > 3-6 < mm Bulk soil
Soil A
Control 0.05 ± 0.03 0.06 ± 0.04 0.04 ± 0.03
Farmyard manure 0.11 ± 0.04 0.06 ± 0.01 0.06 ± 0.03
Sewage sludge 0.10 ± 0.03 0.10 ± 0.04 0.08 ± 0.02
Soil B
Control 0.16 ± 0.03 0.14 ± 0.04 0.21 ± 0.03
Farmyard manure 0.15 ± 0.11 0.17 ± 0.01 0.21 ± 0.03
Sewage sludge 0.38 ± 0.03 0.17 ± 0.04 0.22 ± 0.02
∑hexa-PCBs
< 3 mm > 3-6 < mm Bulk soil
Soil A
Control 0.35 ± 0.08 0.35 ± 0.17 0.31 ± 0.09
Farmyard manure 0.58 ± 0.28 0.39 ± 0.06 0.40 ± 0.12
Sewage sludge 0.68 ± 0.15 0.72 ± 0.29 0.58 ± 0.11
Soil B
Control 1.44 ± 0.08 1.16 ± 0.17 2.02 ± 0.09
Farmyard manure 1.54 ± 0.88 1.71 ± 0.06 1.88 ± 0.12
Sewage sludge 2.03 ± 0.15 2.64 ± 0.29 2.17 ± 0.11
∑hepta-PCBs
< 3 mm > 3-6 < mm Bulk soil
Soil A
Control 0.10 ± 0.06 0.10 ± 0.06 0.09 ± 0.04
Farmyard manure 0.15 ± 0.07 0.12 ± 0.03 0.13 ± 0.05
Sewage sludge 0.20 ± 0.05 0.25 ± 0.16 0.18 ± 0.05
Soil B
Control 0.61 ± 0.06 0.46 ± 0.06 1.01 ± 0.04
Farmyard manure 0.60 ± 0.07 0.70 ± 0.03 0.88 ± 0.05
Sewage sludge 0.78 ± 0.05 1.10 ± 0.16 0.84 ± 0.05
1002 J. SZÁKOVÁ ET AL.

Table 5. The contents of PBDEs in the rhizosphere and bulk soils (µg kg
−1
of dry weight) according to
the individual soils and treatments; data are presented as mean ± standard deviation, n = 6.
∑tetra-BDEs
< 3 mm > 3-6 < mm Bulk soil
Soil A
Control 0.09 ± 0.02 < 0.08 < 0.08
Farmyard manure 0.08 ± 0.01 0.08 ± 0.01 0.09 ± 0.02
Sewage sludge 0.16 ± 0.02 0.15 ± 0.01 0.15 ± 0.00
Soil B
Control 0.08 ± 0.01 0.09 ± 0.02 0.09 ± 0.02
Farmyard manure 0.15 ± 0.07 0.18 ± 0.03 0.20 ± 0.09
Sewage sludge 0.36 ± 0.08 0.32 ± 0.13 0.22 ± 0.08
∑penta-BDEs
< 3 mm > 3-6 < mm Bulk soil
Soil A
Control 0.11 ± 0.04 0.11 ± 0.04 0.12 ± 0.05
Farmyard manure 0.15 ± 0.02 0.15 ± 0.02 0.15 ± 0.03
Sewage sludge 0.27 ± 0.05 0.24 ± 0.03 0.26 ± 0.04
Soil B
Control < 0.08 < 0.08 < 0.08
Farmyard manure 0.11 ± 0.04 0.11 ± 0.04 0.10 ± 0.05
Sewage sludge 0.22 ± 0.06 0.26 ± 0.08 0.28 ± 0.09
∑hepta-BDEs
< 3 mm > 3-6 < mm Bulk soil
Soil A
Control 0.07 ± 0.03 0.06 ± 0.02 0.08 ± 0.04
Farmyard manure 0.04 ± 0.02 0.12 ± 0.02 0.04 ± 0.03
Sewage sludge 0.09 ± 0.02 0.06 ± 0.02 0.06 ± 0.02
Soil B
Control < 0.03 0.05 ± 0.03 0.03 ± 0.01
Farmyard manure 0.04 ± 0.02 0.03 ± 0.01 0.04 ± 0.02
Sewage sludge 0.06 ± 0.03 0.07 ± 0.02 0.06 ± 0.02
∑octa-BDEs
< 3 mm > 3-6 < mm Bulk soil
Soil A
Control 0.09 ± 0.03 0.12 ± 0.08 0.19 ± 0.05
Farmyard manure 0.09 ± 0.03 0.09 ± 0.02 0.13 ± 0.04
Sewage sludge 0.12 ± 0.03 0.11 ± 0.05 0.10 ± 0.03
Soil B
Control < 0.08 0.18 ± 0.05 0.09 ± 0.05
Farmyard manure 0.10 ± 0.03 < 0.08 0.11 ± 0.07
Sewage sludge < 0.08 < 0.08 < 0.08
∑nona-BDEs
< 3 mm > 3-6 < mm Bulk soil
Soil A
Control 0.17 ± 0.08 0.32 ± 0.06 0.35 ± 0.07
Farmyard manure 0.61 ± 0.17 0.41 ± 0.05 0.80 ± 0.19
Sewage sludge 0.36 ± 0.13 0.53 ± 0.17 0.41 ± 0.10
Soil B
Control 0.42 ± 0.17 0.11 ± 0.08 0.69 ± 0.16
Farmyard manure 0.34 ± 0.15 0.10 ± 0.06 0.27 ± 0.05
(Continued)
ARCHIVES OF AGRONOMY AND SOIL SCIENCE 1003

indicated that the sewage sludge can be considered as the potential source of PBDEs in agricultural soils,
and the presence of higher brominated PBDE congeners indicated high stability and probably low
degradability of these congeners.
Table 6 presents the significant (p < 0.05) effects of the soil treatment on increasing the contents of all
the determined PFASs with control < farmyard manure < sewage sludge, whereas no effect of the soil
and rhizosphere section was observed. The PFASs are characterized by surface-active properties and high
chemical and thermal stability. These compounds are widely used (Buck et al. 2011)innumerous
products and applications (e.g., textiles, paper, plastics, cookware, carpets, cleaning agents, metal plating,
fire-fighting foams, etc.) and can be used in many human activities as well as in animal husbandry. Thus,
the presence of PFOSs and PFOA in both sewage sludge and farmyard manure can be expected.
Sepulvado et al. (2011) determined PFOS as the predominant PFAS in sludge-amended soils, with the
soil contents of this compound varying between 2 and 483 µg kg
−1
. In this experiment, the PFASs
contents were substantially lower, but higher values of ∑PFOS compared to PFOA was confirmed.
Soil enzymatic activity in the rhizosphere
In principle, farmyard manure application belongs to the family of reasonable measures to mitigate soil
degradation and, therefore, prevent the potential loss of bacterial diversity in the soil (Ding et al. 2016).
According to Wen et al. (2016), the long-term application of combined farmyard manure and/or mineral
fertilizers can minimize the mineral N losses via stimulation of root growth and improvement of the
N uptake by maize plants. Similar effects can be expected in the case of sewage sludge application.
Positive relationships between microbial communities and soil nitrate nitrogen concentration was
published by Ding et al. (2016). As mentioned above, because the organic fertilizer application rates
were based on the comparable nitrogen rates in the treated variants, the activities of soil enzymes
connected predominantly with the N-cycleinthesoilsweredeterminedintherhizospheresoil,i.e.,β-
glucosaminidase, arylamidase, and protease (Figure 1). These enzymes were chosen for the estimation of
potential changes in the microbial activity in the rhizosphere because of their role in N mineralization in
the soil.
Zhang et al. (2015) observed increasing activity of β-1,4-N-acetylglucosaminidase in manure
treated soils, with a positive correlation between the enzyme activity and soil organic carbon and
total nitrogen content. Similarly, arylamidase activity was enhanced in manure treated soil
(Reardon and Wuest 2016). The activities of β-glucosaminidase and arylamidase are related to
the N mineralization in soil, and significant correlation between the activities of these enzymes was
observed (Tabatabai et al. 2010). Arylamidase catalyzes the hydrolysis of N-terminal amino acids
from arylamides and, therefore, plays an important role in N mineralization (Acosta-Martinez and
Table 5. (Continued).
∑tetra-BDEs
< 3 mm > 3-6 < mm Bulk soil
Sewage sludge 0.13 ± 0.06 0.22 ± 0.11 0.23 ± 0.06
deca- BDE
< 3 mm > 3-6 < mm Bulk soil
Soil A
Control 0.19 ± 0.03 0.82 ± 0.15 0.50 ± 0.19
Farmyard manure 0.83 ± 0.25 0.37 ± 0.18 1.03 ± 0.19
Sewage sludge 0.17 ± 0.06 0.48 ± 0.14 0.16 ± 0.06
Soil B
Control 0.07 ± 0.03 < 0.03 0.08 ± 0.04
Farmyard manure 0.25 ± 0.06 0.17 ± 0.06 0.09 ± 0.03
Sewage sludge 0.23 ± 0.11 0.37 ± 0.07 0.50 ± 0.06
1004 J. SZÁKOVÁ ET AL.

Tabatabai 2000). The arylamidase activity correlates with microbial biomass carbon and nitrogen, as
well (Dodor and Tabatabai 2002). β-glucosaminidase catalyzes the hydrolysis of N-acetyl-b-d-glu-
cosamine residue from the terminal nonreducing ends of chitooligosaccharides (Ekenler and
Tabatabai 2004). Proteases are produced by soil microorganisms to recycle soil organic matter,
and their activities are regulated by many factors, including the presence of organic compounds of
plant and microbial origin (Vránová et al. 2013).
Our results showed higher activity of β-glucosaminidase and protease in soil A and higher
arylamidase activity in soil B (Figure 1). Arylamidase activity is sensitive to soil pH with greater
activity at neutral and/or slightly alkaline pH (Acosta-Martinez and Tabatabai 2000), and soil B is
characterized by near neutral pH in contrast to the acidic soil A. The potential effects of both
treatment and rhizosphere section were not significant, but the results indicated several trends.
The β-glucosaminidase activity tended to decrease with increasing distance from the roots in soil B,
whereas it remained unchanged in soil A. In this case, the role of ectomycorrhizal and/or arbuscular
mycorrhizal activity could be speculated (Corrales et al. 2017), but these predictions need to be
verified by further research. The protease activity tended to increase in the organic fertilizer-treated
soils compared to the control, as already published by many authors (for instance, Yuan et al.
2011). For arylamidase, the enhanced activity of this enzyme was observed in the rhizosphere soil
Table 6. The contents of PFASs in the rhizosphere and bulk soils (µg kg
−1
of dry weight) according to
the individual soils and treatments; data are presented as mean ± standard deviation, n = 6.
PFOA
< 3 mm > 3-6 < mm Bulk soil
Soil A
Control 0.17 ± 0.01 0.17 ± 0.10 0.12 ± 0.06
Farmyard manure 0.25 ± 0.01 0.25 ± 0.11 0.19 ± 0.05
Sewage sludge 0.34 ± 0.05 0.36 ± 0.04 0.31 ± 0.07
Soil B
Control 0.12 ± 0.05 0.14 ± 0.05 0.13 ± 0.06
Farmyard manure 0.19 ± 0.03 0.21 ± 0.03 0.18 ± 0.03
Sewage sludge 0.35 ± 0.06 0.37 ± 0.09 0.37 ± 0.10
Br-PFOS
< 3 mm > 3-6 < mm Bulk soil
Soil A
Control 0.04 ± 0.01 0.04 ± 0.03 0.05 ± 0.03
Farmyard manure 0.07 ± 0.00 0.08 ± 0.04 0.07 ± 0.03
Sewage sludge 0.13 ± 0.01 0.13 ± 0.03 0.14 ± 0.03
Soil B
Control 0.05 ± 0.02 0.05 ± 0.01 0.04 ± 0.02
Farmyard manure 0.07 ± 0.03 0.06 ± 0.02 0.07 ± 0.01
Sewage sludge 0.15 ± 0.04 0.15 ± 0.04 0.14 ± 0.04
L-PFOS
< 3 mm > 3-6 < mm Bulk soil
Soil A
Control 0.25 ± 0.06 0.25 ± 0.06 0.25 ± 0.08
Farmyard manure 0.39 ± 0.01 0.38 ± 0.15 0.37 ± 0.05
Sewage sludge 0.76 ± 0.02 0.76 ± 0.15 0.76 ± 0.11
Soil B
Control 0.20 ± 0.06 0.20 ± 0.04 0.19 ± 0.04
Farmyard manure 0.36 ± 0.08 0.35 ± 0.04 0.33 ± 0.03
Sewage sludge 0.65 ± 0.07 0.70 ± 0.11 0.68 ± 0.10
ARCHIVES OF AGRONOMY AND SOIL SCIENCE 1005

compared to the bulk soil, and the effect of the treatment was suggested by the results with
control < farmyard manure < sewage sludge.
Besides the effect of the organic fertilizers on the activity of soil enzymes, the soil microbiome
and, therefore, the enzymatic activity could be affected by the presence of organic contaminants.
For instance, the enhancement of protease activity in the presence of PAHs was proved by
Margesin et al. (2000). However, as mentioned above, the impact of the treatments on the PAH
contents was negligible, and therefore, the alterations in the soil enzymatic activity cannot be
related to the PAH levels. On the contrary, the decrease in soil enzymatic activity was observed by
Zhang et al. (2013) in PFOA-polluted soil. Thus, the possible adverse effect of the POPs on the soil
microbial activity should be taken into account. However, except for selected OCPs, the levels of
POPs determined were very low, and their impact on the soil microbial activity is negligible. The
adverse effect of OCPs on soil microbial communities and their impact on biochemical reactions
0
20
40
60
Control F. manure S. sludge Control F. manure S. sludge
Soil A Soil B
µg P-nitrophenol g-1 DW h-1
β-glukosaminidase
<3 mm >3-6< mm Bulk soil
0
20
40
60
80
Control F. manure S. sludge Control F. manure S. sludge
Soil A Soil B
µg TYR g-1 DW h-1
Protease
<3 mm >3-6< mm Bulk soil
0
5
10
15
Control F. manure S. sludge Control F. manure S. sludge
Soil A Soil B
µg 2-napthylamine g-1 DW h-1
Arylamidase
<3 mm >3-6< mm Bulk soil
Figure 1. The activities of the investigated soil enzymes; data are presented as mean ± standard deviation, n = 6.
1006 J. SZÁKOVÁ ET AL.

such as mineralization of organic matter, nitrification, denitrification, ammonification, redox reac-
tions, methanogenesis, etc., is widely known (Hussain et al. 2009). In this context, the soil enzyme
activities can be used as indicators of the soil microbiome response to pesticide contamination
(Floch et al. 2011). In this experiment, however, the results confirmed that the elevated values of
OCPs in the soils still do not reach values that are hazardous for organisms.
Conclusions
In model conditions using a rhizobox, the experiment confirmed the limited potential degradability of
POPs in soils, especially in the case of aged contamination when the pollutant residues are still present in
the soil a few decades after their ban. This statement was confirmed in the case of PCBs, and especially
OCPs, for which the levels of ΣDDTs exceeded the preventive values of these compounds in agricultural
soils. For POPs such as PBDEs, PFOS, and PFOA, the results showed that sewage sludge (and to a lesser
extent farmyard manure) could be a source of these contaminants in the soil without any significant
impact of these treatments on the degradability of these compounds in soil even in the rhizosphere
environment. Thus, the regular long-term applicationofsewagesludgecanresultintheregularincrease
of non-degradable POPs in soils. Although the contaminant levels do not represent any direct environ-
mental risk, enhancement of the ability of the soil microbiome to degrade POP residues should be taken
into account, such as through bioaugmentation of the soil with bacterial strains having good POP
biodegradation ability and/or improvement of microbial activity with nutrient addition. Moreover, the
soil organisms are exposed to whole cocktail of pollutants, and potential interactions of these com-
pounds should alter their response to the contaminants compared to the sole exposure. Therefore,
a more detailed description of the quantitative and qualitative characteristics of the soil microbiome as
well as a better elucidation of the mobility and potential bioaccessibility of the POPs will be necessary in
further research.
Acknowledgments
Correction and improvement of language was provided by Proof-Reading-Service.com Ltd., Devonshire Business
Centre, Works Road, Letchworth Garden City SG6 1GJ, United Kingdom.
Funding
This work was supported by the Grantová Agentura České Republiky [16-07441S].
ORCID
Jiřina Száková http://orcid.org/0000-0002-3390-6365
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