Recent advancement on biological technologies and strategies for resource recovery from swine wastewater

Bioresource Technology 303 (2020) 122861

Contents lists available at ScienceDirect

Bioresource Technology journal homepage: www.elsevier.com/locate/biortech

Review

Recent advancement on biological technologies and strategies for resource recovery from swine wastewater

T

Hai-Hsuan Chenga, Birgitta Narindria, Hsin Chua, Liang-Ming Whanga,b,c,

⁎

a

Department of Environmental Engineering, National Cheng Kung University, No. 1, University Road, Tainan 701, Taiwan Sustainable Environment Research Laboratory (SERL), National Cheng Kung University, No. 1, University Road, Tainan 701, Taiwan c Research Center for Energy Technology and Strategy (RCETS), National Cheng Kung University, No. 1, University Road, Tainan 701, Taiwan b

GRAPHICAL ABSTRACT

ARTICLE INFO

ABSTRACT

Keywords: Wastewater Nutrient Anaerobic Microalgae

Swine wastewater is categorized as one of the agricultural wastewater with high contents of organics and nutrients including nitrogen and phosphorus, which may lead to eutrophication in the environment. Insufficient technologies to remove those nutrients could lead to environmental problems after discharge. Several physical and chemical methods have been applied to treat the swine wastewater, but biological treatments are considered as the promising methods due to the cost effectiveness and performance efficiency along with the production of valuable products and bioenergies. This review summarizes the characteristics of swine wastewaters in the beginning, and briefly describes the current issues on the treatments of swine wastewaters. Several biological techniques, such as anaerobic digestion, A/O process, microbial fuel cells, and microalgae cultivations, and their future aspects will be addressed. Finally, the potentials to reutilize biomass produced during the treatment processes are also presented under the consideration of circular economy.

1. Introduction 1.1. Characteristics of swine wastewater According to the Food and Agriculture Organization of the United Nations (http://www.fao.org/faostat/en/#home), nearly a billion pigs were raised for food market worldwide every year (2010–2017) and the ⁎

produced nitrogen was over 7 billion kilogram per year, while total swine wastewater in China was estimated to be approximately 0.16 billion tons per year (Yu et al., 2020). Swine wastewater contains high level of suspended solid, organic matters, nutrients (mostly nitrogen), and several toxic compounds such as heavy metals, antibiotics, and hormones which may cause serious environmental and human health problems (Zhang et al., 2016). The eco-friendly society demand is rising

Corresponding author at: Department of Environmental Engineering, National Cheng Kung University, No. 1, University Road, Tainan 701, Taiwan. E-mail address: [email protected] (L.-M. Whang).

https://doi.org/10.1016/j.biortech.2020.122861 Received 25 November 2019; Received in revised form 18 January 2020; Accepted 20 January 2020 Available online 23 January 2020 0960-8524/ © 2020 Published by Elsevier Ltd.

Bioresource Technology 303 (2020) 122861

H.-H. Cheng, et al.

metabolically ineffective for the microbial nutrient removal activities and reduce the population of viable cells by time (Zeng et al., 2015). The complexity in swine wastewater, i.e. the mixture of polysaccharides, proteins, lipids and many other nutrients, make it a suitable substrate for anaerobic digestion (Córdoba et al., 2016). Recently, the advanced technologies like microbial fuel cell (MFC) (Min et al., 2005), membrane bioreactor (MBR) (Padmasiri et al., 2007), upflow anaerobic sludge blanket (UASB) (Cheng et al., 2019; Song et al., 2010), sequencing batch reactor (SBR) (Yang et al., 2016, 2019), and upflow solid reactor (USR) (Yang et al., 2019), were being tested in order to enhance the COD removal efficiency of anaerobic digestion. On the other hand, the techniques to remove or recover the remaining nutrients like PO43--P and NH4+-N and trace amount of antibiotics in the anaerobic digested wastewater were also being developed (Xu et al., 2019). Some advanced technologies have been observed to recover or remove the nutrients in the swine wastewater like the bioelectrochemical system and membrane technologies, for example, electrodialysis with the series of cation or anion exchange membranes (Ward et al., 2018) or sequencing-batch membrane bioreactor (SMBR) with alteration between anaerobic and aerobic conditions (Xu et al., 2019). The high cost in operational and maintenance requirements are considered as the obstacle in the application feasibility, the requirement for pumping system, maintenance for scaling up, or electrical current requirement are exist with the inefficient removal performance (Kelly and He, 2014). Therefore, as the relatively inexpensive options, biological processes, including aquatic plants, algae and microalgae, and advanced nitrogen removal technologies, are still more attractive for the polishing of anaerobic digested swine wastewater. It was recently summarized that the integrated systems of dark fermentation/digestion and the cultivation of microalgae could be economically feasible and become a bioenergy platform for the treatment of organic wastes (Chen et al., 2018a). In the following sections, advanced biological processes that were used or can be potentially used for the treatment of swine wastewater will be collected.

Table 1 General characteristics of swine wastewaters. Location

Sichuan, China Zhejiang, China Monells, Spain Sichuan, China Lodi, Italy Minnesota, USA Guangzhou, China Yongin, Korea Milano, Italy Kyungbuk, Korea Saitama, Japan

Status

Diluted Settled Settled Raw Raw Filtered Filtered Filtered Filtered Filtered Diluted

TS (SS)

COD (BOD)

TN (NH4+-N) TP

%

g/L

g-N/L

g-P/L

1.0 (0.9) – (0.7) – (1.2) – (0.9) 2.1 (–) 1.1 (–) – (0.5) 5.6 (–) 1.0 (0.8) 6.2 (–) – (0.1)

7.6 (4.2) 7.0 (–) 2.5 (1.2) 8.4 (5.0) 25.0 (–) 8.8 (3.7) 3.7 (–) 92.8 (–) – 130.8 (–) – (90.3)

– (0.3) 1.5 (1.4) 0.3 (0.2) 1.6 (0.6) 1.7 (1.3) 1.2 (0.9) 0.2 (–) 7.3 (4.9) – 7.3 (4.8) 4.5 (–)

– 0.03 – 0.2 – 0.6 0.2 0.5 – – 2.6

Ref.

1 2 3 4 5 6 7 8 9 10 11

1

(Yang et al., 2019); 2(Zeng et al., 2019); 3(Vilajeliu Pons et al., 2017); 4(D. Yang et al., 2016); 5(Schievano et al., 2016); 6(Wu et al., 2015); 7(Zhu et al., 2013); 8(Zhang et al., 2011); 9(Tenca et al., 2011); 10(Ahn et al., 2006); 11(Kim et al., 2004)

especially for the appropriate treatments of industrial, agricultural, and municipal waste. Therefore, sufficient treatments are also required before the swine wastewater discharge (Cheng et al., 2019; Marjakangas et al., 2015; Wang et al., 2015). Swine wastewater usually contains more than 1% of total solid (TS) which are mostly organic, and the concentration, in terms of chemical oxygen demand (COD), is varied between less than 10 g/L to more than 100 g/L in extreme cases, as listed in Table 1. There is also nitrogen and phosphorus in the swine wastewater with the total nitrogen (TN) concentration of 0.2–7.3 g-N/L and the total phosphorus (TP) concentration around 0.2–0.5 g-P/L. Commonly, the swine farm applied simple technologies either in primary or secondary treatment processes, such as lagoon, anaerobic digester (Abdel-Raouf et al., 2012; Cheng et al., 2019; Yang et al., 2019), or three-stage A/O process which consists of solid/liquid separation, anaerobic treatment and aerobic process (Chien et al., 2016), to reduce COD level in their wastewater, while some farms even discharge the wastewater with insufficient treatments (Wang et al., 2015). These traditional processes, in general, only could achieve less than 90% of COD and has limited ability to remove nitrogen or phosphorus in swine wastewater, and the secondary effluent is then discharge with significant amount of inorganic nitrogen and phosphorus which leads to the long-term environmental problem (AbdelRaouf et al., 2012). The anaerobic treated swine wastewater has the COD of 3–15 g/L, NH4+ - N of 0.4–1.4 g/L, TN of 0.6–1.2 g/L, and TP of 100–250 mg/L (D.L. Cheng et al., 2018).

2. Carbon recovery technologies in swine wastewater treatment 2.1. Microalgae cultivation For decades, the cultivation of microalgae and cyanobacteria for treating swine wastewater gains large attraction among the researchers. Regarding to the carbon consumption mechanism, microalgae have the ability to be autotrophic, heterotrophic, or mixotrophic depend on the conditions of the cultivation system. Microalgae grow autotrophically by uptaking inorganic carbon like CO2 in the presence of light as the energy source via photosynthesis, while they grow heterotrophically by consuming organic carbon when light is absent. Several types of microalgae also have the ability to utilize either organic or inorganic carbon simultaneously in the mixotrophic environment (Gupta et al., 2019). Recently, the combination of simultaneous CO2 fixation, swine wastewater nutrients removal, and microalgae cultivation gain the big attraction among the researchers (Choi et al., 2019; Qilu et al., 2018). The application of swine wastewater in the microalgae cultivation system reduces not only the cost in freshwater requirement but also the nutrient supply. Swine wastewater provides essential nutrients for the microalgae growth and instantly the high efficiency in nutrient degradation will be in accordance with the microalgae biomass production (Arias et al., 2018; Gupta et al., 2019; Marjakangas et al., 2015). The microalgae cultivation provides attractive step to treat the nutrient inside the wastewater by the tertiary biological treatment coupled with the potentially valuable products and by-products (Abdel-Raouf et al., 2012; Chen et al., 2019). Fig. 1 displays the metabolic pathways of organic matters, nitrogen, and phosphorus in biological systems, including bacterial and microalgal metabolisms (Batstone et al., 2002; Guo et al., 2013; Gupta et al., 2019; Moreno-Vivián et al., 1999; Sun et al., 2018). Similar to the

1.2. Current difficulties in carbon and nutrients recoveries Several health and environmental risks occurred by the inadequate maintenance and treatment of the swine wastewater. Improper treatment will carry out the human health problem, water eutrophication, soil pollution, antibiotic resistant gene, and the estrogenic activity (Cheng et al., 2019), however, the high operational cost of the wastewater treatment technology in some countries is the main reason to apply ineffective process (Zeng et al., 2015). Conventional wastewater treatment may lack of the variable efficiency due to the nutrient composition, high cost efficiency, and production of the secondary pollution which lead to the incomplete process (Abdel-Raouf et al., 2012). Anaerobic biological treatment, which have been wildly applied in the past decades, is a cost-effective technology due to low energy consumption and the high efficiency in methane-rich biogas production (D.L. Cheng et al., 2018). Anaerobic treatment produces small amount of sludge compared to aerobic system, which lower the risk to discharge problem, since sludge accumulation leads to the environment 2

Bioresource Technology 303 (2020) 122861

H.-H. Cheng, et al.

Fig. 1. Metabolic pathways of carbon, nitrogen, and phosphorus in bacterial and microalgal cells. (G3P, glyceraldehyde 3-phosphate; VFAs, volatile fatty acids; PHAs, polyhydroxyalkanoates).

microorganisms in anaerobic digestion, microalgae metabolism system oxidize the simple organic compounds, such as glucose and volatile fatty acids (VFAs) like acetate, propionate, and butyrate, as the main carbon source, which could be measured as the COD or BOD value and produce CO2 that will be the material for the photosynthetic process. The efficient microalgal biomass production requires large amount of carbon for growth (Qilu et al., 2018), and these organic carbon sources are abundantly available in the anaerobic digested wastewater. Although heterotrophic cultivation of microalgae was wildly examined for treating different types of organic wastewater (Gupta et al., 2019), limited studies focused on swine wastewaters (Cheng et al., 2019). Chlorella vulgaris JSC-6 removed 72–77% of COD when feeding 5–20 times diluted swine wastewater in which initial COD ranged from 1.1 g/L to 3.7 g/L (Wang et al., 2015), while the same group cultivated Neochloris aquatica CL-M1 later on with swine wastewater and achieved 82% of COD removal (Wang et al., 2017). In the cultivation of Parachlorella kessleri QWY28 using non-sterilized raw swine wastewater, 88% of COD was removed and converted to carbohydrate-rich microalgal biomass (Qu et al., 2019). By feeding anaerobically digested swine wastewater with varied dilutions (10–100%), 63–79% of COD was removed by co-cultivating 3 species of microalgae, including Chlorella vulgaris, Scenedesmus obliquus, and Pseudokirchneriella subcapitata, with the fungus Ganoderma lucidum (Guo et al., 2017). In the same study, high CO2 removal capacity of 60–85% was also reported, showing the

feasibility of simultaneous removal of COD and CO2 from swine wastewater. On the other hand, Coelastrella sp. QY01 removed 74–78% inorganic carbon in the anaerobic treated swine wastewater (Luo et al., 2016). 2.1.1. Factors that affect microalgal carbon removal In swine wastewaters, significant amounts of sodium. calcium, potassium, chlorine, sulfur, phosphate, bicarbonate, ammonium and heavy metals could also be presented along with organic carbons, which leads to different environment and affects microbial growth or performances. The release of dissolved organic carbon increased when cultivating Chlorella vulgaris using anaerobically digested swine wastewater due to the production of intracellular and extracellular polysaccharide, which was triggered by the protection system of microalgae to the oxidative stress (Marjakangas et al., 2015). With the decrease of N/P ratio from 15 to 1.5 during cultivation of N. aquatica CL-M1, both COD and ammonia removals increased but the utilization of phosphate was reduced (Wang et al., 2017). Important factors affecting the performance efficiency of heterotrophically microalgae cultivation in the wastewater also include temperature, nutrients availability, algal composition, light intensity, hydraulic retention time (HRT), sludge retention time (SRT), pH value and the cultivation system (Arias et al., 2018). Guo et al. (2017) reported that C. vulgaris performed better COD removal than S. obliquus and P. subcapitata when co-culturing with G. 3

Bioresource Technology 303 (2020) 122861

H.-H. Cheng, et al.

lucidum in anaerobically digested swine wastewater, while P. subcapitata removed the most CO2 among three species. It should be noted that heterotrophic COD assimilation/removal might reduce the efficiency of CO2 capture, although the negative effect from CO2 uptake to COD removal was limited (Wang et al., 2015). Optimal temperature of 30 °C was suggested according to Ratkowsky model for heterotrophic cultivation of N. aquatica using swine wastewater (Wang et al., 2017), while the same temperature was reported to be optimal for P. kessleri QWY28 (Qu et al., 2019). P. kessleri QWY28 under the light intensity of 600 µmol/m2/s between 200 and 800 µmol/m2/s could remove the most COD and TN while produce the highest amount of biomass and carbohydrate, although heterotrophic cultivation of microalgae theoretically requires no light (Zhang et al., 2013).

2.2.1. Factors that affect AD Organic loading rate is an essential factor during anaerobic digestion for swine wastewater, it could lead to accumulation of volatile fatty acids (VFAs), decrease in pH and alkalinity, reduction of biogas production and even bioreactor failure. Padmasiri et al (2007) increased the OLR of their MBR treating swine wastewater from 1 to 2 kg-VS/m3/ d and observed VFAs accumulation of around 3 g/L, mainly acetate and propionate, and nearly no biogas was produced during the operational period. Similar observation that VFA concentration increased from below 100 mg/L to 800 mg/L when decreasing HRT from 10 to 3 days in the self-agitation ABR feeding swine wastewater, while both the removals of VS and COD were also reduced (Jiang et al., 2019). The performance of MBR was recovered by increasing alkalinity and maintaining pH above 7.0, however, the authors concluded that the OLR could not over 3 kg-VS/m3/d after attempting increasing OLR again. The appropriate effluent pH between 7.1 and 7.2 was observed when using horizontal anaerobic bioreactor, which maintained the alkalinity and ensured the ability of converting VFAs to CH4 (Duda et al., 2015). In the comparison using different inoculums, Córdoba et al. (2016) investigate the remaining VFAs above 3 g/L resulted in the low alkalinity and suppressed the CH4 production. By increasing the OLR of semi-continuous CSTR from 0.7 to 1.3 kg-COD/m3/d, the COD removal reduced to 20% immediately and resumed to above 60% afterward, and the biogas production increased but unstable (Liu et al., 2015). In the UASB feeding swine wastewater with increasing OLR from 1.3 to 5.8 kg-COD/m3/d, results show a positive correlation between biogas production and OLR when VFAs concentration remained below 0.1 g/L (Song et al., 2010). A high OLR of 28.5 kg-COD/m3/d was possible when co-digesting swine wastewater with gin spent wash using UASB and achieving a production of 8.4 L/L/d and a COD removal of 97%, however, the swine wastewater only contributed to around 5% of the influent COD (Montes et al., 2019). By co-digesting swine wastewater with algal biomass in the volumetric ratio of 1.5, the biogas production could have 23% of improvement due probably to lower VFAs accumulation (Tsapekos et al., 2018). Temperature is another important parameter to the anaerobic digestion treating swine wastewater, since it could affect the rate of biochemical reactions and the activity of enzymes and thus leads to varied CH4 yield and effluent quality (Zhang et al., 2014). The CH4 yield in ABR treating swine wastewater increased by 3.4- and 2.7-fold at 25 °C than those at 15 and 20 °C, respectively (Jiang et al., 2019). By examining the performance on CH4 under varied temperatures between 15 and 35 °C, Yang et al. (2016) revealed that higher COD concentration in effluent and lower CH4 production at low temperature when treating swine wastewater using SBR. In the study, the COD removal was maintained when increasing OLR at higher temperature as

2.2. Anaerobic digestion (AD) COD in biodegradable wastewaters like swine wastewater can be decomposed both aerobically and anaerobically, however, it was recognized that anaerobic process has many advantages, including lower energy consumption, low nutrients requirement, the low biomass yield resulting in a limited generation of waste sludge as unwanted side product, limiting cost for product separation due to the in situ separation of the product as biohydrogen and methane (H.H. Cheng et al., 2012, 2018). Anaerobic digestion (AD), consisting of hydrolysis, acidogenesis and methanogenesis, is wildly applied to degrade swine wastewater, and produce biogas, such as H2S, CO2, H2, and CH4, and digestate containing remaining COD, nitrogen and phosphorus (Kim et al., 2016; Nagarajan et al., 2019). As reported in previous studies (Table 2), anaerobic processes could be applied to treat swine wastewaters in several configurations, such as batch experiments, semi-continuous operation, anaerobic baffled reactor (ABR), SBR, UASB, MBR, horizontal anaerobic reactor, and their combinations. HRT of anaerobic digestion treating swine wastewater is usually maintained between 1 and 5 days although some studies reported higher HRTs, while the organic loading rates (OLRs) could be high as 5.8 or 7.8 kg-COD/m3/d. Most of anaerobic digestion could achieve 70–80% of COD removal, however, COD removal above 90% were also reported using SBR (Yang et al., 2019), MBR (Padmasiri et al., 2007), or UASB (Montes et al., 2019; Yang et al., 2019). The moderate level of COD removal implies that the digested effluent requires further treatment before being discharge to the environment. Generally speaking, the CH4 yield were around 200–300 mL/g-COD and few of them could produce more than 330 mL/g-COD of CH4, while theoretical CH4 yield at 20 °C is approximately 380 mL/g-COD according to the energy calculation (Heidrich et al., 2011). Table 2 Reported anaerobic treatment processes for swine wastewaters.

a

Process

Reactor

Size (L)

OLR (kg-COD/m3/d)

HRT (d)

COD removal

CH4 yield (mL/g-COD)

Reference

AD AD AD AD AD AD AD AD AD AD AD Fermentation/ADd Co-digestion Co-fermentation

SBR SBR Semi-continuous SBR/USR UASB-filter MBR MBR ABR UASB Horizotal UASB Two-stage SBR UASB SBR

1 2.5 4.5 5 5 6 8 10 20 588 35,000 0.15/2.5 1 0.3

0.2–7.2 7.8 1.3 1.5–7.6 1.5–7.6 1.0–2.0a 1.0–4.7a – 0.8–2.6 – 1.3–5.8 77.7/7.4 28.5 13.1–53.2

1.1–40.0 41.5 5.0 1.0–5.0 1.0–5.0 3.0 1.0–5.0 3.0–10.0 2.0 1.0 3.5–7.0 1.5/40.0 3.3 1.0–3.0

75–92% 49% 60–80% 70–92% 75–91% 96% 40–76%b 66–80% 69% 68% 74–79% 47% 97% 17–40%

75–350 182 – 202–275 273 – 610-770c 330-610c 91 300 280–330 27/154 250 0.5-126e

(Yang et al., 2016) (Schievano et al., 2016) (Liu et al., 2015) (Yang et al., 2019) (Yang et al., 2019) (Padmasiri et al., 2007) (Jiang et al., 2020) (Jiang et al., 2019) (Zhao et al., 2016) (Duda et al., 2015) (Song et al., 2010) (Schievano et al., 2016) (Montes et al., 2019) (Tenca et al., 2011)

kg-VS/m3/d; bVS removal; cmL-CH4/g-VS. H2 fermentation/AD; eH2 yield (mL-H2/g-COD).

d

4

Bioresource Technology 303 (2020) 122861

H.-H. Cheng, et al.

25–35 °C, but the effluent COD increase significantly at low temperature as 15 °C. The CH4 yield at 15 °C was 4–5 times lower than that at 25 °C under the same OLR, and the CH4 yield elevated by around 30% when temperature increased from 25 °C to 35 °C. According to the mathematical model they proposed, the maximum CH4 production rate follows an exponential growth with temperature. It was also reported that two-step heating strategy could increase more temperature by 3.3–9.3 °C compared to conventional heating mode when supplying the same energy input, and it consequently enhance CH4 yield by 10–15% at extreme low temperature as 5–10 °C while the abundances of syntrophic bacteria and hydrogenotrophic methanogens were also increased when applying two-step heating strategy at 10 °C (Liu et al., 2018). Nutrients contents, e.g. ammonia and metal ions, might also be critical to anaerobic digestion. General C/N ratio of swine wastewater locates around 4.0–7.0 while optimal range for anaerobic digestion is between 15 and 30, and thus, co-digestion with other organic waste/ wastewater like food waste was sometimes suggested (Zhang et al., 2011). As for the ammonia concentration, it was known that 1.7–1.8 gN/L of total ammonia nitrogen (TAN) or 80–150 mg-N/L of free ammonia nitrogen (FAN) could inhibit anaerobic digestion (Zhang et al., 2011; Zhao et al., 2016), although some studies presented higher tolerance of methanogens on higher TAN as 3.0–5.0 g/L in swine wastewater after acclimation (Yenigün and Demirel, 2013). In anaerobic digestion, metals like Fe, Co, Ni. Zn, Se, Mo and W were considered essential to methanogenesis (Glass and Orphan, 2012), while Se could significantly improve the degradation of acetate and propionate and Mo and Co moderately enhanced propionate degradation (Jiang et al., 2017). By co-digesting swine wastewater and food waste, Zhang et al. (2011) revealed that the trace metals, such as Co, Mo, Ni, and Fe, existed in swine wastewater were the main reason of improved biogas production and enhanced stability of co-digestion. This observation agree with the conclusion made by Zhou et al. (2018) that mixture of different organic waste/wastewaters could improve anaerobic digestion by providing insufficient nutrients and by diluting the concentration of toxicants.

methanogenesis pathways (H.H. Cheng et al., 2018; Guo et al., 2015). In the MBR treating swine wastewater, Methanosaeta sp. reduced after the elevation of OLR due probably to the accumulation of acetate, Methanosarcina sp., instead, gradually increased after peaked acetate concentration and maintained its dominance throughout the following operation although the OLR was reduced (Padmasiri et al., 2007). Adverse result, increase of Methanosaeta sp. and decrease of Methanosarcina sp. with decreasing HRT from 10 to 3 days, however, was observed in the ABR treating swine wastewater (Jiang et al., 2019). Although aceticlastic methanogens usually dominate the anaerobic digesters by around 70%, hydrogenotrophic methanogens like the genera Methanospirillum, Methanoculleus and Methanoregula and methylotrophic methanogens such as the genera Methanomethylovorans, Methanococcoides, Methanohalophilus and Methanolobus could also be found in anaerobic processes (H.H. Cheng et al., 2018; Guo et al., 2015). In the horizontal anaerobic bioreactor, similar amounts of 107-109 copies16S-rDNA/g-sludge between aceticlastic methanogens and hydrogenotrophic methanogens were detected, in which sufficient hydrogenotrophic methanogens could maintain a low H2 partial pressure in the system (Duda et al., 2015). In contrast, 96% of methanogens were found to be hydrogenotrophic methanogens in the UASB treating swine wastewater, and presumably due to that hydrogenotrophic methanogens are less sensitive to the high concentration of ammonium above 1.7 g/L (Song et al., 2010). 2.2.3. Latest developments on AD As the development time to time, anaerobic processes has been wildly applied to treat many waste/wastewaters. The agro-industrial wastewaters in Netherland are mostly treated by anaerobic processes nowadays (Lier et al., 2008), and a quarter of industrial wastewaters in United Kingdom are presently treated by anaerobic processes (WRAP, 2014). Recent modifications on anaerobic bioreactor tend to isolate SRT from HRT and to produce smaller footprints for more flexible and stable operation, for example, UASB, MBR, SBR, anaerobic fluidized bioreactor (AFBR), anaerobic fluidized membrane bioreactor (AFMBR), and so on (McCarty et al., 2015; Skouteris et al., 2012). Swine wastewaters, usually contains high concentration of ammonia and suspended solid (SS), was considered unfavorable to the formation of granules in UASB, although successful UASB was also reported (Song et al., 2010). In the study comparing three bioreactor designs, including SBR, UASB-filter, and upflow solid reactor (USR), for treating swine wastewater, only SBR could maintain COD removal above 80% when OLR increased from 1.5 to 4.5 kg-COD/m3/d while COD removals in UASB-filter and USR reduced to 75% and 70%, respectively (Yang et al., 2019). The authors also revealed that SBR and UASB-filter could maintain SRT/HRT around 8 at OLR 4.5 kg-COD/m3/d, but that in USR was only below 2 which is closed to CSTR. Another common configuration is MBR, which could potentially produce perfect effluent quality, however, the problems of membrane fouling and it maintenance remain the challenge especially treating high solid wastewater like swine wastewater (Padmasiri et al., 2007). By combining the advantages of both AFBR and MBR, the recent-developed AFMBR, might be an option for future application for swine wastewater, as it were reported only consumed 10% of energy equivalent of its CH4 production for operation (Aslam et al., 2017) and could be operated at OLR above 0.5 kg-COD/m3/d with 90% of COD removal when treating organic wastewater (H.H. Cheng et al., 2018).

2.2.2. Microbial communities in AD The microbial community in anaerobic digesters are usually diverse due to the complex components in swine wastewater. The most abundant bacteria, generally speaking, are the class Clostridia for hydrolysis and fermentation as they can utilize wild-range of substrate and tolerate high concentrations of VFAs and alcohols (Dash et al., 2016; Guo et al., 2015; Jiang et al., 2019; Minton and Clarke, 1989) and the class Bacilli for their abilities to produce acetate and lactate. On the other hand, most of archaea are recognized as methanogens, especially under the class Methanomicrobia (Duda et al., 2015; Guo et al., 2015). Nevertheless, microorganisms possibly exist in anaerobic digesters also include: the class Gammaproteobacteria who can possibly consume oxygen (Hung et al., 2011), the class Deltaproteobacteria in which lots of them were identified as syntrophic acetogens and responsible for acetogenesis (Leng et al., 2018; Müller et al., 2013), the classes Bacteroidetes, Actinobacteria and Anaerolineae for their fermentative abilities (Duda et al., 2015; Guo et al., 2015; Si et al., 2016), and so on. The community could change quickly along with the operative parameters, however, study also claimed that the bacterial community was re-stable after increase of OLR and the compositions were similar before and after OLR increase (Liu et al., 2015). Methanosaeta sp. and Methanosarcina sp. are the most common methanogens found in anaerobic digesters, and their relative proportions could be affected by the operative parameters like OLRs, H2 partial pressure and existence of metal ions (Cai et al., 2016). The genus Methanosaeta is known as the aceticlastic methanogens, and it dominated in many anaerobic systems with the formation of granules or the attached growth on GACs (H.H. Cheng et al., 2018; Song et al., 2010), while the genus Methanosarcina is capable to grow with all three

3. Advanced biological processes to recover nutrients (N, P) in swine wastewater Swine wastewater is categorized as one of the most polluted agroindustrial wastewater due to its high contents of carbon, nitrogen and phosphorus, either in organic or in inorganic. Numerous technologies are applied to utilize and recover ammonium in the wastewater, such as struvite precipitation, ammonium stripping, membrane concentration, 5

Bioresource Technology 303 (2020) 122861

H.-H. Cheng, et al.

however, expenses on the maintenance and performance of the technologies is considered as the negative side of the application (Ye et al., 2018). Phosphorus removal relied on the electrochemical system technologies also required high cost in instrument performance and maintenance (Kelly and He, 2014). As the common growth nutrients for bacteria, archaea, and microalgae, nitrogen and phosphorus in wastewaters could be uptaken, utilized, and/or accumulated in cell body. Therefore, the application of biological processes becomes the reasonable and economical choice for the nutrients removal in swine wastewater.

2017). The requirement of nitrogen supply in the microalgae system is in the range of 1–10% of dry weight and depend on the amount, availability, and type of nitrogen source. C. vulgaris was cultivated in the 5 dilution of swine wastewater and oxidized the ammonium during the first 4 days of the cultivation process from 83 mg/L to 20 mg/L (Marjakangas et al., 2015). Sterilization process may reduce the concentration of the ammonium in the swine wastewater. 90–100% removal of ammonium was achieved by the cultivation of Coelastrella sp. QY01 in the anaerobic treated swine wastewater (Luo et al., 2016). On the other hand, the O2 produced from the photosynthesis process will be utilized to oxidize the organic matter and ammonium in the wastewater and transform it into the microalgae biomass (Ferreira et al., 2018). Banerjee et al. (2019) revealed that the immobilized microalgae beads could improve the performance and help the harvesting process of microalgae cultivation using C. vulgaris, while the adsorption of ammonium nitrogen and phosphate on the alginate matrix due to the hydrogen bonding will supply the nutrients to the microalgae easily. Kwon et al. (2019) reported 99% of ammonia and the highest TP removal of 63% when cultivating C. vulgaris mixotrophically with air-stripped diluted anaerobically digested swine wastewater, while 82% of soluble COD was removed. It was also mentioned that higher specific growth rates occurred when C/N molar ratio was in the optimal C/N ratio range of 5–15 for mixotrophic cultivation of C. vulgari. By cultivating C. vulgaris JSC-6 with different dilutions of swine wastewater, Wang et al. (2015) revealed that ammonia removal was elevated from 40% to 91% under mixotrophic condition while similar ammonia removal of 50–65% was observed under heterotrophic environment, which due probably to the change of C/N ratio when CO2 was provided.

3.1. Microalgae utilization technologies Regarding to the nutrients content, swine wastewater is a great source to supply the required major nutrients (carbon, nitrogen, phosphorus) and also the micronutrients like calcium, chlorine, chromium, cobalt, copper, iron, magnesium, manganese, potassium, silica, sodium, sulfur, and zinc for the microalgae cultivation (Zhang et al., 2016). Along with the advantages of carbon recovery in the swine wastewater as previously discussed, the microalgae biological nutrient removal offers the efficient cost during the process and the production of valuable products. Therefore, nutrients removal with microalgae cultivation was wildly applied recently, and many critical reviews were available (Cheng et al., 2019; Chiu et al., 2015; Lu et al., 2019; Nagarajan et al., 2019). 3.1.1. Microalgae cultivation tolerance of nutrients concentration Several promising advantages are carried out by the microalgae cultivation in the nutrient removal process of the wastewater treatment. The high efficiency in the removal of nitrogen and phosphorus compounds, coupled with the production of the valuable by products are the main attractive advantages from the microalgae cultivation system (Zhang et al., 2016). Compare to the chemical and physical process, microalgae carried out the advantages in high uptake capacity for the inorganic nutrient. Microalgae can achieved 86% inorganic nitrogen removal and 78% inorganic P removal (Abdel-Raouf et al., 2012), however, microalgae have the tolerance concentration of the nutrients in the cultivation system and the high nutrients contents may be harmful for its growth. Other issues, such as light interference by impurities and suspended materials, growth inhibition by organic and inorganic compounds, osmotic and oxidative stress from high salinity, could also affect the microalgal cultivation, and thus, before the application of swine wastewater as cyanobacteria or microalga growth medium, dilution process is generally needed. The high dilution rate, however, will cause the low concentration of nitrogen and phosphorus which are important in biomass growth, and needs another cost on fresh water (Cheng et al., 2019; Chiu et al., 2015). Diluted swine wastewater, which COD concentrations were below 1 g/L, in the cultivation of Chlorella pyrenoidosa performed the ammonia removal above 90% and the highest TP removal of 78% which related to the biomass increment (Wang et al., 2012).

3.1.3. Phosphorus recovery process in microalgae cultivation Due to its low cost efficiency in biological phosphorus removal and recovery, microalgae cultivation is considered as one of the promising method. Phosphorus is categorized as one of the important nutrient for the microalgae growth, which occupied 1% by weight in microalgal biomass (Nagarajan et al., 2019). Phosphorus will be mainly assimilated as inorganic orthophosphate for the synthesis of ATP, phospholipids, nucleotides and nucleic acid in microalgae cell metabolism system (da Fontoura et al., 2017), as shown in Fig. 1. Therefore, the availability of phosphorus in the microalgae system is related with the photosynthesis process (Chiu et al., 2015), and the application of swine wastewater will be suitable for its sufficient phosphorus content. C. vulgaris of microalgae have the ability to remove 32–97% total phosphorus inside the treated swine wastewater, while Coelastrella sp. remove 100% of total phosphorus. López-Pacheco et al. (2019) enhance the total phosphorus and nitrogen removal in the swine wastewater using Arthrospira maxima and C. vulgaris by mixing it with the nejayote or maize cooking wastewater. Along with the other nutrient removal in the anaerobic treated swine wastewater, Coelastrella sp. QY01 removed 90–100% of TP (Luo et al., 2016), while 90–92% of TP could be removed by Chlorella minutissima Fott and Nováková, Acutodesmus obliquus, Oscillatoria sp. and Chlorella sp.-dominated microalgal culture, respectively (García et al., 2018). During the cultivation of N. aquatica, increasing phosphate concentration and correspondingly decreasing N/ P ratio reduced the phosphate removal rate, although the removals of COD and ammonia were both slightly elevated (Wang et al., 2017). Nevertheless, initial phosphorus concentration for microalgae cultivation in swine wastewater was generally below 100 mg-P/L (Cheng et al., 2019; Lu et al., 2019), which is lower than TP concentration in swine wastewater (Table 1) and the tolerant level for A/O process (Table 3).

3.1.2. Nitrogen recovery process in microalgae cultivation The biomass production of microalgae is related to the metabolism of nitrogen and phosphorus, and the nitrogen contents in swine wastewater could act as the major source for the production of proteins, chlorophylls, genetic material, and the energy transfer during microalgae growth. Ammonium, nitrite, and nitrate are the common nitrogen forms in the wastewater with ammonium as the dominant species, and ammonium is the nitrogen source with the high availability for the microalgae growth and make it most preferred from the swine wastewater. Microalgae could also uptake nitrate as the nitrogen source for protein synthesis while nitrifying bacteria might oxidize ammonium in the wastewaters into nitrate (Fig. 1), although ammonia was preferred because energy is required, in the forms of NADH and reduced ferredoxin, for the reduction of nitrate to ammonia (da Fontoura et al.,

3.2. Integrated biological processes for swine wastewater and its anaerobic digested wastewater Although anaerobic digestion is the most popular process for 6

Bioresource Technology 303 (2020) 122861

H.-H. Cheng, et al.

Table 3 Biological processes other than anaerobic digestion treating swine wastewater or its treated wastewater. Process

Separated A/O A/O A/O A/O A/O (SND) SNAD MFC/O MFC MFC MFC Aerobic Photosynthesis Aquatic plant Biofiltrationd Biofiltratione Biofiltrationf Biofiltrationg

Type

Two-stage SBR Step-fed SMBR Step-fed SBR SBR SMBR SBR Continuous Fed-batch Continuous Batch MBR Batch Continuous Continuous Continuous Continuous Continuous

Previous processes

Raw AD Raw Raw Raw AD Raw AD Two-stage AD Raw Simulated AD Three-stagec Raw AD AD AD

SS (Removal)

COD (Removal)

TN (Removal)

TP (Removal)

g/L

g/L

g-N/L

mg-P/L

– – – – – – 1.2 – – – – – 0.1 – 9.1 – 0.1

8.4 (89–97%) 4.4 (97–99%) 8.8 (95%) 90 (99%)a 7.0 (95%) 0.4 (69–83%) 2.5 (36–40%) 6.8 (18%) 6.9 (22%) 8.3 (92%) 34.2 (99%) 4.8 (83%) 0.7 (27%) 0.5 (81%) 21.6 (90%) 1.4 (48%) 0.6 (48%)

1.0 (80–94%) 1.3 (89%) 1.2 (94%) 4.5 (96%) 1.0 (93%) 0.7 (74–83%) 0.3 (44–56%) 1.0 (22%) 0.9 (19%) – – 0.9b (-) 0.5 (44%) 0.4 (-) 4.4 (89%) 0.9 (43%) 0.6c (78%)

216 (75–86%) 344 (75–97%) 601 (93%) 2600 (50%) – 30 (-) – – – – – 21 (-) 46 (23%) – 142 (59%) – –

(-)

(61%) (greater than99%) (-)

Reference

(D. Yang et al., 2016) (Han et al., 2018) (Wu et al., 2015) (Kim et al., 2004) (Sui et al., 2018) (Daverey et al., 2013) (Vilajeliu Pons et al., 2017) (Schievano et al., 2016) (Schievano et al., 2016) (Min et al., 2005) (Inaba et al., 2018) (Wen et al., 2016) (Chien et al., 2016) (Su et al., 2019) (Kim et al., 2016) (Zhao et al., 2016) (Bowei Zhao et al., 2014)

a e

BOD5 (g/L); bNH4+-N; cSolid-liquid separation, anaerobic process, and aerobic process; dtwo-stage infiltration; Coagulation, microfiltration, air-stripping, algae, and ozone; fWood-chip and peat; gWood-chip soil infiltration.

A/O process is capable to remove antibiotics while treating swine wastewaters via biotransformation, biodegradation and biosorption. By feeding synthetic swine wastewater to SMBR, Xu et al. (2019) observed that over 90% of sulfonamides and over 76% of tetracyclines were removed by biodegradation while 40–50% of fluoroquinolones were degraded by the sludge. Wang et al. (2019) monitored two full-scale treatment plants, based on A/O process, for swine wastewater, and observed high removals on antibiotics as 56–95% and 66–96% from liquid phase and solid phase, respectively. The authors also revealed the positive correlations between the removal of antibiotics and the removals of COD and TS, indicating antibiotics might be degraded through co-metabolism with other organics. Higher residual antibiotics in effluent were detected in winter than in summer, again implying antibiotics were mainly removed via biodegradation and it could be affected by the low biological activity at low temperature. Automatically controlled strategies were developed for A/O SBR system, and it was suggested to applied dORP/dt to indicate the status of denitrification and variation in dpH/dt for nitrification, respectively (Kim et al., 2004). Similar strategy, i.e. monitoring dORP/dt and dpH/ dt to automatically control the A/O system, was successfully applied in SMBR treating swine wastewater (Sui et al., 2018). By involving the monitoring data of pH, TS, COD, temperature, and nitrogen concentration, Manu and Thalla (2017) reported that support vector machine (SVM) and adaptive neuro-fuzzy inference system (ANFIS) modeling could be used to predict the effluent nitrogen concentration during the operation of A/O process while SVM had slightly better predictions than ANFIS. The community is usually diverse the anaerobic/anoxic tank, common denitrifiers include the genera Pseudomonas, Flavobacterium, Thauera, etc. It is simpler in aerobic tank, where ammonia-oxidizing bacteria (AOB), like the genera Nitrosomonas and Nitrosospira, and nitrite-oxidizing bacteria (NOB), like the genera Nitrospira and Nitrobacter, are generally dominating. In the A/O system aimed for SND, the abundance of NOBs decreased because of the drop in DO and the relative high pH, leading to the dominance of AOBs (Sui et al., 2018).

treating swine wastewaters, however, anaerobic digestion could only reduce organic carbons and consequently post-treatments aim for nutrients are required. There were several processes other than anaerobic digestion reported for the treatment of swine wastewaters or its anaerobically digested wastewaters, as listed in Table 3. 3.2.1. Anaerobic/oxic (A/O) process Anaerobic/oxic or anoxic/oxic (A/O) process is the most wildlyapplied system for the treatment for swine wastewaters, and most of them were operated as SBR or SMBR. Generally speaking, A/O system could achieve over 90% of COD removal and simultaneously remove 80–96% of TN and over 50% of TP. In the A/O system, phosphorus removal could be reduced by the accumulation or existence of nitrite and nitrate due to the elevated nitrogen loading, and thus, a posttreatment is essential (Han et al., 2018). Yang et al. (2016) separated the swine wastewater into two parts, sediment and supernatant, and the sediment, accounted for 20% of total volume, was sent to anaerobic digestion while the supernatant was directly treated in aerobic tank after mixing with the effluent of anaerobic process. This separated A/O process achieved high removal in COD, TN and TP as 97%, 92% and 86%, respectively, which could be explained by the lower matrix effect from supernatant on anaerobic digestion and the reduced organic loading to the oxic tank. Recent study also presented the short-cut nitrification and denitrification (SND) for swine wastewater treatment, instead of fully nitrification and denitrification, by shortening the aeration period in oxic tank and providing lower organic in anaerobic tank (Sui et al., 2018). Waki et al. (2018) reported similar observation that TN removal increased to 85–96% via SND by controlling DO in the activated sludge system at 0.03–0.07 mg/L when treating swine wastewater. The newly developed process, simultaneously partial nitrification, anammox and denitrification (SNAD), which is similar to A/O process, has gained interests recently, while it only maintains low DO, i.e. below 0.5 mg/L, in a single tank to achieve complete nitrogen removal. By applying SNAD process to treat anaerobically digested swine wastewater, 83% of COD and nitrogen removal could be achieved with a low COD/N ratio below 1.0 since COD could has negatively effect on anammox bacteria (Daverey et al., 2013). It was also reported in the same study that temperature is a critical parameter to SNAD process, specifically, the removals of TN and COD were below 50% and 20%, respectively, at 15–20 °C while they raise to 79% and 77%, respectively, at 27 °C.

3.2.2. Microbial fuel cells Microbial fuel cells (MFCs) have been developed to generate energy from organic wastewaters for years, and swine wastewater is one of the potential substrates though the high ammonia content or the produced VFAs could be inhibitory (Min et al., 2005). The removals of COD and 7

Bioresource Technology 303 (2020) 122861

H.-H. Cheng, et al.

TN when applying MFCs were generally below 40–50%, which were lower than those applying A/O processes (Vilajeliu Pons et al., 2017). The observed TN removal implied that both nitrification and denitrification occurred in the MFC (Schievano et al., 2016). The power density produced from swine wastewater was around 90–280 mW/m3 (Min et al., 2005), while a high density of 4 W/m3 was reported when applying 6-stacked MFC (Vilajeliu Pons et al., 2017). It was suggested to maintain low OLR and nitrogen loading rate (NLR) to yield adequate coulombic efficiency for both anode and cathode (Vilajeliu Pons et al., 2017), however, Schievano et al. (2016) revealed that the low COD in the bulk solution of anode could limit the mass transfer and lead to the decrease in yielded voltage when treating digested swine wastewater. Nevertheless, the cost and durability of electrodes remain the challenges to develop the full-scale MFC for treating swine wastewaters.

detected which implies that wood-chip might be utilized as the carbon source for denitrification (Bowei Zhao et al., 2014). 3.2.5. Potential bioprocesses for treating swine wastewaters To achieve energy neutral wastewater treatment, it was considered that coupled aerobic-anoxic nitrous decomposition operation (CANDO) process, which recover nitrous oxide (N2O) while removing ammonia from wastewaters and use N2O as the co-oxidant for burning, could play an important role (Scherson and Criddle, 2014). CANDO process is a two-stage process, including nitritation and nitrous denitrification, in which ammonia is oxidized to nitrite and the produced nitrite is reduced to N2O with the participation of organics, respectively. Recent research reported successful operation of CANDO process treating reject water from digester containing around 1.1 g/L of nitrogen and 0.4 g/L of COD, which is similar to anaerobically digested swine wastewaters (Weißbach et al., 2018). The authors also presented the possibility of automatically control on SBR for the second-stage of CANDO to optimize the process, and over 60% of nitrite were reduced to N2O. Gao et al. (2017) also reported the CANDO process by using denitrifying polyphosphate-accumulating organism, which has the potential to recover N and P at the same time. CANDO process, however, still requires further study to simplify the complexity of operation (Gao et al., 2017), and the little improvement on the energy production contributed by N2O (Zhang et al., 2019) although the production of N2O will be highly elevated if swine wastewaters instead of domestic wastewaters are used. CH4-based membrane biofilm reactor (MBfR) was recently proposed as another option for nitrogen removal, which microorganisms responsible for denitrifying anaerobic methane oxidation (DAMO) could utilize CH4 produced from AD for denitrification. Allegue et al. (2018) presented a maximum nitrite removal rate of 116 mg-N/L/d with a total nitrogen removal rate of 126 mg-N/L/d, which is closed to the reported NLRs of 100–170 mg-N/L/d for A/O or SNAD processes to treat anaerobically digested swine wastewaters (Daverey et al., 2013; D. Yang et al., 2016). The TN removal rates could be maintained as 1 g-N/ L/d when combing anammox and DAMO in MBfR for treating anaerobically digested liquor even when influent nitrogen concentration above 1 g/L (Xie et al., 2016).

3.2.3. Constructed wetland and photosynthesis Aside from microalgae, constructed wetlands and photosynthetic bacteria (PSB) were also applied in the treatment of swine wastewaters. Construct wetland could work as the polishing process for treated swine wastewater, it was reported more than 27% of SS, ammonia, and COD could be further removed by water hyacinth after being treating by the conventional three-stage treatment process (Chien et al., 2016). Luo et al. (2018) grew watermilfoil in a pilot-scale constructed wetland for lagoon-pretreated swine wastewater and achieved 85–96% of TN removal. According to their estimation, 60–80 mg-N/L of TN was uptaken by plant despite the increasing nitrogen concentration from around 100 mg-N/L to above 300 mg-N/L in the influent, while most of the remaining nitrogen was removed by microbial metabolisms including nitrification and denitrification. By planting swamp cabbages in a pilotscale constructed wetland for anaerobically digested swine wastewater, Han et al. (2019) also presented 85% and 71% of COD and TN removal, respectively, while 80% of TN removal was contributed by nitrification and denitrification. Duckweed is another common aquatic plant for swine wastewater treatment, and it was revealed that the addition of small amount of copper (less than1.0 mg/L) could enhance the removal efficiencies of nitrogen and phosphorus (Zhou et al., 2019). The genus Rhodobacter is one of the common PSBs that being applied in wastewater treatment, and the two strain Rhodobacter blasticus and Rhodobacter capsulatus were used to treat the anaerobically digested swine wastewater in the study presented by Wen et al. (2016). The authors revealed that the mixture of two Rhodobacter sp. had a better performance on COD removal (83%) than those when they were individually enriched.

4. Reuse of the produced sludge and/or algal biomass 4.1. Biomass for bioenergies Both bacterial biomass and algal biomass produced after treating swine wastewaters could be used for bioenergy production, and anaerobic digestion was wildly applied to recover CH4 from bacterial biomass. Algae, including macro algae and microalgae, were recently being considered as the third-generation substrate for bioenergy production, due to their high contents of oil and carbohydrate in the biomass (Zhang et al., 2016). There are several harvesting strategies available for algal biomass, for example, flocculation, centrifugation, membrane filtration, flotation, magnetic separation, which were reviewed previously (Lu et al., 2019). Generally, the oil content, accounted for 17–43% in algal biomass, could be extracted through thermal conversion for biodiesel production, and the remaining residues is available for the fermentation, syngas production or biochar production (Plácido et al., 2019; Tran et al., 2012). The section below summarizes several techniques for the recovery of energies from algal biomass or microbial sludge.

3.2.4. Biofiltration and soil infiltration Biofiltration, including soil infiltration, is another option in the treatment of swine wastewater with many advantages, such as low costs for the construction and operation, easy to maintain and low energy demand (Su et al., 2019; Bowei Zhao et al., 2014). The reported biofiltration processes were connected to anaerobic digestion, i.e. working as an oxic tank in the A/O process, when treating swine wastewaters (Kim et al., 2016; Zhao et al., 2016), although biofiltration could be individually applied (Su et al., 2019). Biofiltration system could generally remove 50–90% of COD, but the nitrogen removal efficiency is limited by poor denitrification due to the sufficient dissolved oxygen and the lack of organic carbon since COD is oxidized before nitrification. The efficiencies of COD removal and nitrification could both be reduced by the increase of OLR (Su et al., 2019; Bowei Zhao et al., 2014). In the biofiltration system treating swine wastewater, the most abundant communities at family level were the families Xanthomonadaceae, Chitinophagaceae, and Bacillales which could be possibly related to the degradation of organic matters and/or heterotrophic nitrification (Su et al., 2019). In the Wood-chip soil infiltration system, besides the aerobes like Nitrobacter, Actinobacteria, and Xanthomonadaceae, anaerobes belongs to the genera Clostridia and Asticcacaulis were also

4.1.1. Biomass as the bioenergy source Microalgae has been known as one of the potential source for the production of oil-rich biomass and the oil contents is depend on the species, cultivation system, reactor designs, and harvesting technology (Marjakangas et al., 2015). C. vulgaris in the non-sterilized swine wastewater cultivation system is capable to produce 30% of lipid, although 8

Bioresource Technology 303 (2020) 122861

H.-H. Cheng, et al.

it was slightly lower than those in sterilized environments (Marjakangas et al., 2015). An isolated microalgae from swine wastewater (Chlorellaceae sp. P5) produced potential lipid source for the biodiesel material with the low degree of unsaturated fatty acid in the biomass composition, and achieved the lipid productivity of 0.13 g/L/day with 5% CO2 supply (Chiang et al., 2018). Biochar, the carbon-rich charcoal, could be produced either from algae biomass or bacterial biomass under limited oxygen supply condition (Chen et al., 2018b; Yu et al., 2017), and it not only could be applied as the bioenergy but also have been used as nanosilica, carbonaceous nanomaterial, the humic substances (Plácido et al., 2019) or the addictive to improve the efficiency of swine manure composting (Ravindran et al., 2019). The microalgae biochar derived from Nannochloropsis oculata was used to produce carbon dots for the detection of heavy metal ions via fluorescence quenching (Plácido et al., 2019). On the other hand, pyrolysis of pig manure and sewage sludge was also the potential choice for biochar production (Wei et al., 2019). Two different paths were carried out to transform the microalgae biomass into syngas: the water gas shift reaction will produce hydrogen while the fischer–tropsch process convert the hydrocarbon into liquid fuels like methanol (López-Pacheco et al., 2019), while gasification of sewage sludge for syngas production is also feasible (Tu et al., 2019).

combination of anaerobic fermentation and microbial fuel cell, was also recently proposed to enhance the energy yield (Xin et al., 2019). 4.2. Biomass for by-products 4.2.1. Bioplastic production The high demand of bioplastic was predicted to reach 5.8 billion US dollars in 2021 (Kavitha et al., 2016), and microalgae becomes one of the alternative source of bio-plastic material with high eco-sustainability value (Carlozzi et al., 2019). The accumulation of bio-plastic material was carried out by the microalgae cultivation system in the form of polyhydroxybutyrate (PHB), as illustrated in Fig. 1, which can be synthesized by the microorganisms with the similar physical and chemical properties as the plastics (Troschl et al., 2018). PHB is one of polyhydroxyalkanoates (PHAs) that can be used in pharmacy, food package, and agriculture (Rahnama et al., 2012). Recent studies revealed microalgae PHB production from wastewater to reduce the cost (Chakravarty et al., 2010; Rahman et al., 2015), and the PHB production highly depends on the cultivation conditions like temperature, pH, inorganic carbon, nutrient availability, and light intensity (Kavitha et al., 2016). Arias et al. (2018) observed the highest PHB production of 104 mg/L using mixed cyanobacterial culture under the limited phosphorus and nitrogen condition. Higher PHB production was carried out by the mutant cyanobacteria strain Synechocystis sp. PCC 6714 which reach 735 mg/L (Kamravamanesh et al., 2018). It should be noted that PHAs could also be synthesized by PHA-accumulating microorganisms in A/O process or type II methanotrophs using CH4 gas produced from anaerobic digestion. In the study treating synthetic wastewater using A/ O process, 49 mg/L of PHB was accumulated with simultaneous removals of COD, nitrate and phosphate (Jena et al., 2015). Fergala et al. (2018) enriched type II methanotrophs using AD centrate with CH4 gas produced from AD and achieved the biomass yield of 0.7 mg-VSS/mgCH4 in which 50% of the biomass weight was PHB.

4.1.2. Anaerobic fermentation and digestion (H2, ABE, and CH4) Another easier way to convert algal biomass, either before or after oil extraction, to bioenergy is through anaerobic fermentation or digestion, and several cases have been reported and listed in Table 4. The conduction heat values were obtained from NIST Chemistry WebBook (U.S.D.o.C. Available from: http://webbook.nist.gov/chemistry/): 286 kJ/mol for H2, 1360 kJ/mol for ethanol, 2673 kJ/mol for butanol, and 889 kJ/mol for CH4. Among all the anaerobic processes, CH4 fermentation, or anaerobic digestion, has the potential to perform higher energy yields as above 10 kJ/g-VSS, however, ethanol fermentation, butanol fermentation or the combination of H2 and butanol fermentations also yielded comparable results when considering energy production rates. Nonetheless, suitable pretreatments, such as hydrolysis with acid, base or enzyme, are required before fermentation, no matter which process is chosen (Cheng et al., 2015; Ding et al., 2016). The butanol yield and production rate could also be enhanced by detoxification with polymer resin after hydrolysis (Gao et al., 2016). As for the waste sewage sludge, AD is always considered an economicalfriendly treatment process, and alternative process, such as the

4.2.2. Pigments production from algal biomass Photosynthetic microorganism including cyanobacteria and microalgae has the potency in the production of pigments, such as phycobiliproteins and carotenoids, and so on, and these pigments usually apply as the nutraceutical compound and/or health supplement (Renugadevi et al., 2018). There are several common phycobiliproteins type in cyanobacteria, including allophycocyanins, phycocyaninms and phycoeritrins. These phycobiliproteins will tend to make larger protein

Table 4 Anaerobic fermentative processes to recover bioenergy from algal biomass. Fermentative products Biomass type Yield of the bioenergy products (mmol/g-VSS) H2 H2 Ethanol Butanol

CH4

H2 and butanol H2 and CH4

Oil-extracted Oil-extracted Raw Raw Raw Raw Oil-extracted Raw Oil-extracted Oil-extracted Oil-extracted Raw Oil-extracted Oil-extracted Oil-extracted Oil-extracted Raw Oil-extracted

1.23 1.46 3.47

0.79 0.58 3.88 1.88

Ethanol

0.91 1.30

Butanol

0.52 0.62 1.05 1.36 1.47*

0.48

CH4

6.64 7.93 9.94 16.29 4.82 12.08 16.01

*With addition of 15 g/L of butanol.

9

Overall energy yield (kJ/g-VSS)

Overall energy generation rate (kJ/g-VSS/d)

Reference

0.35 0.42 1.00 1.25 1.77 1.39 1.66 2.81 3.63 3.92 5.91 7.06 8.83 14.48 1.51 4.45 11.85 14.82

N.A. 0.36 0.33 0.62 0.59 0.35 0.28 0.70 1.21 0.65 0.24 0.28 0.23 0.72 0.68 0.16 0.99 0.60

(Yang et al., 2011a) (Yun et al., 2014) (Xia et al., 2016) (Sasaki et al., 2018) (Amamou et al., 2018) (Castro et al., 2015) (Cheng et al., 2016) (Ellis et al., 2012) (Gao et al., 2016) (Cheng et al., 2016) (Yun et al., 2014) (Molinuevo-Salces et al., 2016) (Cheng et al., 2016) (Zhao et al., 2014) (Cheng et al., 2016) (Cheng et al., 2016) (Ding et al., 2016) (Yang et al., 2011b)

Bioresource Technology 303 (2020) 122861

H.-H. Cheng, et al.

Acknowledgement

complexes called as the phycobillisomes (Lauceri et al., 2018) which contain the chromophore with not-coloured linker peptides (Liang et al., 2018). These compounds are water soluble with different colors, such as bright blue (phycocyanin, and allo-phycocyanin), or red (phycoerithrin) (Lauceri et al., 2018). Phycocyanins, as one of the phycobiliproteins with fluorescent characteristic, are the valuable products as the natural food additives, natural cosmetic dye, and fluorescent marker in biomedical research (Renugadevi et al., 2018). The antioxidant potency in phycocyanins could bring the photodynamic therapy of tumours, act as anti-inflammatory, neuroprotective, anticancer, and immunomodulatory agent (Lauceri et al., 2018). Carotenoids are a group of isoprenoid universal pigments with various structures and functions in photosynthetic organism, including the maintenance of the cellular matrix integrity, light harvesting supporting pigment, prevent and repair photo oxidative damage (Ferreira et al., 2018; Sarnaik et al., 2018). Carotenoids are characterized as the non-water soluble dyes which often associated with protein and they are mainly classified into two big groups including carotenes and oxygenated derivatives known as xanthophylls. Carotenoids family has over 400 types, and several of them could be found in cyanobacteria and microalgae like peridinine, β-carotene, nostoxanthin, xanthophyll, caloxanthin, echinenone, myxoxanthophyll, canthaxanthin, oscillaxanthin, zeaxanthin, and scytonemin (Ferreira et al., 2018; Sarnaik et al., 2018). In the xanthophylls group, the dominant pigments are lutein and zeaxanthin, while both of them are known as the valuable products as the antioxidants diet with zeaxanthin as the strongest antioxidant (Sarnaik et al., 2018).

The authors would like to acknowledge the financial support from the Ministry of Science and Technology of Taiwan [NSC 102-2221-E006 -007 -MY3, MOST 105-2221-E-006-009-MY3, MOST 106-2621-M006 -009 -MY3], and partially financial support from the Ministry of Education of Taiwan under grant for the Top University Project to the National Cheng Kung University (NCKU). References Abdel-Raouf, N., Al-Homaidan, A.A., Ibraheem, I.B.M., 2012. Microalgae and wastewater treatment. Saudi J. Biol. Sci. 19, 257–275. Ahn, J.H., Do, T.H., Kim, S.D., Hwang, S., 2006. The effect of calcium on the anaerobic digestion treating swine wastewater. Biochem. Eng. J. 30, 33–38. Allegue, T., Arias, A., Fernandez-Gonzalez, N., Omil, F., Garrido, J.M., 2018. Enrichment of nitrite-dependent anaerobic methane oxidizing bacteria in a membrane bioreactor. Chem. Eng. J. 347, 721–730. Amamou, S., Sambusiti, C., Monlau, F., Dubreucq, E., Barakat, A., 2018. Mechano-enzymatic deconstruction with a new enzymatic cocktail to enhance enzymatic hydrolysis and bioethanol fermentation of two macroalgae species. Molecules 23. Arias, D.M., Uggetti, E., García-Galán, M.J., García, J., 2018. Production of polyhydroxybutyrates and carbohydrates in a mixed cyanobacterial culture: effect of nutrients limitation and photoperiods. N. Biotechnol. 42, 1–11. Aslam, M., McCarty, P.L., Shin, C., Bae, J., Kim, J., 2017. Low energy single-staged anaerobic fluidized bed ceramic membrane bioreactor (AFCMBR) for wastewater treatment. Bioresour. Technol. 240, 33–41. Banerjee, S., Tiwade, P.B., Sambhav, K., Banerjee, C., Bhaumik, S.K., 2019. Effect of alginate concentration in wastewater nutrient removal using alginate-immobilized microalgae beads: uptake kinetics and adsorption studies. Biochem. Eng. J. 149, 107241. Batstone, D.J., Keller, J., Angelidaki, I., Kalyuzhnyi, S.V., Pavlostathis, S.G., Rozzi, A., Sanders, W.T.M., Siegrist, H., Vavilin, V.A., 2002. The IWA Anaerobic Digestion Model No 1(ADM 1). Water Sci. Technol. 45, 65–73. Cai, M., Wilkins, D., Chen, J., Ng, S.K., Lu, H., Jia, Y., Lee, P.K.H., 2016. Metagenomic reconstruction of key anaerobic digestion pathways in municipal sludge and industrial wastewater biogas-producing systems. Front. Microbiol. 7, 1–12. Carlozzi, P., Giovannelli, A., Traversi, M.L., Touloupakis, E., DiLorenzo, T., 2019. Poly-3hydroxybutyrate and H2 production by Rhodopseudomonas sp. S16-VOGS3 grown in a new generation photobioreactor under single or combined nutrient deficiency. Int. J. Biol. Macromol. 135, 821–828. Castro, Y.A., Ellis, J.T., Miller, C.D., Sims, R.C., 2015. Optimization of wastewater microalgae saccharification using dilute acid hydrolysis for acetone, butanol, and ethanol fermentation. Appl. Energy 140, 14–19. Chakravarty, P., Mhaisalkar, V., Chakrabarti, T., 2010. Study on poly-hydroxyalkanoate (PHA) production in pilot scale continuous mode wastewater treatment system. Bioresour. Technol. 101, 2896–2899. Chen, Y. di, Ho, S.H., Nagarajan, D., Ren, N. qi, Chang, J.S., 2018a. Waste biorefineries — integrating anaerobic digestion and microalgae cultivation for bioenergy production. Curr. Opin. Biotechnol. 50, 101–110. Chen, Y. di, Li, S., Ho, S.H., Wang, C., Lin, Y.C., Nagarajan, D., Chang, J.S., Ren, N. qi, 2018b. Integration of sludge digestion and microalgae cultivation for enhancing bioenergy and biorefinery. Renew. Sustain. Energy Rev. 96, 76–90. Chen, Y., Yang, A., Meng, F., Zhang, G., 2019. Additives for photosynthetic bacteria wastewater treatment: latest developments and future prospects. Bioresour. Technol. Reports 7, 100229. Cheng, D.L., Ngo, H.H., Guo, W.S., Chang, S.W., Nguyen, D.D., Kumar, S.M., 2019. Microalgae biomass from swine wastewater and its conversion to bioenergy. Bioresour. Technol. 275, 109–122. Cheng, D.L., Ngo, H.H., Guo, W.S., Liu, Y.W., Zhou, J.L., Chang, S.W., Nguyen, D.D., Bui, X.T., Zhang, X.B., 2018. Bioprocessing for elimination antibiotics and hormones from swine wastewater. Sci. Total Environ. 621, 1664–1682. Cheng, H.H., Whang, L.M., Wu, C.W., Chung, M.C., 2012. A two-stage bioprocess for hydrogen and methane production from rice straw bioethanol residues. Bioresour. Technol. 113, 23–29. Cheng, H.H., Whang, L.M., Chan, K.C., Chung, M.C., Wu, S.H., Liu, C.P., Tien, S.Y., Chen, S.Y., Chang, J.S., Lee, W.J., 2015. Biological butanol production from microalgaebased biodiesel residues by Clostridium acetobutylicum. Bioresour. Technol. 184, 379–385. Cheng, H.H., Whang, L.M., Wu, S.H., 2016. Enhanced bioenergy recovery from oil-extracted microalgae residues via two-step H2/CH4 or H2/butanol anaerobic fermentation. Biotechnol. J. 11, 375–383. Cheng, H.H., Whang, L.M., Yi, T.F., Liu, C.P., Lin, T.F., 2018. Pilot study of cold-rolling wastewater treatment using single-stage anaerobic fluidized membrane bioreactor. Bioresour. Technol. 263, 418–424. Chiang, Y.L., Chen, Y.P., Yu, M.C., Hsieh, S.Y., Hwang, I.E., Liu, Y.J., Huang, C.Y., Tseng, C.P., Liaw, L.L., 2018. Biomass and lipid production of a novel microalga, Chlorellaceae sp. P5, through heterotrophic and swine wastewater cultivation. J. Renew. Sustain Energy 10. Chien, C.C., Yang, Z.H., Cao, W.Z., Tu, Y.T., Kao, C.M., 2016. Application of an aquatic plant ecosystem for swine wastewater polishment: a full-scale study. Desalin. Water Treat. 57, 21243–21252.

5. Challenges and future perspectives Carbon and nutrients removal processes is essential for the swine wastewater before being discharged into the environment system. In this article, several biological techniques are reviewed, including anaerobic digestion, A/O processes, MFCs, and microalgae cultivation, which the appropriate combinations of them could remove not only COD but also the major nutrients, such as N and P. Although biological removals are economical and generally easy to operate, several major challenges still exist during practical applications according to the discussions above. Biological processes are sensitive to environmental factors, for example, HRT, temperature, pH, COD/nutrients loading, C/ N/P ratios in wastewater, etc., and the response to those factors could be different depending on the species cultured. Therefore, it should be thoughtful when determining which biological process or integrated system is more suitable in each case. On the other hand, it is also important to encourage pig farm owners to accept the newly-developed technologies and to communicate to them to properly operate the bioreactors or microalgae ponds, and thus, topics on stabilization or simplification of the processes like automatic control system are suggested for future researches. 6. Conclusion This article reviewed potential and currently available biological processes for swine wastewater treatment, including their removal efficiencies on COD and nutrients and factors affect their performance. Integrated systems would be the best solution for swine wastewater treatment, since it is still difficult to remove all the concerned pollutants using an individual bioprocess. Production of beneficial by-products could also be achieved by reutilizing the microalgal or microbial biomass, such as bioplastics, pigments compound, and bioenergies. Declaration of interests The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. 10

Bioresource Technology 303 (2020) 122861

H.-H. Cheng, et al. Chiu, S.Y., Kao, C.Y., Chen, T.Y., Chang, Y. Bin, Kuo, C.M., Lin, C.S., 2015. Cultivation of microalgal Chlorella for biomass and lipid production using wastewater as nutrient resource. Bioresour. Technol. 184, 179–189. Choi, Y.Y., Patel, A.K., Hong, M.E., Chang, W.S., Sim, S.J., 2019. Microalgae bioenergy with carbon capture and storage (BECCS): an emerging sustainable bioprocess for reduced CO2 emission and biofuel production. Bioresour. Technol. Reports 7, 100270. Córdoba, V., Fernández, M., Santalla, E., 2016. The effect of different inoculums on anaerobic digestion of swine wastewater. J. Environ. Chem. Eng. 4, 115–122. da Fontoura, J.T., Rolim, G.S., Farenzena, M., Gutterres, M., 2017. Influence of light intensity and tannery wastewater concentration on biomass production and nutrient removal by microalgae Scenedesmus sp. Process Saf. Environ. Prot. 111, 355–362. Dash, S., Ng, C.Y., Maranas, C.D., 2016. Metabolic modeling of clostridia: current developments and applications. FEMS Microbiol. Lett. 363, 1–10. Daverey, A., Su, S.-H., Huang, Y.-T., Chen, S.-S., Sung, S., Lin, J.-G., 2013. Partial nitrification and anammox process: a method for high strength optoelectronic industrial wastewater treatment. Water Res. 47, 2929–2937. Ding, L., Cheng, J., Xia, A., Jacob, A., Voelklein, M., Murphy, J.D., 2016. Co-generation of biohydrogen and biomethane through two-stage batch co-fermentation of macro- and micro-algal biomass. Bioresour. Technol. 218, 224–231. Duda, R.M., daSilva Vantini, J., Martins, L.S., deMello Varani, A., Lemos, M.V.F., Ferro, M.I.T., deOliveira, R.A., 2015. A balanced microbiota efficiently produces methane in a novel high-rate horizontal anaerobic reactor for the treatment of swine wastewater. Bioresour. Technol. 197, 152–160. Ellis, J.T., Hengge, N.N., Sims, R.C., Miller, C.D., 2012. Acetone, butanol, and ethanol production from wastewater algae. Bioresour. Technol. 111, 491–495. Fergala, A., Alsayed, A., Khattab, S., Ramirez, M., Eldyasti, A., 2018. Development of methane-utilizing mixed cultures for the production of polyhydroxyalkanoates (PHAs) from anaerobic digester sludge. Environ. Sci. Technol. 52, 12376–12387. Ferreira, A., Marques, P., Ribeiro, B., Assemany, P., deMendonça, H.V., Barata, A., Oliveira, A.C., Reis, A., Pinheiro, H.M., Gouveia, L., 2018. Combining biotechnology with circular bioeconomy: From poultry, swine, cattle, brewery, dairy and urban wastewaters to biohydrogen. Environ. Res. 164, 32–38. Gao, H., Liu, M., Griffin, J.S., Xu, L., Xiang, D., Scherson, Y.D., Liu, W.-T., Wells, G.F., 2017. Complete nutrient removal coupled to nitrous oxide production as a bioenergy source by denitrifying polyphosphate accumulating organisms. Environ. Sci. Technol. 51, 4531–4540. Gao, K., Orr, V., Rehmann, L., 2016. Butanol fermentation from microalgae-derived carbohydrates after ionic liquid extraction. Bioresour. Technol. 206, 77–85. García, D., Posadas, E., Blanco, S., Acién, G., García-Encina, P., Bolado, S., Muñoz, R., 2018. Evaluation of the dynamics of microalgae population structure and process performance during piggery wastewater treatment in algal-bacterial photobioreactors. Bioresour. Technol. 248, 120–126. Glass, J.B., Orphan, V.J., 2012. Trace metal requirements for microbial enzymes involved in the production and consumption of methane and nitrous oxide. Front. Microbiol. 3, 1–20. Guo, G., Cao, W., Sun, S., Zhao, Y., Hu, C., 2017. Nutrient removal and biogas upgrading by integrating fungal–microalgal cultivation with anaerobically digested swine wastewater treatment. J. Appl. Phycol. 29, 2857–2866. Guo, J., Peng, Y., Ni, B.J., Han, X., Fan, L., Yuan, Z., 2015. Dissecting microbial community structure and methane-producing pathways of a full-scale anaerobic reactor digesting activated sludge from wastewater treatment by metagenomic sequencing. Microb. Cell Fact. 14, 1–11. Guo, J., Peng, Y., Wang, S., Ma, B., Ge, S., Wang, Z., Huang, H., Zhang, J., Zhang, L., 2013. Pathways and organisms involved in ammonia oxidation and nitrous oxide emission. Crit. Rev. Environ. Sci. Technol. 43, 2213–2296. Gupta, S., Pawar, S.B., Pandey, R.A., 2019. Current practices and challenges in using microalgae for treatment of nutrient rich wastewater from agro-based industries. Sci. Total Environ. 687, 1107–1126. Han, Z., Chen, S., Lin, X., Yu, H., Duan, L., Ye, Z., Jia, Y., Zhu, S., Liu, D., 2018. Performance and membrane fouling of a step-fed submerged membrane sequencing batch reactor treating swine biogas digestion slurry. J. Environ. Sci. Heal. - Part A Toxic/Hazard. Subst. Environ. Eng. 53, 65–72. Han, Z., Dong, J., Shen, Z., Mou, R., Zhou, Y., Chen, X., Fu, X., Yang, C., 2019. Nitrogen removal of anaerobically digested swine wastewater by pilot-scale tidal flow constructed wetland based on in-situ biological regeneration of zeolite. Chemosphere 217, 364–373. Heidrich, E.S., Curtis, T.P., Dolfing, J., 2011. Determination of the internal chemical energy of wastewater. Environ. Sci. Technol. 45, 827–832. Hung, C.-H., Cheng, C.-H., Guan, D.-W., Wang, S.-T., Hsu, S.-C., Liang, C.-M., Lin, C.-Y., 2011. Interactions between Clostridium sp. and other facultative anaerobes in a selfformed granular sludge hydrogen-producing bioreactor. Int. J. Hydrogen Energy 36, 8704–8711. Inaba, T., Hori, T., Navarro, R.R., Ogata, A., Hanajima, D., Habe, H., 2018. Revealing sludge and biofilm microbiomes in membrane bioreactor treating piggery wastewater by non-destructive microscopy and 16S rRNA gene sequencing. Chem. Eng. J. 331, 75–83. Jena, J., Kumar, R., Dixit, A., Pandey, S., Das, T., 2015. Evaluation of simultaneous nutrient and COD removal with polyhydroxybutyrate (PHB) accumulation using mixed microbial consortia under anoxic condition and their bioinformatics analysis. PLoS One 10, e0116230. Jiang, M., Qiao, W., Ren, Z., Mahdy, A., Wandera, S.M., Li, Y., Dong, R., 2019. Influence of operation conditions on methane production from swine wastewater treated by a self-agitation anaerobic reactor. Int. Biodeterior. Biodegrad. 143, 104710. Jiang, M., Westerholm, M., Qiao, W., Wandera, S.M., Dong, R., 2020... High rate anaerobic digestion of swine wastewater in an anaerobic membrane bioreactor. Energy

193, 116783. Jiang, Y., Zhang, Y., Banks, C., Heaven, S., Longhurst, P., 2017. Investigation of the impact of trace elements on anaerobic volatile fatty acid degradation using a fractional factorial experimental design. Water Res. 125, 458–465. Kamravamanesh, D., Kovacs, T., Pflügl, S., Druzhinina, I., Kroll, P., Lackner, M., Herwig, C., 2018. Increased poly-Β-hydroxybutyrate production from carbon dioxide in randomly mutated cells of cyanobacterial strain Synechocystis sp. PCC 6714: mutant generation and characterization. Bioresour. Technol. 266, 34–44. Kavitha, G., Kurinjimalar, C., Sivakumar, K., Kaarthik, M., Aravind, R., Palani, P., Rengasamy, R., 2016. Optimization of polyhydroxybutyrate production utilizing waste water as nutrient source by Botryococcus braunii Kütz using response surface methodology. Int. J. Biol. Macromol. 93, 534–542. Kelly, P.T., He, Z., 2014. Bioresource Technology Nutrients removal and recovery in bioelectrochemical systems: a review. Bioresour. Technol. 153, 351–360. Kim, H.C., Choi, W.J., Chae, A.N., Park, J., Kim, H.J., Song, K.G., 2016. Evaluating integrated strategies for robust treatment of high saline piggery wastewater. Water Res. 89, 222–231. Kim, J.H., Chen, M., Kishida, N., Sudo, R., 2004. Integrated real-time control strategy for nitrogen removal in swine wastewater treatment using sequencing batch reactors. Water Res. 38, 3340–3348. Kwon, G., Nam, J.-H., Kim, D.-M., Song, C., Jahng, D., 2019. Growth and nutrient removal of Chlorella vulgaris in ammonia-reduced raw and anaerobically-digested piggery wastewaters. Environ. Eng. Res. 25, 135–146. Lauceri, R., Chini Zittelli, G., Maserti, B., Torzillo, G., 2018. Purification of phycocyanin from Arthrospira platensis by hydrophobic interaction membrane chromatography. Algal Res. 35, 333–340. Leng, L., Yang, P., Singh, S., Zhuang, H., Xu, L., Chen, W.H., Dolfing, J., Li, D., Zhang, Y., Zeng, H., Chu, W., Lee, P.H., 2018. A review on the bioenergetics of anaerobic microbial metabolism close to the thermodynamic limits and its implications for digestion applications. Bioresour. Technol. 247, 1095–1106. Liang, Y., Kaczmarek, M.B., Kasprzak, A.K., Tang, J., Shah, M.M.R., Jin, P., KlepaczSmółka, A., Cheng, J.J., Ledakowicz, S., Daroch, M., 2018. Thermosynechococcaceae as a source of thermostable C-phycocyanins: properties and molecular insights. Algal Res. 35, 223–235. Lier, J.B.van, Mahmoud, N., Zeeman, G., 2008. Anaerobic wastewater treatment. In: Henze, M., Loosdrecht, M.C.M.van, Ekama, G.A., Brdjanovic, D. (Eds.), Biological Wastewater Treatment: Principles Modelling and Design. Liu, A.C., Chou, C.Y., Chen, L.L., Kuo, C.H., 2015. Bacterial community dynamics in a swine wastewater anaerobic reactor revealed by 16S rDNA sequence analysis. J. Biotechnol. 194, 124–131. Liu, Y., Ma, S., Huang, L., Wang, S., Liu, G., Yang, H., Zheng, D., Cheng, J., Xu, Z., Deng, L., 2018. Two-step heating mode with the same energy consumption as conventional heating for enhancing methane production during anaerobic digestion of swine wastewater. J. Environ. Manage. 209, 301–307. López-Pacheco, I.Y., Carrillo-Nieves, D., Salinas-Salazar, C., Silva-Núñez, A., ArévaloGallegos, A., Barceló, D., Afewerki, S., Iqbal, H.M.N., Parra-Saldívar, R., 2019. Combination of nejayote and swine wastewater as a medium for Arthrospira maxima and Chlorella vulgaris production and wastewater treatment. Sci. Total Environ. 676, 356–367. Lu, W., Asraful Alam, M., Liu, S., Xu, J., Parra Saldivar, R., 2019. Critical processes and variables in microalgae biomass production coupled with bioremediation of nutrients and CO2 from livestock farms: a review. Sci. Total Environ. 135247. Luo, L., He, H., Yang, C., Wen, S., Zeng, G., Wu, M., Zhou, Z., Lou, W., 2016. Nutrient removal and lipid production by Coelastrella sp. in anaerobically and aerobically treated swine wastewater. Bioresour. Technol. 216, 135–141. Luo, P., Liu, F., Zhang, S., Li, H., Yao, R., Jiang, Q., Xiao, R., Wu, J., 2018. Nitrogen removal and recovery from lagoon-pretreated swine wastewater by constructed wetlands under sustainable plant harvesting management. Bioresour. Technol. 258, 247–254. Manu, D.S., Thalla, A.K., 2017. Artificial intelligence models for predicting the performance of biological wastewater treatment plant in the removal of Kjeldahl Nitrogen from wastewater. Appl. Water Sci. 7, 3783–3791. Marjakangas, J.M., Chen, C.Y., Lakaniemi, A.M., Puhakka, J.A., Whang, L.M., Chang, J.S., 2015. Simultaneous nutrient removal and lipid production with Chlorella vulgaris on sterilized and non-sterilized anaerobically pretreated piggery wastewater. Biochem. Eng. J. 103, 177–184. McCarty, P.L., Kim, J., Shin, C., Lee, P., Bae, J., 2015. Anaerobic fluidized bed membrane bioreactors for the treatment of domestic wastewater. In: Environmental Anaerobic Technology, pp. 211–242. Min, B., Kim, J., Oh, S., Regan, J.M., Logan, B.E., 2005. Electricity generation from swine wastewater using microbial fuel cells. Water Res. 39, 4961–4968. Minton, N.P., Clarke, D.J., 1989. Biotechnology Handbooks: Clostridia. Springer, New York and London. Molinuevo-Salces, B., Mahdy, A., Ballesteros, M., González-Fernández, C., 2016. From piggery wastewater nutrients to biogas: microalgae biomass revalorization through anaerobic digestion. Renew. Energy 96, 1103–1110. Montes, J.A., Leivas, R., Martínez-Prieto, D., Rico, C., 2019. Biogas production from the liquid waste of distilled gin production: Optimization of UASB reactor performance with increasing organic loading rate for co-digestion with swine wastewater. Bioresour. Technol. 274, 43–47. Moreno-Vivián, C., Cabello, P., Martínez-Luque, M., Blasco, R., Castillo, F., 1999. Prokaryotic nitrate reduction: molecular properties and functional distinction among bacterial nitrate reductases. J. Bacteriol. 181, 6573–6584. Müller, B., Sun, L., Schnürer, A., 2013. First insights into the syntrophic acetate-oxidizing bacteria–a genetic study. Microbiologyopen 2, 35–53. Nagarajan, D., Kusmayadi, A., Yen, H.-W., Dong, C.-D., Lee, D.-J., Chang, J.-S., 2019.

11

Bioresource Technology 303 (2020) 122861

H.-H. Cheng, et al. Current advances in biological swine wastewater treatment using microalgae-based processes. Bioresour. Technol. 289, 121718. Padmasiri, S.I., Zhang, J., Fitch, M., Norddahl, B., Morgenroth, E., Raskin, L., 2007. Methanogenic population dynamics and performance of an anaerobic membrane bioreactor (AnMBR) treating swine manure under high shear conditions. Water Res. 41, 134–144. Plácido, J., Bustamante-López, S., Meissner, K.E., Kelly, D.E., Kelly, S.L., 2019. Microalgae biochar-derived carbon dots and their application in heavy metal sensing in aqueous systems. Sci. Total Environ. 656, 531–539. Qilu, C., Ligen, X., Fangmin, C., Gang, P., Qifa, Z., 2018. Bicarbonate-rich wastewater as a carbon fertilizer for culture of Dictyosphaerium sp. of a giant pyrenoid. J. Clean. Prod. 202, 439–443. Qu, W., Zhang, C., Zhang, Y., Ho, S.H., 2019. Optimizing real swine wastewater treatment with maximum carbohydrate production by a newly isolated indigenous microalga Parachlorella kessleri QWY28. Bioresour. Technol. 289, 121702. Rahman, A., Putman, R.J., Inan, K., Sal, F.A., Sathish, A., Smith, T., Nielsen, C., Sims, R.C., Miller, C.D., 2015. Polyhydroxybutyrate production using a wastewater microalgae based media. Algal Res. 8, 95–98. Rahnama, F., Vasheghani-Farahani, E., Yazdian, F., Shojaosadati, S.A., 2012. PHB production by Methylocystis hirsuta from natural gas in a bubble column and a vertical loop bioreactor. Biochem. Eng. J. 65, 51–56. Ravindran, B., Nguyen, D.D., Chaudhary, D.K., Chang, S.W., Kim, J., Lee, S.R., Shin, J.Du., Jeon, B.H., Chung, S.J., Lee, J.J., 2019. Influence of biochar on physico-chemical and microbial community during swine manure composting process. J. Environ. Manage. 232, 592–599. Renugadevi, K., Valli Nachiyar, C., Sowmiya, P., Sunkar, S., 2018. Antioxidant activity of phycocyanin pigment extracted from marine filamentous cyanobacteria Geitlerinema sp TRV57. Biocatal. Agric. Biotechnol. 16, 237–242. Sarnaik, A., Nambissan, V., Pandit, R., Lali, A., 2018. Recombinant Synechococcus elongatus PCC 7942 for improved zeaxanthin production under natural light conditions. Algal Res. 36, 139–151. Sasaki, Y., Takagi, T., Motone, K., Shibata, T., Kuroda, K., Ueda, M., 2018. Direct bioethanol production from brown macroalgae by co-culture of two engineered saccharomyces cerevisiae strains. Biosci. Biotechnol. Biochem. 82, 1459–1462. Scherson, Y.D., Criddle, C.S., 2014. Recovery of freshwater from wastewater: upgrading process configurations to maximize energy recovery and minimize residuals. Environ. Sci. Technol. 48, 8420–8432. Schievano, A., Pepé Sciarria, T., Gao, Y.C., Scaglia, B., Salati, S., Zanardo, M., Quiao, W., Dong, R., Adani, F., 2016. Dark fermentation, anaerobic digestion and microbial fuel cells: an integrated system to valorize swine manure and rice bran. Waste Manag. 56, 519–529. Si, B.C., Li, J.M., Zhu, Z.B., Zhang, Y.H., Lu, J.W., Shen, R.X., Zhang, C., 2016. Biotechnology for Biofuels Continuous production of biohythane from hydrothermal liquefied cornstalk biomass via two - stage high - rate anaerobic reactors. Biotechnol. Biofuels 1–15. Skouteris, G., Hermosilla, D., López, P., Negro, C., Blanco, Á., 2012. Anaerobic membrane bioreactors for wastewater treatment: a review. Chem. Eng. J. 198, 138–148. Song, M., Shin, S.G., Hwang, S., 2010. Methanogenic population dynamics assessed by real-time quantitative PCR in sludge granule in upflow anaerobic sludge blanket treating swine wastewater. Bioresour. Technol. 101, S23–S28. Su, C., Huang, Z., Chen, M., Liu, F., Lu, Y., Nong, Z., Zhu, X., 2019. Effects of infiltrator structure and hydraulic loading rates on pollutant removal efficiency and microbial community in a modified two-stage constructed rapid infiltration systems treating swine wastewater. Environ. Prog. Sustain. Energy 1–7. Sui, Q., Jiang, C., Yu, D., Chen, M., Zhang, J., Wang, Y., Wei, Y., 2018. Performance of a sequencing-batch membrane bioreactor (SMBR) with an automatic control strategy treating high-strength swine wastewater. J. Hazard. Mater. 342, 210–219. Sun, H., Zhao, W., Mao, X., Li, Y., Wu, T., Chen, F., 2018. High-value biomass from microalgae production platforms: strategies and progress based on carbon metabolism and energy conversion. Biotechnol. Biofuels 11, 1–23. Tenca, A., Schievano, A., Perazzolo, F., Adani, F., Oberti, R., 2011. Biohydrogen from thermophilic co-fermentation of swine manure with fruit and vegetable waste: maximizing stable production without pH control. Bioresour. Technol. 102, 8582–8588. Tran, D.-T., Yeh, K.-L., Chen, C.-L., Chang, J.-S., 2012. Enzymatic transesterification of microalgal oil from Chlorella vulgaris ESP-31 for biodiesel synthesis using immobilized Burkholderia lipase. Bioresour. Technol. 108, 119–127. Troschl, C., Meixner, K., Fritz, I., Leitner, K., Romero, A.P., Kovalcik, A., Sedlacek, P., Drosg, B., 2018. Pilot-scale production of poly-β-hydroxybutyrate with the cyanobacterium Synechocytis sp. CCALA192 in a non-sterile tubular photobioreactor. Algal Res. 34, 116–125. Tsapekos, P., Kougias, P.G., Alvarado-Morales, M., Kovalovszki, A., Corbière, M., Angelidaki, I., 2018. Energy recovery from wastewater microalgae through anaerobic digestion process: methane potential, continuous reactor operation and modelling aspects. Biochem. Eng. J. 139, 1–7. Tu, Z., Ren, X., Zhao, J., Awasthi, S.K., Wang, Q., Awasthi, M.K., Zhang, Z., Li, R., 2019. Synergistic effects of biochar/microbial inoculation on the enhancement of pig manure composting. Biochar 1, 127–137. Vilajeliu Pons, A., Puig, S., Salcedo-Dávila, I., Balaguer, M.D., Colprim, J., 2017. Longterm assessment of the six-stacked scaled-up MFCs treating swine manure with different electrode materials. Environ. Sci. Water Res. Technol. 3, 947–959. Waki, M., Yasuda, T., Fukumoto, Y., Béline, F., Magrí, A., 2018. Treatment of swine wastewater in continuous activated sludge systems under different dissolved oxygen conditions: reactor operation and evaluation using modelling. Bioresour. Technol. 250, 574–582. Wang, H., Xiong, H., Hui, Z., Zeng, X., 2012. Mixotrophic cultivation of Chlorella

pyrenoidosa with diluted primary piggery wastewater to produce lipids. Bioresour. Technol. 104, 215–220. Wang, R., Feng, F., Chai, Y., Meng, X., Sui, Q., Chen, M., Wei, Y., Qi, K., 2019. Screening and quantitation of residual antibiotics in two different swine wastewater treatment systems during warm and cold seasons. Sci. Total Environ. 660, 1542–1554. Wang, Y., Guo, W., Yen, H.W., Ho, S.H., Lo, Y.C., Cheng, C.L., Ren, N., Chang, J.S., 2015. Cultivation of Chlorella vulgaris JSC-6 with swine wastewater for simultaneous nutrient/COD removal and carbohydrate production. Bioresour. Technol. 198, 619–625. Wang, Y., Ho, S.H., Cheng, C.L., Nagarajan, D., Guo, W.Q., Lin, C., Li, S., Ren, N., Chang, J.S., 2017. Nutrients and COD removal of swine wastewater with an isolated microalgal strain Neochloris aquatica CL-M1 accumulating high carbohydrate content used for biobutanol production. Bioresour. Technol. 242, 7–14. Ward, A.J., Arola, K., Thompson Brewster, E., Mehta, C.M., Batstone, D.J., 2018. Nutrient recovery from wastewater through pilot scale electrodialysis. Water Res. 135, 57–65. Wei, S., Zhu, M., Fan, X., Song, J., Peng, P., Li, K., Jia, W., Song, H., 2019. Influence of pyrolysis temperature and feedstock on carbon fractions of biochar produced from pyrolysis of rice straw, pine wood, pig manure and sewage sludge. Chemosphere 218, 624–631. Weißbach, M., Thiel, P., Drewes, J.E., Koch, K., 2018. Nitrogen removal and intentional nitrous oxide production from reject water in a coupled nitritation/nitrous denitritation system under real feed-stream conditions. Bioresour. Technol. 255, 58–66. Wen, S., Liu, H., He, H., Luo, L., Li, X., Zeng, G., Zhou, Z., Lou, W., Yang, C., 2016. Treatment of anaerobically digested swine wastewater by Rhodobacter blasticus and Rhodobacter capsulatus. Bioresour. Technol. 222, 33–38. WRAP, 2014. A survey of the UK Anaerobic Digestion industry in 2013, Prepared by LRS Consultancy. Wu, X., Zhu, J., Cheng, J., Zhu, N., 2015. Optimization of three operating parameters for a two-step fed sequencing batch reactor (SBR) system to remove nutrients from swine wastewater. Appl. Biochem. Biotechnol. 175, 2857–2871. Xia, A., Jacob, A., Tabassum, M.R., Herrmann, C., Murphy, J.D., 2016. Production of hydrogen, ethanol and volatile fatty acids through co-fermentation of macro- and micro-algae. Bioresour. Technol. 205, 118–125. Xie, G.-J., Cai, C., Hu, S., Yuan, Z., 2016. Complete nitrogen removal from synthetic anaerobic sludge digestion liquor through integrating anammox and denitrifying anaerobic methane oxidation in a membrane biofilm reactor. Environ. Sci. Technol. 51, 819–827. Xin, X., Hong, J., He, J., Qiu, W., 2019. An integrated approach for waste activated sludge management towards electric energy production/resource reuse. Bioresour. Technol. 274, 225–231. Xu, Z., Song, X., Li, Y., Li, G., Luo, W., 2019. Removal of antibiotics by sequencing-batch membrane bioreactor for swine wastewater treatment. Sci. Total Environ. 684, 23–30. Yang, D., Deng, L., Zheng, D., Wang, L., Liu, Y., 2016. Separation of swine wastewater into different concentration fractions and its contribution to combined anaerobicaerobic process. J. Environ. Manage. 168, 87–93. Yang, H., Deng, L., Liu, G., Yang, D., Liu, Y., Chen, Z., 2016. A model for methane production in anaerobic digestion of swine wastewater. Water Res. 102, 464–474. Yang, H., Deng, L., Wang, L., Zheng, D., Liu, Y., Wang, S., Huang, F., 2019. Comparison of three biomass-retaining reactors of the ASBR, the UBF and the USR treating swine wastewater for biogas production. Renew. Energy 138, 521–530. Yang, Z., Guo, R., Xu, X., Fan, X., Luo, S., 2011a. Fermentative hydrogen production from lipid-extracted microalgal biomass residues. Appl. Energy 88, 3468–3472. Yang, Z., Guo, R., Xu, X., Fan, X., Luo, S., 2011b. Hydrogen and methane production from lipid-extracted microalgal biomass residues. Int. J. Hydrogen Energy 36, 3465–3470. Ye, Y., Ngo, H.H., Guo, W., Liu, Y., Chang, S.W., Nguyen, D.D., Liang, H., Wang, J., 2018. A critical review on ammonium recovery from wastewater for sustainable wastewater management. Bioresour. Technol. 268, 749–758. Yenigün, O., Demirel, B., 2013. Ammonia inhibition in anaerobic digestion: a review. Process Biochem. 48, 901–911. Yu, J., Hu, H., Wu, X., Zhou, T., Liu, Y., Ruan, R., Zheng, H., 2020.. Coupling of biocharmediated absorption and algal-bacterial system to enhance nutrients recovery from swine wastewater. Sci. Total Environ. 701, 134935. Yu, K.L., Show, P.L., Ong, H.C., Ling, T.C., Chi-Wei Lan, J., Chen, W.H., Chang, J.S., 2017. Microalgae from wastewater treatment to biochar – Feedstock preparation and conversion technologies. Energy Convers. Manag. 150, 1–13. Yun, Y.-M., Cho, S.-K., Jung, K.-W., Kim, M.-S., Shin, H.-S., Kim, D.-H., 2014. Inhibitory effect of chloroform on fermentative hydrogen and methane production from lipidextracted microalgae. Int. J. Hydrogen Energy 39, 19256–19261. Zeng, X., Guo, X., Su, G., Danquah, M.K., Zhang, S., Lu, Y., Sun, Y., Lin, L., 2015. Bioprocess considerations for microalgal-based wastewater treatment and biomass production. Renew. Sustain. Energy Rev. 42, 1385–1392. Zeng, Z., Zhang, M., Kang, D., Li, Y., Yu, T., Li, W., Xu, D., Zhang, W., Shan, S., Zheng, P., 2019. Enhanced anaerobic treatment of swine wastewater with exogenous granular sludge: performance and mechanism. Sci. Total Environ. 697, 134180. Zhang, B., Wang, L., Riddicka, B.A., Li, R., Able, J.R., Boakye-Boaten, N.A., Shahbazi, A., 2016. Sustainable production of algal biomass and biofuels using swine wastewater in North Carolina. US, Sustain, pp. 8. Zhang, C., Su, H., Baeyens, J., Tan, T., 2014. Reviewing the anaerobic digestion of food waste for biogas production. Renew. Sustain. Energy Rev. 38, 383–392. Zhang, L., Lee, Y.W., Jahng, D., 2011. Anaerobic co-digestion of food waste and piggery wastewater: focusing on the role of trace elements. Bioresour. Technol. 102, 5048–5059. Zhang, M., Gu, J., Liu, Y., 2019. Engineering feasibility, economic viability and environmental sustainability of energy recovery from nitrous oxide in biological wastewater treatment plant. Bioresour. Technol. 282, 514–519.

12

Bioresource Technology 303 (2020) 122861

H.-H. Cheng, et al. Zhang, T.Y., Wu, Y.H., Zhu, S., feng, Li, F.M., Hu, H.Y., 2013. Isolation and heterotrophic cultivation of mixotrophic microalgae strains for domestic wastewater treatment and lipid production under dark condition. Bioresour. Technol. 149, 586–589. Zhao, B., Li, J., Buelna, G., Dubé, R., LeBihan, Y., 2016. A combined upflow anaerobic sludge bed and trickling biofilter process for the treatment of swine wastewater. Environ. Technol. (United Kingdom) 37, 1265–1275. Zhao, Bowei, Li, J., Leu, S.Y., 2014. An innovative wood-chip-framework soil infiltrator for treating anaerobic digested swine wastewater and analysis of the microbial community. Bioresour. Technol. 173, 384–391. Zhao, Baisuo, Ma, J., Zhao, Q., Laurens, L., Jarvis, E., Chen, S., Frear, C., 2014. Efficient anaerobic digestion of whole microalgae and lipid-extracted microalgae residues for

methane energy production. Bioresour. Technol. 161, 423–430. Zhou, M., Yan, B., Wong, J.W.C., Zhang, Y., 2018. Enhanced volatile fatty acids production from anaerobic fermentation of food waste: A mini-review focusing on acidogenic metabolic pathways. Bioresour. Technol. 248, 68–78. Zhou, Q., Li, X., Lin, Y., Yang, C., Tang, W., Wu, S., Li, D., Lou, W., 2019. Effects of copper ions on removal of nutrients from swine wastewater and on release of dissolved organic matter in duckweed systems. Water Res. 158, 171–181. Zhu, L., Wang, Z., Shu, Q., Takala, J., Hiltunen, E., Feng, P., Yuan, Z., 2013. Nutrient removal and biodiesel production by integration of freshwater algae cultivation with piggery wastewater treatment. Water Res. 47, 4294–4302.

13