Science of the Total Environment 722 (2020) 137888

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Science of the Total Environment

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

Reusing oil and gas produced water for agricultural irrigation:

Effects on soil health and the soil microbiome
Hannah Miller a, Kandis Dias a, Hannah Hare b, Mikayla A. Borton a, Jens Blotevogel c, Cloelle Danforth d,
Kelly C. Wrighton a, James A. Ippolito a, Thomas Borch a,b,c,⁎
a
Department of Soil and Crop Sciences, Colorado State University, Fort Collins, CO 80523, United States of America
b
Department of Chemistry, Colorado State University, Fort Collins, CO 80523, United States of America
c
Department of Civil and Environmental Engineering, Colorado State University, Fort Collins, CO 80523, United States of America
d
Environmental Defense Fund, Boulder, CO 80302, United States of America

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• Oil/gas produced water (PW) effects on

soil health was determined for potential
beneficial reuse.
• Wheat was grown in a greenhouse and
irrigated with various dilutions of PW.
• Irrigation with 5% PW led to decreased
soil health, wheat yields, and microbial
diversity.
• Decreases were likely due to a variety of
contaminants in PW.

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

Article history: Produced water (PW) is a major waste-product of oil and gas production that some consider a viable agricultural
Received 30 December 2019 irrigation water source. However, the presence of petroleum hydrocarbons, toxic metals and potentially high sa-
Received in revised form 5 March 2020 linity of PW may be deleterious for soil health. Thus, we irrigated wheat with minimally treated PW to investigate
Accepted 10 March 2020
effects on soil health, wheat growth, and the soil microbiome. Irrigation treatments included control irrigation
Available online 14 March 2020
water (IW), 1% and 5% PW dilutions (1% PW, 5% PW), and a saltwater solution with salinity equivalent to the
Editor: Jay Gan 5% PW dilution (SW). Wheat was irrigated three times a week, for a total of 2.1 L per pot by harvest. During
wheat growth, we measured plant physiological parameters, soil electrical conductivity, as well as profiled soil
Keywords: microbial diversity by performing 16S ribosomal ribonucleic acid (rRNA) gene analysis. Soil health parameters
Produced water were measured after harvest, including chemical, biological, physical, and nutrient properties that were used
Crop yield to calculate an overall soil health index (SQI). SQI analysis revealed that the SW and 5% PW treatments had sig-
Water reuse nificantly reduced soil health as compared to the control. Furthermore, the 16S rRNA gene analysis showed that
Agricultural irrigation the microbial community membership and structure was significantly different between irrigation treatments,
Soil microbiome
highlighting shifts in the soil microbiome which may impact soil biochemical cycling. Both the SW- and 5%
PW-treated wheat had reduced yields as compared to the control. Our results indicate that irrigating wheat
with minimally treated PW may result in yield decreases, as well as reducing both overall soil health and soil

⁎ Corresponding author at: Department of Soil and Crop Sciences, Colorado State University, Fort Collins, CO 80523, United States of America.
E-mail address: Thomas.borch@colostate.edu (T. Borch).

https://doi.org/10.1016/j.scitotenv.2020.137888
0048-9697/© 2018 Published by Elsevier B.V.
2 H. Miller et al. / Science of the Total Environment 722 (2020) 137888
microbial community diversity. Future large-scale field studies are needed to determine the long-term soil health
effects of PW on different soil types and crops.
1. Introduction
Large volumes of produced water (PW) are generated in the United
States due to the popularity of both hydraulic fracturing and conven-
tional oil and gas operations. Kondash et al. (2017) and Veil (2015) es-
timate that 630 to 840 billion gallons of PW are generated annually in
the U.S. Frequently, PW is injected underground into Class II disposal
wells; however, this can lead to negative environmental consequences
such as earthquakes and contamination of surface and groundwater
(Ellsworth, 2013; Vidic et al., 2013). Thus, alternative PW uses are
being explored, and one attractive option is the use of PW for agricul-
tural crop irrigation in water scarce regions.
PW is a complex wastewater and has several constituents of concern
that may impact crop yields, soil health, and human health. The chem-
istry and toxicity of PW discharged to surface waters has already been
well characterized (McDevitt et al., 2019, 2020; McLaughlin et al.,
2020a). PW may contain salts, heavy metals and metalloids, naturally-
occurring radioactive materials (NORMs), and organic compounds
(Clark and Veil, 2009; Dolan et al., 2018; Ferrer and Thurman, 2015;
McAdams et al., 2019; Oetjen et al., 2018). The majority of PW salt is so-
dium chloride (NaCl), and can be deleterious to soil health because ex-
cess sodicity causes soil dispersion (Burkhardt et al., 2015a). Heavy
metal and metalloid accumulation, commonly of arsenic, can be detri-
mental to crop growth and human consumption (Shariq, 2019). Radium
and uranium may also be found in PW, which if absorbed by crops can
also harm humans upon consumption (Sheppard and Evenden, 1988).
Furthermore, high concentrations (N5 mg/L) of organic compounds
found in PW can significantly reduce plant yields (Pica et al., 2017).
Before PW is widely used for agricultural crop irrigation, the poten-
tial hazards to soil and crop health need to be assessed. The long-term
viability of cropland is an essential natural resource that, once deterio-
rated, is not easy to restore. Maintaining soil health is not only necessary
for ensuring food quality and security, but soils also influences water
quality, quantity, and ecosystem biodiversity (National Science and
Technology Council, 2016). Soils contain microorganisms, invertebrates,
and organic matter that mediate biogeochemical cycling, increase plant-
available nutrients, encourage soil aggregation, and improve soil poros-
ity, aeration, water infiltration and percolation. Ascertaining whether
PW degrades these complex soil characteristics is of paramount
importance.
Previous studies on the overall effect of PW on agroecosystem health
are limited. Irrigation with PW has been shown to reduce crop yields
and negatively impact crop physiological parameters (Sedlacko et al.,
2019), even when diluted by as much as 90% with tap water. Simulated
PW was used to irrigate non-food biofuel crops, leading to reduced
yields due to high PW salinity and excess organic carbon (Pica et al.,
2017). Pica et al. (2017) found that PW total organic concentrations
should be b5 mg/L in order to maintain biomass production. Further-
more, PW has recently been found to suppress plant immune response
to pathogens (Miller et al., 2019). However, the accumulative effect of
PW on soil health has not been assessed. Studies focused on spreading
PW near well pads have hypothesized that: 1) excess sodium will de-
crease soil aeration, infiltration, and permeability; 2) excess salts will
cause plants to die and sodium will accumulate when PW is applied to
aridic soils; 3) native plant species will be out-competed by new species
more tolerant of biogeochemical soil alterations; and 4) salt-tolerant
plant species will likely become more prevalent (Pitchel, 2016). Fur-
thermore, models have been used to simulate irrigating sugar beets
with a variety of PW compositions and assessed the impacts on soil sa-
linity, sodicity, pH and crop yield (Echchelh et al., 2019). The authors
© 2018 Published by Elsevier B.V.
found that the soil type irrigated with PW has a large impact on overall
soil health effects, and thus reuse needs to be assessed on a case-by-case
basis (Echchelh et al., 2019). However, this research was not based on
empirical studies.
Although the impact of PW on soil quality is largely unknown, sev-
eral U.S. states are irrigating crops with diluted PW, including California,
Montana, and Wyoming (California Water Boards, 2019; Dolan et al.,
2018). Since 1994, two districts in California have used treated PW by
blending it with irrigation water and applying it to grapes, citrus, al-
monds, and pistachios (Waldron, 2005). Blended PW from hydraulic
fracturing was used in an experimental study in Texas to irrigate cotton
(Lewis et al., 2015). Typically, states provide guidelines to suggest cer-
tain irrigation water salt content ceiling limits for irrigating crops in
order to preserve soil health. However, the overall effect of PW on soil
health has not been assessed.
To address this critical knowledge gap, we performed a greenhouse
study to investigate the feasibility of reusing PW for wheat irrigation
with a focus on the effects on soil health and the soil microbiome. We
obtained PW from a well in the Denver-Julesburg (DJ) basin and agricul-
tural soil from eastern Colorado, USA. We chose wheat as a surrogate
crop because the DJ basin (encompassing eastern Colorado, northwest-
ern Kansas, and southwestern Nebraska, USA) produces a large majority
of wheat in the US (USDA NASS, 2018), and because wheat has a rela-
tively high salinity tolerance level of 6 mS cm−1 (Havlin et al., 2014).
Produced water is already being discharged into surface waters after
minimal treatment (McDevitt et al., 2020, 2019; McLaughlin et al.,
2020a, 2020b). Using varying PW dilutions compared to control water
treatments, we measured impacts of PW irrigation on soil health pa-
rameters, wheat yield, and soil microbial community composition.
This holistic approach was used to determine the feasibility of using
PW in irrigated agricultural settings.
2. Methods
2.1. Greenhouse experiment
Utah State University ‘Apogee’, a hard red spring wheat (Triticum
aestivum L.) is a fast growing, and salt tolerant dwarf variety cultivar
(Bugbee and Koerner, 1997) that was chosen for the study. A 500-
gallon PW sample was obtained from a 10-well unconventional pad
that was in operation for more than three years at the time the water
was received. Thus, the water was clearly PW and not hydraulic fractur-
ing flowback. The PW was withdrawn from the Niobrara formation in
the DJ basin in Weld County, Colorado. The PW chemistry is detailed
in Table 1, with data collected by collaborators at Colorado School of
Mines. Our collaborators consistently received samples every
1–3 weeks from this 10-well pad for over a year, and every batch was
analyzed for water quality and the results were consistent with the
chemistry shown in Table 1. This water chemistry is representative of
the DJ basin, with an average salinity of approximately 15,000 mg/L.
A fine sandy loam soil was collected from the USDA Agricultural Re-
search Service limited irrigation research farm in eastern Colorado. The
dominant crop grown over the previous decade was irrigated maize
(Smith et al., 2018). This soil was chosen because it was within close
proximity to the highest concentration of oil and gas operations in
Colorado.
The soil was returned to Colorado State University and then passed
through a 1.2 cm sieve to remove large organic debris and rocks. How-
ever, this process compromised the soil structure and became too dense
for wheat seeds to germinate. Therefore, the soil was mixed with sand
 H. Miller et al. / Science of the Total Environment 722 (2020) 137888 3

Table 1 Then, the remaining soil from the 0–5 and 5–10 cm depths was hand-
Water chemistry of undiluted produced water from Denver-Julesberg Basin. collected and then sieved for additional analyses. First, the soil was
Significance Constituent Unit Value sieved through an 8-mm sieve to remove large pieces of organic debris.
Water quality pH Unitless 7.4
Approximately 150 g of the sieved soil was placed in a Ziplock plastic
TSS mg/L 271 bag and stored at 4 °C for subsequent soil microbial biomass carbon
Potential contaminants B mg/L 28 analysis. Another 150 g of the 8-mm sieved soil was passed through a
Sr mg/L 179 2-mm sieve, and this soil along with the remainder of the 8-mm sieved
Salts Ca mg/L 786
soil was allowed to air-dry at room temperature.
Mg mg/L 107
Na mg/L 10,500 Soil characterization, on either the 8-mm and 4 °C stored, 8-mm air-
SAR unitless 497 dried, or 2-mm air-dried soils, included soil bulk density, soil organic
Chloride (Cl-) mg/L 20,800 carbon, microbial biomass carbon, water stable aggregates, potentially
Bromide (Br-) mg/L 227 mineralizable nitrogen, pH and electrical conductivity (EC), plant-
TDS mg/L 35,900
Conductivity dS/m 49
available potassium and phosphorus, soil texture, and beta-
Potential nutrients Nitrite (NO−
2 ) mg/L 30 glucosidase activity. These characteristics were utilized either individu-
K mg/L 67 ally or combined to determine soil health indices using the Soil Manage-
TN mg/L 55 ment Assessment Framework (SMAF) as described by Andrews et al.
Organics DOC mg/L 156
(2004). Further details about the methods used to determine soil char-
TOC mg/L 180
acteristics are described in the Supplemental Information. Most of the
above soil characteristics are commonly quantified, but several are not
(2 parts sand:1 part soil) to maintain proper aeration, infiltration, and routinely determined in research or testing facilities and thus are briefly
percolation. The sand was industrial quartz Granusil size 4075. After described here. Potentially mineralizable nitrogen quantifies the
mixing with sand, the soil texture was 4% clay, 2% silt, and 94% sand. amount of organic N that can be mineralized to NH4-N and nitrified to
While mixing the soil with sand led to a compromised analog for field NO3-N by microorganisms over a 4-week aerobic incubation procedure;
conditions, it should be noted that most greenhouse studies cannot this indirectly measures the nitrogen available for crops (NRCS, 2014).
properly mimic large agricultural field settings. However, field studies Beta-glucosidase activity provides insight into rates of enzyme degrada-
with produced water trials were not an option due to the potential for tion of cellulosic material, and thus is sensitive to soil management
soil contamination. changes (Stege et al., 2010). After collection, all soil characterization
Three wheat seeds per plot were planted in a total of 40 pots. Each data was entered in SMAF in order to determine soil physical, chemical,
pot could hold 2.6 L and had a top inner diameter of 24.77 cm. and a nutrient, biological, and overall soil health indices. Output from SMAF
height of 22.54 cm. All pots had four drainage holes and had plastic provides indices that vary from 0 to 1, with 1 the theoretical greatest
holders underneath the pot to catch any water that drained out during and 0 the worst soil health.
irrigation. All pots were initially watered with irrigation water until all Statistical analysis was performed using the R statistical package
plants contained approximately three leaves. The control irrigation “emmeans” and “outliers” (R Core Team, 2018). Outliers in the soil
well water was obtained from the Colorado State University's experi- data were data points that were outside 1.5*Inter quartile range,
mental agricultural station groundwater well. It was not cleaned or which is the difference between the 75th and 25th quartiles. All soil
treated prior to use in the greenhouse experiment, but it meets Colo- characteristic data, along with all soil health indices, were analyzed in
rado agricultural water recommendations. Then, the greenhouse R by generating a linear model (function “lm”) and then calculating
wheat pots were split into four different irrigation treatments: control the estimated marginal means (EMMs, function “emmeans”). The sig-
irrigation well water (IW), 1% and 5% PW dilutions (1% PW, 5% PW), nificance threshold for p values was set at 0.05.
and a salt-water treatment with salinity equivalent to the 5% PW dilu-
tion (SW). These concentrations were determined by calculating the 2.3. 16S rRNA amplicon sequencing and analysis
concentrations of boron, chloride, and overall sodium adsorption ratio
(SAR) to ensure levels were either below, or just slightly above, recom- Five sets of soil samples for DNA extraction were collected: four dur-
mended agricultural irrigation water concentrations for eastern Colo- ing the wheat growing period, and one at harvest. At harvest, soil was
rado crops (Bauder et al., 2014) (Supplemental Table 1). sampled from every pot from both the top 5 cm and bottom 5–10 cm
We used a randomized complete block design to arrange the four ir- of soil, but in previous samplings, only 20 total samples were collected,
rigation treatments to account for potential greenhouse light, tempera- 5 from each treatment. Total nucleic acids were extracted with the
ture, and air flow differences. Plants were watered with 150 mL of their DNeasy Powersoil kit (Qiagen) and eluted with 10 μL of elution buffer,
respective treatments three times a week, to 80–100% water holding ca- then stored at −20 °C before sequencing. DNA was sequenced at the
pacity to prevent drought stress conditions (~ 70% water holding capac- Colorado State University next-generation sequencing facility. 16S
ity), for a total of 2.1 L of water over the entire experiment. Soil electrical rRNA gene libraries were prepared according to the Illumina 16S
conductivity (EC) and plant height were measured once a week. Ap- Metagenomic Sequencing Library Preparation Protocol (Part 15044223 Re-
proximately 3 g of soil from each pot was sampled at 5 different vision B). Briefly, universal primers 515F and 806R were used for PCR
timepoints for 16S rRNA gene analysis; background soil prior to exper- amplification of the V4 hypervariable region of 16S rRNA gene using
imental setup was also analyzed. 38 cycles. The 515F primer contained a unique sequence tag to barcode
The wheat was harvested 65 days after planting, once it had each sample. Both primers contained sequencer adapter regions. Indi-
completely dried. The entire above ground biomass (including the stalks vidual libraries were pooled at approximately equimolar ratios and li-
and seeds) was cut and placed in brown paper bags. The plants were brary QC included visualization on with Tapestation HS D1000
dried at 60 °C for 72 h, and then total biomass, grain weight, and reagents (Agilent, Inc.) and qPCR using Library Quantification Master
seeds per plant were determined. Wheat yield was calculated by deter- Mix and Standards (Roche Ltd.). The pooled libraries were sequenced
mining the average weight of the seeds per plant. at 10pM on the MiSeq instrument (Illumina Inc.) using the 500 cycle
(2 × 250 base pair) V2 Reagent Kit with 15% PhiX spike-in to increase
2.2. Soil characterization and health analysis base-call heterogeneity during the run.
Reads were demultiplexed and analyzed within QIIME2 (Qi et al.,
Following wheat harvest, soil was collected for bulk density analysis 2015) using DADA2 (Callahan et al., 2016) to produce an amplicon se-
from the 0–5 and 5–10 cm depths using a 3.2 cm diameter soil corer. quence variant (ASV) by sample table (Supplemental Information
4 H. Miller et al. / Science of the Total Environment 722 (2020) 137888

Table 3). Raw reads below 5000 were discarded due to low data quality.
The ASV table was analyzed using the statistical package “vegan” (R
Core Team, 2018). Alpha diversity was calculated with the diversity
function to investigated both richness and Shannon's diversity. Beta di-
versity was calculated by analyzing Bray-Curtis dissimilarities using the
relative abundance of samples, and then plotting these values with non-
parametric multi-dimensional scaling (NMDS) plots in R. Both a multi
response permutation procedure and mean dissimilarity matrix
(mrpp) function and an analysis of similarities (anosim) function
were calculated to determine the significance of differences between
sample groups. Raw reads were deposited in NCBI, under XX accession
numbers.
Statistical analysis was performed using the R statistical package
“vegan” (R Core Team, 2018). Alpha diversity was calculated with the
diversity function to investigate both richness and the Shannon diver-
sity index. Beta diversity was calculated by analyzing Bray-Curtis dis-
similarities using the relative abundance of samples, and then plotting
these values with non-parametric multi-dimensional scaling (NMDS)
plots in R. Both a multi-response permutation procedure and mean dis-
similarity matrix (mrpp) function, and an analysis of similarities
(anosim) function, were calculated to determine the significance of dif-
ferences between sample groups.
Linear discriminant analysis effect size (LEfSe (Segata et al., 2011))
was used to find the discriminatory features among different sample
groups. LEfSe uses the Kruskal-Wallis test (a = 0.05) along with the
pairwise Wilcoxon test (a = 0.05), paired with linear discriminant anal-
ysis (threshold LDA = 2) to determine the features responsible for the
biological differences between samples.
3. Results
3.1. Soil health
Most soil characteristics showed little response to treatment (Sup-
plemental Fig. 1), yet soil EC was determined as being an important
soil health indicator when using PW. There were significant differences
in soil EC in the top 5 cm of the soil (Fig. 1A). Both SW (which had equiv-
alent salinity to 5% PW) and 5% PW had statistically higher ECs than IW
and the 1% PW treated soils. The EC value for the 5% PW was ~6.2 mS
cm−1 and thus higher than the maximum acceptable EC for wheat (6
mS cm−1). The 5 to 10 cm soil depth had significantly lower EC values
than the 0 to 5 cm depth; both SW and 5% PW values were approxi-
mately 4 mS cm−1 less than the top values. In the bottom portion of
the soil, the EC value for the control soils was statistically lower than
the other three treatments.
The additive biological SQI was determined using the Soil Manage-
ment Assessment Framework (SMAF) with microbial biomass carbon,
potentially mineralizable nitrogen, beta glucosidase, and soil organic
carbon data (Fig. 1B). SW and 5% PW treatments had statistically
lower soil health index (SQI) values than IW and 1% PW treatments in
the top portion of the soil. In the bottom portion of the soil, SW had a
significantly lower SQI than IW and 1% PW.
Individual soil parameters (Supplemental Fig. 1) were compiled to
determine an overall SQI (Fig. 1C). In the top 5 cm of soil, both SW
and 5% PW showed similar reductions in soil health as compared to
the IW control and 1% PW treatment. The treatments were not different
within the bottom portion of the soil.

Fig. 1. Significant results from soil health analysis. “Top 5 cm” and “Bottom 5–10 cm” indicates that the soil was obtained from the 0 to 5 cm and 5 to 10 cm depths, respectively. Electrical
conductivity (A) was determined to be a key soil chemical property in quantifying soil health, with the dashed line at 6 mS cm−1 as the threshold above which is unacceptable for
productive cropland. The biological SQI (B) was calculated from the microbial biomass carbon (MBC), potentially mineralizable nitrogen (PMN), beta-glucosidase (BG), and soil organic
carbon (SOC) analyses. The additive SQI (C) combines all soil indicator results into one metric. IW: irrigation water, 1% PW: 1% dilution of produced water, 5% PW: 5% dilution of PW,
and SW: salt water with salinity equivalent to PW. Different letters indicate statistical significance (p b 0.05) between samples, both between treatments and across depths.
 H. Miller et al. / Science of the Total Environment 722 (2020) 137888 5

3.2. Soil microbiome
Soils from the 0–5 and 5–15 cm depths, sampled over time, were
used for the 16S rRNA analysis. There were no differences in microbial
communities between treatments in the lower soil depth (Supplemen-
tal Fig. 2), but differences existed in the upper portion. The variability in
microbial communities from the 0–5 cm depth, between treatments,
was examined by calculating a Bray-Curtis dissimilarity matrix and vi-
sualized using a non-metric dimensional scaling (NMDS) plot (Fig. 2).
Multiple response permutation procedure (MRPP) analysis revealed
5% PW treated soils had significantly different (p b 0.001) microbial
communities than IW and 1% PW treated soils, but 5% PW treated
soils were not significantly different (p N 0.05) than SW microbial com-
munities. Further MRPP analysis showed difference (p b 0.001) between
SW and IW soil microbial communities, but not between SW and 1% PW
communities. There was no statistical difference between IW and 1%
PW treated soil microbial communities with MRPP analysis. Notably,
changes in microbial soil community compositions are significantly cor-
related with additive SQI in IW and 1% PW (Fig. 2, arrow).
Linear discriminant analysis (LDA) was performed on this dataset to
find the microbial communities responsible for the differences between
the IW and 5% PW treated soils at harvest (Supplemental Fig. 3). The
discriminant features enriched in the 5% PW treatment included mem-
bers from the phyla Planctomycetes, Acidobacteria, and Bacteroidetes,
whereas members of the Actinobacteria and Chloroflexi were more
abundant in the IW treatment. Although there was significant difference
in soil beta diversity in these samples, the alpha diversity (e.g. measured
richness and Shannon's diversity), did not significantly vary (Supple-
mental Fig. 4).
The differences in the overall soil microbial community were also
assessed over time (Fig. 3). Day 1 samples were collected 14 days fol-
lowing the planting of the seeds, when all soil treatments were receiv-
ing irrigation with the control water. However, immediately after
sampling soil on Day 1, the pots began receiving treated waters; day
65 was the harvest day. Alpha diversity, in the form of Richness, was cal-
culated over time (Fig. 3). The mean richness at day 1 was greater than
the mean richness measured at harvest. Multiple response permutation
procedure (MRPP) analysis revealed soil samples collected at harvest
(October; day 65) had significantly different (p b 0.001) microbial com-
munities than soil samples at the beginning of the experiment (August;
day 1) (Supplemental Fig. 5).
3.3. Crop yield
Crop yield was calculated by determining the average weight of the
seeds per plant (Fig. 4). The IW-treatment was used as the control and
point of comparison for other treatments; thus, it had a yield of 100%.
SW and 5% PW had significantly reduced yields as compared to IW,
with 70% and 60% yields, respectively. However, the 1% and 5%-PW irri-
gated, and 1%-PW and SW-irrigated wheat had indistinguishable yields.
There were limited physical differences in plant health observed, the
four treatments were indistinguishable at day 35 (Supplementary
Fig. 6). However, by day 56, the SW and 5% PW treated plants both
showed yellowing of their tallest leaf (flag leaf). Chlorophyll measure-
ments were performed at three different time points during the green-
house study, but there were no differences between photosynthetic
parameters for the water treatments (Supplementary Fig. 7).
4. Discussion
4.1. Salinity
The integration of the above results provides a view of potential
agroecosystem changes due to irrigation with reused produced water.
There was reduced yield, reduced biological soil health, and a reduction
in overall soil health due to irrigation with SW and 5% PW waters. It ap-
pears that salinity was the primary driver because the SW and 5% PW
treatments shared similar EC values. The SW control contained pure

Fig. 2. Non-metric dimensional scaling (NMDS) plot showing the varying soil microbial communities between irrigation treatments in the 0 to 5 cm soil depth. The sdditive soil health data
was superimposed on the NMDS; the black arrow points towards the IW and SW microbial communities, which indicates that soil health varies significantly with microbial community
composition. Bray-Curtis similarity metric from the four treatment samples (stress = 0.148) show a statistically significant (MRPP, p b 0.001) separation from 5% PW samples from both
IW and 1% PW samples, as indicated by the circles separating the sample treatments. SW samples are also significantly different than IW samples, but not 1% PW samples. 1% PW (red), 5%
PW (green), IW (blue) and SW (purple) dots represent the varying soil microbial communities, down to the feature level. (For interpretation of the references to colour in this figure
legend, the reader is referred to the web version of this article.)
6 H. Miller et al. / Science of the Total Environment 722 (2020) 137888
Fig. 3. Alpha diversity expressed as Richness was assessed for five soil sampling events over the duration of the experiment. The four soil irrigation treatments are all included in this data
and separate colors reflect the treatment. The dots represent soil samples from individual pots.
sodium chloride, which is toxic to plants both due to the sodium cations
and chloride anions. Chloride ions reduce the osmotic potential of the
plants, which reduces their ability to absorb water. Additionally, chlo-
ride ions reduce plant photosynthetic capacity due to chlorophyll degra-
dation (Tavakkoli et al., 2010). Sodium ions are toxic to plants; they
interfere with plant uptake of calcium and potassium ions and cause de-
pressed photosynthesis and growth (Burkhardt et al., 2015a; Tavakkoli
et al., 2010). Oftentimes, more saline irrigation waters with high ECs are
due to a combination of less toxic salts such as Ca, Mg, and CO3.
Furthermore, the 1% PW treatment did not significantly differ in
plant yield or soil health parameters as compared to the control, thus
Fig. 4. Percent yield from each irrigation treatment, with IW (i.e., the control) considered
100% yield. Yield was calculated as the average weight of seeds per plant. IW: irrigation
water, 1% PW: 1% dilution of produced water, 5% PW: 5% dilution of PW, and SW: salt
water with salinity equivalent to PW. Different letters indicate statistical significance
(p b 0.05) between samples.
the addition of organics at a 1% dilution (~2 mg/L TOC) did not seem
to negatively impact soil health; this is in accordance with Pica et al.
(2017) who reported crop yield declines at N5 mg/L TOC. However,
the comparison between SW and the 1% PW implies that organics
were not the main cause of differences, and further supports EC
(i.e., Na+ and Cl−) as a main factor causing suppressions in yield and
soil health. However, it is important to note that this particular study
used PW high in salinity, and the dilution also heavily diluted organic
compounds that have the potential to be problematic in other PW
reuse situations. As shown previously, high concentrations of organic
compounds in irrigation water can lead to suppressed crop immune re-
sponse to pathogens (Miller et al., 2019), thus investigating only soil
health parameters does not completely assess impacts of irrigation
water quality on crops.
Excess salinity is a common soil health problem. In saline solutions,
the osmotic pressure in the soil is greater than that of plant cells, thus
depriving plants of water. In the PW irrigation solution, the salinity
was mainly due to NaCl, whereas in other soils Mg and Ca can contribute
to overall salinity. Thus, PW irrigation leads to large sodium adsorption
values (N10), which can cause soil to lose its structure and permeability
(Bauder et al., 2014; Davis et al., 2012). Soils that contain N30% smectitic
clay are most at risk of reduced soil health due to sodicity. Clay loams,
silty clay loams, and some sandy clay loams that are commonly used
for agriculture in Colorado contain smectite (Bauder et al., 2014). Our
greenhouse soil only contained 4% clay; thus, it was not surprising
that we did not see changes in density with PW irrigation. However,
soils that contain high percentages of expanding clays are common in
agricultural lands; a future study would benefit from exploring different
soil types in conjunction with PW affected irrigation waters.
Wheat is a relatively salt-tolerant crop, with a salinity threshold
level of 6 mS cm−1, above which yield is limited (Havlin et al., 2014),
which made it ideal for this study. Irrigated wheat is grown in Colorado,
 H. Miller et al. / Science of the Total Environment 722 (2020) 137888
but not as extensively as irrigated corn. Corn is a moderately salt-
sensitive crop, with a salinity threshold of 1.7 mS cm−1; beans are
more sensitive with a salinity threshold value of 1 mS cm−1 (Havlin
et al., 2014). Crops are frequently rotated on the same land; thus, the
least salt tolerant crop needs to be considered before using a saline irri-
gation source. Irrigated beans are typically on a 3 to 4-year rotation with
corn, barley, wheat and alfalfa, whereas wheat is typically rotated with
wheat-corn-fallow or wheat-sorghum fallow (McDonald et al., 1997a,
1997b) This further highlights the importance of considering crop salin-
ity tolerance when reusing minimally treated produced water.
Previous studies have utilized high salt containing oil and gas waste-
water to irrigated crops. Coalbed natural gas water was used in Wyo-
ming to irrigate corn, switchgrass and biofuel species; these studies
indicate that irrigation with produced water increased the soil sodium
content, and led to elevated sodium in plant leaves and limited potas-
sium and phosphorous uptake (Burkhardt et al., 2015a). Although our
study did not look at plant uptake, our soil did have an increased SAR
after only one irrigation cycle with PW. Although our soil nutrient anal-
ysis did not show significant changes in potassium or phosphorous con-
centrations, this is probably due to the short length of our irrigation
experiment (three months) compared to the Wyoming study above
(two years). Detailed soil chemical analysis in the Wyoming experiment
revealed reduced soil physical properties, including clay and organic
matter dispersion, surface crusting, reduced infiltration, and reduced
hydraulic conductivity, all due to high sodicity (Ganjegunte et al.,
2005). Furthermore, a similar greenhouse study of coal-bed natural
gas wastewater found that average sodium concentrations of
1160 mg/L hampered plant growth and development (Burkhardt
et al., 2015b). This supports the finding of this study, in that the reduced
yields in both the SW and 5% PW irrigated wheat had sodium concen-
trations N1100 mg/L.
However, excess salinity is not the only contaminant of concern
leading to reduced soil health and yield declines. This experiment was
not designed to isolate the specific contaminants responsible for soil
and crop quality declines, but it does show negative changes associated
with PW irrigation that need to be further investigated. Previous studies
have seen similar reductions in crop yields and plant health declines
due to irrigation with PW, however, organic compound concentration
seemed to have been more important in those studies (e.g., Miller
et al., 2019; Sedlacko et al., 2019). However, the previous studies irri-
gated plants with 10% and 50% PW dilutions, as compared to the 1%
and 5% dilutions in this study. Additionally, this study used a more real-
istic soil matrix than the previous studies, which sorbs more organic
matter, metals and/or NORMS, which would make them less available
to plants.
It is important to note that the PW chemistry varies widely by geo-
logic formation and geographic location. Although our samples are rep-
resentative of the DJ Basin, PW from the Marcellus Shale, for example, is
much more saline that in Colorado, and PW from California is oftentimes
less saline (Kahrilas et al., 2016). The results of this study should not be
viewed as applicable to all PW, but they do provide an evaluation of the
effects of late-stage PW (post-flowback) from the DJ Basin in Colorado
on eastern Colorado soil health. While late-stage PW tends to be rela-
tively stable in terms of salinity concentrations (Oetjen et al., 2018),
more site-specific studies would need to be conducted to verify these ef-
fects on soils from other regions irrigated with PW from different geo-
logic formations. However, the effects on soil health can be estimated
by comparing different PW to the water chemistry of the PW used in
this study.
4.2. Soil health indices
The Soil Management Assessment Framework is unique because it
allows for site-specific comparisons rather than computing absolute
soil health parameters (Andrews et al., 2004). Thus, we cannot compare
the results of the soil quality indices (SQIs) to other studies, but only to
7
the internal control. The differences in chemical SQI, as calculated by
measuring pH and EC, show that the main effects due to salinity are iso-
lated to the top five cm of the soil. It is likely that a wheat seed planted in
our soil would have difficulties germinating due to elevated soil surface
salinity. However, if the seed has already germinated and then the soil
becomes saline, the plant may be more likely to survive because the
bulk of the roots (90%) are in the top 60 cm of soil (Havlin et al.,
2014). Furthermore, the rooting depths of plants vary greatly; sugar
beet roots can have a depth of 20 cm (McDonald, 2003), whereas alfalfa
can have a rooting depth of over 300 cm (Havlin et al., 2014;
Undersander, 2011). An understanding of salinity, crop, and rooting
depth are required to make cropping systems adjustments when utiliz-
ing PW for irrigation.
The physical SQI was similar between treatments because the bulk
density and water stable aggregates were all similar. Excess salinity
and sodium lead to reduced soil infiltration in soils high in clay, which
is reflected in a higher bulk density. However, this soil was mixed
with sand in order to grow wheat in the greenhouse, which changed
the overall bulk density. The average bulk density of the artificial soil
was 1 g cm−3, which is well within the range of healthy soil densities
for loamy sands (b1.60 g cm−3; (USDA (United States Department of
Agriculture), 1999). Bulk density is an important physical soil parame-
ter that varies from 1.10–1.60 g cm−3 based on soil type, with heavier
textured soils (e.g., clays) unable to tolerate greater bulk densities as
compared to lighter textured soils (e.g., sandy soils, as used in the cur-
rent study; (USDA (United States Department of Agriculture), 1999).
This is simply due to the function of pore sizes present between both
textures, with sandy soils containing a fewer number of but larger
pores, sizes as compared to heavier textured soils. Additional studies
utilizing a wider array of soil textures, under field conditions, is war-
ranted for PW irrigation water use and its potential effect on soil phys-
ical properties.
The nutrient SQI suggests the PW may have slightly enriched the soil
with phosphorous and potassium. These are necessary crop nutrients,
so it is possible that reusing wastewater may provide crops with some
essential nutrients for growth. However, it does not appear that this
slight benefit outweighed the adverse effects of the other PW
constituents.
Biological and biochemical SQIs were assessed by combining data
from the soil organic carbon, microbial biomass carbon, potentially min-
eralizable nitrogen, and beta-glucosidase assays. Although there were
no differences between treatments (Supplemental Fig. 3c), the SW
and 5% PW samples tended to have lower average SQI values than IW
and 1% PW. This suggests that the soil was starting to experience
changes in both the soil organic carbon and soil microbial community
activity, which we investigated further with the 16S rRNA data from
the soil microbiome.
4.3. Soil microbial community
Microbes are essential to soil biogeochemical cycling, as well as soil
organic matter formation and decomposition, all of which greatly influ-
ence soil fertility (Anderson, 2003; Thiele-Bruhn et al., 2012). Studies
have shown that certain agricultural practices, such as heavy fertilizer
and pesticide use or intensive land usage, can shift the microbial com-
munity structure and alpha diversity (Thiele-Bruhn et al., 2012; Wang
et al., 2019). More research is needed to determine the effects of man-
agement practices, including PW use, on soil biodiversity and microbial
community structure and function.
Here we report that 5% PW and a NaCl-based salinity control have an
impact on the soil bacterial and archaeal community structure, resulting
in a shift of dominant members, which could impact nutrient cycling
and soil stability. The current study attempted to address this knowl-
edge gap. There was greater mean richness in the soil microbial commu-
nities at the beginning of the experiment versus the end when the
wheat was harvested. Reduced soil diversity has been reported to
8 H. Miller et al. / Science of the Total Environment 722 (2020) 137888
disrupt many key ecosystem functions, such as decomposition, nutrient
retention and nutrient cycling (Wagg et al., 2014). Thus, we infer that
the loss of diversity observed by the end of the experiment due to PW
irrigation could indicate negative impacts on soil function, resulting ul-
timately in reduced soil health and crop productivity. We also showed
significant differences in soil microbial community structure and mem-
bership between treatments in the top portion of the soil. Although the
exact functional changes in nutrient cycling cannot be assessed from
16S rRNA data, this information provides the first insights into microbial
community responses to PW treatment, paving the way for other micro-
bial aspects that can be interrogated in the future. Additional investiga-
tions may use higher-resolution microbial analyses such as
metagenomics and metatranscriptomics to interrogate changes in
microbiome function and activity in response to produced water
amendments.
5. Conclusions
Reusing PW may be mutually beneficial to both farmers and oil and
gas companies. Produced water reuse has the potential to be less expen-
sive and disruptive than underground disposal, as well as cheaper than
traditional water sources for irrigation purposes. However, results indi-
cate that insufficiently treated PW (5% PW dilution) is not a desirable
agricultural water source because it leads to decreased yields, decreased
soil health, and changing soil microbiomes. It is unclear if a 1% PW dilu-
tion is acceptable for maintaining soil health and yields. Although this
greenhouse experiment did not show significantly harmful reductions
in soil health and yield with a 1% PW dilution, this result only reflects
three months of irrigation. Future studies should investigate the effects
of longer-term irrigation. Furthermore, field-scale studies need to be
conducted to investigate if differences exist due to scaling up, or if var-
iations in soil structure and organic content will greatly affect irrigation
design strategies.
From this study, it appears that treatment of PW, rather than simple
dilution, is required for sustainable reuse of PW for crop irrigation. Ad-
vanced treatment, e.g. using membrane-based desalinization is re-
quired before the PW can potentially be used for crop irrigation.
Future studies should be conducted with treated produced water, be-
yond dilution. It would be relevant to irrigate crops with varying salinity
threshold levels (e.g., wheat versus corn versus beans) with sufficiently
treated PW removed of excess salinity (i.e., NaCl) or other less desirable
constituents. Assessing long-term effects on crop yields and soil health
under common agroecosystem management practices, when utilizing
PW, is required. The results of this study can provide farmers, regulators,
and oil and gas companies insight into the effects of produced water on
soil health but also help guide development of effective treatment op-
tions for PW. However, it is important to note that the salinity, organic
content, and heavy metal content of produced water varies by well
and geologic formation; thus, these findings are not universally applica-
ble. This study highlights some of the biggest concerns to soil health
when irrigated with alternative, complex water sources.
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.scitotenv.2020.137888.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influ-
ence the work reported in this paper.
Acknowledgements
This work was supported by the Environmental Defense Fund (EDF).
Thank you to the Plant Growth Facility at Colorado State University for
providing the greenhouse space; watering and analysis help from
Merritt Logan and Dustin Diaz from Colorado State University (CSU);
irrigation recommendations from Allan Andales (CSU); and Tzahi Cath
from Colorado School of Mines for providing the produced water.
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