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Ecotoxicology and Environmental Safety 208 (2021) 111419

Contents lists available at ScienceDirect

Ecotoxicology and Environmental Safety


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

Research paper

Domestic wastewater infiltration process in desert sandy soil and its


irrigation prospect analysis
Caixia Liu a, Fulai Liu b, Mathias N. Andersen c, Gongming Wang d, Kun Wu a, Quanlin Zhao a,
Zhengfang Ye a, *
a
Department of Environmental Engineering, Peking University, State Environmental Protection Key Laboratory of All Materials Flux in Rivers, The Key Laboratory of
Water and Sediment Sciences, Ministry of Education, Beijing 100871, China
b
Department of Plant and Environmental Sciences, Faculty of Science, University of Copenhagen, Taastrup, Denmark
c
Department of Agroecology, Faculty of Science and Technology, Aarhus University, Tjele, Denmark
d
Department of Automation, Tsinghua University, Beijing 100084, China

A R T I C L E I N F O A B S T R A C T

Edited by Professor Bing Yan Although domestic wastewater and its reclaimed water are alternative water resources in arid region, investi­
gation of their negative effect must be done to prevent environmental pollution. In this paper, a short-term
Keywords: column experiment was conducted to simulate the infiltration process of wastewater in desert soil. Alfalfa was
Water reuse planted and irrigated with fresh water for control (CK), tertiary treated domestic wastewater (TTW), secondary
Desert soil restoration
treated domestic wastewater (STW) and raw domestic wastewater untreated (RW). The effect of wastewater
Vegetation recovery
application on desert soil, drainage and plant properties was evaluated. Experimental results demonstrated that
Infiltration
Alfalfa the tested desert soil has no soil structure, organic matter, nor microbial community while possess high infil­
tration rate. The use of wastewater significantly improved plant growth, and the biomass of TTW, RW, STW were
5.5, 4.3, 2.9 times of CK. The infiltration rate of water in bare soil was high (high to low: TTW, CK, RW, STW),
while plant growth reduced infiltration rate (ca. 40% with TTW and RW). Wastewater irrigation and plant
growth decreased soil zeta potential, while increased formation of aggregates and bacterial abundance and di­
versity in soil. Top soil (0–30 cm) accumulation of nitrogen (N), phosphorus (P), organic matter and E. coli was
evidenced and all could go down to deep soil and drainage with constant wastewater use. It was concluded that
domestic wastewater had big potential in desert soil vegetation recovering and function restoration. Neverthe­
less, the N, salt, P and organic matter and E. coli in wastewater could give rise to desert soil and groundwater
contamination if improper treatment was used.

1. Introduction result, huge amount of domestic wastewater is produced. Domestic


wastewaters mainly come from food preparation, kitchens, baths, rest­
The desert lands are characterized as having large evaporation, room usage, and laundry (Ma et al., 2019). Due to low population
strong winds, sparse vegetation, low precipitation and low groundwater density, lack of reliable and easy to-implement and low-cost technology
level (Gross, 2018). While the desert soil usually has low organic matter and treatment facilities to collect, treat and reuse of wastewater in an
content, course soil texture, no soil aggregation and poor water and optimal manner, 11% of the total cultivated area in the world is using
fertilizer holding capacity (van Asperen et al., 2014; Laghari et al., untreated wastewater for irrigation (Thebo et al., 2017). The domestic
2015). The shortage of water limited plant growth and yield; the wind wastewater from approximately 96% of the villages in rural areas of
erosion and rare rainfall and uneven rainfall distribution in time and China and 50% of the wastewater in small city is usually untreated and
space has led to frequent dust storms, which seriously affect human directly discharged into nearby surface water bodies or to the soil, or
activities such as traffic and construction in these areas. ground, causing serious environmental problems (Zou et al., 2012; Wu
On the other hand, the demand for freshwater has sharply increased et al., 2013; Han et al., 2016). Most of the domestic wastewater is being
due to increased population and development of human society. As a recycled and re-used for agricultural purpose due to lack of freshwater,

* Corresponding author.
E-mail address: yezhengfangiee@163.com (Z. Ye).

https://doi.org/10.1016/j.ecoenv.2020.111419
Received 26 July 2020; Received in revised form 24 September 2020; Accepted 25 September 2020
Available online 16 October 2020
0147-6513/© 2020 Elsevier Inc. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
C. Liu et al. Ecotoxicology and Environmental Safety 208 (2021) 111419

especially in arid and semi-arid area (Hamilton et al., 2007). Domestic replicates.
wastewater has a high nutritive content of organic matter, macro- and
micro-nutrients, especially N and P that could promote crop production 2.1. Sampling area and soil properties
(Kiziloglul et al., 2007), benefit soil structure and fertility (Lubello et al.,
2004; Xu et al., 2010; Adrover et al., 2012; Yuan et al., 2019), and profit The desert soil used for this experiment was taken from Kubuqi
soil organic matter accumulation (Angin et al., 2005; Manas et al., Desert. The Kubuqi Desert is located in Inner Mongolia, China. It is
2009), while has relatively low contaminates compared with industrial bordered by the Yellow River to the west, north and east, having an area
wastewater. of 1.45 × 104 km2 and an altitude of 1200–1400 m above sea level. The
Reuse of wastewater has already been practiced for centuries in arid annual precipitation is approximately 150–400 mm, 60%− 70% of
and semi-arid countries such as Israel, Kuwait, Saudi Arabia, Libya, which occurs from June to October. Annual sunshine hours are
Egypt, and Tunisia (Shelef, 1991; Abdel-Shafy et al., 2003; Travis et al., 3000–3200 h. Annual evaporation is 2100–2700 mm. Strong winds
2010). And around 10% of the people globally are using untreated occur frequently in spring moths (March-June), and the average wind
wastewater for crop production(Khalid et al., 2018). Using wastewater velocities 3–4 m/s. Soil was randomly collected from surface to a depth
for forest irrigation and sand-fixation was also being tried in northwest of 1 m, mixed evenly and air dried. The soil is sand, with 94.5% sand,
of China. However, wastewater reuse may cause environmental risk of 0.5% silt and 5% clay, with a particle size distribution of 86.3% between
elevated salinity and heavy metal contamination (Abdel-Shafy et al., 0.05 and 0.2 mm, water content 0.8%, pot holding capacity 15.38% (v/
2003; Mohammad and Mazahreh, 2003; Angin et al., 2005; Gupta et al., v), organic matter content 0.02 g/kg, total N 0.012 g/Kg, Olsen P 1 mg/
2010; Frenk et al., 2014), soil compaction, and input of pathogens, vi­ kg, water soluble P 0.27 mg/kg, mineral N (NH+ 4 0, NO2 0 and NO3 0.04)
– –

ruses, and protozoa (Akponikpe et al., 2011) and nitrogen (N), phos­ mg/kg, pH 8.19, specific gravity 2.64 g/cm3, bulk density 1.47 g/cm3,
phorus (P) and endocrine(Katz et al., 2009; Huang et al., 2019)into porosity 44.25%, seepage velocity 15.37 mm/min, soil aggregates
soil and groundwater, as well as the change of the soil microbial com­ (≥0.25 mm) 0 g. No fertilizer was applied to the above soil.
munity (Guo et al., 2018).
The main processes of contaminant attenuation in wastewater reuse
2.2. Wastewater properties
include physical filtration, sorption onto the soil particle, microbial
biodegradation and plant uptake. The environmental effect, e.g. changes
The wastewater used in current experiment was sediment effluent of
of soil properties, plant growth, bacterial communities and change of domestic wastewater collected from wastewater treatment plants
soil enzyme activity should be monitored in desert soil following located in Peking University. The choose of wastewater from university
wastewater application to ensure that the final product quality, soil and was based on the consideration of simple personnel composition and
groundwater health and human protection are not compromised (Jung source of wastewater inlet in the studied area. They were RW having no
et al., 2005). treatment but through primary settling tanks; STW from aeration tank;
In recent years, although pollutants in wastewater can be predicted TTW was wastewater effluent from outlet pipe and CK with tape water.
with a higher accuracy (Wang et al., 2020), wastewater management The above treated wastewater was collected from membrane bio-reactor
and sustainable challenge remains for further research. A critical (MBR) process. As the wastewater collected from aeration tank had mass
knowledge gap still exists on how to treat and reuse domestic waste­ amount of microbes and metabolites, the suspended solid of STW was
water in undeveloped area in northwest China, and how ecosystems higher than TTW. The heavy metal contained in the above RW was lower
(groundwater, plant and soil) respond to domestic wastewater irrigation than national standard for drinking water. The detected heavy metal in
at present. The study of infiltration of wastewater in desert soil could be current RW was Cu, Zn, As, Cd, Pb with 0.006, 0.004, 0.002, 0.000,
used for local wastewater management and advice. Thereupon, this 0.000 ug/L, respectively. Basic analysis of the wastewater was listed in
study aimed to investigate the environmental health risks to soil and Table S1.
groundwater associated with short term wastewater disposal practices.
In a controlled environment, domestic wastewater of different treatment
2.3. Experimental design
levels was applied to desert soil and followed Alfalfa planting. The
infiltration process of wastewater in desert soil was simulated; the effect
2.3.1. Wastewater infiltration in desert soil
of domestic wastewater application on soil, drainage and plant growth
The infiltration of wastewater in desert soil was simulated in an in­
properties were evaluated; and the soil physical, biochemical properties
door experiment with columns. A ponding height of 5 cm above the soil
were analyzed; the effect of soil, plant and microbes on wastewater
surface in column was maintained by Mariotte reservoir placed over a
contaminant interception, uptake and decomposition were estimated.
digital balance throughout the experiment. The infiltration depth and
quantity were recorded every 10, 30, 60 s for calculation of cumulative
2. Material and methods
infiltration and infiltration rate. Then the drainage was collected at 10
min, 20 min, 40 min, 1 h, 2 h, 1 day, 2 day, 3 day, 4 day.
Column experiments were carried out in a climate-controlled room
Philips infiltration equation was applied to fit infiltration data,
in Peking University, China using cylindrical columns to simulate the
where sorptivity (S) and constant (A) was obtained by fitting the infil­
wastewater transport in desert soil with a volume of 1.38 × 103 cm3 (4
tration rate values to the Philips equation in a non-linear regression
cm in inner-diameter and 110 cm deep). An elution bottle with constant
function:
pressure was connected to the inlet opening where 10 cm from the top of
the column. Sampling holes with a diameter of 1 cm were arranged I = St1/2 + At (1)
every 10 cm alongside of the column. The bottom of column was ended
with 1 cm diameter opening for drainage. Each column was filled with where I represent the cumulative infiltration (cm), S represents the
dry soil to a dry bulk density of 1.43 g/cm3. Experiment was conducted sorptivity (cm/min1/2), and A represents a constant that is theoretically
from July 2019 to October 2019. equal to the saturated hydraulic conductivity multiplied by a certain
The desert soil was irrigated with 4 types of water: tertiary treated number.
domestic wastewater (TTW) and secondary treated domestic wastewater The K(θ) (unsaturated hydraulic conductivity) was obtained when
(STW) and raw domestic wastewater untreated (RW) freshwater for an infiltration rate of 60 min was recorded.
control (tap water, CK). The experiments were divided into two stages:
infiltration with wastewater at first, following planting of Alfalfa. A 2.3.2. Planting of Alfalfa
complete randomized design was conducted with 4 water treatments, 3 Alfalfa (Medicago sativa L.) seeds were pre-germinated by putting

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C. Liu et al. Ecotoxicology and Environmental Safety 208 (2021) 111419

seeds on top of wetted paper (humidity at 70%− 75%), and cultured in Composite soil samples were pre-soaked for 10 min in the distilled water
dark at 25 ℃. When sprout came out, three germinated seeds were and afterwards, a 250 g composite soil sample was put over a nest sieve
planted in column soil. One plant with similar size was kept when they of diameters 0.25 mm and get oscillated vertically with 4 cm amplitude
emerged from soil. The plants were irrigated to a 90% pot holding ca­ at the rate of 1 oscillation/s for 20 times in water. The wet soil left on
pacity in each column by drip irrigations every second day. The drip sieve was dried at 65 ℃ to constant weight and weighted. Soil ζ-po­
tubes used had an inner diameter of 3.5 mm, and no clogging was evi­ tential was measured with topsoil of 0–10 cm depth using zeta SIZER
denced. The top of the columns was equipped with metal-halide lamps (Malvern Nano-ZS90).
providing extra light for solar radiation. The plant growth condition was
set as 22/18 ℃ day/night temperature, 14:10 h photoperiod and> 2.4.3. Chemical analysis of soil and water
500 µmol/m2/s photosynthetic active radiation. The chlorophyll of the The NO–3, NO–2 and NH+ 4 were measured at each sampling time by
leaves was measured with Chlorophyll Meter SPAD-502 plus one day pooled supernatants after sequential extractions of 1 g of fresh soil
before harvest. Soil samples were sterilely collected when plants were shaken with 1 M KCl for 1 h at 20 ℃ followed by centrifuging for 10 min
harvested. The impact of plant growth on infiltration was also measured at 10,733 g with a spectrophotometer (HACH, DR-5000) with NO–3 at
with water table maintained at 5 cm above the soil surface in column by 220 and 275 nm), NO–2 at 540 nm and NH+ 4 at 420 nm (Chinese Envi­
using the elution bottle to provide constant presser. ronment standards HJ/T 346–2007). Before NO–3, NO–2 and NH+ 4 analysis,
all the water samples were filtered by 0.45 µm water membrane. The
2.3.3. Harvest filtrates were analyzed for NO–3, NO–2 and NH+ 4 , total organic carbon
Harvest occurred 72 days after transplanting. Soil samples were (TOC), pH, salinity (soluble salt content), total P (TP) and water soluble
collected from side of soil column with 0 cm, 10 cm, 30 cm, 50 cm, P (WSP) and the data was obtained by averaging through repeated
70 cm, 90 cm at harvest day. The plants leaf area was calculated: sampling. TOC was measured with total organic carbon analyzer TOC-V
0.83 × length × width (cm) × number of leaves. Total biomass was the CPN SHIMADZU. The pH value was measured by pH meter (Hanna
sum of shoot fresh mass and root fresh mass; plants were dried at 60 ◦ C Corporation, Italy) in a 1: 2.5 (w:v) soil to deionized water ratio. Salt
until constant weight to obtain dry biomass; root properties were content was measured by oven dry. TP by the persulfate digestion
measured in each layer with root diameter and root volume by overflow method with a spectrophotometer at 890 nm after the addition of
of water; root weight density and root length density were calculated: vanadate molybdate (Sissingh, 1971). WSP in the soil was measured at
each harvest time in pooled supernatants after two sequential extrac­
RDw = W d /vs (2)
tions of 1 g of fresh soil shaken with 50 mL of deionized water for 1 h at
20 ◦ C followed by centrifuging for 30 min at 10,733 g at 20 ◦ C and was
RDL = Lr /vs (3)
analyzed with a spectrophotometer at 890 nm after the addition of
/
Lr = 4V i πd2i (4) vanadate molybdate (Sissingh, 1971). Soil urease activity was deter­
mined as described by Kandeler and Gerber (1988). Briefly, a fresh soil
RDW root weight density (g/cm3); RDL root length density (cm/cm3); Wd sample equivalent to 5.0 g oven-dry weight was added with 2.5 mL of
dry root weight (g); vs soil volume (cm3). Lr root length in layer i (cm); Vi urea (720 mM) and 20 mL borate buffer (pH 10) and incubated at 37 ◦ C
root volume in layer i (cm3); di average root diameter in layer i (cm). for 2 h. Then, after adding 50 mL of a mixture of KCl (1 M) and HCl
(0.01 M) solution, the mixed solution was shaken for 30 min (25 ◦ C) at
125 rpm. The suspension was filtered, and the ammonia concentration
2.4. Measurements, calculations and statistical analyses in the filtrate was measured photometrically at 690 nm. Urease activity
was expressed as the amount of NH3-N produced per unit mass of soil per
2.4.1. Microbial analysis of soil 24 h (μg N/g dry soil/ 24 h).
The soil and water samples that used for counting the number of the
total bacteria and Escherichia coli (E. coli) were analyzed immediately 2.4.4. Statistical analysis
after sampling (within 12 h). Soil samples were diluted in a sterile vial Sampling data was statistically compared between treatments by
with 0.005 M pyrophosphate buffer (pH = 7) for bacterial extraction, one-way ANOVA, Tukey test analysis of variance at the significance
afterwards, the diluted samples were shaken for 1 h to take supernatant level of 0.05 using SAS (9.3). The correlation analysis was done with
and then the total bacteria were measured by the pour plate method CORR procedure in SAS (9.3). The microbial community analysis was
using Luria–Bertani Agar (LB) while E. coli Tryptone Bile X-glucuronide performed using the online platform of Majorbio I-Sanger Cloud
Agar (TBX). Platform.
The soil samples for microbial community analysis were collected
10 cm from top of the soil columns and were stored at − 20 ◦ C. The 3. Results and discussion
genomic DNA of the samples was extracted and purified using soil DNA
kits (Omega Bio-tek, Norcross, GA, USA). The primers used for microbial 3.1. Wastewater infiltration with or without plants
diversity analysis was 338F (5′ -ACTCCTACGGGAGGCAGCAG-3′ ) and
806R (5′ -GGACTACHVGGGTWTCTAAT-3′ ) provided by Illumina The infiltration rates of different water treatments in sand soil grown
MiSeq. The PCR reactions was with 3 min of denaturation at 95 ◦ C, 27 with or without plants were shown in Fig. 1. Infiltration is part of the
cycles of 30 s at 95 ◦ C, 30 s for annealing at 55 ◦ C, and 45 s for elon­ terrestrial water cycle and it is the process of water penetrating into the
gation at 72 ◦ C, and extension for 10 min at 72 ◦ C. The PCR products soil profile. This process can be affected by water supply and soil
were extracted from a 2% agarose gel and purified using the AxyPrep permeability (Ebel and Moody, 2013) with soil permeability is a factor
DNA Gel Extraction Kit (Axygen Biosciences, Union City, CA, USA). being affected by soil texture, structure, water content and mineral
Purified amplicons were paired-end sequenced (2 × 300) on an Illumina composition. In current experiment, the initial infiltration rates were
MiSeq platform (Illumina, San Diego, USA) according to the standard differentiated rapidly and unstable in the first 3 min. By irrigating with
protocols by Majorbio Bio-Pharm Technology Co. Ltd. (Shanghai, either wastewater or tape water, a high infiltration rate was found in
China). bare soil. By comparing the stable infiltration (by skipping the first
5 min) with a constant water table, the highest infiltration rate was
2.4.2. Physical analysis of soil found in TTW soil, followed by CK, RW and STW (Fig. 1) when no plant
Water stable soil aggregates bigger than 0.25 mm were separated via was grown in soil. The lower infiltration rate with STW and RW treat­
wet-sieving procedure as described by Kemper and Chepil (1965). ments was attributed to the suspended solid particles in wastewater

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Fig. 1. Infiltration rates (cm/min) of sand soil subjected to different water treatments (raw wastewater, RW; secondary treated wastewater, STW; tertiary treated
wastewater, TTW; tape water, CK) (values are means).

water. And the largest K(θ) value (which is almost equivalent to the significantly correlated to root biomass with R2 = 0.82 and R2 = 0.72,
constant infiltration rate) in TTW (Table 1) showed that the chemical in respectively. These results indicated that the decrease of stable infil­
wastewater also affected K(θ) during their flow through pores in sand. tration rate was caused by root growth, which was contrary to what was
As it is known that the hydraulic conductivity correlates to the fluid normally found in cultivated soil where high density root system in­
density and inversely related to the fluid viscosity (Tindall et al., 1999). crease soil matrix water infiltration capacity via vital channels for water
When subjected to salinity water with Na+, cultivated soils tend to infiltration by forming macropores and root channel (Liu et al., 2019).
disperse and break down into smaller aggregates, giving rise to a surface Moreover, the root exudates and their physical contact with soil parti­
seal and a reduction in infiltration rate through the exchange and cles could cause soil physical, chemical, and biological alterations,
equilibrium processes between the soil soluble and solid thus unstable of which in turn impact the soil permeability (Bronick and Lal, 2005).
soil aggregates and/or the entrapment of air (Raine et al., 2007). But this The Philip infiltration parameters and relates statistics were pre­
may vary among soils, as the clay content is different. As to sand soil, sented in Table 1. The Philip infiltration model was successfully fitted to
where no soil aggregation exists in original soil, the salt facilitated raise the infiltration data of different water treated sand soil. Growing plants
of solution density may contribute the increased infiltration rate in TTW increased sorptivity compared to soil without plants, except with RW
treatments. Whilst the RW and STW treatments had higher organic treatments. For example, the sorptivity of pure water increased from
matter content which may contribute to the formation of soil hydro­ 12.1 to 14.68 cm/min1/2. Sorptivity describes the tendency of the me­
phobicity following wastewater irrigation (Wallach et al., 2005). Be­ dium to absorb and transmit the solution by capillary action (Hall and
sides, the infiltration rate tends to decrease due to crust formation on the Hoff, 2012), thereby, affecting the infiltration rate of liquid into soil.
surface of sand soil following wastewater irrigation especially in STW Smaller pores hold more water by capillary force (Fredlund and Xing,
and RW treatments. 1994) comparing to the large pores in sand soil. The cutting off of
The infiltration rate was detected again before harvest of plants. It capillary force could inhibit salt transporting to surface of soil. Besides,
showed that plants growth significantly reduced the permeability and the increased sorptivity may also imply an increased water holding ca­
extended the time water efflux from the bottom of soil column from pacity after plant growth.
25–37 min to 37–52 min (Fig. 1), especially with TTW and RW treat­
ments. The stable infiltration rates with those two treatments were
3.2. Analysis of drainage before planting of Alfalfa
reduced by ca. 40%. Correlation analysis showed that both the time of
water run out of soil column and the decrease of infiltration were
Fig. 2 presented the dynamic exudate analysis from soil column

Table 1
The fitting parameters of soil hydraulic properties. A: a constant in Philip equation; K(θ): unsaturated hydraulic conductivity, observed during infiltration process with
different water treatment (tape water, CK; raw wastewater, RW; secondary treated wastewater, STW; tertiary treated wastewater, TTW) in desert soil with or without
plants.
Without plant With plant

Sorptivity (cm/min1/2) A (cm/min) Adj. R2 K (θ) (cm/min) Sorptivity (cm/min1/2) A (cm/min) Adj. R2 K (θ) (cm/min)

CK 12.10 1.16 0.992 1.52 14.68 0.85 0.994 1.43


TTW 7.28 2.14 0.999 1.71 8.97 0.79 0.996 1.08
STW 7.95 1.1 0.993 1.28 8.35 0.71 0.998 0.95
RW 10.5 1.08 0.994 1.43 9.94 0.44 0.997 0.82

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C. Liu et al. Ecotoxicology and Environmental Safety 208 (2021) 111419

Fig. 2. NH+4 and NO3 concentration (mg/L), total phosphorus and total organic carbon (TOC) concentration (mg/L), total salt (mg/L) and E. coli (cfu/mL) con­

centration in effluent collected from the bottom of soil column that subjected to different water treatments (raw wastewater, RW; secondary treated wastewater,
STW; tertiary treated wastewater, TTW; tape water, CK) treatments (values are means).

during 4 days’ wastewater treatments. As shown in Table S1, initially concentration with initial P level in wastewater, since P has higher
NH+ 4 was the main form of N in RW. Yet, the N form changed from NH4
+
reactivity than N, and binds easily to soil constituents (Frossard et al.,
to NO–3 in TTW, and partially changed to both NH+ 4 and NO3 in secondary

2000; Liu et al., 2015, 2017, 2018). The total organic carbon in effluent
treated wastewater (STW). The NO–2 data was not presented, as the NO–2 showed no sign of reaching similar level with initial concentration in
content in all wastewater and effluent was negligible. Both NH+ 4 and wastewater within 4 days’ infiltration (Fig. 2), which was finally only
NO–3 in wastewater were ready to precipitate downward to the bottom about one third of initial level both with RW and STW. The reduction of
soil or groundwater as the sandy soil used here has little colloids and the organic carbon was a result of organic matter accumulation on top layer
transportation of NH+ 4 and NO3 in soil solution is easy. As a result,

of soil column (Fig. S1).
groundwater N content in wastewater in irrigated area would be high. All wastewater treatments had similar salinity (Table S1). The sol­
The NH+ 4 content in effluent increased rapidly between 2 h and 24 h, and uble salt flued out easily from soil column, and a rapid raise of salt
eventually reached a similar content with influent of RW and STW concentration was evidenced from the start of the infiltration process. A
(Fig. 2), which indicating that the NH+ 4 in raw wastewater could be constant salt concentration was obtained with most of the treatments
partly intercepted by sand. Whilst, there was no NH+ 4 in effluent in CK within a day (Fig. 2). Due to large E. coli content especially with RW and
and TTW, due to no NH+ 4 input. Differ from NH4 , NO3 from soil column
+ –
STW, E. coli in wastewater could pollute soil and groundwater as it could
effluent decreased rapidly between 10 min and 40 min in all water go down to deep soil with water (Fig. 2).
treatments, and reached a lower NO–3 content within 4 days compared
with STW influent. The intercepted NH+ 4 transformed to NO3 in soil and

3.3. Soil interception of wastewater elements after harvest
this part of N can rapidly flow out of soil column with water and give rise
to possible environmental and health problems. And this was also re­
Figs. 3 and Fig. S1 showed soil interception of wastewater elements
ported in previous work by Tran and Zuo et al. (2014, 2018).
after 4 days’ wastewater treatments and 72 days’ plant growth. No NH+ 4
The total P concentration in effluent also increased with time (Fig. 2).
was detected in soil samples as NH+ 4 in soil can easily transformed to
Yet, compared to NH+ 4 , it takes longer time for P to reach a similar
NO–3 with help of microbes. NO–3 showed stepwise decrease from top to

5
C. Liu et al. Ecotoxicology and Environmental Safety 208 (2021) 111419

Fig. 3. Soil NO–3, water soluble phosphorus total salt concentration (mg/Kg) and pH collected from different depth of soil column that subjected to different water
treatments (raw wastewater, RW; secondary treated wastewater, STW; tertiary treated wastewater, TTW; tape water, CK) (values are means).

50 cm of the soil column in wastewater irrigated soil, e.g. it was significant larger amount of E. coli while the total bacteria quantity in
18.5 mg/Kg in the surface layer and 1.9 mg/Kg in the bottom layer in both RW and TTW were large, particularly in the layer of 0–30 cm. This
RW treated soil. TTW and STW treatments had relatively less NO–3 was in accordance with the significant high E. coli in RW (Table S1).
intercepted in top soil compared with RW treatments. Compared with N, While the high total bacteria quantity in TTW might be a result of root
water soluble P also decrease with soil depth with wastewater treated growth.
soil and was concentrated in top soil lays of 0–10 cm. There was also salt
accumulation with wastewater treatments in top soil lays, especially 3.4. Plant growth properties
with RW and STW. Results also indicated that wastewater disposal to
desert sandy soil could result in elevated pH level regardless of the level The plant growth properties of biomass, root weight density and
of wastewater treated. Increase of soil pH following wastewater or Chlorophyll were shown in Table 2 and Fig. 4. The establish of plant
greywater application has also been demonstrated in previous research biomass can increase soil nutrient stocks through plant return and
work (Pinto et al., 2010; Siggins et al., 2016). decomposition. Alfalfa (Medicago sativa L.) is one of the most important
The biogeochemical activity of microbiota is considered the most forage legumes in the world and it is widely planted in northwest China.
important aspect of soil quality, with implications in soil fertility and It has deep root system and can serve as high-quality feed with high
quality. An increased biological activity was normally connected to the protein content. The legume growth requires sufficient water and
grown number of hot spots (Nannipieri et al., 2003), such as aggregates, nutrient for adequate growth, and the wastewater irrigation compensate
particulate organic matter and root rhizospheres. The mineralization of this limitation in desert lands. Thus, the planting of Alfalfa may intercept
soil organic matter is mainly accomplished by hydrolytic enzymes such part of the nutrients in wastewater and improve soil quality and increase
as sucrase, urease. Urease is involved in cycling of N as it catalyzes the carbon and N pools in arid loess land. The use of wastewater as irrigation
release of NH+4 from urea (Caldwell, 2005). As the bare desert soil had no water for resource and energy recovery (e. g. plant biomass) has been
organic matter content, the total organic carbon was analyzed to successfully practiced in production of olive trees (Pedrero et al., 2020),
determine accumulation of organic compounds as a result of wastewater sugar beet, alfalfa, maize, napier grass, sunflower and canola (Shilpi
irrigation. With wastewater treatment and plant growth, soil urease and
organic matter showed stepwise decrease with soil depth and was
Table 2
mainly active in the soil lays of 0–30 cm. RW and STW soil had a higher Plant total biomass (g/plant), leaf area (cm2/plant) and Chlorophyll (SPAD) as
urease and organic matter content compared to TTW soil. affected by water treatments (tape water, CK; raw wastewater, RW; secondary
The microbiology of soils is an important consideration for waste­ treated wastewater, STW; tertiary treated wastewater, TTW). Values are means
water reuse. Soil microbes connected closely with organic matter (n = 3). Significant differences are indicated by letters: Different small letters
mineralization and are potential indicators of soil health (Yang et al., within a column indicate significant difference due to irrigation method at
2017). When an increase in the microbial biomass was observed, it may P < 0.05.
have been due to the supplying of additional organic C and other nu­ Total biomass Leaf area Chlorophyll (SPAD)
trients by wastewater (Fatta-Kassinos et al., 2011). Moreover, pathogens
CK 12.46d 3.86c 21.82c
in wastewater may survive in soil and potentially compromise public TTW 69.02a 102.52a 58.87a
health. Soil E. coli was measured as a surrogate of pathogen persistence STW 36.24c 17.32bc 37.1b
in the soil. Among all wastewater, only RW irrigated soil intercepted RW 53.49b 105.54a 61.77a

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C. Liu et al. Ecotoxicology and Environmental Safety 208 (2021) 111419

Fig. 4. Root weight density (mg/cm3) and length density (cm/cm3) alongside soil column that subjected to different water treatments (raw wastewater, RW;
secondary treated wastewater, STW; tertiary treated wastewater, TTW; tape water, CK) (values are means).

et al., 2019) and microalgae (Nagarajan et al., 2020). The extraction of microbial DNA failed in tape water irrigated sand
As showed in Table 2 and Fig. 4, wastewater reuse significantly soil. Thus, the CK treatment was not included in the following microbial
enhanced plant growth, which may largely due to the nutrient contained community analysis. It can be seen that the coverage was close to 100%
in wastewater (Kiziloglu et al., 2008). N and P is the first and second (Table S2), suggesting that the sequencing results would be a good
major nutrient element for plant growth. Thus, the significant high reflection of microbial diversity. The detected sequence number was
content of N and P in TTW and RW (Table S1) explained the great plant also in accordance with total bacteria in Fig. S1. The Alpha diversity
growth promotion within these treatments. The biggest total biomass indices of Sobs, Ace and Shannon showed community richness and
was with TTW treatments, followed by RW, then STW and CK. The leaf community diversity respectively. Largest diversity was found in RW,
area and Chlorophyll were similar in TTW and RW treatments and which then TTW soil, and was smallest in STW soil, indicating a decreasing
were significantly larger than STW and CK. Results indicated that plant trend of OTU (Operational Taxonomic Units) level from RW to TTW and
can hardly grow in desert soil, due to its poor nutrition condition; whilst to STW.
the wastewater irrigation met the basic plant growth needs. Comparing The predominant bacteria at both phylum and genus levels by
with STW plants, both TTW and RW plants grow strongly. Rotting roots taxonomic analysis were shown in Fig. S2. In all wastewater irrigated
in STW treatments was observed in the layer of active sludge sediment soils, Proteobacteria, Actinobacteria, Chloroflexi, Bacteroidetes were
later in plant growth stage which also kept the roots from growing into the dominant phyla with Proteobacteria amounted for the largest pro­
deeper soil layers (Fig. 4). portion. Whilst, the most abundant genera in wastewater irrigated soils
Plant roots grown down to 90 cm of the soil column in all treatments were Pseudomonas, Allorhizobium-Neorhizobium-Pararhizobium-Rhizo­
after 72 days (Fig. 4). The greatest root weight and length density was bium, Brevundimonas, Acidovorax, Ellin6055 (Figs. S2 and 5). It also
found with TTW, which was ca. 3 times that of RW, 10 times that of STW indicated that STW had relatively low diversity than TTW and RW, as
and 27 times that of CK. The data suggested that to use wastewater, TTW Pseudomonas, Allorhizobium-Neorhizobium-Pararhizobium-Rhizobium,
might be the best choice as it promoted root growth which may subse­ Brevundimonas, Acidovorax summed up for 51.1% of total reads. Rhizo­
quently contribute to magnificent desert soil fixation. The tested soil in bium is one of six plant-associated species within family Rhizobiaceae,
current experiment had a low water holding capacity, thus the irrigated and is mostly associated with plant promoting characteristics (Rodri­
water could easily go down to the bottom of column soil, leading to an guez and Fraga, 1999) and it was found in all wastewater irrigated soils.
uneven distribution of water. Previous studies have shown that plant Root exudates such as sugars, organic acids, amino acids, mucilage, etc.
root adapts to drought stress, with not only a big shallow root biomass to are vital driving force in recruiting rhizosphere microbiomes (Qu et al.,
take surface water and also a deeper rooting system to find deep water 2020). Alfalfa roots is well known that can assemble rhizobium and form
(Ward et al., 2013). In current work, root weight and length density was rhizobium-legume symbiosis. The symbiosis plays an important role in
significantly greater at the 0–20 cm soil layer than the other soil layers nitrogen fixation, improve plant growth and biocontrol for several plant
(p < 0.01; Fig. 4) in CK and STW treatments; while the root weight and diseases (Das et al., 2017). This may explain the existence of Rhizobium
length density in RW treatments was great both at 20–40 cm and in all soils. As Acidovorax was potentially plant-pathogenic to many
80–100 cm; and the root weight and length density in RW treatments economically important plants, such as rice, oats, corn, millet, sugar­
was greatest at 60–100 cm, indicating extensive root growth into a deep cane, and foxtail (Brigida et al., 2016), and which may contribute to the
soil layer to take up water with TTW and RW treated plants, even though rotting roots in STW treatments and lead to reduced plant growth.
a longer term studies are warranted. The cluster heatmap with two-dimensional matrix was generated to
analyze the similarities and differences of community at genus level
3.5. Soil microbial community abundance and diversity after harvest (Fig. 5). The cluster analysis was conducted on the distance matrix of soil
microbial samples and a hierarchical clustering tree of microorganisms
The microbial sequencing information and community diversity under different wastewater treatment was demonstrated in Fig. 5 in
characteristics of soil irrigated with different wastewater were presented order to study the similarities and differences of microbial community
in Table S2. The composition of microbial communities plays important composition. It showed that the TTW and RW soils which had less dif­
role in soil functioning. Almost 80–90% of the microorganisms inhab­ ference in total plant biomass had more similarity in microbial com­
iting soil are on solid surfaces by interacting factor of extracellular munity structure, and clearly distinct from the STW soil. The results of
polysaccharides produced by microbial cells. Clearly, the soil used in Figs. S2 and 5 showed that wastewater application altered the bacterial
current experiment is not a good microhabitat as there is no aggregates composition, and was accordance with Guo et al. (2018).
or organic matter or roots in original soil. As the original desert soil and tape water had little microbial

7
C. Liu et al. Ecotoxicology and Environmental Safety 208 (2021) 111419

Fig. 5. Community cluster heatmap at genus level in soil subjected to different water treatments (raw wastewater, RW; secondary treated wastewater, STW; tertiary
treated wastewater, TTW).

abundance and diversity in current experiment, the changed soil com­ can lead to instability in colloidal systems which may result in rapid
munity may come from wastewater, plant root growth and etc. In flocculation of colloids, pore clogging and deposition, following a
Table S3, a liner regression analysis was done with relative abundances possible decrease of infiltration rate. The measurements of ζ-potential
of bacterial genus and soil physicochemical and plant growth properties. were made to determine electrical potential changes due to wastewater
It revealed that soil pH, NO–3, plant growth, organic matter were the irrigation as the organic matter and microbes in wastewater can coat
main environmental predictors controlling bacterial community struc­ surface of soil particles and which may cause ζ-potential changes of soil
ture. On the other way round, the bacterial community structure is a key (Elimelech et al., 2000; Zhuang and Yu, 2002). Even though minor
factor for nutrient (N) cycling and plant growth, especially the existence changes were observed to the overall measured ζ-potential of the het­
of plant promoting microbes, e.g. Rhizobium. This was indicated by the erogeneous porous sand, a decreased ζ-potential (more negative) was
strong correlation of plant biomass and Rhizobium (R2 = 0.83, data was found with wastewater treatments compared with freshwater treat­
not presented in table). The organic matter in wastewater can be shortly ments. Similar result was also reported by Zhuang and Yu (2002). This
degraded by microorganisms, and introduce a burst of microbial indicated a possible more stable colloids state in wastewater irrigated
booming and in the meantime produce high concentrations of dissolved sand, and this may also explain the higher infiltration rate in TTW
organic matter into soil and water (Moran et al., 2000). irrigated soil.
Even though increased organic matter content was evidenced in RW
and STW treated soil in current experiment, no correlation was observed
3.6. Soil physical properties after harvest
in ζ-potential and organic matter content. While ζ-potential significantly
corrected to decrease of stable infiltration rate due to plant growth (R2
The water stable aggregates bigger than 0.25 mm and zeta (ζ)-po­
= 0.88). This may indicate that the plant growth contributed to the
tential were shown in Table S4. The original desert soil was sandy soil
stability of the colloidal system.
with no soil structure. The determined aggregates of CK, TTW, STW and
The above results indicated that plant and soil can be used as a low-
RW treated soil indicated sign of formation of soil structure with plant
cost infiltration media to treat wastewater with the help of microbial
growth and organic matter accumulation. The poor soil structural of
activity. Nevertheless, the composition of wastewater can be very
desert sand was mainly due to its extremely low organic matter content,
different due to the source of wastewater inlet. Even though, the
thus the relative high organic matter content and suspended solids in
personnel composition and source of wastewater inlet in the studied
STW precipitated on top of soil and contributed the significant large soil
area is also simple compared with the wastewater from university. Still,
aggregate formation. Besides, plant roots and their exudates can enmesh
the wastewater from university might be different from desert waste­
and realign soil particles thus result in formation of soil aggregates.
water that disposed, since wastewater from university mostly come from
While the improved microbial community in soil may also take impor­
young and healthy people. As a result, wild experiment by using local
tant role in water retention and aggregates formation, as the production
wastewater is urgently needed to further confirm the above founding.
of extracellular polysaccharide and mycelium by microbes is proved to
be able to adhesion soil particles (Caesar-Tonthat, 2002; Flemming and
4. Conclusions
Wingender, 2001).
ζ-potential is defined as the electrical potential at the shear plane of
Results demonstrated that wastewater application induced
the electric double layer. Changes in the magnitude of the ζ-potential

8
C. Liu et al. Ecotoxicology and Environmental Safety 208 (2021) 111419

significant changes in plant growth and soil physical, bio-chemical Caldwell, B.A., 2005. Enzyme activities as a component of soil biodiversity: a review.
Pedobiologia 49 (6), 637–644.
properties. The used desert soil has no aggregate structure. Its porosity
Das, K., Prasanna, R., Saxena, A.K., 2017. Rhizobia: a potential biocontrol agent for
is large and permeability is strong, thus water seepage rate is fast. If the soilborne fungal pathogens. Folia Microbiol. 62 (5), 425–435.
untreated wastewater is directly discharged into desert soil, it is easy to Ebel, B.A., Moody, J.A., 2013. Rethinking infiltration in wildfire-affected soils. Hydrol.
pollute soil and groundwater because it facilitates the accumulation of Process. 27 (10), 1510–1514.
Elimelech, M., Nagai, M., Ko, C.H., Ryan, J.N., 2000. Relative insignificance of mineral
N, P, salt, E. coli and pH level in top soil layer. However, domestic grain zeta potential to colloid transport in geochemically heterogeneous porous
wastewater irrigation and its improved plant growth resulted in soil media. Environ. Sci. Technol. 34 (11), 2143–2148.
function restoration which were indicated by decreased infiltration rate; Fatta-Kassinos, D., Kalavrouziotis, I.K., Koukoulakis, P.N., Vasquez, M.I., 2011. The risks
associated with wastewater reuse and xenobiotics in the agroecological
formation of soil structural; accumulation of organic matter; increased environment. Sci. Total Environ. 409 (19), 3555–3563.
soil enzyme activity, microbial abundance and diversity. The TTW Flemming, H.C., Wingender, J., 2001. Relevance of microbial extracellular polymeric
containing less pollutants had big promise in circular bioeconomy and substances (EPSs) – Part I: Structural and ecological aspects. Water Sci. Technol. 43
(6), 1–8.
ecosystem restoration referring to desert vegetation recovery and sand Fredlund, D.G., Xing, A.Q., 1994. Equations for the soil-water characteristic curve. Can.
fixation, due to magnificent promotion in root growth. The result of Geotech. J. 31 (4), 521–532.
current experiment also indicated a great promise in using plant and soil Frenk, S., Hadar, Y., Minz, D., 2014. Resilience of soil bacterial community to irrigation
with water of different qualities under Mediterranean climate. Environ. Microbiol.
as infiltration media to treat wastewater in rural areas. Further research 16 (2), 559–569.
is needed to estimate the ecological effect of other contaminants in Frossard, E., Condron, L.M., Oberson, A., Sinaj, S., Fardeau, J.C., 2000. Processes
domestic wastewater e.g. hormone. Long term experiment and data governing phosphorus availability in temperate soils. J. Environ. Qual. 29 (1),
15–23.
collection from the wild desert environment should be warranted before
Gross, M., 2018. China’s water challenges. Curr. Biol. 28 (4), R135–R138.
reuse of wastewater in desert soil. Guo, W., Qi, X., Xiao, Y., Li, P., Andersen, M., Zhang, Y., Zhao, Z., 2018. Effects of
reclaimed water irrigation on microbial diversity and composition of soil with
reducing nitrogen fertilization. Water 10 (4), 365.
CRediT authorship contribution statement Gupta, S., Satpati, S., Nayek, S., Garai, D., 2010. Effect of wastewater irrigation on
vegetables in relation to bioaccumulation of heavy metals and biochemical changes.
Caixia Liu, Zhengfang Ye, and Quanlin Zhao conceived the project. Environ. Monit. Assess. 165 (1–4), 169–177.
Hall, C., Hoff, W.D., 2012. Water Transport in Bricks, Stone and Concrete, second ed.
Caixia Liu, Fulai Liu and Mathias N. Andersen contributed to the Taylor and Francis,, London and New York.
experimental design. Caixia Liu performed the experiments. Caixia Liu Hamilton, A.J., Stagnitti, F., Kumarage, S.C., Premier, R.R., 2007. RIRA: A tool for
and Gongming Wang carried out data analysis. Caixia Liu wrote the conducting health risk assessments for irrigation of edible crops with recycled water.
Comput. Electron. Agric. 57 (1), 80–87.
manuscript. All authors edited the manuscript.
Han, D.M., Currell, M.J., Cao, G.L., 2016. Deep challenges for China’s war on water
pollution. Environ. Pollut. 218, 1222–1233.
Huang, G.Y., Liu, Y.S., Liang, Y.Q., Shi, W.J., Yang, Y.Y., Liu, S.S., Hu, L.X., Chen, H.X.,
Declaration of Competing Interest Xie, L., Ying, G.G., 2019. Endocrine disrupting effects in western mosquitofish
Gambusia affinis in two rivers impacted by untreated rural domestic wastewaters.
Sci. Total Environ. 683, 61–70.
The authors declare that they have no known competing financial Kandeler, E., Gerber, H., 1988. Short-term assay of soil urease activity using colorimetric
interests or personal relationships that could have appeared to influence determination of ammonium. Biol. Fertil. Soils 6 (1), 68–72..
the work reported in this paper. Katz, B.G., Sepulveda, A.A., Verdi, R.J., 2009. Estimating nitrogen loading to ground
water and assessing vulnerability to nitrate contamination in a large Karstic Springs
Basin, Florida. J. Am. Water Resour. Assoc. 45 (3), 607–627.
Acknowledgement Kemper, W.D., Chepil, W.S., 1965. Size distribution of aggregation. In: Black, C.A., et al.
(Eds.), Part 1: Monograph. American Society of Agronomy, pp. 499–510.
Khalid, S., Shahid, M., Natasha, Bibi, I., Sarwar, T., Shah, A., Niazi, N., 2018. A review of
We thank Lei Li and Halo Chen for their technical assistance with environmental contamination and health risk assessment of wastewater use for crop
laboratory analyses. We thank The National Key Research and Devel­ irrigation with a focus on low and high-income countries. Int. J. Environ. Res. Public
opment Project of China (No.2019YFC0409202) for funding of the Health 15 (5), 895.
Kiziloglul, F.M., Turan, M., Sahin, U., Angin, I., Anapali, O., Okuroglu, M., 2007. Effects
project. of wastewater irrigation on soil and cabbage-plant (Brassica olerecea var. capitate
cv. yalova-1) chemical properties. J. Plant Nutr. Soil Sci. 170 (1), 166–172.
Kiziloglu, F.M., Turan, M., Sahin, U., Kuslu, Y., Dursun, A., 2008. Effects of untreated and
Appendix A. Supporting information
treated wastewater irrigation on some chemical properties of cauliflower (Brassica
olerecea L. var. botrytis) and red cabbage (Brassica olerecea L. var. rubra) grown on
Supplementary data associated with this article can be found in the calcareous soil in Turkey. Agric. Water Manag. 95 (6), 716–724.
online version at doi:10.1016/j.ecoenv.2020.111419. Laghari, M., Mirjat, M.S., Hu, Z., Fazal, S., Xiao, B., Hu, M., Chen, Z., Guo, D., 2015.
Effects of biochar application rate on sandy desert soil properties and sorghum
growth. Catena 135, 313–320.
References Liu, Y., Cui, Z., Huang, Z., Lopez-Vicente, M., Wu, G.L., 2019. Influence of soil moisture
and plant roots on the soil infiltration capacity at different stages in arid grasslands
of China. Catena 182, 104147.
Abdel-Shafy, H.I., Anwer, S., Hassan, S., Yahia, T., 2003. Risk assessment of sewage reuse
Liu, C.X., Liu, S.R.F., Liu, F.L., Rubaek, G.H., Andersen, M.N., 2018. Arbuscular
on the sandy soil of Abu-Rawash Desert, Egypt. Environ. Prot. Eng. 26, 31–42.
mycorrhizal fungi alleviate abiotic stresses in potato plants caused by low
Adrover, M., Farrus, E., Moya, G., Vadell, J., 2012. Chemical properties and biological
phosphorus and deficit irrigation/partial root-zone drying. J. Agric. Sci. 156 (1),
activity in soils of Mallorca following twenty years of treated wastewater irrigation.
46–58.
J. Environ. Manag. 95, S188–S192.
Liu, C., Liu, F., Ravnskov, S., Rubaek, G.H., Sun, Z., Andersen, M.N., 2017. Impact of
Akponikpe, P.B.I., Wima, K., Yacouba, H., Mermoud, A., 2011. Reuse of domestic
wood biochar and its interactions with mycorrhizal fungi, phosphorus fertilization
wastewater treated in macrophyte ponds to irrigate tomato and eggplant in semi-
and irrigation strategies on potato growth. J. Agron. Crop Sci. 203 (2), 131–145.
arid West-Africa: benefits and risks. Agric. Water Manag. 98 (5), 834–840.
Liu, C.X., Rubaek, G.H., Liu, F.L., Andersen, M.N., 2015. Effect of partial root zone drying
Angin, I., Yaganoglu, A.V., Turan, M., 2005. Effects of long-term wastewater irrigation on
and deficit irrigation on nitrogen and phosphorus uptake in potato. Agric. Water
soil properties. J. Sustain. Agric. 26 (3), 31–42.
Manag. 159, 66–76.
van Asperen, H.L., Bor, A.M.C., Sonneveld, M.P.W., Bruins, H.J., Lazarovitch, N., 2014.
Lubello, C., Gori, R., Nicese, F.P., Ferrini, F., 2004. Municipal-treated wastewater reuse
Properties of anthropogenic soils in ancient run-off capturing agricultural terraces in
for plant nurseries irrigation. Water Res. 38 (12), 2939–2947.
the Central Negev desert (Israel) and related effects of biochar and ash on crop
Manas, P., Castro, E., de las Heras, J., 2009. Irrigation with treated wastewater: effects on
growth. Plant Soil 374 (1–2), 779–792.
soil, lettuce (Lactuca sativa L.) crop and dynamics of microorganisms. J. Environ.
Santa Brigida, A.B., Rojas, C.A., Grativol, C., de Armas, E.M., Entenza, J.O.P.,
Sci. Health Part a-Toxic. /Hazard. Subst. Environ. Eng. 44 (12), 1261–1273.
Thiebaut, F., Lima, M.F., Farrinelli, L., Hemerly, A.S., Lifschitz, S., Ferreira, P.C.G.,
Ma, Y.H., Zhai, Y.K., Zheng, X.Y., He, S.B., Zhao, M., 2019. Rural domestic wastewater
2016. Sugarcane transcriptome analysis in response to infection caused by
treatment in constructed ditch wetlands: Effects of influent flow ratio distribution.
Acidovorax avenae subsp avenae. Plos One 11 (12), e0166473.
J. Clean. Prod. 225, 350–358.
Bronick, C.J., Lal, R., 2005. Soil structure and management: a review. Geoderma 124
Mohammad, M.J., Mazahreh, N., 2003. Changes in soil fertility parameters in response to
(1–2), 3–22.
irrigation of forage crops with secondary treated wastewater. Commun. Soil Sci.
Caesar-Tonthat, T.C., 2002. Soil binding properties of mucilage produced by a
Plant Anal. 34 (9–10), 1281–1294.
basidiomycete fungus in a model system. Mycol. Res. 106, 930–937.

9
C. Liu et al. Ecotoxicology and Environmental Safety 208 (2021) 111419

Moran, M.A., Sheldon, W.M., Zepp, R.G., 2000. Carbon loss and optical property changes Tindall, J.A., Kunkel, J.R., Anderson, D.E., 1999. Unsaturated Zone Hydrology for
during long-term photochemical and biological degradation of estuarine dissolved Scientists and Engineers. Prentice Hall, Inc., New Jersey, USA.
organic matter. Limnol. Oceanogr. 45 (6), 1254–1264. Tran, N.H., Hu, J.Y., Li, J.H., Ong, S.L., 2014. Suitability of artificial sweeteners as
Nagarajan, D., Lee, D.J., Chen, C.Y., Chang, J.S., 2020. Resource recovery from indicators of raw wastewater contamination in surface water and groundwater.
wastewaters using microalgae-based approaches: a circular bioeconomy perspective. Water Res. 48, 443–456.
Bioresour. Technol. 302, 122817. Travis, M.J., Wiel-Shafran, A., Weisbrod, N., Adar, E., Gross, A., 2010. Greywater reuse
Nannipieri, P., Ascher, J., Ceccherini, M.T., Landi, L., Pietramellara, G., Renella, G., for irrigation: effect on soil properties. Sci. Total Environ. 408 (12), 2501–2508.
2003. Microbial diversity and soil functions. Eur. J. Soil Sci. 54 (4), 655–670. Wallach, R., Ben-Arie, O., Graber, E.R., 2005. Soil water repellency induced by long-term
Pedrero, F., Grattan, S.R., Ben-Gal, A., Vivaldi, G.A., 2020. Opportunities for expanding irrigation with treated sewage effluent. J. Environ. Qual. 34 (5), 1910–1920.
the use of wastewaters for irrigation of olives. Agric. Water Manag. 241, 106333. Wang, G.M., Jia, Q.S., Qiao, J.F., Bi, J., Liu, C.X., 2020. A sparse deep belief network with
Pinto, U., Maheshwari, B.L., Grewal, H.S., 2010. Effects of greywater irrigation on plant efficient fuzzy learning framework. Neural Netw. 121, 430–440.
growth, water use and soil properties. Resour. Conserv. Recycl. 54 (7), 429–435. Ward, D., Wiegand, K., Getzin, S., 2013. Walter’s two-layer hypothesis revisited: back to
Qu, Q., Zhang, Z., Peijnenburg, W.J.G.M., Liu, W., Lu, T., Hu, B., Chen, J., Chen, J., the roots! Oecologia 172 (3), 617–630.
Lin, Z., Qian, H., 2020. Rhizosphere microbiome assembly and its impact on plant Wu, Y.F., Zhu, W.B., Lu, X.W., 2013. Identifying key parameters in a novel multistep bio-
growth. J. Agric. Food Chem. 68 (18), 5024–5038. ecological wastewater treatment process for rural areas. Ecol. Eng. 61, 166–173.
Raine, S.R., Meyer, W.S., Rassam, D.W., Hutson, J.L., Cook, F.J., 2007. Soil-water and Xu, J.A., Wu, L.S., Chang, A.C., Zhang, Y.A., 2010. Impact of long-term reclaimed
solute movement under precision irrigation: knowledge gaps for managing wastewater irrigation on agricultural soils: a preliminary assessment. J. Hazard.
sustainable root zones. Irrig. Sci. 26 (1), 91–100. Mater. 183 (1–3), 780–786.
Rodriguez, H., Fraga, R., 1999. Phosphate solubilizing bacteria and their role in plant Yang, W., Guo, Y., Wang, X., Chen, C., Hu, Y., Cheng, L., Gu, S., Xu, X., 2017. Temporal
growth promotion. Biotechnol. Adv. 17 (4–5), 319–339. variations of soil microbial community under compost addition in black soil of
Shelef, G., 1991. The role of waste-water reuse in water-resources management in Israel. Northeast China. Appl. Soil Ecol. 121, 214–222.
Water Sci. Technol. 23 (10–12), 2081–2089. Yuan, H.J., Qin, S.P., Dong, W.X., Hu, C.S., Manevski, R., Li, X.X., 2019. Denitrification
Shilpi, S., Lamb, D., Bolan, N., Seshadri, B., Choppala, G., Naidu, R., 2019. Waste to watt: rate and controlling factors for accumulated nitrate in the deep subsoil of intensive
anaerobic digestion of wastewater irrigated biomass for energy and fertiliser farmlands: a case study in the North China Plain. Pedosphere 29 (4), 516–526.
production. J. Environ. Manag. 239, 73–83. Zhuang, J., Yu, G.R., 2002. Effects of surface coatings on electrochemical properties and
Siggins, A., Burton, V., Ross, C., Lowe, H., Horswell, J., 2016. Effects of long-term contaminant sorption of clay minerals. Chemosphere 49 (6), 619–628.
greywater disposal on soil: a case study. Sci. Total Environ. 557, 627–635. Zou, J., Guo, X.S., Han, Y.P., Liu, J.X., Liang, H.W., 2012. Study of a novel vertical flow
Sissingh, H.A., 1971. Analytical technique of Pw method, used for assessment of constructed wetland system with drop aeration for rural wastewater treatment.
phosphate status of arable soils in Netherlands. Plant Soil 34 (2), 483-48. Water Air Soil Pollut. 223 (2), 889–900.
Thebo, A.L., Drechsel, P., Lambin, E.F., Nelson, K.L., 2017. A global, spatially-explicit Zuo, R., Jin, S., Chen, M., Guan, X., Wang, J., Zhai, Y., Teng, Y., Guo, X., 2018. In-situ
assessment of irrigated croplands influenced by urban wastewater flows. Environ. study of migration and transformation of nitrogen in groundwater based on
Res. Lett. 12 (7), 074008. continuous observations at a contaminated desert site. J. Contam. Hydrol. 211,
39–48.

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