A comparative study of phosphorus removal using biopolymer from aerobic granular sludge: A factorial experimental evaluation

Journal Pre-proof A comparative study of phosphorus removal using biopolymer from aerobic granular sludge: A factorial experimental evaluation Patricia Dall’ Agnol, Nelson Libardi Junior, Jose´ Miguel Muller, ´ Jessica Antunes Xavier, Dayane Gonzaga Domingos, Rejane Helena Ribeiro da Costa

PII:

S2213-3437(19)30664-5

DOI:

https://doi.org/10.1016/j.jece.2019.103541

Reference:

JECE 103541

To appear in:

Journal of Environmental Chemical Engineering

Received Date:

17 September 2019

Revised Date:

5 November 2019

Accepted Date:

12 November 2019

Please cite this article as: Agnol PD, Junior NL, Muller JM, Xavier JA, Domingos DG, da Costa RHR, A comparative study of phosphorus removal using biopolymer from aerobic granular sludge: A factorial experimental evaluation, Journal of Environmental Chemical Engineering (2019), doi: https://doi.org/10.1016/j.jece.2019.103541

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A comparative study of phosphorus removal using biopolymer from aerobic granular sludge: A factorial experimental evaluation

Patricia Dall’ Agnola*, Nelson Libardi Juniora, José Miguel Mullerb, Jéssica Antunes Xaviera, Dayane Gonzaga Domingosa, Rejane Helena Ribeiro da Costaa. a

Department of Sanitary and Environmental Engineering, Federal University of Santa

Catarina - UFSC, 88040-970, Florianópolis, Brazil. Department of Food Engineering, Federal University of Santa Catarina - UFSC,

88040-970, Florianópolis, Brazil.

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*[email protected] (corresponding author).

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Graphical Abstract

Highlights 

ALE is a new biomaterial to be considered in real-life biorefinery context.

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

The ALE recovery yield of 21.3% was obtained from spent aerobic granules.



The phosphorus removal of 72% was achieved using ALE beads through adsorption.



Phosphorus adsorption and desorption improve ALE’s potentiality as biosorbent.

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Abstract

This work presented an integrated approach to recover nutrients and biomaterials

from wastewater, resulting in a phosphorus-enriched biomaterial with the potential for

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additional applications. The present investigation explored phosphorus removal from

liquid samples using ALE recovered from aerobic granular sludge. The pH of the

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phosphorus solution, dosage of ALE beads, temperature and initial phosphorous

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concentration were factors tested through a factorial experimental design, with the results compared with commercial seaweed alginate. The ALE recovery from

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discarded aerobic sludge granules was 21.29±1.57%. ALE beads demonstrated the potential to remove phosphorus (49.54±2.23%) from liquid samples better than

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commercial seaweed alginate (36.78±2.10%). The results from the factorial experiment indicated pH and dosage of ALE beads as the main parameters for

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phosphorus removal. Regeneration of ALE beads and the phosphorus recovery experiments showed the potential of using this biomaterial as a biodegradable phosphorus slow-release source. Keywords Phosphorus removal; Biosorption; Alginate-like exopolymer; Phosphorus Recovery; Aerobic granular sludge.

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1. Introduction Phosphorus is widely used in animal feed, detergents, beverages, chemical pesticides and water treatment [1]. Phosphorus and nitrogen are essential nutrients for food production; more than 95% of the mined phosphorus and 88% of ammonia are used for fertilizer production and animal supplementation [2]. Two antagonistic scenarios have focused attention on these nutrients. First, is the contribution of these nutrients to water bodies through runoff, untreated sewage disposal and inefficient nutrient removal [3]. Second, phosphorus demand is increasing, primarily for

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agricultural use, which is having an impact on mineral reserves and, consequently, on prices. Furthermore, phosphate deposits are lacking in some regions of the world.

Known reserves are centered in Morocco, China and the United States and are thus

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subjected to international political influences, making them dependent on importation

and market fluctuations [1, 4, 5]. Humanity is mining five times more phosphorus

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than is used, due to losses at each stage of processing, from rock mining through the

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food chain. It is estimated that phosphate reserves could be exhausted in the next 50100 years, leading the European Commission to classify phosphate as a critical raw material [4, 5]. Close to 100% of the ingested phosphorus is excreted in urine and

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feces, accounting for a yearly load of 3 million tons, turning wastewater treatment plants into phosphorus “hotspots” [4]. The excess of nutrients produces a hypertrophic

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environment. In aquatic ecosystems, enrichment with nutrients like phosphorus is

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termed eutrophication. Eutrophication of water resources is considered to be the leading cause of changes in surface water quality, which restricts water usage [6]. Adsorption has been employed as a promising technique for the removal and

recovery of phosphorus because of its cost-effectiveness, simplicity, insensitivity to toxic pollutants, biodegradability and environmental-friendliness [7]. Different types of adsorbents have been produced from wastes that are capable of removing

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phosphate from liquids samples [8, 9]. An alternative is to turn some waste in adsorbents [8, 10, 11, 12] or using bio-based materials [13, 14, 15, 16, 17]. Bio-based materials deriving from natural resources, called biosorbents, are naturally occurring, renewable, and have lower costs compared to synthetic adsorbents. In addition, they have high adsorption capacity, properly remove potentially hazardous materials, and have low environmental risks [5, 18]. Biosorbents could be converted into valueadded post-sorption by-products that can be applied to other uses, e.g., as fertilizers in agriculture. This characteristic can overcome the main drawback of the adsorption

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technique--the non-destructive nature of non-biological adsorbents [5, 19]. Biological sludge is produced on the order of a million tons annually during the operation of a wastewater treatment plant, and is considered an environmental and

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economic concern due to its treatment and disposal [20]. The use of bioproducts extracted from biological sludge would reduce the impacts of this residue in a

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sustainable way. In this sense, industrial units called wastewater biorefineries have

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been developed, allowing for the production of high added-value co-products from the residual wastewater and biomass. This encompasses concepts of the circular economy, foreseeing less waste, maximization of used resources and transformation

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of residues into economically attractive products [21]. Egle et al. [5] proposed that municipal wastewater contains a phosphorus load that, if recovered, would replace

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half of the yearly-applied phosphorus fertilizer demand for European agriculture.

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Alginate-like exopolymer (ALE) has been described as a new biomaterial extractable from aerobic granular sludge (AGS) [8, 22, 23]. AGS is a promising wastewater treatment technology characterized by the formation of dense microbial aggregates and extracellular polymeric substances (EPS) naturally induced in sequencing batch reactors (SBR) [22]. The aerobic granules are formed by aerobic, anoxic and anaerobic microbial layers, allowing the simultaneous removal of carbon, nitrogen

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and phosphorus in a single reactor, resulting in smaller constructed areas and lower energy demands [24]. The recently described structural similarities between ALE and alginate extracted from seaweeds, such as their hydrogel behavior [22], favors their use for similar applications. Although seaweed alginate can be used for a wide variety of applications, the costs of its production are increasing due to restricted seaweed availability. ALE, then, is an interesting candidate to replace seaweed alginates in some applications [25]. In the environmental field, alginate-based hydrogels have

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been used for the adsorption of different classes of pollutants. The application of ALE for the adsorption of pollutants was recently proposed by Ladnorg et al. [26], who tested the adsorption of methylene blue by ALE in comparison with alginate beads.

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The authors found that ALE beads achieved dye removal efficiencies (69%) similar to those of alginate beads (79%).

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The simultaneous recovery of phosphorus from liquid samples with aim of

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reusing it in conjunction with the recovery of ALE from discarded aerobic granular sludge is in keeping with the actual demands for the removal and recovery of phosphorus from wastewater by the use of new biomaterials with added-value. With

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this in mind, our aims were: (1) to identify optimal conditions (pH, temperature, initial phosphorus concentration, and dosage of alginate and ALE beads) for

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phosphorus removal; (2) to evaluate and compare the capacities of alginate and ALE

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beads to remove phosphorus from liquid samples; (3) to evaluate the extraction yields of ALE from the aerobic granular sludge of a pilot plant and (4) to evaluate the capacity of ALE beads to release phosphorus in different solutions.

2. Material and methods 2.1 ALE source and extraction - Aerobic granular sludge sequencing batch reactor 5

A pilot-scale SBR with a working volume of 980 L and a volumetric exchange ratio of 50% was operated for 342 days treating domestic wastewater. The reactor was operated under room temperature, without pH control, aerated from the bottom with an airflow of 234 L per min and up-flow velocity of 0.55 cm s-1. The treatment process was carried out in sequential 6-hour batches: 90 min of simultaneous feeding and withdrawal, 240 min of aeration and 30 min of settling. The mean sludge retention time was maintained at 199 days; discarded sludge was collected and frozen until its use in extraction experiments.

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Sludge volumetric index (SVI) was determined by measuring biomass volume after 5, 10 and 30 min of settling. Volatile suspended solids (VSS) were monitored

according to APHA [27]. Granulometric analyses were performed according to

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Laguna et al. [28] using sieves of various mesh sizes.

The ALE extraction procedure was performed according to Felz et al. [23]

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with some adaptations. EPS was solubilized from biomass under alkaline, high

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temperature and agitation conditions followed by precipitation of the biopolymer under acidic conditions. The ALE extraction procedure started with the centrifugation of the sludge sample at 2,150 g (KASVI, K14-4000, BR) for 30 min. The sludge

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pellet was then transferred to 250 mL baffled Erlenmeyer flasks for alkaline extraction with Na2CO3 at 80ºC and stirred for 35 min at approximately 400 rpm. A

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second centrifugation step at 2,150 g for 25 minutes was used to separate the EPS in

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the supernatant fraction. ALE was extracted from EPS by the addition of 1 M HCl to a final pH of 2.2 ±0.05 while stirring at approximately 100 rpm. Afterwards, a new centrifugation step was performed to recover the extracted ALE. Extraction yields of ALE from AGS were calculated based on the analysis of total solids (TS) and volatile solids (VS), performed in triplicate [23, 27]. The yield was calculated according to Equation 1, where η corresponds to yield (%), VSALE

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corresponds to the ALE volatile solids (mg g-1), and VSsludge corresponds to the volatile sludge solids (mg g-1).

VSALE

η = (VS

sludge

) × 100

(Equation 1)

2.2 Phosphorus removal experiments A standard stock solution of phosphorus at 100 mgP L-1 was prepared with K2HPO4. The phosphorus concentration in the samples was measured by the ascorbic

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acid method [27]. A spectrophotometer (Hach, DR3900, BR) set at a wavelength of 880 nm was used to measure the absorbance; the readings were compared to a

previously constructed calibration curve with concentrations ranging from 0.0 mg L-1

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to 2.5 mg L-1.

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Phosphorus removal tests using ALE and alginate beads were conducted through batch experiments. ALE in the spherical form (beads) was obtained by first

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adjusting the extracted ALE pH to 8.5, forming a gel-like material, which was then dripped into a 12.5% (w/v) CaCl2 solution using a Pasteur pipette. Beads were kept in

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the CaCl2 solution for 15 min, washed with deionized water to remove excess calcium chloride and stored in distilled water at 2°C for 24h until used.

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Calcium alginate beads were investigated for use as basis of comparison to determine the efficacy of ALE beads as an adsorbent material. Sodium alginate 0.5%

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(w/v) was dissolved in distilled water using a mechanical stirrer (Thelga, TMA10R, BR). The resulting solution was dripped with a burette into a 12.5% (w/v) CaCl2 solution to form alginate beads. Alginate beads were washed with deionized water to remove calcium chloride excess.

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Both alginate and ALE beads were used in the wet form since drying destroys their spherical structure. Fig. S1 in the supplementary material shows ALE beads before and during the adsorption experiments in the synthetic phosphorus solution. To evaluate the combined effects of all of the parameters tested, a full factorial design was applied. The Box–Behnken matrix of 24 factorial design shows the 16 treatments performed in duplicate, requiring 32 experiments, as presented in the supplementary material (Table S1). Factors and levels were selected according to preliminary experiments which were based in others studies presented in Table S2.

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The low and high levels tested are shown in Table 1. The dry mass of the beads was determined by the gravimetric method after drying at 105 ºC for 19 h [27]. Dry mass was further used to determine the dose of beads used on a dry mass basis.

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Experiments were conducted in a thermostatic bath with reciprocal agitation (Marq Labor, BM/DR, BR). A synthetic phosphorus solution (100 mg L-1) was added

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to 250 mL Erlenmeyer flasks containing 40 mL of K2HPO4. Removal kinetics were

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evaluated after 120 min, when 0.5 mL samples were collected. Samples were centrifuged (Novatecnica, NT 805, BR) at a rotational speed equivalent to 2,753 g for 2 min in 1.0 mL tubes. The supernatant was collected, and the phosphorus

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concentration of the supernatant analyzed.

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Table 1 Factors and levels used in the factorial design.

Factors

T

Temperature

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Initials

Levels (-)

(+)

Units

25.0

45.0

(°C)

4.0

8.0

pH

pH

C

Initial phosphorus concentration

10.0

100.0

(mgP L-1)

d

Beads dosage

0.39

3.95

(g L-1)

Statistica (StatSoft, USA) software was used in the development of the experimental design, with a randomized experimental order to avoid systematic

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mistakes. A first-order polynomial model was used to identify all possible interactions of selected factors obtained from the Box–Behnken model. The model was calculated using 2-way interactions between factors, at a confidence level of 95%. Factors or their combinations resulting in p-values higher than 0.05 were discarded. Equation 2 shows the model with two predictors and interaction terms. This equation was expanded for four factors, where y corresponds to the response variable, xi is the variable that represents factors, o is a constant, 1 is the partial regression coefficient,

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ij is the coefficient of the interaction of the factors, and ϵ is the error.

y = β0 + β1 x1 + β2 x2 + β12 x1 x2 + ϵ

(Equation 2)

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The effects of the individual factors in addition to interactions for the simultaneous variations in the factors were evaluated based on the kinetics of

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phosphorus removal efficiency (Er) (%). Er was calculated using Equation 3, where CI

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corresponds to initial phosphorus concentration (mg P L-1) and Ct corresponds to the

CI −Ct CI

× 100

(Equation 3)

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Er =

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final phosphorus concentration (mg P L-1).

To compare the real adsorption of ALE with others materials the adsorption

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capacity (q) in mg P g-1 was obtained by the Equation 4 which relates the CI corresponds to initial phosphorus concentration (mg P L-1), Ct corresponds to the final phosphorus concentration (mg P L-1), adsorbent dry mass (g), and volume of phosphorus solution (L). q=

(CI −Ct ) × V m

(Equation 4)

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Significant effects, those considered for the model and that most influenced the response, were obtained by the least-squares method and statistically evaluated by analysis of variance (ANOVA). This statistical analysis allowed us to determine the significant factors influencing response for interaction model.

2.3 Characterization of beads 2.3.1 Point of zero charge of ALE and alginate beads Point zero of charge (pHpzc) was determined according to Mustafa et al. [31].

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For this analysis 6.0 g of beads were added to 40 mL 0.01 M NaCl solutions, set in at a pH range between 2 and 11, and kept in Erlenmeyer flasks for 24 h at 25°C. Before

the final pH measurement, flasks were agitated for 30 min. The pHPZC is the point on

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the graph of initial pH versus ΔpH where the line crosses the x-axis, in other words,

when the pHf – pHi= 0 [22]. The exact pHpzc value was obtained by the arithmetic

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mean of the final pH values forming the plateau in the initial pH versus final pH plot.

2.3.2 Characterization of ALE beads - before and after phosphorus removal Scanning Electron Microscopy (SEM) equipped with Energy Dispersive

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Spectroscopy (EDS) was used to observe the morphology and the chemical composition of the tested materials. To analyze microstructure and composition,

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samples were frozen then lyophilized for 48 h in a benchtop lyophilizer (Liotop L101,

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Brazil). Lyophilized samples were fixed with silver glue on an aluminum support and sputtered-coated with gold. Analyses were conducted using a scanning electron microscope (JEOL JSM-6390LV, USA) operating at 10 kV, with magnifications ranging from 50x up to 1,000x at a resolution of 1 µm to 500 µm. Fourier-transform infrared spectroscopy (FTIR) analyses were carried out using a spectrometer (Agilent, Cary 600 Series, USA) with a horizontal attenuated

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total reflectance accessory (ZnSe), in the wavenumber region of 400–4000 cm-1, resolution of 4 cm-1, using 20 scans for each sample. Samples were lyophilized prior to the analyses.

2.4 Release study Phosphorus release after phosphorus removal was evaluated using ALE beads loaded in a synthetic phosphorus solution at pH 8. 6 g of ALE beads (0.158 g dry mass) were added to 40 mL of the release solutions in Erlenmeyer flasks. The

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following release solutions were used: distilled water; 0.01 and 1.0 M of HCl; 0.01 and 1.0 M of NaCl; 0.01 and 1.0 M of NaOH. Flasks were stirred for 120 min at 25°C

at 200 rpm in a thermostatic bath and the final concentration of released phosphorus

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measured.

Regeneration of ALE beads was tested through a second removal/release

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cycle, using a 100 mg L-1 phosphate solution. The efficiency of released phosphorus

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from the beads was calculated by dividing the amount of phosphorus released by the

3. Results

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amount of phosphorus removed from the test solution, in terms of relative percentage.

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3.1 AGS production and recovery of ALE The aerobic granules used for ALE extraction procedures presented an SVI30

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mean value of 9838 mL g-1 and ratios SVI30/SVI10 and SVI30/SVI5 of 0.8 and 0.6, respectively. The average VSS during the operation period was 1,345  679 mgVSS L-1. The majority of the granules (mean of 45%) presented a diameter between 212 and 300 μm. The AGS used in the ALE recovery process resulted in a concentration of 212.87±15.65 mgVSALE gVSsludge-1 (representing a yield of 21.29±1.57%).

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Considering the mean sludge production of 271 gVSS day-1 and the treatment flow capacity of 1,960 L day1, it is possible to assume that the pilot plant operation followed by the ALE recovery procedure used in this investigation would yield 28.6 g ALE m-3 of treated wastewater.

3.2 Kinetics of phosphorus removal The highest phosphorus removal efficiency (72.50±2.79%) was achieved using a pH value of 8.0, an initial phosphorus concentration of 100 mg L-1, and ALE beads

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dosage of 3.95 g L-1 at 45 ºC (Fig. 2D). With these experimental conditions, ALE

beads showed an increase of 37% in removal efficiency compared to that obtained using alginate beads (53.11±1.50%).

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A more detailed analysis was conducted for the phosphorus removal kinetics

with respect to pH and dose of beads, the two factors that most influenced phosphorus

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removal efficiency when using the ALE beads. Kinetics shows that the maximum

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removal value, considered as the equilibrium, was reached in the first few minutes of the experiment, between 10 and 20 minutes.

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Comparisons with low and high pH levels are shown in Figs. 1 and 2, respectively. Regarding the pH of the tested solutions, pH 8 resulted in higher

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removal efficiencies compared to pH 4, and this effect was greater for higher phosphorus concentrations. An examination of the results at a constant temperature

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(25°C) indicates that the mean removal efficiency for ALE beads is 21.68 ± 2.22% (Fig. 1C), which is increased to 62.60 ±3.16% (Fig 2C) by increasing the pH from 4 to 8. For alginate beads at a temperature of 45°C, these values are increased from 9.02±5.33% at pH 4 to 53.11±1.50% at pH 8. Comparing the phosphorus removal between different temperatures for ALE beads, an increase of 20°C caused a threefold

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increase in removal efficiency. This was observed at both pH 4.0 (Fig. 1A and 1B) pH

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8.0 (Fig. 2A and 2B).

Fig. 1 Kinetics of phosphorus removal (mean ± standard deviation) at pH 4.0, beads

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dosage (d) of 3.95 g L-1 and variation of the initial phosphorus concentration (C) and temperature (T). A) C = 10 mgP L-1; T = 25°C; B) C = 10 mgP L-1; T= 45°C; C) C=

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100 mgP L-1; T = 25°C ; D) C = 100 mgP L-1; T= 45°C.

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Fig. 2 Kinetics of phosphorus removal (mean ± standard deviation) at pH 8.0, beads dosage (d) of 3.95 g L-1 and variation of the initial phosphorus concentration (C) and

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temperature (T). A) C = 10 mgP L-1; T = 25°C ; B) C = 10 mgP L-1; T= 45°C; C) C=

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100 mgP L-1; T = 25°C ; D) C = 100 mgP L-1; T= 45°C.

3.3 Experimental design analysis for phosphorus removal

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The experimental model for removal efficiency was determined based on the

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60 min phosphorus removal test (supplementary Table S1). A regression equation was developed based on the experimental results obtained in the ANOVA analyses (supplementary Tables S3, for alginate and S4 for ALE). For each tested material (ALE and alginate), different analysis and experimental models were proposed. The Pareto diagram shows the statistically significant factors, which were considered input factors in the model (Fig. 3). The

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Pareto diagram for alginate beads (Fig. 3A) shows that fewer factors influencing the efficiency of phosphorus removal are significant when compared to efficiency of ALE beads (Fig. 3B). Initial phosphorus concentration, pH and beads dosage are significant

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for both biosorbents.

Fig. 3 Pareto chart for the absolute effect values for phosphorus removal considering

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p = 0.05: A) alginate beads B) ALE beads.

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The response surface diagram for the combination of the factors for phosphorus removal using ALE beads shows that the combinations with more

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significant effects were pH and temperature (Fig. 4A and 4B). For alginate beads, the combinations of factors influence phosphorus removal less than was the case for ALE

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beads (Fig. 5). Only the combination of C and pH resulted in a surface indicating a maximum point of phosphorus removal. For the alginate beads, other combinations

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were less important.

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Fig. 4 Interactions of the controllable factors for the use of ALE beads (warm colors

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indicate higher phosphorus removal values).

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Fig. 5 Interactions of the controllable factors for the use of alginate beads (warm

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colors indicate higher phosphorus removal values).

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The regression coefficient (R²) for alginate beads was 0.76 and the adjusted coefficient (R) was 0.73. Also, for the ALE beads, the coefficients were 0.91 (R²) and

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0.87 (R). The ANOVA results are presented in the supplementary material (Table S3 and Table S4). The regression equation for phosphorus removal efficiency (Er %) by the alginate (ErALGINATE) and ALE beads (ErALE) were obtained for the factors, using their coded values. The model for code units is presented in Equations 5 and 6 for ALE and alginate, respectively. Table S5 and S6 show the standard error to the regression coefficient for ALE and alginate beads, respectively. 17

Er ALE (%) = 24.86 + 16.66 × d + 9.13 × pH + 5.81 × pH × d + 5.40 × T × d + 5.33 × T + 4.85 × pH × C + 4.00 × C– 4.85 × T × C

(Equation 5)

Er ALGINATE (%) = 17.03 + 8.34 × C + 7.95 × d + 6.87 × pH + 4.29 × pH × C (Equation 6) In terms of the adsorption capacity of ALE beads the best results in the samples for the time span of 60 min were q= 57.25 ± 12.18 mg P g-1 for T= 45°C,

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pH=8, C=100 mg P L-1 and d= 0.39 g L-1. Alginate beads presented values in the same order of magnitude but higher value than ALE beads, q = 69.15 ± 28.02 mg P g-1 the

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same experimental conditions for ALE beads.

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3.4 Characterization of beads

3.4.1 Point of zero charge of ALE and alginate beads

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Point of zero charge for the phosphorus removal for both ALE (Fig. 6A and Fig 6B) and alginate beads (Fig. 7A and Fig. 7B) are in the range of pH 7.0. A

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horizontal line (Fig. 6B and 7B) between pH values without variation after 24 h indicates that the buffering effect is in this range. NaCl acts as a buffer solution for

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pH between 3.0 and 10.0 for ALE and 4.0 and 10.0 for alginate beads. The exact

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values of pHpzc are 7.02 ± 0.45 for ALE bead, and 6.72 ± 1.22 for alginate beads.

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Fig. 6 A) Plots of ΔpH vs initial pH; B) Plots of final pH vs initial pH for salt addition method for 0.01 M NaCl (mean ± standard deviation, n = 2) for ALE beads.

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Fig. 7 A) Plots of ΔpH vs initial pH; B) Plots of final pH vs initial pH for salt addition

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method for 0.01 M NaCl (mean ± standard deviation, n = 2) for alginate beads.

3.4.2 Characterization of ALE beads - before and after phosphorus removal

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No porosity was observed on the surface of the bead, but Fig. 8D and 8H

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reveal the various layers formed in the beads interior. The main aspect observed in SEM images is the presence of adhered particles to the bead surface as well as in its

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inner layers after the process (Fig. 8E to Fig. 8H).

Fig. 8 SEM images at different magnifications before phosphorus removal A) 50 x; B) 200 x; C) 1,000 x; D) 200 x cutting; After the phosphorus removal E) 50 x; F) 200

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x; G) 1,000 x and H) 200 x cutting. Conditions for beads: pH of 8.0, initial phosphorus concentration of 100 mg L-1 and ALE beads dosage of 3.95 g L-1.

The EDS analysis (Table 2) shows that ALE beads are composed mainly of carbon and chlorine. Quantities of each element are variable after and before the phosphorus removal. Besides the main elements, phosphorus and potassium were also identified after phosphorus removal.

process.

C-K

Before phosphorus removal Weight % Atom % 44.50 65.65

C-K

After phosphorus removal Weight % Atom % 27.00 59.77

6.72

8.50

N -K

3.16

6.00

O -K

6.56

7.26

O -K

4.08

6.78

Na -K

0.21

0.17

Na -K

0.04

0.04

Cl - K

22.71

11.35

Cl - K

9.13

6.85

Ca - K

13.45

5.94

Ca - K

7.74

5.14

P-K

0.00

0.00

P-K

1.86

1.59

K–K

0.00

0.00

K–K

1.24

0.84

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5.85

1.13

Other elements*

45.75

12.98

100.00

100.00

Total

100.00

99.99

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Total

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N -K

Other elements*

Elements like Nb, Tc and Rb.

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*

Element

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Element

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Table 2 ALE beads composition by EDS before and after phosphorus removal

The FTIR-ATR spectrum of the ALE beads before (blue line) and after

phosphorus removal (red line) (Fig. 9) shows the similarity between the two spectra. The 3370 cm-1 wave numbers are associated with the free hydroxyl group in the symmetry of the H-O-H bond vibration. The aliphatic C-H stretching vibrations are observed at 2945-2850 cm-1. The bands around 1656-1432 cm-1 correspond to the

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symmetrical and asymmetrical stretching of the vibration of the carboxylate ions (OC-O) [32]. An approximation in the spectra shows a wavelength at 1240 cm-1, indicating the presence of acetyl ester. According to Luo et al. [13], the P-O stretching

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region is generally observed in the range of 1000-1100 cm-1.

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Fig. 9 A: FTIR analysis of ALE beads before (blue line) and after (red line) the

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phosphorus removal process. B: approximation of the FTIR analysis.

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3.5 Phosphorus release

The Fig. 10 shows the condition of the beads after the regeneration process,

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and the Fig. 11 shows the release of phosphorus using different solutions. For the first cycle, solutions of HCl resulted in an adhered phosphorus release of 55.05% and

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60.80% for 0.01M and 1M, respectively. Results of the same order of magnitude were obtained for NaOH solutions. The smallest concentration released 56.60% and the

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highest 61.60%. However, it was not possible to carry out a second cycle since the NaOH solution caused the disintegration of the ALE beads (Fig. 10). The use of HCl 0.01M as release solution resulted in a 33.06% phosphorus release in the second cycle. The second cycle using 1M HCl did not result in any phosphorus removal. For NaCl, the second cycle showed the highest relative release of phosphorus--78.10% for 1M of solution.

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Fig. 10 ALE beads after the regeneration using different solutions: A) NaOH, which

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the ALE beads collapsed; B) NaCl ; C) deionized water and D) HCl.

Fig. 11 Relative release percentage of phosphorus in different release solutions (C1:

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first cycle of removal and release; C2: second cycle of removal and release).

4. Discussion

4.1 ALE recovery from AGS The granular biomass used for ALE extraction procedures was in line with the aerobic granulation standard proposed by De Kreuk et al. [33] and Liu et al. [34], in which about 50% of the particles had diameters above 200 µm. In addition, the

22

SVI30/SVI10 ratio was close to 0.9, as proposed by Liu and Tay [35] for a complete granulation process. These parameters are of great importance since the diameter of the granules is associated with the polysaccharides excreted around the microbial biomass. Although the development and long-term maintenance of AGS treatments in real domestic wastewater is challenging, it is central to obtaining high ALE titres and ensuring an efficient treatment. High efficiencies for carbonaceous as well as for nitrogenous organic matter were observed. ALE extracted from the AGS resulted in a yield of 21.29±1.57%, similar to the

ro of

yield (16%) obtained by Lin et al. [22], using the HCl extraction route. Other studies reported ALE recovery efficiencies ranging from 5% to 33% [23, 36]. The limited number of scientific publications regarding the yield of ALE extracted from AGS

-p

leads to a comparison with the seaweed alginate. Manns et al. [37] reported the

ethanol extraction route from Laminaria digitata and Saccharina latissima, resulting

re

in alginate yields from 16 to 36%. Vauchel et al. [38] used the HCl extraction route

lP

for Laminaria digitata and reported extraction yields of 38%. However, the ALE extraction process was not yet extensively studied and optimized, since research in this area is more recent [22].

na

The pilot plant used in this work would achieve 1.7 Kg of dry ALE per month, considering the amount of sludge obtained and the yields ALE. This result is based on

ur

simple assumptions; more in-depth technical studies need to be performed. However,

Jo

the magnitude of ALE recovery indicates the potential for resource recovery. Considering existing projects for ALE recovery on a real scale WWTP [39], it is possible to achieve higher recovery yields with the development of this technology.

4.2 Phosphorus removal

23

The adsorption capacity allows comparing the different materials. The results for this variable shows that the ALE and alginate beads present similar capacity compared with others materials (Table S2) as alginate-derived bead constituted of poly(N-isopropylacrylamide interpenetrated in alginate-Zr4+ network [13] and chitosan bead [29]. Regression coefficients for experimental models indicated the best results obtained for ALE beads; the interaction of dose of beads and pH showed a synergic effect on phosphate removal. The reduction of phosphorus in synthetic solutions

ro of

occurred in the first 20 min for both ALE and alginate beads, indicating that phosphorus removal is faster than for other adsorbent materials [8, 40, 10]. Most of the phosphorus present in the synthetic solution was removed by ALE beads

-p

(72.50±2.79%) in the kinetic analyses. This result was similar to that obtained by Li et

al. [8], who also achieved removal efficiencies around 75% using beads of drinking

re

water treatment residuals.

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The influence of bead dosage was also observed by other authors for phosphorus removal using different biosorbents, such as fly ash [11] and red mud [10]. These authors observed that the reduction of bead dosage decreases the

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phosphorus removal as well as the Ca+2 concentration. However, part of the phosphorus removal reported by the authors may be attributed to the chemical bond

ur

between orthophosphate and the aluminum (Al) and iron (Fe) present in the adsorbent

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[8]. These authors analyzed the solution supernatant after either centrifugation [10] or filtration [11, 12, 17, 30] of the samples. This procedure may also remove secondary particles and consequently interfere with the quantification of phosphorus and calcium in solution. However, these studies reported an inverse relationship between pH and initial phosphorus concentration for phosphorus removal. This can be explained by

24

the presence of Ca+2 ions in the chemical composition of the tested adsorbent materials. The natural characteristic interaction between phosphorus and Ca+2 produces precipitated solid particles, like those observed for Al and Fe, as cited above. Different solid forms of orthophosphate (PO4-3, HPO4-2 e H2PO-) are obtained when combined with cations, (e.g. calcium chloride as a coagulant) that can form inorganic salts in water [41]. Rietra et al. [42] attempted to minimize precipitation and favor the adsorption on goethite. They observed that at high pH values, Ca+2 has its strongest

ro of

influence on PO4 binding. For adsorption on goethite, the dominance of electrostatics regulates the cation and anion adsorption by a reversible process controlling the sorption behavior.

-p

Regarding pH, since the pKa of sodium alginate is about 3.2 [43], and considering that alginate is an acid with low pKa, this substance tends to be ionized in

re

the presence of an alkali. This favors the swelling and disintegration of the alginate

lP

beads at basic pH values (pH = 7.4), which is sufficient to start this process [43, 44]. Therefore, the best result for the phosphorus removal should be addressed carefully since the disintegration of the beads could release calcium that could precipitate

na

phosphorus. Additionally, the pHpzc results showed that the solution pH should be lower than 7.0 to allow positively charged ions to form on the surface of the bead,

ur

which can attract the negatively charged phosphorus. Analysis of pHpzc indicates that

Jo

values of the beads were neutral, so above these values the beads present negative charges and therefore can bind with compounds of positive charges. Considering phosphate as the sorbing anion, it will form a covalent chemical bond with a metallic cation at the sorbent surface [45]. The removal of phosphorus is improved when the beads’ charge is positive, so the pH of the solution must be below 7.0. Therefore, the real adsorption occurred at pH 4.0, with phosphorus removal efficiencies of

25

36.78±2.10% for alginate beads (Supplementary Table S1, line 4), and 49.54±2.23% for ALE beads (Supplementary Table S1, line 11).

4.3 Phosphorus adhered in ALE beads The SEM analysis at the surface of ALE beads after phosphorus removal enables us to observe particles that could be calcium bound with phosphorus. Sujitha and Ravindhranath [17] observed a very similar aspect when adsorbed phosphorus on calcium alginate beads. Another observation with SEM was that the structure of the

ro of

bead remained intact after the phosphorus removal process, indicating its resistance to the agitation and chemical stress [8].

The composition obtained by EDS shows that ALE beads (Table 2) were

-p

similar to those of sodium alginate, a salt derived from alginic acid, which is mainly composed of carbon, hydrogen, sodium and oxygen [46]. The chemical structure

re

between seaweed alginates and ALE extracted by aerobic granular sludge are similar

lP

in terms of the composition because the (1→4)-α-L-guluronic acid blocks (GG) that provides the gel characteristics [22, 47]. However, the ALE composition is very complex and can vary according to the wastewater source.

In general, ALE is

na

composed around 38% of protein, 13.8% of sugar, 28.6% of humic acid equivalent and 7.2% of uronic acids [48].

ur

Calcium and chlorine in EDS are due to the presence of CaCl2 used as the

Jo

reticulation solution. But these elements were reduced in the EDS before and after the adsorption. Two possible aspects can explain the weight and percentage chloride and calcium. First, the excess of these elements in the reticulation solution may be removed of the beads by the agitation during the experiment. Other aspect is the potential ligation and precipitation of the calcium and chloride with elements of the synthetic solution (K2HPO4). The occurrence and increment in weight and percentage

26

of phosphorus and potassium (Table 2) is a result of the adsorption and ligation of particles on the surface of ALE beads. Though, a weight reduction in calcium and chlorine exist, maybe due to the precipitation of these elements with potassium and phosphorus by their chemical affinity. Other elements in EDS are classified as metals and are not common in real wastewater. The x-ray peaks for Nb, Tc, P and Au (2.166, 2.424, 2.013 and 2.120 KeV, respectively) were very similar, which could overlap each other. Gold (Au) as the coating material for SEM preparation may overlap with x-rays produced from the

ro of

elements in the sample. Also, Rb has a peak of 1.694 keV, a very close value to the Na (1.041 keV) and Al (1.486 keV), possibly overlapping these elements. Na is part of the composition of the ALE beads, and Al is part of the supporting material for

-p

SEM and EDS analysis. The composition results obtained by EDS indicate that removal of phosphorus occurs from the liquid fraction. Similar results were presented

re

by Li et al. [8], who attributed the different form of the peak/values of EDS before

lP

and after the adsorption to the phosphorus adsorption.

Identification of free hydroxyl groups in FTIR indicates that both samples presented hygroscopic characteristics, as seen through the high-frequency region with

na

the elongation vibrations of O-H bonds [49], indicating the presence of moisture in the sample. Identification of acetyl esters corresponding to the production of bacterial

ur

alginate is also reported in seaweed alginate [50]. Finally, phosphorus in the beads

Jo

was identified after liquid sample phosphorus removal as a small displacement between the peaks 1000 - 1079 cm-1 about the blue line, which indicates the adsorption of the phosphate by the polymer. However, this also indicates that the chemical interaction between polymer and phosphorus is weak, and no substantial chemical changes are observed in the sample after adsorption.

27

Sometimes the chemisorption and physiosorption may occur simultaneously. The kinetics behavior analysis may not be sufficient to identify and differentiate these processes. Both cases may have low or high velocity in reaching equilibrium, consequently high or low activation energy [51]. The low chemical interaction reported by FTIR analysis (Fig. 9) should be carefully evaluated. Chemisorptions are characterized only by the binding of the adsorbent active sites [51]. Since the FTIR analysis just used an aliquot of the crushed ALE beads, only part of the active sites the spheres were evaluated, underestimating the phosphorus content. In addition, there

ro of

are complex processes between phosphate, OH− and humic substances, present in the sphere composition and/or synthetic solution [52]. According to the conditions of the solution and the amount of P adsorbed, there are interferences in the organic matter

-p

release. The hydrolysis and ligand exchange processes also influence the adsorption

re

process [52].

lP

4.4 Phosphorus recovery and ALE bead regeneration

The regeneration process for biosorbents (e.g., ALE beads) is of extreme

na

importance both for the recovery of the adhered molecule of interest (e.g., phosphorus) and to replenish the active sites of the biosorbent for reuse. However,

ur

few studies were carried out in this sense, even though tests of the regeneration processes are important to analyze the economic viability of the material and to

Jo

minimize the produced waste [40, 53]. The use of an alkaline solution like NaOH has been suggested as desorption

solution for phosphate recovery, since hydroxide ions act as a strong Lewis base, in concentrations from 0.1 to 1 M [40]. However, the use of this alkali caused the disintegration of the ALE beads and a second regeneration cycle was not possible. This phenomenon was related to the contact of alginate with alkaline solutions, which

28

was previously discussed. According to Kumar et al. [40], both chemisorption and surface precipitation can occur depending on the nature of the biosorbent. Calcium precipitates could be formed and blocked the ALE beads’ active sites so a previous acid wash to remove precipitates followed by NaOH regeneration would be beneficial to increase removal efficiencies over the successive cycles. With NaCl and ultrapure water as regeneration solutions, the second cycle presented the highest relative release of phosphorus. However, this was due to the low adsorbed phosphorus in the second cycle, which was efficiently released. This

ro of

behavior was also observed by Kumar et al. [45], using iron oxide-based adsorbents for phosphorus removal from wastewater.

Since ALE beads have calcium in their structure, which will probably interact

-p

with phosphate in solutions and form precipitates, successive adsorption and

regeneration cycles will be negatively impacted. Therefore, from a technological point

re

of view, ALE beads enriched with phosphorus could be used as post-sorption material

lP

that could be disintegrated and used, e.g., as a slow-release phosphorus material [19]. Since most of the compounds in ALE beads are organic, ALE enriched beads could be used in agriculture or animal feed, after detailed studies about their possible

na

toxicity and nutritional composition.

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4.5 Practical implications

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ALE is a new biopolymer recovered from AGS and able to be used for

phosphorus recovery from wastewater. Its low cost and organic nature contribute to the economic feasibility of this technology. However, higher removal capacities and regeneration cycles are necessary to make this bioproduct more cost-effective and to expand its lifetime. Chemical modification could be used to increase its selectivity towards phosphate. However, any change in the ALE beads must be made with a

29

focus on keeping the beads as a material that can be used as a secondary source of phosphorus. The low market acceptance for products recovered from wastewater sludge is still an obstacle for food or medical applications. Nevertheless, industrial-grade alginate applications in the environmental and agricultural field seem to be promising. The use of ALE beads for phosphorus removal from wastewater and their application as a phosphorus slow-release material sounds interesting. Before it can be used as a fertilizer, complete chemical characterization and biological compatibility studies

ro of

should be performed to comply with legal parameters for the agricultural use of sludge residues.

Seaweed alginate production depends on high-energy demands for pumping,

-p

biomass dewatering and concentration, resulting in operational costs of 1,080 USD

per ton of alginate [55]. Meanwhile, AGS is produced as a by-product of the waste-

re

water treatment process, and it can be directly used for ALE extraction. The market

lP

prices for industrial-grade alginate products are in the range of 2,000 to 10,000 USD/ton and it is even higher for food- and pharmaceutical grade products [56]. Clearly, there is an apparent market demand and technological opportunity for the

na

recovery ALE from AGS, with the central advantage of being a residue transformed

ur

in value-added product.

Jo

5. Conclusion

In this study, the pilot-scale SBR produced AGS and ALE was extracted and

recovered from the AGS in yields similar to those obtained in other studies. ALE beads showed a potential to remove phosphorus (49.54±2.23%) from liquid samples, better than commercial alginate (36.78±2.10%). Bead dosage, pH, temperature and initial phosphorus concentration all influenced the amount of phosphorus removed.

30

Although phosphorus surface precipitation is possible, characterization techniques indicated a real adsorption process. Regeneration of ALE beads provided phosphorus recovery but combined acid and alkali solutions would increase the lifecycle of the ALE beads and increase recovery yields. ALE is a new material with the potential to be used as biosorbent to improve water quality in terms of phosphorus removal. Simultaneously, phosphate enriched ALE can be used as a phosphorus source in a

ro of

wide range of applications.

Funding

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This work was financed by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Brasil (CAPES) (Finance code 001), Conselho Nacional de

CAPES PRINT 01/2018 programe.

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Desenvolvimento Científico e Tecnológico-Brasil (CNPq), Brazil and CG/UFSC

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Declarationsof interest

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Declarationsof interest: none

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Acknowledgements

We thank for the Laboratory of Thermodynamics and Supercritical

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Technology, Central of Analysis of the Department of Chemical Engineering and Food Engineering, and Central Laboratory of Electronic Microscopy both in the Federal University of Santa Catarina by the characterization analyzes.

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