Science of the Total Environment 779 (2021) 146205

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Science of the Total Environment

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Organomineral fertilizers pastilles from microalgae grown in

wastewater: Ammonia volatilization and plant growth
Alexia Saleme Aona de Paula Pereira ⁎, Jackeline de Siqueira Castro, Vinícius José Ribeiro, Maria Lúcia Calijuri
Federal University of Viçosa, Department of Civil Engineering, Viçosa, Minas Gerais, Brazil

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

• A fertilizer composed of microalgae and

urea in distinct proportions is proposed.
• The nitrogen assimilation capacity by
plants and effect in the soil were
assessed.
• 40% MB presented the highest accumu-
lated ammonia volatilization.
• The maximum N content is reached in
the proportion of 25% MB.
• The highest N recovery rates by plants
were achieved with 15% and 30% MB.

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

Article history: With the increasing demand for food, it is increasingly important to maintain soil fertility with the application of
Received 6 November 2020 fertilizers to supply the nutritional needs of plants. However, the nutrients applied to the soil can suffer signifi-
Received in revised form 22 February 2021 cant losses, impacting the environment, and increasing production costs. Using alternative sources, such as
Accepted 25 February 2021
microalgae biomass (MB) generated in the treatment of wastewater, in the production of organomineral fertil-
Available online 3 March 2021
izers is a way to recover nutrients from the sewage, in addition to contributing to the improvement in soil fertility
Editor: Huu Hao Ngo and favoring crop growth, which can guarantee agricultural sustainability. In the present study, MB was grown in
the effluent 00from the food industry and, subsequently, a pelleted organomineral fertilizer (POF) was produced
consisting of the combination of MB and synthetic fertilizer (urea), in different proportions. The performance of
Keywords: the proposed fertilizer was analyzed for losses due to ammonia volatilization (N-NH3) over time, for nitrogen as-
Microalgae similation capacity (N) by corn plants (Zea mays L.), and its structure was evaluated by scanning electron micros-
Ammonia volatilization copy. The study concluded that the highest accumulated volatilization of N-NH3 was in the proportion of 40% of
Nutrient recycling MB and the maximum content of N is reached in the proportion of 24.55% of MB. From the proportion of 25% of
Nitrogen fertilizer
MB, there is no increase in N absorbed by plants, at the same time that the volatilization of N-NH3 grows with the
increase in MB. The most important factors for obtaining these results were the interaction between MB and urea
in the produced organomineral fertilizer tablet, where an increasingly thicker physical barrier was formed with
the increase in the proportion of MB; in addition to the POF pH, in which the increase in MB proportions directly
favored the pH increase.
© 2021 Elsevier B.V. All rights reserved.

⁎ Corresponding author at: Department of Civil Engineering, Federal University of 1. Introduction

Viçosa (Universidade Federal de Viçosa/UFV), Av. Peter Henry Rolfs, s/n, Campus
Universitário, Viçosa, Minas Gerais 36570-900, Brazil.
E-mail addresses: [email protected] (A.S.A.P. Pereira),
The constant need to increase food production imposes extra
[email protected] (J.S. Castro), [email protected] (V.J. Ribeiro), charges on the soil, making the use of chemical fertilizers inevitable.
[email protected] (M.L. Calijuri). However, much is discussed about the efficiency of these fertilizers in

https://doi.org/10.1016/j.scitotenv.2021.146205
0048-9697/© 2021 Elsevier B.V. All rights reserved.
A.S.A.P. Pereira, J.S. Castro, V.J. Ribeiro et al. Science of the Total Environment 779 (2021) 146205

the face of large losses in the field and their impact on the environment. 2.1. Production and characterization of the microalgae biomass
Coupled with population growth, urbanization, and industrialization
processes, the generation of wastewater is increasing and the environ- The production of microalgae biomass was carried out in two HRAPs
mental impacts caused by its release without proper treatment are ob- on a pilot scale, using an N-rich effluent as the culture medium to obtain
served worldwide. Wastewater is rich in nutrients (Craggs et al., MB. The primary flotation effluent from the meat processing industry,
2014) and recovery can be carried out by treating the effluent in high- located in the municipality of Viçosa, MG, Brazil, was used. The charac-
rate algal ponds (HRAPs) (Kang et al., 2018; Singh et al., 2019; Zhu, teristics of this effluent are best described in the studies carried out by
2015). Using microalgae biomass (MB), generated in the treatment of Costa (2016), Castro et al. (2017) and Souza et al. (2019).
wastewater, in the production of organic mineral fertilizers, is a way The HRAPs used in the experiment are constructed of fiberglass with
to recover nutrients from the sewage, in addition to contributing to the following dimensions: width of 1.28 m, length of 2.86 m, total depth
the improvement in soil fertility and favoring the growth of crops, of 0.5 m, useful depth of 0.3 m, surface area of 3.3 m2, and volume of
being able to guarantee agricultural sustainability. 1 m3. To allow a continuous flow of the effluent, stainless steel pedals
In 2018 in Brazil, the amount of nitrogen fertilizer consumed for ag- are used, with six blades each, which are powered by a 0.5 hp electric
ricultural use reached 5 million tons, where 89.8% of this demand is met motor. To guarantee a speed of approximately 0.10 to 0.15 m s−1, a
by imports (FAO - Food and Agriculture Organization of the United gearbox controlled by a frequency inverter (brand WEG series CFW-
Nations, 2018). Among the most imported nitrogen fertilizers, urea 10) is attached to the motor.
(61%), ammonium sulfate (25%), ammonium nitrate (11%), and ammo- The HRAPs operation was carried out in batches for seventeen days.
nia (3%) stand out (Ministry of Economy, 2019). The use of these nitro- After the beginning of the experiment, the variables chlorophyll-a and
gen fertilizers implies nitrogen (N) losses via nitrate leaching (NO− 3 ), volatile suspended solids (VSS) were monitored every three days until
nitrous oxide emission (N2O), and ammonia volatility (NH3) (Castro the decay phase of algal growth was observed. After reaching this
et al., 2017; Khan et al., 2019). stage, the phytoplankton community was characterized in qualitative
Among the environmental impacts caused by these losses, the eutro- and quantitative terms using an inverted optical microscope (Olympus
phication of water bodies and indirect influence in the increase of CK2), according to the methodology of Utermöhl (1958). The morphol-
greenhouse gases, due to NO2 and NO emissions (Gregorich et al., ogy, morphometry, reproductive and vegetative cycles of species of sig-
2015), are highlighted. Several studies analyze alternatives to increase nificant taxonomic values were also analyzed, as described in the
the efficiency of nitrogen fertilizers to minimize these losses, either by literature (Komárek and Fott, 1983; Parra et al., 1982; Wetzel and
the type of management or by the use of slow-release fertilizers Likens, 1991). Thus, taxonomic characterization revealed Chlorophyta
(Ferraz-Almeida and Sanches, 2012; Kitonyo et al., 2018; Zhang et al., (58.47% Chlorella vulgaris, 1.17% Didymocystis inermis, and 2.93%
2016). Tetradesmus obliquus) and Bacillariophyta (37.43% Navicula sp.) as
An alternative is the production of biofertilizer using microalgae the main phyla present in the crude microalgae biomass. Regarding
grown in wastewater. The use of microalgae biofilm favored smaller the biochemical composition, 7.42% carbohydrates, 2.49% lipids,
N losses via volatilization of N-NH3, as observed by Castro et al. 27.40% proteins, and 32.99% inert material were obtained.
(2017) in addition to increasing the organic matter content in the Biomass was collected after the treatment of the batch effluent and the
soil. In addition, the production of microalgae can occur in wastewa- establishment of algal growth. For this procedure, the pH of the algal ponds
ter, promoting the recycling of nutrients normally lost in conven- was increased to 12, by adding 50% NaOH (v/v), followed by intense man-
tional treatment. Several studies assess the treatability and the ual agitation. Subsequently, the ponds remained at rest for 24 h, to allow
production of MB in wastewater from different sources (Arbib sedimentation of the biomass. Then, the clarified supernatant was
et al., 2017; Craggs et al., 2014; García et al., 2017; Godos et al., discarded and the biomass sedimented at the bottom was collected. After
2009; Park et al., 2011). The valorization of this biomass through biomass collection, the pH was neutralized with the addition of HCl 1:1
the production of biofertilizers is still little investigated and can be (v/v). The biomass was frozen, and finally, lyophilized to remove moisture.
advantageous since the application of organic compounds can bring The dry biomass was analyzed following the specifications of
numerous benefits to the soil and crops (Bonanomi et al., 2020; Embrapa (2009) and obtained the following chemical characteris-
Mandal et al., 2019; Yang et al., 2020). tics: 504,400 mg kg−1 of carbon; 85,100 mg kg−1 of Hydrogen (H);
The objective of this paper is to investigate the effects of the applica- 60,300 mg kg −1 of Nitrogen (N); 5220 mg kg −1 of Sulfur (S);
tion of a pelleted organomineral fertilizer (POF), regarding the losses by 18,700 mg kg−1 of Phosphorus (P); 3800 mg kg−1 of Potassium
volatilization of N-NH3 and the capacity of assimilation of N by corn (K); 26,600 mg kg−1 of Calcium (Ca); 6100 mg kg−1 of Magnesium
plants (Zea mays L.) in comparison to the commercial fertilizer. The in- (Mg); 14,900 mg kg−1 of Sodium (Na), 27.91 mg kg−1 of Copper
novation of the present study is the production of a POF composed by (Cu); 4462 mg kg −1 of Iron (Fe); 367.32 mg kg−1 of Zinc (Zn);
mix, in different proportions, of synthetic fertilizer (urea) and 74,700 mg kg−1 of Manganese (Mn); 11.05 mg kg−1 of Nickel (Ni);
microalgae biomass generated in HRAPs using wastewater as a means 5.10 mg kg−1 of Lead (Pb); 25.58 mg kg−1 of Chromium (Cr).
of cultivation.
2.2. Production of the organomineral fertilizer
2. Material and methods
The production of the organomineral fertilizer was carried out
The experiment was conducted at the Laboratory of Sanitary and through a tablet mold made of stainless steel. Initially, it was necessary
Environmental Engineering of the Federal University of Viçosa, in to submit the dry microalgae biomass as well as the synthetic fertilizer
Viçosa, Minas Gerais, Brazil (20° 46′07,05″ S e 42° 51′30,84″ W). The cli- (granulated urea) separately, to the maceration process to obtain a ma-
mate in the municipality is humid with rainy summers and dry winters, terial of smaller particle size. This procedure was carried out in a mortar
with a water deficit between May and September, and a surplus and, later, sieved through a 100-mesh screen.
between December and March. According to the National Institute of Afterward, these materials were weighed in the proper proportions
Meteorology (Instituto Nacional de Meteorologia (INMET), 2017), con- and mixed with liquid gum Arabic in a beaker until homogeneous. This
sidering the historical series from 1998 to 2017, the average annual pre- slightly moist mixture was pressed into the tablet mold, followed by
cipitation is 1260 mm, and the relative humidity is 79%. The average drying at 35 °C in a forced circulation oven to remove the moisture
temperature during the rainy season, between October and March, is from the tablets. Finally, the tablet fertilizers were analyzed visually
20.3 °C and during the dry season, between April and September, it is using the scanning electron microscope (SEM) JSM-6010LA, and their
17.4 °C. pH was determined as described by Almeida et al. (2012).

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A.S.A.P. Pereira, J.S. Castro, V.J. Ribeiro et al. Science of the Total Environment 779 (2021) 146205

2.3. Soil characterization diameter and 10 cm high. With the aid of the funnel, each base was filled
with samples of 0.5 dm3 of air dried soil through circular movements to
To set up this experiment, subsurface samples (20–40 cm) of an avoid the segregation of soil aggregates.
Oxisol, collected in the region of Viçosa, were used. The collected mate- After this process, a multi-nutrient solution without N (Novais
rial was air-dried, stripped, and passed through a 2 mm sieve to obtain et al., 1991) was applied to the soil, in addition to water so that
air dried soil. The analysis to determine the physical and chemical char- the soil reached 80% of the field capacity. For the next three days,
acteristics of the soil were carried out according to Teixeira et al. (2017) the bases, filled with soil, were kept at a temperature of 25 °C, for
and Almeida et al. (2012), and the results are shown in Table 1. acclimatizing the soil biota and producing urease (Koefender
et al., 2013).
2.4. Experimental design At the end of this period, the POF were superficially applied to the
soil in the center of the rings. Immediately after applying the fertilizer,
Two experiments were conducted, one to evaluate the POF influence a collecting chamber (Araújo et al., 2009) was installed on the base to
on the volatilization of N-NH3 in the soil and the other to verify the influ- trap and collect the N-NH3 released by the fertilizer.
ence of the nutrient source for the plants. The experiments were orga- The chamber for the quantification of N-NH3 volatilization
nized in a randomized block design (RBD) with four repetitions per block. worked in a static-free system and was developed following the
All treatments received sources of N equal to 100 mg dm−3 except methodology of Araújo et al. (2009). The collecting chambers were
for the control, where no N was added. The treatments were Urea + 5% made from a transparent plastic bottle of polyethylene terephthalate
Microalgae Biomass (MBU5); Urea + 15% Microalgae Biomass (PET) without the base, diameter 10 cm, and an area of 80 cm2. Inside
(MBU15); Urea + 30% Microalgae Biomass (MBU30); Urea + 40% the bottle, a vertically suspended absorber system composed of a
Microalgae Biomass (MBU40); Urea + 50% Microalgae Biomass polyurethane foam sheet with the following dimensions was placed:
(MBU50); and Urea (UR). 3.0 mm thick, 2.5 cm wide, and 25 cm long. The foam was affixed
In all experiments, soil samples (2 dm3) were placed in plastic bags using a rigid wire, 1.5 mm diameter, coupled to the cover of the
for liming, by the method of neutralizing Al3+ and increasing the levels PET franc. At the time of installation, a flask of 50 mL capacity was
of Ca2+ + Mg2+ (Ribeiro et al., 1999), with the correction of pH at 6.0. added, containing 10 mL of 1 mol L−1 solution of H 2 SO 4 + 2%
Then, the soil moisture was adjusted to 80% of the field capacity. After glycerin (v/v).
21 days of incubation, the soil was air-dried, ground, and passed During the installation of the N-NH3 absorber system, the foam sheet
through a 2 mm sieve air dried soil. The experiments, described was compressed in a bottle with an acidic solution to absorb the largest
below, were conducted in a greenhouse, also located at LESA. possible amount of this solution. The foam sheet remained in the closed
bottle until installation. The lower end of the slide was kept inside the
2.4.1. Quantification of N-NH3 volatilization from nitrogen sources 50 mL flask, to avoid splashing the acidic solution on the soil. To keep
The experiment was carried out in a greenhouse for thirty days. The the foam upright, its end was attached to the top of the rigid wire.
experimental units consisted of polyvinyl chloride rings with 10 cm in Thus, the rigid wire, alongside with the 50 mL flask and the acid-
soaked foam, were hung by the top edge and suspended 1.5 cm from
the soil surface.
The volatilized N-NH3 was captured as (NH4)2SO4. Samples were
Table 1
Physico-chemical characteristics of the soil used. taken during the thirty days concurrently with the corn conduction ex-
periment. The N-NH3 emissions of were sampled 1, 2, 3, 4, 5, 6, 7, 8, 10,
12, 17, 23 and 30 days after transplanting (DAT).
Physical characteristics of the soil

Coarse sanda 14.5 % 2.4.2. Evaluation of the efficiency of sources in the corn crop Zea mays L.
Thin sanda 9.4 %
For the cultivation of the culture in 2 dm 3 pots, six corn seeds
Silta 7.2 %
Claya 68.9 % (Biomatrix BM709 PR02) were sown, at 2 cm depth, evenly distrib-
uted. The fertilizers were applied to the soil, in solid form, on the sur-
Chemical characteristics of the soil face in a centralized manner. A multi-nutrient solution without N
pH in waterb 4.52 – was added on the 1, 10, and 20 DAT according to Novais et al.
Nitrogen (N)c 0.14 dag kg−1 (1991). After seven days, thinning was carried out, leaving only
Organic matter (OM)d 3.29 dag kg−1 three plants per pot.
Phospor (P)e 0.60 mg dm−3
Phosphorus remaininge 6.40 mg L−1
Soil moisture was controlled daily to maintain a field capacity of
Sum of exchangeable basesf 0.18 cmolc dm−3 around 80%. After thirty days of cultivation, the corn plants were sec-
Hydrogen plus aluminum (H + Al3+)f 7.70 cmolc dm−3 tioned 0.5 cm from the soil, and then packed in paper bags and taken
Potassium (K)e 11.00 mg dm−3 to the forced air circulation oven at 60 °C, (up to constant weight) to
Calcium (Ca2+)g 0.12 mg dm−3
obtain the shoot dry mass matter (SDMM) and then were ground to
Magnesium (Mg2+)g 0.03 mg dm−3
Aluminum (Al3+)g 1.07 mg dm−3 determine the N content, digesting 0.5 g of SDMM, with H2SO4 and
Sulfur (S)h ND mg dm−3 H2 O 2 plus the digestion mixture (Na 2SO4 , CuSO 4·5H2 O) followed
Boron (B)i 0.31 mg dm−3 by semi-micro steam distillation Kjeldahl, according to Tedesco
Copper (Cu)e 0.40 mg dm−3 et al. (1995).
Manganese (Mn)e 2.00 mg dm−3
Finally, the nutrient content in the plant was obtained by Eq. (1):
Iron (Fe)e 99.30 mg dm−3
Zinc (Zn)e 0.37 mg dm−3
mDM  NT
a
Pipette method (Almeida et al., 2012). NC ¼ ð1Þ
b
Soil to water ratio 1:2.5. 1000
c
Nitrogen total-Kjeldahl method (Teixeira et al., 2017).
d
Nelson and Somers (1982). where:
e
Mehlich extractor (Embrapa, 2009).
f
Calcium acetate extraction method 0.5 mol/L-pH 7.0 (Embrapa, 2009).
NC = nutrient content (mg pot−1);
g
Potassium chloride extraction method 1 mol L−1 (Embrapa, 2009).
h
Monocalcium phosphate in acetic acid extraction method (Embrapa, 2009). mDM = weight dry matter (g pot−1);
i
Hot water extractor (Embrapa, 2009). ND - undetectable. NT = nutrient tenor (g kg−1).

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A.S.A.P. Pereira, J.S. Castro, V.J. Ribeiro et al. Science of the Total Environment 779 (2021) 146205

The recovery rate (RR) of N was also performed (Eq. (2)): 3. Results

3.1. N-NH3 volatilization

ðNCT–NCC Þ
RR ð%Þ ¼ ⁎100 ð2Þ
ðTAN Þ The N-NH3 emissions observed in the treatments and controls are
shown in Fig. 1a. After the application of POF, N-NH3 emissions in-
creased with the peak of emission occurring on the third day of the ex-
where:
periment. Other peaks of volatilization were also observed on the 10
NCT = N content in the aerial part of the fertilized treatment and 17 DAT. For all treatments, the volatilization of N-NH3 gradually de-
(mg pot−1); creased over time. Cumulative losses are shown in Fig. 1b. The losses in-
NCC = N content in the aerial part of the control treatment creased over time until the first seven days, followed by stabilization,
(mg pot−1); indicating that this process happened quickly.
TAN = total amount of N added (mg pot−1). In particular, the cumulative losses of N-NH3 volatilization showed
2.5. Statistical analysis significant differences between the treatments in which MB was
added and the treatment in which only UR was applied. By the Tukey
The results of the determination of volatilized N-NH3 as a function of test, it was observed that there was no statistically significant difference
the incubation time were adjusted to the logistic equation (Eq. (3)) (p > 0.05) between the treatments in which MB was added. The highest
using the Curve Expert 1.4 software (Hyams, 1997). accumulated volatilization was obtained in the fertilizer composed of
40% of MB.
  The cumulative emissions of N-NH3 as a function of the percentage
Y ¼ a= 1 þ exp −ðbþcxÞ ð3Þ of MB in fertilizers followed the linear regression model (p < 0.05) as
per Fig. 2.
It is observed that the increase in the proportion of MB favored the
The levels of N absorbed by the plant at the end of the experiment, as process of volatilization. Although MB has formed a physical barrier in
well as the values of volatilized N-NH3 were subjected to regression the fertilizer granule, it did not prevent the volatilization of N-NH3
analysis at the level of 5% probability of error, using the Minitab® from happening. On the other hand, the difference in volatilization, in
15.1.30.0 software. Finally, the cumulative values of volatile N-NH3 ob- terms of magnitude, was not significant. Thus, the result obtained in
served in the treatments with POF and conventional urea were com- the growth of plants can compensate for the negative result of volatili-
pared by the Tukey test, at the significance level of 5%. zation since the objective is to achieve synchrony between the release

Fig. 1. Daily (a) and cumulative (b) losses of N-NH3 volatilization after application of the different sources of N over time.

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A.S.A.P. Pereira, J.S. Castro, V.J. Ribeiro et al. Science of the Total Environment 779 (2021) 146205

and the UR fertilizer leaned towards a neutral pH. The high pH values
may be due to the biomass collection process, due to the elevation of
the pH that allows sedimentation and separation between algal biomass
and supernatant. Despite the subsequent pH correction, the algal bio-
mass was restored to alkaline form after drying.
These results can directly influence the pH of the soil and, conse-
quently, the rate of volatilization of N-NH3 and the rate of incorporation
of nutrients by plants. The method of application used in this study may
have favored the volatilization of N-NH3, so that the superficial applica-
tion exposed POF to temperature and humidity conditions.

3.2. Nutrients source efficiency in the Zea mays L. maize crop

3.2.1. N recovery rate by the plants

The presence of MB in the POF influenced the absorption of N in corn
Fig. 2. Accumulated volatilization (kg ha−1) as a function of different MB rates applied. ** plants. The results of the N content as a function of the percentage of MB
significant at 5% probability by t-test. applied followed the quadratic regression model (p < 0.05) as shown in
Fig. 3.
In analysis, the N content in the plant reaches its maximum in the
of the nutrient, its absorption by the plant, and minimization of the N proportion of 24.55% of MB, and reaches 196.85 mg pot−1 of N, which
losses through volatilization. means that from this proportion there is no increase in the N content
The values of accumulated volatilization over time were also ad- absorbed by the plant with the increase of MB. The rate of N recovery
justed to the logistic equation [Y = a/(1 + exp−(b+cx))] in order to un- by plants was 46.43% in MBU5; 54.23% in MBU15; 53.18% in MBU30;
derstand the behavior of each fertilizer tested against coefficients 51.93% in MBU40, 42.03% in MBU50; and 44.11% in UR. Thus, the
related to their release in the environment. Table 2 shows the coeffi- increase in the proportion of MB allowed the absorption of more N
cients obtained for each treatment. The “a” coefficient represents the by the plant up to a certain proportion. However, from the point of
saturation point of the curve, which is the maximum accumulation of inflection of the curve, where the MB concentration is approximately
volatilized N-NH3; “B” represents a position parameter that shifts the 25%, the N recovery rate tended to decline and, therefore, the ideal
curve through the x-axis, thus, the higher its value, the longer the proportion for the production of POF should be between 15 and
time to reach the maximum volatilization of N-NH3; and “c” is related 30% of MB.
to the rate of growth of the function and, therefore, is directly associated
with the volatilization of N-NH3. 3.2.2. Dry matter mass production of the plants and accumulation of macro
By obtaining these coefficients, it was possible to estimate the time and micronutrients
needed to reach half of the maximum N-NH3 emission (t1/2), which in- The application of POF influenced the SDMM production, as well as
dicates the time in which the inflection of the curve occurred. This value the macro and micronutrient content in the aerial part of the corn plants
infers on the speed in time (days) and the emission of volatilized N-NH3. (Fig. 4). The treatment that obtained the highest productivity, which
Analyzing the logistic equation (Table 2), the treatments with the means the highest SDMM was the MBU50 treatment followed by the
highest accumulative N-NH3 saturation values (coefficient “a”) showed MBU5, MBU40, MBU15, MBU30 last UR.
an increasing trend with the increase in MB in the fertilizer, pointing out Despite the addition of a multi-nutrient solution in all treatments,
that higher proportions of microalgae biomass favored the volatilization the macro and micronutrients present in MB may have had a positive
of N-NH3. Also, these treatments obtained a higher growth rate of the lo- result in the chemical composition of plants. Two examples of this are
gistic function (coefficient “c”), indicating that the volatilization process the elements Boron (B) and Sodium (Na), which followed linear regres-
happened more quickly. sion (p < 0.05), where it was observed that the increase in MB positively
The increase in the volatilization of N-NH3 due to the increase in the favored the concentration of these micronutrients. The presence of Na
proportion of MB may be related to two main factors: the pH of the POF in plants is due to the addition of NaOH during the algal biomass har-
and the method of application of the fertilizer in the soil. Regarding the vesting process. For the other macros (P and K) and micronutrients
results of the pH parameter of the POF produced, the following values (Fe, S, Zn), non-significant quadratic or linear regression behavior was
were observed: 8.58 (MBU5); 9.17 (MBU15); 9.52 (MBU30); 9.42 observed (p > 0.05). The high Fe values may be due to the type of soil
(MBU40); 9.55 (MBU50); and 6.75 (UR). An alkaline tendency was ob-
served as the proportions of MB increased in the composition of the POF

Table 2
Coefficients of the logistic equation and time necessary to reach half the cumulative max-
imum production of volatilized N-NH3 in a period of 30 day for the different nitrogen
sources.

Treatments Logistic equation coefficients r S

aa ba ca t1/2

MBU5 14.20 −2.51 0.59 4.23 0.98 1.01

MBU15 14.84 −2.60 0.64 4.07 1.00 0.98
MBU30 15.21 −2.49 0.61 4.09 0.98 1.08
MBU40 15.21 −2.57 0.66 3.86 0.98 1.17
MBU50 15.08 −2.53 0.63 4.00 0.98 1.09
UR 13.83 −2.84 0.60 4.72 0.99 0.93
a
Logistic equation Y = a/(1 + exp−(b+cx)); MBU5 = 5% of MB + urea; MBU15 = 15% Fig. 3. N content (mg pot−1) of the aerial part of the corn plant (Zea mays L.) as a function
of MB + urea; MBU30 = 30% of MB + urea; MBU40 = 40% of MB + urea; MBU50 = 50% of the concentrations of Microalgae Biomass (%) present in the POF. Error bars indicate
of MB + urea; UR = urea. standard deviation. ** significant at 5% probability by t-test.

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A.S.A.P. Pereira, J.S. Castro, V.J. Ribeiro et al. Science of the Total Environment 779 (2021) 146205

Fig. 4. Macro and micronutrient characteristics present in the plants at the end of the experiment.

used in the experiment, but the presence of MB may have increased the 3.2.3. Characterization of the pastured organomineral fertilizer
availability of this nutrient and, consequently, increased the absorption The results obtained by SEM are shown in Fig. 5. In Fig. 5a, referring
by the plant. This result may have been influenced by the dynamics of to UR tablets, it is observed that the crystals that form the fertilizer are
nutrient release present in MB. larger and more visible, when compared to the produced POF. As the

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A.S.A.P. Pereira, J.S. Castro, V.J. Ribeiro et al. Science of the Total Environment 779 (2021) 146205

Fig. 5. Scanning electron microscope (SEM) image of the produced fertilizer tablets. (a) Urea; (b) MBU5; (c) MBU15; (d) MBU30; (e) MBU40; (f) MBU50.

proportion of microalgae biomass in the fertilizer increases (Fig. 5b, c, d, day of the experiment followed by a sharp drop, as observed by Yang et al.
e, f), the urea crystals become proportionally more “coated” and less (2020) who investigated the effects of combinations of Azolla,1 urea, and
visible. urease inhibitor on N-NH3 volatilization and in the rice productivity. The
The availability of N may be associated with some factors. The coat- main peak of volatilization occurred between the second and third day
ing of the fertilizer granules by organic matter is one of the factors that of the experiment, followed by secondary peaks on a smaller scale for a
may have acted as a physical barrier, affecting the release of N, and si- field experiment. Also, the authors observed that of the total applied
multaneously it may have favored macro and micronutrients present (270 kg N ha−1), 13.70% was lost via volatilization in the urea treatment,
in MB. Thus, as this nutrient is released, both the availability and assim- and the greatest reduction was in the treatment that combined urea,
ilation of N from plants and the rate of volatilization of N-NH3 in the soil Azolla, and urease inhibitor, reducing the volatilized accumulated N-
can be influenced. NH3 in half (Yang et al., 2020). In all treatments evaluated by Li et al.
(2018) the peak of volatilization was reached on the first or second day
4. Discussion after application of the N fertilizer, followed by a sharp drop, and the
flow almost disappeared after the fifth day.
Several technical approaches have been studied to reduce the vola- The presence of organic compounds can influence the increase or
tilization of N-NH3 through biofertilizer or the combination of synthetic decrease in the volatilization of N-NH3, as shown in Table 3. These or-
fertilizers and organic compounds (Castro et al., 2017; Mandal et al., ganic compounds are also directly related to the chemical formula in
2019; Yang et al., 2020), as it's shown in Table 3.
It was observed that the N-NH3 volatilization process showed results 1
Azolla is an aquatic pteridophyte that fixes atmospheric N and forms a symbiotic asso-
that are consistent with what was observed in other studies that applied ciation with cyanobacteria, Anabaena azollae. Azolla is an efficient and fast-growing N fix-
organic sources to the soil. The peak of volatilization occurred on the third ative (Subedi and Shrestha, 2015).

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A.S.A.P. Pereira, J.S. Castro, V.J. Ribeiro et al. Science of the Total Environment 779 (2021) 146205

Table 3
Results of other studies regarding the volatilization of N-NH3 in the soil.

Sources Application method N Experiment N-NH3 Volatilization Reference

(kg ha−1) time (days) volatilization rate (%)
(kg ha−1)

MBU5 Solid and surface application 200 30 15.00 7.50 This paper
MBU15 15.81 7.91
MBU30 16.08 8.04
MBU40 16.29 8.15
MBU50 16.10 8.05
Biofertilizer Liquid and surface application 272 7 17.95 5.46 Yang et al. (2020)
Urea + Azolla + urea inhibitor
Urea 270 40.00 13.70
Poultry manure neutral biochar Solid and embedded in the soil 600 30 120 20.00 Mandal et al.
Neutral green waste biochar 140 23.33 (2019)
Soil + NPK 380 63.33
Biofilm of microalgae produced in Liquid and surface application in the 120 60 5.55 4.63 Castro et al. (2017)
wastewater soil
Wheat straw biochar + urea Solid and embedded in the soil 360 70 83.86 23.29 Sun et al. (2017)
Urea 400 54.60 13.65

− −
which N is available to the plant. However, several external factors, such ðNH4 Þ2 CO3 þ H2 O ! NHþ
4 þ OH þ HCO3 ð5Þ
as temperature, moisture, and soil pH, can determine how these two
−
processes will happen, in addition to the characteristics of the NHþ
4 þ OH ! NH3 þ H2 O ð6Þ
fertilizer used.
The physicochemical characteristics of the fertilizer tablets produced Thus, the increase in pH is caused by the hydrolysis reaction through
may also explain many of the observed effects. As seen in Fig. 5, the urea the consumption of protons and, therefore, urea is subject to volatiliza-
crystals were coated by the MB and could affect the availability of N and tion even in acidic soils (Novais et al., 2007). Interesting scientific ad-
its losses through volatilization of N-NH3. This coating may have acted vances have been developed to solve this problem regarding the
as a physical barrier during the release of the nutrient, as observed by increase in pH and the consequent increase in N-NH3 volatilization
Castro et al. (2020a, 2020b), who investigated the effects of P bioavail- rates. An example of this is research with neutral pH biochar derived
ability on the soil caused by the application of a granulated fertilizer from poultry manure and plant residues, which obtained reductions of
composed of triple superphosphate combined with MB. 47% and 38% of N N-NH3 emissions (Mandal et al., 2019). The re-
Several factors can, directly and indirectly, influence the volatility of searchers also found that the increase in plant biomass is due to reduc-
N-NH3. Many studies have been developed to follow and better under- tions in N-NH3 emissions, which means that reducing losses through
stand the chemical and biological processes that govern this process. volatilization provided an increase in the supply of N to plants. Sun
Matsushima et al. (2009), while evaluating the interactive effects of et al. (2017) evaluated the potential of biochar derived from wheat
types of compounds derived from cattle manure (low and high urease straw applied at varying rates in weight in delaying N losses by leaching
activity) and the form of synthetic fertilizers (urea and ammonium sul- and volatilization of N-NH3 in saline soils. The results showed that the
fate) on the volatilization of N-NH3, observed that the application of highest volatilization loads occurred in treatments with 2% and 4% bio-
both urea and ammonium sulfate, regardless of the type of compound, char and concluded that this increase in volatilization of 25.6% and
resulted in increased volatilization of N-NH3, compared to treatments 53.6%, respectively, was induced by the addition of alkaline biochar.
without compound. These authors attributed this behavior to the alka- The pH of the POF evaluated in this paper may have directly influ-
line pH of the compost, around 8.0, and thus the application of the com- enced the pH of the soil, due to its alkaline tendency and favored the
post can result in an increase of the soil pH. process of volatilization of N-NH3. The biomass harvesting step per-
The loss by volatilization of N-NH3 is influenced by several factors formed favored an increase in pH to promote sedimentation and sepa-
and mainly by the pH. The balance between the ammonium ion ration of the biomass and the supernatant through the addition of a
(NH+ 4 ) and ammonia (NH3) dictates how the availability of each of chemical agent. This stage is still a bottleneck for the production of
these elements will occur, as in acidic pH the predominant form is algal biomass, however, many works have been developed with the ob-
NH+ 4 . Tasca et al. (2011) evaluated, under laboratory, conditions the ef- jective of improving the process of harvesting and separation of
fect of pH (4.0; 5.5; 6.3 and 6.8), temperature (18 and 35 °C), dose (100 microalgae. Assis et al. (2020) proposed a hybrid system, on a pilot
and 190 kg ha−1) on N-NH3 volatilization. The daily loss was influenced scale, composed of a biofilm reactor coupled to an effluent treatment
by the increase in temperature, where the volatilization of N-NH3 was system, formed by HRAPs and decantation. This system indicates an in-
4.6 times lower in treatments at 18 °C compared to those observed at crease in the production and harvest of MB, in comparison with the sys-
35 °C. Soils with more alkaline pH also increased volatilization. There- tem composed only by the HRAPs. Ferreira et al. (2020), comparing
fore, in this study, where the average temperature varied between different biomass harvesting methods, observed that the performance,
23.6 °C and 18.4 °C, the N-NH3 volatilization process was favored by concerning biomass harvesting, was better in the method that uses tan-
the temperature at which the experiment was conducted. nin as a coagulant, with subsequent gravitational sedimentation. Thus,
This temperature effect is directly related to the acceleration of the the use of new methodologies in the MB harvest stage can favor the per-
urea hydrolysis process that releases ammoniacal N. Temperature and formance of the POF evaluated in this work, both in the sense of reduc-
pH are closely linked to the hydrolysis of urea [CO(NH2)2]. This process ing the volatilization of N-NH3 and in the productivity of the plants.
occurs due to the urease enzyme, resulting in the formation of ammo- The way of handling the fertilizer can also contribute to the volatili-
nium carbonate (Eq. (4)), which quickly decomposes into ammonium, zation of N-NH3. According to Tasca et al. (2011), observed that the
bicarbonate, and hydroxyl (Eq. (5)), raising the pH around the fertilizer physical state (solid and liquid) and the form of application of the fertil-
tablets. Therefore, NH+ 4 is converted to NH3 (Eq. (6)), which can be lost izer (superficial and incorporated) influenced the effect of the tempera-
to the atmosphere if not incorporated into the soil (Novais et al., 2007). ture increase in the N-NH3 volatilization process. For the temperature of
18 °C, the greatest losses occurred when the urea was applied in liquid
CO ðNH2 Þ2 þ 2H2 O ! ðNH4 Þ2 CO3 ð4Þ form, while for 35 °C, the application of solid urea provided greater

8
A.S.A.P. Pereira, J.S. Castro, V.J. Ribeiro et al. Science of the Total Environment 779 (2021) 146205

volatilization. Also, they pointed out that the incorporated application of agricultural production (Alvarez et al., 2021; Amenorfenyo et al.,
fertilizers made it possible to reduce the volatilization of N-NH3. Li et al. 2019; Renuka et al., 2018).
(2018) investigated the effects of application methods for different rates According to Renuka et al. (2018), there is a lot of progress in the use
of urea application and observed that the greatest losses occurred under of microalgae-based biofertilizers on a commercial scale. Products based
fertigation treatments, followed by diffusion and banding. Ribeiro et al. on microalgae grown in artificial environments that make it possible to
(2016) evaluated the loss of N-NH3 from different nitrogen fertilizers, increase plant productivity and soil fertility are already on the market
management methods (surface application and incorporated into the (Amenorfenyo et al., 2019; Renuka et al., 2018). The use of wastewater
soil) and observed that the urea treatment combined with organic ma- is a strategy to reduce the costs of cultivating microalgae, making algal
terial obtained greater accumulated volatilization of N-NH3 and that the biofertilizer economically competitive.
incorporated management reduced losses compared to surface applica- The reproducibility of the process and possible scenario of scale in-
tion. Castro et al. (2017) used algal biomass for the establishment of bio- crease should consider the influences caused by the characteristics of
film in the superficial layer of the soil, which led to lower losses via N- the wastewater and by the local environmental variables involved, es-
NH3 volatilization, in addition to providing an increase in the organic pecially during the stages of biomass cultivation and application of fer-
matter content in the soil, and the N tenor assimilated by plants did tilizer in the soil. These variables influence the diversity and
not differ in relation to the application of chemical fertilizer. productivity of microalgae and involve abiotic factors such as light in-
The use of microalgae biofertilizers is a more sustainable production tensity, temperature, climate, pH, the concentration of nutrients; biotic
alternative, allowing the recovery of nutrients commonly lost, for exam- factors such as the presence of microorganisms (species of bacteria,
ple, in conventional wastewater treatment. The results of this study in- microalgae, and viruses); in addition to operating conditions such as hy-
dicate that the combination of urea and microalgae favored an increase draulic holding time, mixing rate and biomass harvest (Gonçalves et al.,
in N tenor and content in plants. The nutritional potential of microalgae 2017).
is widely studied. Mulbry et al. (2005) found 4.51% of N and 1% of P in Still regarding the large-scale applicability, the scaled effects of soil
the biomass of algae produced from milk manure effluent. The authors toxicity caused by the application of the proposed fertilizer must be con-
also demonstrated that the supply of N and P to the cucumber and sidered, although it was not the focus of this study. Thinking about the
corn plants was the same for both the application of microalgae biomass possibility of scaling up, the importance of these analyzes should be em-
and the use of synthetic fertilizer. The nutritional potential of MB can be phasized due to the presence of heavy metals and pathogens in waste-
influenced by the variety of microalgae species cultivated (Khan et al., water, mainly due to the micro-algae bioremediation capacity (Hussain
2019). This nutritional potential is closely related to the chemical form et al., 2021; Leong and Chang, 2020). The main research needs that limit
that N becomes available. According to Mulbry et al. (2005), only 5% the use of microalgae biomass in the agricultural context mainly con-
of the N of the biomass is available in the mineralized form, and thus cern the production of microalgae on a large scale and to minimize
can be qualified as a slow-release fertilizer. costs and environmental impacts (Gonçalves et al., 2017). These aspects
Also, the addition of organic material has been proposed as an alter- of toxicity and other potential environmental impacts of large-scale
native strategy to improve soil management since the use of synthetic production can be evaluated through life cycle analysis (LCA) carried
fertilizers can negatively compromise microbial diversity, in addition out in several studies, as addressed by Arashiro et al. (2018) and
to causing acidification and salinization of the soil (Bonanomi et al., (Castro et al., 2020a, 2020b).
2020). Among the benefits, the improvement in hydraulic conductivity,
pH, total C, and total N, in addition to the cation exchange capacity (CEC)
5. Conclusion
observed by Uzoma et al. (2011) who investigated the effect of applying
cow dung weed in different proportions can be highlighted. The applica-
The results presented in this paper offer important information for
tion of microalgae biomass in the soil is also advantageous because, in
the development of technologies that promote the sustainability of ag-
addition to increasing the CEC, it also favors the establishment of a
ricultural production. The POF produced, composed of the combination
microalgae biofilm that allows the increase of the organic matter con-
of MB and synthetic fertilizer in different proportions, did not show any
tent in the soil, as observed by Castro et al. (2017). In the long run, as
difference in relation to the UR treatment regarding the accumulated
noted by Yu et al. (2020), who investigated the application of different
volatilization of N-NH3. The treatment with the highest accumulated
organic materials, the application of organic material increased the
volatilization of N-NH3 was MBU40. The highest rates of recovery of N
tenor of C and N fractions, even providing an increase in soil microbial
absorbed by plants were achieved in the MBU15 and MBU30 treatment,
biomass. Bonanomi et al. (2020), evaluating the effects of four types of
54.23%, and 53.18%, respectively. The highest recovery rate would be
organic additives (alfalfa straw, glucose, buffalo dung, and wood bio-
achieved in the proportion of 24.55% of MB.
char), concluded that long-term application (two years) improved
When the proportion of MB is 25%, there is no increase in N absorbed
crop productivity, plant health, in addition to increasing the quality of
by plants, at the same time that the volatilization of N-NH3 increases
the microbiota and the chemical properties of the soil, when compared
with the increase in MB. The application of the developed POF promotes
to the application of synthetic fertilizers, either alone or combined with
the absorption of nutrients, mainly N, but it's necessary to improve
fumigation.
some stages, as in the MB harvest, for the production of a neutral and ef-
ficient biofertilizer. Analyzing the sustainability of the fertilizer in terms
4.1. Future perspectives
of the environmental impacts generated is also important to measure
the potential for reducing impacts. Thus, it is suggested to evaluate the
The treatment of wastewater combined with the generation of
life cycle of the POF developed in this work and compare it with syn-
value-added products based on microalgae enables the development
thetic fertilizer, accounting for all incoming and outcoming of inputs
of the circular bioeconomy, through the recovery of nutrients, avoiding
during the production stage until their application to the soil.
the use of synthetic compounds for the production of this microalgae
biomass (Korhonen et al., 2018). Microalgae biomass in the agricultural
context is capable of stimulating the growth and development of several CRediT authorship contribution statement
crops, and can be considered a slow-release organic fertilizer because it
contains macro, micronutrients and contains substances that promote Alexia Saleme Aona de Paula Pereira: Conceptualization, Data
plant growth (Coppens et al., 2016; Ronga et al., 2019; Stirk et al., curation, Writing – original draft. Jackeline de Siqueira Castro: Concep-
2013), besides allowing the increase of the organic carbon stock and tualization, Supervision, Writing – review & editing. Vinícius José
the retention of water in the soil, and providing the sustainability of Ribeiro: Conceptualization, Supervision, Writing – review & editing.

9
A.S.A.P. Pereira, J.S. Castro, V.J. Ribeiro et al. Science of the Total Environment 779 (2021) 146205

Maria Lúcia Calijuri: Funding acquisition, Project administration, loading rates. Bioresour. Technol. 100, 4332–4339. https://doi.org/10.1016/j.
biortech.2009.04.016.
Supervision. Gonçalves, A.L., Pires, J.C.M., Simões, M., 2017. Review article a review on the use of
microalgal consortia for wastewater treatment. Algal Res. 24, 403–415. https://doi.
Declaration of competing interest org/10.1016/j.algal.2016.11.008.
Gregorich, E., Janzen, H.H., Helgason, B., Ellert, B., 2015. Chapter two - nitrogenous gas
emissions from soils and greenhouse gas effects. Advances in Agronomy, pp. 39–74
The authors declare that they have no known competing financial https://doi.org/10.1016/bs.agron.2015.02.004.
interests or personal relationships that could have appeared to influ- Hussain, F., Shah, S.Z., Ahmad, H., Abubshait, S.A., Abubshait, H.A., Laref, A., Manikandan,
ence the work reported in this paper. A., Kusuma, H.S., Iqbal, M., 2021. Microalgae an ecofriendly and sustainable wastewa-
ter treatment option: biomass application in biofuel and bio-fertilizer production. A
review. Renew. Sustain. Energy Rev. 137, 110603. https://doi.org/10.1016/j.
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Code 001] and the Brazilian National Council for Scientific and Kang, D., Kim, K., Jang, Y., Moon, H., Ju, D., Kwon, G., Jahng, D., 2018. International Biode-
Technological Development (CNPq) (grant number 420429/2018-2). terioration & Biodegradation Enhancement of wastewater treatment e ffi ciency
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