Abstract

Solid-phase denitrification is a promising approach to enhance nitrate removal. In this work, polybutylene succinate (PBS) and peanut shell (PS) (with crosslinked polyvinyl alcohol–sodium alginate (PVA-SA) as carrier) were used to prepare a composite solid carbon source (3P) to denitrify the secondary effluent. The results showed that for carbon release performance, 3P had not only a large release of organics, like PS, but also the excellent sustainability of PBS. Among the short chain fatty acids released by PBS, PS, PVA-SA and 3P, the percentages of acetic acid were 59.42%, 72.54%, 72.29% and 92.11%, respectively. When 3P was used as external carbon source, denitrification performance could be enhanced with effluent dissolved organic carbon lower than 20 mg/L. The prepared 3P could improve denitrification, from both microbial and kinetic aspects. The relative abundance of Gammaproteobacteria increased from 39.32% to 43.58%, and the half saturation constant of the fitting Monod equation was 21.28 mg/L. The prepared 3P is an ideal carbon source for secondary effluent denitrification. Using multiple crosslinking methods to produce carrier is an effective way to show the properties of each material.

HIGHLIGHTS

  • A modular composite solid-phase carbon source (3P) was prepared using polybutylene succinate and peanut shell, with crosslinked polyvinyl alcohol–sodium alginate as carrier.

  • The organics released from 3P showed good biodegradability and solubility.

  • The prepared 3P could improve denitrification from both microbial and kinetic aspects.

INTRODUCTION

In China, nitrogen pollution of surface water is among the most pressing environmental issues (Li et al. 2016a). Drainage from municipal wastewater treatment plants (WWTPs), the main runoff source for many Chinese rivers, is considered as one of the main pollution sources (Pan et al. 2016). Nowadays, most WWTPs implement the discharge standard of GB18918–2016 promulgated by the Ministry of Ecology and Environment of China (MEE 2016), and the total nitrogen concentration is limited to less than 15 mg/L (Shi et al. 2015). In the effluent, most nitrogen exists in the form of nitrate, and due to the low carbon to nitrogen ratio it is very difficult to achieve the standard (Feng et al. 2016). Although some novel biological nitrogen removal technologies have been developed to improve nitrogen removal performance, such as partial nitrification, simultaneous nitrogen and denitrification, and anaerobic ammonia oxidation, the most widely used process is still the traditional full-path nitrification and denitrification (Liu et al. 2017).

Solid-phase denitrification, in which the carbon source for denitrification is decomposed from organic solid, has been considered as a promising approach to enhance nitrate removal of secondary effluent (Wu et al. 2012). Compared to the traditional liquid-phase denitrification, solid-phase denitrification is easier to control, and is often used in denitrification filters and constructed wetlands (Xie et al. 2017). During the last two decades many different solid carbon sources have been tested (Li et al. 2016b). These carbon sources could be divided into two categories. One is agricultural wastes such as corncob, wheat straw, peanut shell (PS), and so on (Bao et al. 2016), which have huge yields and could achieve the effect of ‘treating waste by waste’ through removing nitrate from wastewater. However, the organics released from agricultural wastes are concentrated in the first few days (Huang 2017). Another is synthetic polymers, including polylactic acid, polybutylene succinate (PBS), polycaprolactone (PCL), and so on (Pierro et al. 2017), which could release organics continuously for several months, but they are more expensive than agricultural wastes. To overcome the above problems, blending agricultural wastes with synthetic polymers is a feasible approach. Xie et al. (2017) blended straw, bagasse and cob with poly-hydroxyalkanoates to produce a composite carbon source. Liu et al. (2014) blended PCL and starch to denitrify low carbon to nitrogen ratio wastewater. Shen et al. (2013) used starch and synthetic polymers to prepare a solid carbon source for biological denitrification. Although the above solid carbon sources all could improve denitrification performance, they were just scattered mixtures. Thus if a modular composite solid carbon source could be explored (spherical or massive solid), it will greatly improve the convenience in the application. However, few studies have been done to develop a suitable carrier and investigate how to crosslink the raw materials.

In the present study, synthetic polymer PBS and agricultural waste PS were selected as carbon source materials, with polyvinyl alcohol (PVA) and sodium alginate (SA) to form a carrier (Zain et al. 2011; Kumar et al. 2017). Through combining chemical crosslinking (PVA–boric acid) and physical crosslinking (freeze-thawing) (Bai et al. 2010), a modular composite solid carbon source PBS-PS-PVA-SA (3P) was prepared. The performances of carbon release and denitrification were investigated. The kinetics of denitrification and the variations of microbial community structure were also analyzed. These findings contribute to providing a comprehensive basis for practical application.

MATERIALS AND METHODS

Experimental materials

PS was collected from harvested peanuts, and PBS (molecular weight 50,000–80,000) was purchased from Taobao; they were both dried in the oven at 50 °C for 4 h.

PVA (polymeriation degree of 1,800) and SA were supplied by Shenzhen Huixin Co. (China). PVA and SA were dissolved in purified water to prepare a mixture (Mixture A) containing 8% PVA (w/v) and 1% SA (w/v), and then dropped into the saturated boric acid and CaCl2 (4%) solution. Finally it was kept at 4 °C to form spherical PVA-SA.

To prepare 3P, PS and PBS were dissolved by Mixture A to obtain a solution containing 8% PS (w/v) and 8% PBS (w/v), which was frozen at −20 °C with a 1 cm3 mold, and then dropped into the saturated boric acid and CaCl2 solution (4%) to crosslink at 4 °C for 24 h. Finally, the solid-phase carbon source of 3P was obtained. Its density is 1 g/cm3 and its compressive strength is greater than 260 N. The structure is shown in Figure 1.

Figure 1

Structure of PBS-PS-PVA-SA (3P).

Figure 1

Structure of PBS-PS-PVA-SA (3P).

Carbon release and denitrification tests

The carbon release tests were carried out in four 1,000 mL flasks (one flask for each carbon source). Each solid carbon source weighing 5 g was immersed in 800 mL ultra-pure water, respectively. During the 7 days of the carbon release test, samples were collected each day for short chain fatty acids (SCFAs), dissolved organic carbon (DOC) and chemical oxygen demand (COD) measurements.

The inoculated sludge for the denitrification test was collected from the anoxic tank of an urban WWTP (anaerobic–anoxic–oxic process, 15 × 104 t/d). It showed excellent denitrification performance and tawny color. Its mixed liquid suspended solid was around 3,000 mg/L. The inoculated sludge was idled for 12 h to exhaust the internal carbon source, then was washed twice by purified water and concentrated for 2 min (100 rpm). The denitrification tests were carried out in five 1,000 mL flasks (one flask for each carbon source, and one flask for no carbon source), which were placed on thermostatic shaking incubators (60 rpm, 25 °C). KNO3 was added to the synthetic wastewater with NO3-N of 20 mg/L; 5 g carbon source, 8 mL concentrated sludge (10,000 mg/L) and 800 mL synthetic wastewater were mixed in each flask. Both the carbon release test and the denitrification test were performed three times. Water samples were taken for DOC, NO3-N and NO2-N measurements each day. The denitrification kinetics is described by the Monod equation:
formula
(1)
where V is the denitrification rate of NO3-N, mg/(L·h); X is the mixed liquid suspended solid (MLSS), mg/L; Vm is the maximum specific denitrification rate, mg/(g·h); Ks is the half saturation constant, mg/L.

Measurements

The surface morphology of solid carbon source was observed with a JSM-7001F scanning electron microscope (SEM) combined with energy dispersive spectroscopy (EDS) (Japan). High throughput sequencing was measured by Majorbio Bio-engineering Biotechnology Co. Ltd (Shanghai, China). Water samples were taken and filtered by a 0.45 μm membrane before analysis. COD, NO3-N, NO2-N and MLSS were measured according to standard methods (APHA 2002). DOC was measured using a total organic carbon (TOC) analyzer (Hach, IL530 TOC). Dissolved oxygen (DO) and pH were monitored by a WTW 340i DO meter. Acetic acid, propionic acid and butyric acid were measured by a Dionex Integrion HPIC analyzer (Thermo Fisher Co., China).

RESULTS AND DISCUSSION

The performance of carbon release

The release of DOC from each carbon source is shown in Figure 2. The DOC concentration released from each carbon source decreased in the order of PS, PVA-SA, 3P, PBS, which corresponded to 122.59, 101.41, 30.21, and 17.58 mg/L, respectively. The amount of released organics from 3P lied between agricultural waste (PS) and synthetic polymer (PBS). It should be noted that although the released amount of PS was the biggest, most organics were released in the first 24 h, while 3P showed the best sustainable release performance. In addition, the ratio of COD to DOC can represent the biodegradability of organics (Khursheed et al. 2018). When the organics are soluble, 1 g DOC equates to 2.67 g COD (Xiong et al. 2019). For PS, PVA-SA, 3P and PBS, the average COD/DOC of the released organics was 1.96, 3.54, 3.06 and 3.24, respectively. The COD/DOC ratio of 3P was closest to 2.67, which indicated, considering biodegradability and solubility of the released organics, 3P was the optimal carbon source.

Figure 2

DOC release of each carbon source.

Figure 2

DOC release of each carbon source.

The cumulative released acetic acid, propionic acid and butyric acid of each carbon source are shown in Figure 3. The cumulative released SCFAs decreased in the order of PVA-SA, PS, 3P, PBS, which corresponded to 0.743, 0.737, 0.520 and 0.482 mg/g, respectively. For each carbon source, acetic acid is the main component, followed by butyric acid except for PBS. As a polymer of bytanediol and succinic acid, PBS released more propionic acid than butyric acid. In addition, for PVA-SA, PS, 3P and PBS, the percentages of acetic acid in the cumulative released SCFAs were 72.29%, 72.54%, 92.11% and 59.43%, respectively. The biodegradability of the SCFAs improved with the increase of the percentage (Khursheed et al. 2018). The SCFAs released by 3P were the most biodegradable, which was consistent with the COD/DOC ratio.

Figure 3

SCFAs release of different carbon sources.

Figure 3

SCFAs release of different carbon sources.

The performance of nitrate removal

Changes in NO3-N and DOC in the denitrification test are presented in Figure 4. It should be noted that because of the excellent adsorption capacity of activated sludge (AS), even when AS was added alone, NO3-N could be reduced, from 20.00 mg/L to around 12.68 mg/L. Adding external carbon source improved denitrification performance, especially in the first 24 h, and no obvious NO2-N accumulation was observed. The quick acclimation could be attributed to the components of the released organics, which could be utilized and metabolized by many kinds of microorganisms. Although the carbon sources with more released organics improved denitrification, they also increased the effluent DOC. For the flasks with added PVA-SA, PS, PBS and 3P, the final NO3-N concentrations were 0.07, 0.05, 9.31 and 6.33 mg/L, respectively. Correspondingly, the final DOC concentrations were 75.23, 86.23, 14.52 and 19.53 mg/L, respectively.

Figure 4

Denitrification performances under each carbon source: (a) PVA-SA; (b) PS; (c) PBS; (d) 3P.

Figure 4

Denitrification performances under each carbon source: (a) PVA-SA; (b) PS; (c) PBS; (d) 3P.

Kinetics analysis of denitrification was calculated based on the Monod equation. NO3-N denitrification rates under each carbon source were measured in two steps: the first step was to calculate the apparent slope by observing changes in concentrations of NO3-N over time; the second step was to calculate the differences between the slopes under each external carbon source and only AS. The evaluated parameter values are shown in Table 1. For each carbon source, a good agreement between the Monod equation and measured denitrification rates was achieved, while carbon source with higher released organics agreed better. The carbon source with a bigger Vm indicates it could achieve a higher maximum specific denitrification rate. Based on the evaluated Vm, PS presents the maximal Vm. The carbon source with lower Ks indicates it could present the maximum denitrification performance at lower NO3-N concentration. According to the evaluated Ks, PBS and 3P could maximize their denitrification capacity when treating the secondary effluent (NO3-N is around 15.00 mg/L).

Table 1

Parameter values of denitrification kinetics under different external carbon sources (where R2 is the fitting correlation coefficient)

Carbon sourceMonod equation
Ks (mg/L)Vm (mg/(g·h))R2Fitted equation
PVA-SA 75.10 20.08 0.95 y = 3.74x + 0.05 
PS 38.30 20.41 0.97 y = 1.88x + 0.05 
PBS 24.22 0.46 0.79 y = 52.26x − 2.20 
3P 21.28 0.66 0.73 y = 32.48x − 1.53 
Carbon sourceMonod equation
Ks (mg/L)Vm (mg/(g·h))R2Fitted equation
PVA-SA 75.10 20.08 0.95 y = 3.74x + 0.05 
PS 38.30 20.41 0.97 y = 1.88x + 0.05 
PBS 24.22 0.46 0.79 y = 52.26x − 2.20 
3P 21.28 0.66 0.73 y = 32.48x − 1.53 

Different from other research which only used chemical crosslinking, 3P also used physical crosslinking, i.e. freezing. The variation of the organics released by multiple crosslinking also affected its denitrification performance. PVA-SA was prepared only by chemical crosslinking; from Table 1 it could be seen that its maximum specific denitrification rate was similar to that of PS. The reason was chemical crosslinking by saturated boric acid and CaCl2 solution could form a porous structure on the micro level (Wu et al. 2012). When combining chemical and physical crosslinking, as the main carrier of 3P, its maximum specific denitrification rate decreased from 20.08 mg/(g·h) to 0.66 mg/(g·h). This was because freezing reduced the porosity of the carbon source (Takei et al. 2011).

Denitrification mechanism

3P was sampled immediately after fresh preparation, the carbon release test and the denitrification test to observe the surface morphology. The surface of fresh 3P was coarse with hollows under SEM observation (Figure 5(a)). After the carbon release test, its surface changed little, while the distribution of C element became denser under EDS observation (Figure 5(b)). After the denitrification test, the surface of 3P became more coarse due to microorganism corrosion, and the distribution of C element became less dense (Figure 5(c)). These indicated the organics degraded by 3P diffused from inside to the surface, and would be utilized as electron donor for denitrification or carbon source for assimilation.

Figure 5

SEM and EDS (distribution of C element) images on the surface of 3P. (a) Fresh preparation; (b) after carbon release; (c) after denitrification.

Figure 5

SEM and EDS (distribution of C element) images on the surface of 3P. (a) Fresh preparation; (b) after carbon release; (c) after denitrification.

The inoculated AS, the AS after denitrification without external carbon source (AS-AD) and with 3P as external carbon source (AS-AD-3P) were sampled for high throughput sequencing. The results covered more than 98.0% of microbial species; in each sample most bacteria were grouped into Gammaproteobacteria and Bacteroidia, and the sum of both classes accounted for around 58.40%, 47.93% and 60.50% in AS, AS-AD and AS-AD-3P, respectively (shown in Figure 6). Both Gammaproteobacteria and Bacteroidia were reported as denitrifying bacteria (Lu et al. 2014; Bojko et al. 2018). Gammaproteobacteria were further enhanced in the denitrification process to increase from 39.32% to 43.58%. In the AS collected from a WWTP, Gammaproteobacteria accounted for more than 35% of total effective bacterial sequences (Wang et al. 2018), which was consistent with the results of this study. Nitrospira are known to be the prevalent nitrification bacteria (Ge et al. 2015), and their relative abundance decreased from 1.50% of the AS to 0.84% of the AS-AD-3P. The reduction of Nitrospira indicated that the groups belonging to nitrification bacteria had no competitive advantage in the habitats using 3P as external carbon source.

Figure 6

Relative abundances of the predominant phylogenetic groups of activated sludge at genus level.

Figure 6

Relative abundances of the predominant phylogenetic groups of activated sludge at genus level.

The percentage of nitrogen removed through denitrification was calculated according to nitrogen and carbon balances. For carbon balance, the DOC concentrations when external carbon sources and AS were separately and together added were used to calculate the carbon utilized for nitrogen removal. For nitrogen balance, the residual NO3-N concentrations with and without external carbon source were used to calculate the removed NO3-N. Theoretically, completely denitrifying and assimilating 1 g NO3-N will consume 1.07 and 4.28 g DOC, respectively (Ge et al. 2015; Han et al. 2019). Based on this, when PVA-SA, PS, PBS and 3P were used as external carbon source, the percentages of NO3-N removed through denitrification were 43.21%, 18.27%, 9.32% and 37.63%, respectively.

Through the analysis above, it could be seen that 3P is a suitable solid-phase carbon source for nitrate removal in secondary effluent. When it was used for application in a full-scale WWTP, to achieve ideal denitrification performance, we could not only change the dosage (Xiong et al. 2019), but also increase the proportion of agricultural wastes in the component. The agricultural wastes such as rice straw and corncob could be used as solid carbon source (Dai et al. 2018). Although the amount of released organics from these materials in the initial phase was high (Yang et al. 2015), combining chemical and physical crosslinking has been proved to be an available method to slow down the releasing rate of organics.

CONCLUSIONS

A modular composite solid carbon source, 3P, was prepared by synthetic polymers PBS and agricultural waste PS with PVA-SA as carrier. The prepared 3P is an ideal carbon source to denitrify secondary effluent; the percentage of acetic acid in released SCFAs was 92.11%, and the half saturation constant was 21.28 mg/L. The 3P could not only improve denitrification performance with effluent DOC concentration lower than 20 mg/L, but also enhance the relative abundance of Gammaproteobacteria from 39.32% to 43.58%. Based on the treated wastewater, adjusting the ratios of raw materials to prepare a corresponding solid carbon source is the direction of future research.

ACKNOWLEDGEMENTS

This study was financially supported by Key Scientific Research in Colleges and Universities of Henan Province Project (No. 20B560018), the National Major Science and Technology Project for Water Pollution Control and Treatment (2015ZX07204-002), and Henan Province Key Research and Development and Promotion Special Projects (182102311041).

DATA AVAILABILITY STATEMENT

All relevant data are included in the paper or its Supplementary Information.

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