Anaerobic digestion to reduce biomass and remove arsenic from As-hyperaccumulator Pteris vittata

Environmental Pollution 250 (2019) 23e28

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Anaerobic digestion to reduce biomass and remove arsenic from As-hyperaccumulator Pteris vittata* Evandro B. da Silva a, b, Wendy A. Mussoline a, Ann C. Wilkie a, Lena Q. Ma a, b, * a b

Soil and Water Sciences Department, University of Florida, Gainesville, FL, 32611, United States Institute of Environment Remediation and Human Health, South West Forestry University, Yunnan, 650224, China

a r t i c l e i n f o

a b s t r a c t

Article history: Received 11 January 2019 Received in revised form 26 March 2019 Accepted 28 March 2019 Available online 2 April 2019

The lack of efficient methods to treat As-rich biomass is a drawback for phytoremediation technology. In this study, we applied anaerobic digestion to reduce biomass and remove As from As-rich Pteris vittata biomass. P. vittata biomass including control (3.1 mg kg
1 As) and As-rich (2665 mg kg
1 As), together with positive and negative controls, was anaerobically digested at 35  C for 35 d. Arsenic partitioning among gas, liquid and solid phases after anaerobic digestion was determined. Methane index potential assay was used to assess methane yields whereas liquid-displacement method was used to measure methane gas production. After 35 d, As partitioning in the liquid, solid and gas phases was 79, 30 and 1%, respectively. Besides, volatile solid was decreased from 91 to 12e17% total solid, while P. vittata biomass was decreased by 73e83%. Moreover, anaerobic digestion solubilized 76% As from P. vittata biomass, with 90% soluble As at 4.95 mg L
1 being recovered by As-Mg precipitation. Finally, methane production after 35 d was 197e212 LNCH4/kg volatile solid, showing slight As inhibition. Effective As removal from P. vittata biomass prior to disposal can improve the phytoremediation process. Published by Elsevier Ltd.

Keywords: Arsenic removal Solubilization Partition Biomass disposal Methane production Precipitation

1. Introduction Arsenic is the most hazardous element as its chronic exposure causes cancers (Gress et al., 2015). It is naturally present in soils at 0.1e67 mg kg
1. However, anthropogenic activities have increased its concentrations in soils (da Silva et al., 2018a; Mandal and Suzuki, 2002). Arsenate (AsV) and arsenite (AsIII) are its two primary forms in soils, with AsV being the main form in aerobic environment while AsIII dominates under anoxic condition (Bohn et al., 2002). The main pathway for As exposure in humans is through consumption of contaminated food and water (ATSDR, 2017; Gress et al., 2016, 2014). Arsenic contaminated sites are present in all 5 continents, and in the US there are over 600 sites that require cleanup actions (Bagchi, 2007; USEPA, 2017). However, conventional remediation technologies are laborious and expensive (Missimer et al., 2018). As a perennial plant, As-hyperaccumulator Chinese brake fern (Pteris vittata L.) is suitable to phytoremediate As-contaminated soils (da Silva et al., 2018b). During

*

This paper has been recommended for acceptance by Prof. Wen-Xiong Wang. * Corresponding author. Institute of Environment Remediation and Human Health, South West Forestry University, Yunnan, 650224, China. E-mail address: lqma@ufl.edu (L.Q. Ma). https://doi.org/10.1016/j.envpol.2019.03.117 0269-7491/Published by Elsevier Ltd.

phytoremediation, metals are accumulated in the shoots, which can be collected and disposed off-site (Ma et al., 2001; Singh et al., 2018). However, its effectiveness depends on soil properties, metal bioavailability, and plant's biomass and ability to accumulate metals (Hare et al., 2019). It is known that P. vittata can accumulate up to 23 g kg
1 As in the fronds (Ma et al., 2001; Tu and Ma, 2002), which is mostly water soluble (da Silva et al., 2018c). Thus, improper disposal of As-rich biomass may cause As contamination in the environment. Conventional disposal methods of contaminated biomass include disposal at landfills and incineration (Fangueiro et al., 2018). In Florida, it was estimated that 884 million m3 of As-treated wood was disposed in unlined landfills in 2000 alone (Solo-Gabriele et al., 2003). However, under anaerobic conditions in landfills, As-treated wood can leach >11% of total As, with concentration being 4000 times higher than the maximum contaminant level for groundwater (Jambeck et al., 2006). Therefore, it is important to treat P. vittata biomass prior to its disposal. Recently, an alternative method to treat As-rich biomass was developed, which coupled ethanol extraction with anaerobic digestion (da Silva et al., 2019). The method solubilized ~98% As from P. vittata biomass, with soluble As being recovered by As-Mg precipitation. However, the potential of anaerobic digestion to solubilize As without ethanol

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extraction was not tested. Anaerobic digestion is a complex system where symbiotic microbes transform organic C into biogas under anoxic environment, leaving refractory organic C (Wilkie, 2008). Anaerobic digestion can strip metals from the biomass, allowing its further recovery. However, metal availability is affected by contaminants and components in biomass, and redox potential (Cheng et al., 2015). Moreover, microbes use organic C as an energy source, thereby reducing biomass and disposal cost. Besides, As volatilization is minimal during this process (Sierra-Alvarez et al., 2004). Therefore, anaerobic digestion may be used directly to treat As-rich biomass. However, it is necessary to assess its effectiveness and As partition during this process. The goal of this study was to assess the potential of anaerobic digestion to treat As-rich biomass. The specific objectives were to: 1) examine substrate utilization kinetics of P. vittata biomass during anaerobic digestion; 2) compare the degradation kinetics of As-rich and control biomass; and 3) assess As partition in different phases after anaerobic digestion. Arsenic recovery from P. vittata biomass and decrease in P. vittata biomass help to improve phytoremediation application. 2. Material and methods 2.1. Chemical reagents and P. vittata biomass All labware was cleaned in 1 M HNO3 for 24 h and rinsed several times with DI water. Nitric acid (trace metal grade) and H2O2 were from Fisher Scientific (Waltham, MA). For As speciation, Sep-Pak AccellPlus QMA Plus Short cartridges were used (Waters Corporation, Milford, MA). All biomass in this study was from P. vittata fronds. While Asrich P. vittata biomass was harvested in July 2013 from a longterm phytoremediation experiment (da Silva et al., 2018b), biomass with no As was harvested in 2009 from a greenhouse. All biomass was oven-dried at 65  C to constant weight, grinded to <1 mm size and properly stored. Characterization of P. vittata frond biomass is shown in Table 1. 2.2. Methane index potential from P. vittata biomass Anaerobic digestion was used in this study to reduce biomass and solubilize As from P. vittata. Treatments included: controlbiomass (3.1 mg kg
1 As) and As-rich biomass (2665 mg kg
1 As) (Table 1). Methane index potential assay was used to assess methane yields from P. vittata biomass (Wilkie et al., 2004). For this study, P. vittata biomass was anaerobically digested similarly to da Silva et al. (2019). Briefly, P. vittata biomass was added to 250-mL anaerobic serum bottles [2.0 g volatile solids (VS) per liter (g VS L
1)], with 200 mL of inoculum. The inoculum was

Table 1 Characterization of P. vittata biomass including control biomass and As-rich biomass. Data are means ± standard deviation (n ¼ 3).

pH (0.01 M CaCl2) Total solids (%) Volatile solids (%TS) Total COD (g/kg) As (mg kg
1) Cu (mg kg
1) Zn (mg kg
1) Ca (mg kg
1) Mg (mg kg
1) K (mg kg
1)

As-rich biomass

control biomass

5.14 93.1 ± 0.3 90.6 ± 0.1 877 ± 121 2665 ± 31 9.9 ± 0.2 63.1 ± 2.1 7710 ± 180 6890 ± 420 25,916 ± 1510

5.61 92.6 ± 0.1 91.1 ± 0.1 1020 ± 151 3.10 ± 0.03 8.1 ± 1.2 51 ± 3.5 3500 ± 250 4410 ± 198 12,815 ± 751

from a mesophilic anaerobic digester, which was fed with food waste and characterized similarly as P. vittata biomass. Total solids (TS) was determined by drying the samples in an oven at 105  C for 24 h, and VS was determined by heating the sample in a muffle furnace at 550  C (da Silva et al., 2019). Total solids and VS were determined before and after anaerobic digestion. The inoculum had a pH of 7.62 ± 0.01, 0.66% TS, 28.9% VS and As concentration <0.01 mg L
1. Inoculum was included as a negative control, and positive control consisted of glucose, cellulose and starch. P. vittata biomass, with positive and negative controls, was assayed in triplicate. Bottles were sealed with a rubber septum, crimped with an aluminum cap, and inverted to prevent potential gas leakage, which were incubated at 35  C for 35 d. A liquid-displacement method with 3 M KOH as the barrier solution was used to measure methane gas production (Wilkei et al., 2004). Gas production was calculated as the difference between initial and final meniscus level in the glass bottle. During peak methane production, gas measurement was recorded daily, and later at longer intervals based on gas production. The methane volumes were corrected after subtracting the methane volume from the inoculum control, which were then normalized to standard temperature and pressure (0  C and 760 mm Hg). The methane yields are reported as normalized liter (i.e., LN) of methane produced per kg of VS added. After anaerobic digestion, biomass and VS mass balances were performed. Biomass mass balance was obtained by subtracting the final biomass and inoculum TS from the TS of initial biomass. Volatile solids mass balance was obtained by subtracting final biomass and inoculum VS from the VS of initial biomass. After anaerobic digestion, As in liquid phase was precipitated from the anaerobic digestate supernatant by adding MgCl2 at As:Mg ratio of 1:400 and pH 9.5 (da Silva et al., 2018c). Arsenic in solution was determined using inductively coupled plasma mass spectrometry (ICP-MS, PerkinElmer Corp., Norwalk, CT). In addition, a standard reference material from the National Institute of Science and Technology (NIST 1547 e peach leaves, Gaithersburg, MD) and appropriate reagent blanks, internal standards and spikes were used as quality control to ensure method accuracy and precision, which were within 80e120% recovery. Arsenic detection limit was 0.005 mg L
1. 2.3. Arsenic analysis in plant biomass and mass balance P. vittata biomass was digested using USEPA Method 3050B (Environmental Express hot block, Ventura, CA). Briefly, 0.5 g of dried biomass was added to 15 mL 1:1 HNO3:water, which was heated at 105  C for 8 h. After cooling, 1 mL of 30% H2O2 was added and the sample was digested for 30 min before bringing samples to a 50 mL volume with DI water. Arsenic mass balance was calculated after anaerobic digestion (da Silva et al., 2019). Briefly, samples were centrifuged for 15 min at 4200 rpm and filtered (Whatman N. 42 filters). Solid phase was oven-dried at 60  C for 24 h and separated into two components: P. vittata biomass and other solids. Finally, homogeneous sub-samples (liquid and solid phases) were digested and As concentration was determined by ICP-MS. Arsenic in the gas phase was determined by trapping the gas in 20 mL of 2 M nitric acid and analyzing for total As using ICP-MS. 2.4. Statistical analyses All data are presented as the mean of three replicates with standard deviation after checking for normality using Shapiro-Wilk test. Significant differences were determined using one-way analysis of variance and treatment means were compared by Tukey's

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multiple range test at p < 0.05 using R software (Team, 2005). 3. Results and discussions Anaerobic digestion converts organic C to energy plus biogas by a consortium of microbes under anoxic conditions (Wilkie, 2008). P. vittata biomass had high organic C and volatile solids at 91.1 and 90.6 g kg
1 (Table 1), common for plants. Besides, the inoculum presented satisfactory methanogenic activity to convert glucose, cellulose and starch from the positive control data (data not shown). 3.1. Arsenic partition after anaerobic digestion Several methods have been used to extract As from biomass including 2.1% HCl, 2.1% H3PO4, 1 M NaOH and 35e50% ethanol (da Silva et al., 2018c; Tan et al., 2018; Zhao et al., 2015). It is known that AsV is more recalcitrant than AsIII as it tends to accumulate in the cell walls while AsIII is often stored in plant vacuoles (Yuan et al., 2005). For P. vittata, almost all As is present as inorganic form (Ma et al., 2001). Though AsIII is the major species in fresh P. vittata biomass, 99% As is present as AsV in dry biomass (da Silva et al., 2018c). In addition, for P. vittata biomass, ~90% As was extracted using 35% ethanol (da Silva et al., 2019). However, after the extraction, P. vittata biomass did not decrease, with 10% As being left in the biomass. In comparison, anaerobic digestion can not only remove As but also decrease biomass quantity. However, it is imperative to understand As partition among three phases and its biomass degradation. Arsenic partition is an important indication of the efficiency of anaerobic digestion. Based on Fig. 1, anaerobic digestion efficiently solubilized and recovered As from P. vittata biomass. After 35 d, As partition in the liquid, solid and gas phases was 79, 30 and 1%, respectively (Fig. 1A). Among the three phases, most of the As was in the aqueous phase at 79%. Arsenic was released into solution during anaerobic digestion of organic C by microbes. The soluble As in solution was 4.95 mg L
1 after anaerobic digestion (Fig. 1B). Other studies have reported lower As solubilization being 2e49% (Ghosh et al., 2006; Mestrot et al., 2013; Webster et al., 2016). For the 30% As in the solid phase, 24% was in P. vittata biomass while 6% was in other solids associated with microbial inoculum (Fig. 1A). Compared to liquid and solid phase, As volatilization was low in this study at 1%, similar to other studies (Cortinas et al., 2006; Mestrot et al., 2013). Studies reporting high As volatilization are usually based on differences in the liquid and solid phases rather than actual measurement in the gas phase (Cao et al., 2010; Turpeinen et al., 2002; Webster et al., 2016). Besides As partition, we also determined the changes in the volatile solids and P. vittata biomass. Reduction of volatile solids in P. vittata biomass was similar to other biomass, decreasing from 91 to 12e17% total solid (Fig. 2A) (Li et al., 2014). In addition, P. vittata biomass was decreased by 73e83%, with As concentrations in the remaining biomass being increased from 2665 to 3048 mg kg
1 (Fig. 2B). Cao et al. (2010) noticed 20% As enrichment in P. vittata biomass after aerobic composting. In another study, 45% As from rice straw was solubilized at 5% TS content and pH 8 (Xin et al., 2018). However, volatile solid was decreased only by 40%, indicating low inoculum efficiency as As concentration was much lower compared to As-rich P. vittata biomass (6.45 vs. 2665 mg kg
1). Compared to ethanol extraction followed by anaerobic digestion, anaerobic digestion alone was not as efficient in solubilizing As from P. vittata biomass (da Silva et al., 2019). By coupling ethanol extraction with anaerobic digestion, As concentration in the biomass was decreased by 98% from 2665 to 60 mg kg
1 with similar biomass degradation rate. At this level, P. vittata biomass is a

Fig. 1. Arsenic partitioning among gas, solid (1 ¼ P. vittata biomass; 2 ¼ Other solids) and liquid phases in P. vittata biomass (A) and solution arsenic removal as As-Mg precipitate using MgCl2 at As:Mg ratio of 1:400 and pH 9.5 (B). Bars followed by the same letters are not significantly different at p < 0.05. *As in the solid phase was 30%.

safe material by USEPA regulations (<100 mg kg
1). Therefore, ethanol extraction is a recommended step, however, it can be done after anaerobic digestion as there is less biomass to be extracted. Nevertheless, in both cases, anaerobic digestion of As-rich P. vittata biomass can reduce the As impact in landfill as soluble As was removed, with the most recalcitrant forms remaining in the biomass. Compared to aerobic composting, anaerobic digestion was more effective in As solubilization and biomass reduction. For example, arsenic volatilization was 18% in aerobic composting and can be as high as ~100% during incineration (Cao et al., 2010; Han et al., 2018). Besides, degradation rate of As-rich biomass in aerobic composting was only 38%, with 25% As decrease. In this study, biomass reduction was 73e83% (Fig. 2B), with 76% As decrease in PV biomass (Fig. 1A). Therefore, based on our data, anaerobic digestion of P. vittata biomass was satisfactory and can be used to treat As-rich biomass. 3.2. Methane production from P. vittata biomass After 35 d of anaerobic digestion, methane production from P. vittata biomass was 197e212 LNCH4/kg VS (Table 2 and Fig. 3). Compared to methane yield from corn stover or grass (304e410 LNCH4/kg VS), P. vittata biomass was lower (Sawatdeenarunat et al., 2015; Triolo et al., 2011). Nevertheless, it showed similar yield with

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Fig. 3. Cumulative methane yield (LNCH4/kg VS) of P. vittata biomass after 35 d of anaerobic digestion. Treatments included control biomass and As-rich biomass. Bars represent standard deviation (n ¼ 3).

Fig. 2. Initial and final volatile solids (%TS) (A) and remaining P. vittata biomass (%) (B) after 35 d of anaerobic digestion. Treatments included control biomass and As-rich biomass. Treatments followed by the same letters are not significantly different at p < 0.05. Numbers inside bars represent initial As concentrations, and initial and final biomass.

Table 2 Cumulative methane yield (LNCH4/kg VS) for control and As-rich P. vittata biomass. Data are means ± standard deviation (n ¼ 3). Days

Control

As-rich

Difference in CH4 yield (%)a

0 1 2 3 5 7 9 11 14 18 22 26 30 35

0.00 ± 0.00 14.5 ± 1.17 33.0 ± 1.17 55.4 ± 1.81 95.2 ± 1.72 125 ± 1.49 142 ± 1.17 151 ± 0.33 164 ± 0.33 178 ± 0.33 190 ± 0.00 198 ± 0.56 205 ± 0.86 212 ± 0.56

0.00 ± 0.00 6.6 ± 2.54 30.8 ± 0.65 52.7 ± 1.69 83.7 ± 1.49 111 ± 0.86 132 ± 0.65 143 ± 0.56 155 ± 0.86 168 ± 0.56 178 ± 0.33 185 ± 0.56 191 ± 0.65 197 ± 0.98

0.00 54.5 6.82 4.75 12.0 11.3 7.40 5.33 5.61 5.60 6.22 6.53 6.76 6.83

a

Calculated as: [(control biomass - As-rich biomass)  100] ÷control biomass.

other feedstocks. For instance, sorghum and rice straw yielded 195e231 LNCH4/kg VS (Dinuccio et al., 2010; Mussoline et al., 2012). In this study, methane production kinetics from P. vittata biomass was similar to other feedstock, yielding 84e85% (178e168 LNCH4/ kg VS) after 18 d of anaerobic digestion (Fig. 3). Methane production is affected by biomass composition, which can limit lignocellulosic substrates accessibility during fermentation. Compared to control biomass (3.1 mg kg
1 As), the overall methane yield was decreased by 7% in As-rich biomass (Fig. 3 and Table 2). The fact that microbes were able to degrade P. vittata biomass containing 2665 mg kg
1 As indicated their resistance to As. After 35 d of anaerobic digestion, As in aqueous solution was 4.95 mg L
1, which should be toxic to microbes. It is known that As

at 1.16 mg L
1 reduces acetate-utilizing methanogen activity by 50% (Sierra-Alvarez et al., 2004), while at 2.03 mg L
1 As, the activity of hydrogen-utilizing methanogens are reduced by 50%. In this study, the water soluble As concentration was 4.47e4.95 mg L
1 (data not shown) (Field et al., 2004). Though As concentration was much greater than those reported in other studies, As had limited impact on methane yield. It should be noted that other studies target certain methanogenic species by feeding them with specific C sources (Sierra-Alvarez et al., 2004). In this study, slight As inhibition was observed, with methane yield being reduced by 7% after 35 d of anaerobic digestion. Besides As toxicity, reduction in methane production in the final phase can be related to less biomass and inoculum decadency. Furthermore, solid phase (17e27%, Fig. 2B) might reduce As toxicity by providing protection from As inhibition (Chen et al., 2008). Though biogas production was not the scope of this study, it adds value to anaerobic digestion as a method to treat As-rich biomass to decrease landfill disposal. 3.3. Precipitation of water-soluble As from P. vittata biomass After anaerobic digestion, soluble As in the solution requires further treatment. The As concentration in aqueous phase was 4.95 mg L
1 for As-rich biomass (Fig. 1B). Arsenic removal from effluents can be achieved by precipitation with Fe oxides, adsorption and electrocoagulation (Bissen and Frimmel, 2003; Sullivan et al., 2003). In addition, AsV can be precipitated with Mg. In fact, spontaneous precipitation of As with Mg may occur at pH 7e10 depending on As:Mg molar ratio; however, at pH > 9.5, Mg(OH)2 starts to precipitate, affecting precipitation efficiency (Tabelin et al., 2013). In this study, we added MgCl2 at 1:400 As:Mg molar ratio and pH 9.5, which reduced As concentration in solution from 4.95 to 0.51 mg L
1 (Fig. 1B). Residual Mg can be precipitated as Mg(OH)2 by increasing pH to >11, allowing its reuse in As removal after acid dissolution (da Silva et al., 2019). The As-Mg precipitate can be reused or sent to landfill. 4. Conclusions A new method to treat As-rich biomass was developed using anaerobic digestion, followed by precipitating soluble As with MgCl2, which produced satisfactory results. Methane yield, a byproduct of anaerobic digestion, was 197e212 LNCH4/kg VS after

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35 d of anaerobic digestion. Compared to control biomass, the presence of As reduced methane yield by 7% in As-rich biomass. In addition, volatile solid and P. vittata biomass were decreased from 91 to 12e17% and 73e83%, respectively. Anaerobic digestion solubilized As from P. vittata biomass by 76%, with As in the remaining biomass being 3048 mg kg
1 due to slightly As enrichment. As a final step, 90% of the soluble As in aqueous phase was recovered by As-Mg precipitation, decreasing As concentration from 4.95 to 0.51 mg L
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