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Journal of Cleaner Production 228 (2019) 63e72

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Journal of Cleaner Production

journal homepage: www.elsevier .com/locate/ jc lepro

An integrated process of chemical precipitation and sulfate reductionfor treatment of flue gas desulphurization wastewater from coal-firedpower plant

Jia Yan a, b, Wenhuan Yuan a, Jian Liu a, Weizhuo Ye a, Jinlan Lin a, Jiahao Xie a,Xuan Huang a, Shanshan Gao a, Jiehui Xie a, Shinian Liu c, Wenzhong Chen d,Hongguo Zhang a, b, *

a School of Environmental Science and Engineering, Guangzhou University, Guangzhou, 510006, PR Chinab Guangzhou University-Link€oping University Research Center on Urban Sustainable Development, Guangzhou University, 510006, Guangzhou, Chinac Guangdong Diankeyuan Energy Technology Co., Ltd, 510006, Guangzhou, Chinad Zhan Jiang Zhong Yue Energy Co., Ltd, 524033, Zhanjiang, China

a r t i c l e i n f o

Article history:Received 8 February 2019Received in revised form16 April 2019Accepted 18 April 2019Available online 24 April 2019

Keywords:Flue gas desulphurization wastewaterSulfate reductionMetal removalRefractory organics removalWastewater recycling

* Corresponding author. School of EnvironmentaGuangzhou University, Guangzhou, 510006, PR China

E-mail address: hgzhang@gzhu.edu.cn (H. Zhang).

https://doi.org/10.1016/j.jclepro.2019.04.2270959-6526/© 2019 Elsevier Ltd. All rights reserved.

a b s t r a c t

Flue gas desulphurization process in coal-fired power plants, produces wastewater with concentratedsulfate, chloride, metals and refractory organic compounds, which leads to serious pollution andcorrosion problem during recycling. In this study, an integrated process of chemical precipitation andsulfate reduction for treatment of coal-fired power plant flue gas desulphurization wastewater wasdeveloped. Without additional of heavy metal trapping and strong oxidizing agents, chemical precipi-tation was performed as pre-treatment for removal of suspended solid (97%) in raw flue gas desul-phurization wastewater. Comparison study on treatment of pre-treated flue gas desulphurizationwastewater were performed in three parallelly operated sequencing batch reactors, by cultured sulfatereducing bacteria strain BY7, SR10 and SR3, respectively. This study demonstrated that strain BY7 andSR10 sulfate reducing bacteria were able to adapted to high-salinity flue gas desulphurization waste-water, with high efficiencies of sulfate reduction (86e94%), metals (70e100%) and refractory organiccompounds removal (85e95%). The highest sulfate loading rate of 0.5 kg SO4

2�/m3$d was achieved insequencing batch reactors with strain BY7 and SR10. Besides, a sustainable removal of chloride andfluoride were achieved (about 35% and 55%, respectively), which probably relate to co-precipitation orbiosorption processes. Up to 14 out of 25 refractory organic compounds in flue gas desulphurizationwastewater could be completely removed after integrated treatment process. As response to flue gasdesulphurization wastewater stress, abundance of monounsaturated fatty acids were increased, andupregulated expression of genes related to salt detoxification were observed in SBR_BY7 and SBR_SR10.Therefore, this study provided a potential low-cost flue gas desulphurization wastewater recyclingtechnology with simultaneously removal of sulfate, refractory organic compounds, heavy metal and salts.

© 2019 Elsevier Ltd. All rights reserved.

1. Introduction

Coal-fired power plant plays important role in electricity pro-duction, although nuclear power plants and renewable energyproduction have remarkable development recently (Cui et al.,2018). Coal-fired power plants emit a large amount of dust and

l Science and Engineering,.

sulfur dioxide (SO2), which cause PM2.5 and acid rain (Wang et al.,2011).

Flue gas desulphurization (FGD) system is commonly usedtechnology to remove dust and SO2 from large coal-fired powerplant, in a wet scrubber with wet limestone, seawater, alkali orammonia as absorbent (C�ordoba, 2015). Wet limestone FGD is mostwidely used in coal-fired power plants in China, since China hasrich limestone resources. In wet limestone FGD process, SO2 reactswith CaCO3 to form CaSO3, which can be further oxidized to CaSO4(gypsum) (Lee et al., 2018). SO2 and dust removal can reach up to

J. Yan et al. / Journal of Cleaner Production 228 (2019) 63e7264

98% in wet limestone FGD system (C�ordoba, 2015). However, astream of concentrated wastewater is produced during precipita-tion or dewatering of gypsum slurry, which is so-called FGDwastewater. The composition of FGD wastewater is very complex,including refractory organic compounds, chloride, fluoride, metals(Ca2þ, Mg2þ, Fe3þ, Zn2þ, Cu2þ, Ni2þ, Cr3þ, Sn2þ, Hg2þ, etc.), sulfateand so on.

Chemical precipitation is commonly used for FGD wastewatertreatment all over the world. Typically, this process includes 1)neutralization, with addition of alkaline chemicals to balance pHvalue, and remove part of metals; 2) heavy metal removal, metaltrapping reagent, such as organic sulfur, is used to remove dissolvedmetals; 3) coagulation and clarification, which is performed toenhance removal of particles and colloids, with addition of floc-culants (PAC, PAM (C�ordoba, 2015) or FeCl3 (Ma et al., 2016). Insome cases, strong oxidizing agents is complemented for oxidationof residual organics, SO2 and NOx (Hutson et al., 2008). A largeamount of chemicals are required in traditional chemical precipi-tation of FGD wastewater, which leads to high operation cost.Nevertheless, recycling of FGDwastewater causes serious corrosionproblem, because of limited removal of chloride, fluoride and sul-fate during chemical precipitation (Ma et al., 2016).

Recently, new treatment technologies of FGD wastewater havebeen developed, such as membrane filtration and evaporation.Forward osmosis, reverse osmosis (Lee et al., 2018) and membranedistillation (Jia andWang, 2017) are applied for desalination of FGDwastewater, but membrane fouling is a crucial problem for con-trolling the system, which raises up maintaining cost of membranefiltration (Tong and Elimelech, 2016). Evaporation technology hasbeen utilized for FGD wastewater recirculation, with advantage offine particles and most of trace element caption. However, theapplication of evaporation is limited due to extremely high oper-ation cost (Shaw, 2008). Therefore, it is urgent to find effective FGDwastewater treatment technology with low operation cost, sincethe requirement of zero liquid discharge from government andpressure of water crisis.

Anaerobic sulfate reduction process converts sulfate to sulfide,by utilization of organic carbon or H2 as electron donor. Meanwhile,the produced sulfide becomes reagent for chemical precipitation ofheavy metals (Zhang et al., 2016). Therefore, simultaneous removalof organic carbon, sulfate and heavy metal can be achieved throughheterotrophic sulfate reduction. Bio-FGD technology uses citric acidas electron donor for sulfate reduction in treatment of flue gas, butinformation about Bio-FGD is very poor since this is patentedtechnology of Paques (Muyzer and Stams, 2008). FGD wastewatercan be used as sulfur sources in co-treatment with freshwatersewage, through a microbial SANI (Sulfate reduction, Autotrophicdenitrification and Nitrification Integrated) process, whichdemonstrated the possibility of FGDwastewater treatment throughbioprocess. Although salt tolerance and metal-resistant sulfate re-ducers are present (Alexandrino et al., 2011), salinity (Vallero et al.,2003) and heavy metal (Zhang et al., 2017) negatively affect the

Table 1FGD wastewater characteristics before and after coagulationa.

pH SS COD DOC

Raw FGD wastewater 7.17± 0.04 0.101± 0.006 725± 20 12.0FGD wastewater after coagulation

and precipitation8.94± 0.05 0.003± 0.001 108± 12 5.2±

Biotreatmentb 3.65± 0.45 e 28± 5 e

- Not detected.a Unit was mg/L, except pH value.b Average value in SBR-BY7 and SBR-SR10 in effluent of each cycle.

growth and activity of most of the sulfate reducers. Fatty acidcomposition (Sakamoto and Murata, 2002) and transcriptomics(Zhao et al., 2012) analyses are sensitive methods, to explore theresponses of microorganism under salt and metal stress.

In this study, an integrated process of chemical precipitation andsulfate reduction (CP-SR) was established, for treatment of coal-fired power plant FGD wastewater. Coagulation and precipitationwere performed as pre-treatment, aiming to remove suspendedsolid in raw FGDwastewater. Then, comparison study on treatmentof pre-treated FGD wastewater were performed in three parallellyoperated sequencing batch reactors (SBRs), by previously culturedsulfate reducing bacteria (SRB) strain BY7, SR10 and SR3, respec-tively. Removal activity and capacity of sulfate, metal, chloride,fluoride, and organic carbon were investigated. Fatty acid compo-sition and transcriptomics of sulfate reducing bacteria werecompared before and after treatment of FGD wastewater. Thus, apotential FGD wastewater recycling technology with low operationcost was provided in this study.

2. Materials and methods

2.1. FGD wastewater and chemical precipitation

Raw FGD wastewater used in this study was collected from a120MW coal-fired power plant located in Zhanjiang city, Guang-dong, P. R. China (110�250E, 21�190N). Part of characteristics of rawFGD wastewater were listed in Table 1. Limestone, PAC and PAM(cation) were received at reagent grade (ACMEC, Shanghai, China),and used for chemical precipitation of raw FGD wastewater. Opti-mization of chemical dosage for each reagent was performedindividually in batch experiment, including limestone, PAC andPAM. Raw FGD wastewater after chemical precipitation (pre-treated FGD wastewater) was used for further biotreatment.

2.2. Setup of SBR reactors

Three parallelly operated 1L anaerobic SBR reactors were usedto investigate sulfate reduction process of pre-treated FGD waste-water. Sulfate reducing bacteria of strain BY7 (Yan et al., 2018b),SR10 (Yan et al., 2018a) and SR3 (this study) were inoculatedindividually to each reactor (1%, v/v), which was operated under30 �C and 100 rpm with synthetic wastewater (Yan et al., 2018a),before introduction of pre-treated FGD wastewater. Sulfatereducing of strain BY7, SR10 and SR3 were also available in GDMCC(Guangdong Microbial Culture Collection Center), with accessionnumber of GDMCC1.1349, GDMCC1.1031 and GDMCC1.1571. Allsulfate in synthetic wastewater was depleted when pre-treatedFGD wastewater was introduced. Lactate was complemented toSBR reactor, as additional organic carbon source with SO4

2�/C of1:1.5. In SBR-BY7 and SBR-SR10, drainage ratio of reactors were 10%(volume of wastewater replaced every time/effective volume ofreactor) during the first 5 cycles, and increased to 20% afterwards.

SO42- Cl� F� TN TP

± 0.8 12530± 750 5390± 120 56± 2 3.48± 0.01 0.0167± 0.00270.3 9370± 210 5110± 85 54± 3 3.45± 0.02 0.0088± 0.0018

168 ± 55 3440± 40 24± 5 e e

J. Yan et al. / Journal of Cleaner Production 228 (2019) 63e72 65

SBR-SR3 was only operated for 20 days with drainage ration of 10%.For each cycle of SBR, influent (10min), gas exchange (20min),reaction, settling (120min) and effluent (10min) were performedin order. Reaction time was 6.9 day during the first 5 cycles, whichwas shorten to 3.9 day afterwards. Nitrogen gas was used tomaintain anaerobic condition during gas exchange. pH in SBR wascontrolled at 7.5 after influent in each cycle, by additional of 1mMNaOH. Liquid samples were taken every day for analyses of pHvalue, OD600 and sulfate. COD was monitored in effluent after eachcycle. Effluent of SBR-BY7 and SBR-SR10 were collected after eachcycle, on day 24, 27 and 30, while effluent of SBR-SR3 on day 2, 6, 11were used, for analyses of metals, chloride, fluoride and organiccomposition. All biomass were collected by centrifugation(� 1000 g, 15min under 4 �C), for fatty acid composition andtranscriptomics analyses at the end of the experiment (day 30 forSBR-BY7 and SBR-SR10, and day 18 for SBR-SR3).

2.3. Analytical methods

Cell density (OD600), sulfate and COD were monitored as pre-viously reported (Yan et al., 2018a). Ion chromatography (DIONEXICS-1100, Thermo Fisher, USA) was used for quantification ofchloride and fluoride (Müller et al., 2012). Concentration of metals,including Al, Ba, Cd, Cr, Mg, Fe, Li, Ni, Pb, Tb, Sn, Zn and Mn, weremeasured by inductively coupled plasma mass spectrometry (ICP-MS) (Sahan et al., 2007). Hg2þ concentration was analyzed byatomic fluorescence spectrometry (AFS, AFS-820, Beijing, P. R.China) (Wang et al., 2018). DOC and TN were tested by TOC-Lanalyzer (Shimadzu, Japan). Suspension solid (SS) and TP weredetected according to standard methods (APHA, 2005). For iden-tification and quantification of refractory organic compounds,liquid sample was extracted with dichloromethane twice, by vortexgenerator for 10min and ultrasonication for 6 h. The concentratedextracts after vaporization was used for GC-MS analysis (Agilent7890B-5977, with HP-5 column), peak area was used for quanti-fying relative abundance of each organic compounds.

2.4. Fatty acid composition

Cellular fatty acids were obtained as previously described(Srivastava et al., 2014). Then, the purified extracts were analyzedby GC (Agilent GC6890), with 1707 column and FID detector (H2was used as carrier gas). Identification of fatty acid was controlledby Sherlock Microbial Identification System (MIDI, USA).

Fig. 1. Removal of multiple metals after coagulation pre-treatment ( ), and bio-treatment byion chromatography.

2.5. cDNA library construction, sequencing and data analysis

Total RNA was extracted by miRNA isolation kit (Ambion, Lifetechnology), then, rRNA was removed by Ribo-Zero Magnetic Kit(Epicentre) according to instructions. The purified mRNA was usedfor first-strand cDNA synthesis, by iScript cDNA synthesis kit(BioRad) with random primers. The second-strand cDNAs weresynthesized with additional of DNA polymerase I, RNase H, dNTPand buffer (Takara). Double-strand cDNAs were used for Illuminasequencing (HiSeq TM 4000) after ligation.

Illumina sequencing and data analysis were performed by GeneDenovo Biotechnology Co. (Guangzhou, China). Raw data obtainedfrom Illumina sequencing were filtered, rRNA removed and map-ped to reference by Bowtie2 (Li et al., 2009). Gene expression wascalculated to RPKM (reads per kilo bases per million reads)(Mortazavi et al., 2008). Then, difference of gene expression of eachgene was calculated, after versus before (control) treatment of FGDwastewater. Differential expression genes (DEGs, changes� 2 fold,and false discovery rate (FDR)< 0.05) were selected. DEGs werethen enrichment analyzed according to GO function and KEGGpathway database (Zhang et al., 2013). Details for raw readsfiltering, assembly and data analysis were described in the sup-plementary information. Clean sequencing data were available onNCBI databases with accession number of PRJNA516985.

3. Results

3.1. Pretreatment of FGD wastewater-chemical precipitation

FGD wastewater was polluted by concentrated sulfate, heavymetals, organic compounds and salts, see Table 1 and Table S1.Withaspect of removal SS from raw FGDwastewater, coagulation processwas optimized, by testing the dosage of each chemicals (PAC, PAMand limestone), as shown in Fig. S1. According to the results, theoptimal dosage of PAC, PAM and limestone were 70mg/L, 3mg/Land 0.7 g/L, respectively. Removal efficiency of SS and COD achieved97% and 85%, respectively (Table 1). Removal of sulfate was about25%, Cl� and F� were hardly removed through chemical precipi-tation, which was in good accordance with previous study (Maet al., 2016). Heavy metal removal efficiency was very poor (25%on average), without additional of heavy metal trapping and strongoxidation reagent, as shown in Fig. 1 pH value of raw FGD waste-water after chemical precipitation was about 9.0, which wasexcellent to balance the acid produced in bio-treatment, thus, FGDwastewater after chemical precipitation (pre-treated FGD

stain BY7 ( ), SR10 ( ) and SR3 ( ) sulfate reducing bacteria monitored by ICP-MS and

J. Yan et al. / Journal of Cleaner Production 228 (2019) 63e7266

wastewater) was used for further bio-treatment in this study.

3.2. Sulfate reduction in SBRs

Three different sulfate reducing bacteria (strain BY7, SR10 andSR3, as shown in Fig. S2) were pre-cultured in each SBRs individ-ually until OD600 reaching about 0.4. Evolutionary history of stainBY7, SR10 and SR3 and others sulfate reducing bacteria was shownin Fig. S2. Strain BY7 (Yan et al., 2018a) and SR10 (Yan et al., 2018b)sulfate reducing bacteria were isolated previously, which were ableto use various carbon and sulfur sources for sulfate reduction. StrainSR3 sulfate reducing bacteria was newly isolated and firstly used inthis study. Doubling time and maximum growth rate of SR3 was21 h and 0.033 h�1, respectively. Sulfate and COD removal duringgrowth of SR3 was shown in Fig. S3.

Sulfate and organic carbon in effluent of each reactor werealmost depleted when pre-treated FGDwastewater was introducedto SBRs. In SBR-BY7 and SBR-SR10, drainage ratio of reactors were10% during the first 5 cycles, and increased to 20% afterwards. SBR-SR3 was only operated for 18 days with drainage ratio of 10%, sincethe activity of sulfate reduction was lost, as shown in Fig. 2. Sulfateconcentration in SBRs was nearly doubled after increasing drainageratio to 20%, because of increasing of sulfate loading. Sulfate loadingrate was 0.14 kg SO4

2�/m3$d during the first 5 cycles, whichincreased to 0.5 kg SO4

2�/m3$d afterwards. Sulfate concentrationdecreased over time, without inhibition by FGD wastewater in SBR-BY7 and SBR-SR10. In SBR-BY7, average sulfate removal efficiencyachieved 75% and 82%, and sulfate removal efficiency reached 85%

Fig. 2. Evolutions of sulfate concentration ( ), pH value ( ) and OD600 ( ) during treatmenreactor was 10% and 20% during blue and green period, respectively. (For interpretation of ththis article.)

and 87% in SBR-SR10, when drainage ratio were 10% and 20%,respectively. Sulfate removal was not inhibited by increasing ofdrainage ratio and sulfate loading. Sulfate reduction activity wastotally vanished in SBR-SR3 after 11 days, probably relate to saltstress of FGD wastewater.

COD removal of about 75% was observed in SBR-BY7 and SBR-SR10. Lactate was complemented to SBR reactor, as additionalorganic carbon source with SO4

2�/C of 1:1.5. Stoichiometry ratio ofsulfate and carbon consumption was 1:2 during heterotrophicsulfate reduction (Muyzer and Stams, 2008). This indicated insuf-ficient carbon source for sulfate reducing bacteria, which enhancedutilization of refractory organic carbon and endogenous respirationin reactors. Remarkable decreasing of cell density were observed inall reactors during the first 11 days, after treatment of FGD waste-water, which might relate to salt adaption and endogenousrespiration.

3.3. Metals and halogens removal

Heavy metal removal efficiency through chemical precipitationwas very limited, particularly, no removal was observed for Ba, Li,Tb and Hg. In SBRs, multiple heavy metals were removed with ef-ficiency higher than 90% (Al, Cd, Mg, Fe, Ni, Pb, Sn, Zn, Hg, Tl), asshown in Fig. 1. Removal of Ba, Cr, Li and Tb efficiency were ob-tained in the range of 50%e80%. Sulfate concentration was linearlycorrelated to decrease of pH value in SBRs (see Fig. 3, R2 of0.92e0.94), which indicated simultaneously sulfate reduction,metal sulfide precipitation and acid production (Kieu et al., 2011).

t of FGD wastewater by SRBs. A, SBR_BY7; B, SBR_ SR10; C, SBR_ SR3. Drainage ratio ofe references to colour in this figure legend, the reader is referred to the Web version of

Fig. 3. Sulfate concentration and pH value of stain BY7 ( ), SR10 ( ), and SR3 ( )sulfate reduction bacteria during treatment of FGD wastewater.

J. Yan et al. / Journal of Cleaner Production 228 (2019) 63e72 67

Nevertheless, production of metal sulfide was not the only metalremoval pathway, since sulfide was not precipitated by Al, Cr, Mgand Li. Removal of Al, Cr, Mg and Li might contributed to co-precipitation or formation of metal hydroxide, which also led topH decreasing (Yan et al., 2018b). Co-precipitation of multiplemetals was found by different researchers, such as Al, Zn, Mg (Leeet al., 2007) and Ni, Co, Li (Theiss et al., 2016).

Cl� and F� was hardly removed through chemical precipitation,with efficiency of 5.6% and 3.6%, respectively. A sustainable removalof Cl� was observed in SBRs, with efficiency of 35%, 37% and 22% inSBR-BY7, SBR-SR10 and SBR-SR3, respectively. Removal efficiency of

Fig. 4. Organic compounds removal efficiency after chemical precipitation ( ), and bio-treaSR3 with 10% drainage ratio ( ) sulfate reducing bacteria. Negative removal efficiency indi

F� was also obtained, with efficiency of 57%, 53% and 14% in SBR-BY7, SBR-SR10 and SBR-SR3, respectively. Cl� and F� was not ableto be utilized or converted by sulfate reducing bacteria, desalina-tion of Cl� and F� were normally conducted by electrochemicalprocess (Elsener and Angst, 2007) ormembrane filtration (Lee et al.,2018). The observed removal of Cl� and F� in SBRs might contrib-uted to biosorption by biomass (Mohan et al., 2007), or co-precipitation with ferric (Fe3þ) in SBRs (Chen et al., 2013).

3.4. Refractory organic compounds removal

There was very little references about organic compoundscomposition in FGD wastewater, while researches focused on thecomposition of volatile organic compounds (VOCs) in flue gas(Peterson et al., 2004). Composition and abundance of organiccompounds in FGD wastewater were analyzed by GC-MS in thisstudy. There were 25 kinds of organic compounds be identified inraw FGD wastewater, including long-chain (>11 carbon atoms) al-kanes, esters, aromatic hydrocarbons and halohydrocarbon, asshown in Fig. 4. Structure of each organic compound was shown inFig. S4. Long-chain alkanes were dominate organic compounds inFGD wastewater, such as docosane, heneicosane, tetracosane,pentacosane and hentriacontane, which might contribute toincomplete incineration of coral. Composition of organic com-pounds in FGD wastewater showed significant difference tocomposition of VOCs in flue gas, which was dominated by volatileshort-chain organic compounds, organic acid, esters and aromatichydrocarbons, with 2e5 carbon atoms (Peterson et al., 2004),which might contribute to relatively complete incineration of coral.

After chemical precipitation, 5 out of 25 kinds of organic com-pounds were completely removed, including 2-azido-2,4,4,6,6-pentamethylheptane (C12H25N3), 2,6,11,15-tetramethylhexadecane(C16H34), 1-iodooctadecane (C18H37I), sulfurous acid, butyl

tment by stain BY7 with 20% drainage ratio ( ), SR10 with 20% drainage ratio ( ) andcated production of organic compound.

Table 2Fatty acid composition of sulfate reducing bacteria stain BY7, SR10 and SR3 before(_b) and after (_a) treatment of flue gas desulfurization wastewater.

Fatty acid composition Relative abundance (%)

BY7_b BY7_a SR10_b SR10_a SR3_b SR3_a

C12:0 0.45 4.28 0.86 1.44 0.35 e

C12:0 3OH e 1.7 e e e e

iso-C14:0 0.77 1.21 0.37 0.17 0.8 1.07C14:0 0.94 2.23 2.51 8.99 0.74 1.71iso-C15:0 4.39 6.05 3.97 1.72 5.34 11.63anteiso-C15:0 17.29 8.16 14.37 4.54 15.83 26.58Sum In Feature 2 e 1.18 1.99 6.2 e e

C16:0 N alcohol e e 0.45 e e e

iso-C16:0 9.03 5.4 4.02 2.22 7.11 5.99anteiso-C16:0 e e e 0.2 e e

Sum In Feature 3 2.67 12.25 1.95 3.47 3.86 1.44C16:0 11.89 19.64 19.09 30.12 9.79 9.92iso-C17:0 3.6 2.62 3.2 1.87 4 4.02anteiso-C17:0 29.51 10.11 23.52 11.93 27.58 26.33C17:1 u7c e 3.11 1.04 4.40 0.43 e

C17:0 cyclo e 3.09 6.11 8.59 e e

C17:0 e 0.36 e 0.56 e e

iso-C18:0 0.76 e e 0.25 0.53 e

Sum In Feature 5 e 1.17 0.91 0.99 e 1.75C18:1 u9c 8.74 13.58 0.43 1.26 16.19 5.41Sum In Feature 8 1.11 0.56 3.03 3.7 1.4 0.89C18:0 6.35 2.15 5.04 3.23 4.78 3.26iso-C19:0 e 0.5 e 0.3 e e

anteiso-C19:0 0.48 e 0.47 0.19 0.51 e

Sum In Feature 7 0.64 e e e 0.76 e

C19:0 cyclo u8c e 0.65 4.96 2.95 e e

J. Yan et al. / Journal of Cleaner Production 228 (2019) 63e7268

heptadecyl ester (C21H44O3S) and hentriacontane (C31H64). Removaldynamics of each organic compounds were shown in Fig. 4,increasing abundance of following organic compounds wereobserved after chemical precipitation, including 2,6,10,14-tetramethylhexadecane (C20H42), 2,6,10,15-tetramethylheptadecane(C21H44), 2,4-di-tert-butylphenol (C14H22O), 2,2,4,4,6,8,8-heptamethylnonane (C16H34), 1-iododotriacontane (C32H65I), 1-iodoeicosane (C20H41I), peneicosane (C21H44), pentacosane(C25H52). This phenomenon was probably related to decompositionof hentriacontane (C31H64) and 1-iodooctadecane (C18H37I).

In effluent of SBR-BY7, SBR-SR10 and SBR-SR3, there were only11, 12, 12 kinds of organic compounds be identified (see Fig. 5),respectively. In general, most of organic compounds with carbonchain shorter than 20 were depleted after treatment in SBR, whileorganic compounds with longer carbon chain (>20) were residuallypresent in the effluent of SBRs. About 70% of organic compounds inpre-treated FGD wastewater were degraded in SBRs (71% for SBR-BY7, 77% for SBR-SR10, 64% for SBR-SR3), which was agreed withCOD results. However, a species-specific preference on refractoryorganic compounds degradation were observed for sulfatereducing bacteria. For instance, carbonic acid, decyl undecyl ester(C22H44O3) and 4,6-dimethyldodecane (C14H30) were residuallypresent in effluent of SBR-SR10, but not in SBR-BY7 and SBR-SR3.Tetracosane (C24H50) and 2,6,10,15-tetramethylheptadecane(C21H44) was depleted only in SBR-BY7. Strain SR10 sulfatereducing bacteria was able to completely degrading 1-iododo-triacontane (C32H65I), which was not observed in others reactors.

C19:0 e e 0.69 0.4 e e

C20:0 1.38 e 1.02 0.31 e e

3.5. Fatty acid composition

To investigate the regulation of themembrane lipids in responseto FGD wastewater, fatty acid composition of sulfate reducingbacteria before and after treatment of FGD wastewater wereexamined, as shown in Table 2 anteiso-C17:0, anteiso-C15:0 and C16:0

Fig. 5. Relative abundance of each organic compound present in raw FGD wastewater, after cwith 20% drainage ratio and SR3 with 10% drainage ratio.

were predominant fatty acids in all sulfate reducing bacteria beforetreatment of FGD wastewater. Abundance of anteiso-C17:0 andanteiso-C15:0 remarkably decreased 65% and 53% in strain BY7, and49% and 68% in strain SR10, respectively, after treatment of FGD

oagulation pre-treatment, and biotreatment by stain BY7 with 20% drainage ratio, SR10

J. Yan et al. / Journal of Cleaner Production 228 (2019) 63e72 69

wastewater. Increasing abundance of C16:0 were observed in bothstrain BY7 and SR10, with 65% and 63%, respectively. The amount ofmonounsaturated fatty acid C17:1 u7c and C18:1 u9c increasedremarkably after treatment of FGD wastewater in strain BY7 andSR10. Increasing abundance of saturated straight-chain and un-saturated fatty acids, and decreasing of iso-branched fatty acidswere observed by Bacillus subtilis after adaption to salinity condi-tion (Lopez et al., 1998). Polyunsaturated was not detected in allsamples, which agreed with previous research on Desulfovibrio sp.sulfate reducing bacteria (Vainshtein et al., 1992). On the contrary,increasing abundance of anteiso-C15:0 was obtained in strain SR3.C17:1 u7c and C18:1 u9c showed notable decline of 100% and 67%,respectively.

3.6. Gene expression after FGD wastewater treatment

By illumine sequencing, about 10 million cleaned reads wereobtained for each reactor samples before and after FGD treatment(with average length 150 bp). Numbers of cleaned reads andunigenes for each sample were listed in Table S2. Gene expressionof sulfate reducing bacteria in each SBRs were compared, DEGs of5231 and 5600 were achieved in SBR_BY7 and SBR_SR10, respec-tively, while significantly less DEGs of 954 were identified inSBR_SR3, see Fig. 6. Among the DEGs, 3124 and 3030 genes up-regulated expressed under FGD wastewater stress, which contrib-uted to 60% and 54% of total DEGs in SBR_BY7 and SBR_SR10.Numbers of genes with no difference expression identified inSBR_SR3 (3427) were notably higher than SBR_BY7 (1985) andSBR_SR10 (2268).

According to GO databased classification, a large number ofDEGs were found in SBR_BY7 and SBR_SR10, which were remark-ably higher than DEGs in SBR_SR3, as shown in Fig. 7. In SBR_BY7and SBR_SR10, up-regulated DEGs related to biological regulation,metabolic process, single-organism process, catalytic activity,binding, membrane and membrane part, outnumbered down-regulated DEGs. Number of down-regulated DEGs related tocellular process were notably higher than up-regulated DEGs,which were 123 and 264 down-regulated DEGS, and 83 and 209up-regulated DEGs in SBR_BY7 and SBR_SR10, respectively. Aconverse trend was obtained in SBR_SR3, down-regulated DEGsoutnumbered up-regulated DEGs in all three categories of

Fig. 6. Number of DEGs in SBR_BY7 (A), SBR_SR10 (B) and SBR_SR3 (C) reactors, afterFGD wastewater treatment. Up-regulated ( ), down-regulated ( ) and no differentialexpression ( ).

biological process, molecular function and cellular component. Thetwo different trends observed in among three SBRs might indicatepromotive effect of bacteria in SBR_BY7 and SBR_SR10 (An et al.,2016), and inhibitory effect in SBR_SR3 (Ghanbari et al., 2017). AllDEGs were matched to 135, 127 and 98 KEGG pathways, as listed inTable S3. Pathway associated with biosynthesis of antibiotics,biosynthesis of secondary metabolites, purine metabolism,biosynthesis of amino acids, carbon metabolism, glycolysis/gluco-neogenesis, ABC transporters, pyruvate metabolism, microbialmetabolism in diverse environments, two-component system andribosome were significantly changed after treatment of FGDwastewater in SBRs.

4. Discussions

4.1. Potential application of integrated process (CP-SR) fortreatment of FGD wastewater

FGD wastewater was a stream of polluted wastewater producedin wet flue gas desulphurization process in coal-fired power plants,which consisted of sulfate, chloride, fluoride, heavy metals andrefractory organic compounds. Recirculation of FGDwastewater ledto serious corrosion because of high dissolved ionic strength (Mg2þ,Cl�, SO4

2� etc). Besides, recirculation of FGD also causes activitydecline of limestone, due to coating of CaF2 on the surface oflimestone (C�ordoba, 2015). Chemical precipitation was commonlyused in coal-fired power plant for treatment of FGD wastewater,with addition of alkaline chemicals (limestone or NaOH), organicsulfur, PAC, PAM and strong oxidizing agents (NaClO or H2O2).Chemical precipitation was used as pre-treatment process in thisstudy, which achieved remove of SS up to 97%, meanwhile, a sus-tainable amount of COD and heavy metal were also removed. Incomparisonwith traditional chemical precipitation applied for FGDwastewater, organic sulfur and strong oxidizing agents were notintroduced in this study, which apparently benefited to loweringoperation cost.

Biological treatment of synthetic FGD wastewater through sul-fate reduction were realized in SrUASB and SANI system, whichachieved high sulfate and COD removal (Jiang et al., 2013; Qianet al., 2015). However, composition of actual FGD wastewater wasmuch more complicated, because of the presence of multiplemetals, chloride, fluoride and refractory organic compounds. Sul-fate reduction process under high salinity condition (50 g/L NaCland 1 g/L MgCl2) had been established in UASB and membranebioreactors, with salt tolerance Desulfobacter halotolerans sulfatereducing bacteria (Vallero et al., 2005). According the results, sul-fate reducing bacteria strain BY7 and SR10 in SBRs were able toadapt to high-salinity FGD wastewater, but strain SR3 could notmaintain sulfate reducing activity under stress of FGD wastewaterafter 12 days. Extremely high removal of sulfate and heavy metalswere achieved in SBR_BY7 and SBR_10, linearly correlated sulfatereduction and acid production was observed in SBRs due to pre-cipitation of metal sulfide. Multiple metals, including Al, Cd, Mg, Fe,Ni, Pb, Sn, Zn, Hg, Tl, Ba, Cr, Li and Tb, could be efficaciouslyremoved through metal sulfide precipitation, metal hydroxideprecipitation and co-precipitation process. Degradation of re-fractory organic compounds was commonly reported in catalytic-and electro-chemical oxidation system, which decomposed re-fractory organic compounds through free-radical reaction, such asozonation (Saroj et al., 2005), Fenton oxidation (Liu et al., 2012) andcatalytic oxidationwith the presence of various catalyzer (Nie et al.,2015). Anaerobic biodegradation was an attractive candidate forrefractory organic compounds removal (Huang et al., 2016), whichmight couple to sulfate reduction (Ying et al., 2013). Chlorophenoldegradation through sulfate reducers was observed previously

Fig. 7. Comparison of expression levels of genes associated with biological process, molecular function and cell component after FGD wastewater treatment in SBR_BY7 (A),SBR_SR10 (B) and SBR_SR3 (C) reactors.

J. Yan et al. / Journal of Cleaner Production 228 (2019) 63e7270

(H€aggblom, 1998). In this study, induced degradation of refractoryorganic compounds could be obtained in SBRs, up to 77% of re-fractory organic compounds removal was achieved in SBR_SR10.Meanwhile, a considerable chloride (~35%) and fluoride (~55%)removal were obtained simultaneously in SBR, although themechanism for chloride and fluoride removal was not thoroughlyclear yet. Removal of sulfate, heavy metal, organic compounds,chloride and fluoride apparently benefited to decreasing corrosionand toxicity to limestone during FGD wastewater recirculation.

Therefore, chemical precipitation followed by sulfate reduction,which performed in SBR reactor with selected sulfate reducers,could be used as an appropriate solution for FGD wastewatertreatment. This integrated process CP-SR could be convenientlyapplied for updating existing FGD wastewater treatment system,since chemical precipitation was widely used in coral-fire plant.Moreover, the CP-SR process developed in this study might befurther integratedwithmembrane filtration technology, such as NF,RO (Jia and Wang, 2017), FO (Park et al., 2017) and MD (Lee et al.,2018), for intensive treatment of FGD wastewater. Thus, mem-brane fouling caused by sulfate, heavy metals and refractoryorganic compounds could be eliminated by CP-SR process, chlorideand fluoride residual present in the effluent of SBR could be desa-linated through membrane filtration. This study was a laboratory

scale investigation, to be able to scaling up for industrial scaleapplication in future, technical problems, such as long-termbiomass maintaining, optimization of operation parameters andhazardous sludge treatment, were all awaiting to be explored.

4.2. Response of sulfate reducing bacteria after treatment of FGDwastewater

FGD wastewater consisted of concentrated sulfate, heavy metal,organic compounds, chloride and fluoride. However, toxicity of FGDwastewater to sulfate reducing bacteria might mainly cause by saltstress, since most of sulfate, heavy metal and organic compoundshad been removed during CP-SR process. During adaptation ofbacteria to high salinity condition, rearrangement of fatty acidcomposition and structure might occur, and expression of relatedgenes might be different. Therefore, in this study, variation of fattyacid composition and gene expression of sulfate reducing bacteriawere compared, with responses to FGD wastewater stress. Sulfatereducing bacteria adaptable to salinity (BY7 and SR 10) andinhibited by salinity condition (SR3) showed adverse trends in fattyacid composition and gene expression. In SBR_BY7 and SBR_SR10,increasing abundance of unsaturated fatty acids of sulfate reducingbacteria were observed after treatment of FGD wastewater, which

J. Yan et al. / Journal of Cleaner Production 228 (2019) 63e72 71

might stimulate the activity of Naþ/Hþ antiport system (Hahneet al., 2010). Up-regulated gene expression of fatty acid desatur-ase and Naþ/Hþ antiporter were achieved in SBR_BY7 andSBR_SR10. Thus, the results demonstrated, to adapt to FGD waste-water condition, sulfate reducing bacteria increased fluidity ofmembrane by desaturating part of saturated fatty acids to unsat-urated fatty acids, then sulfate reducing bacteria enhanced theefflux of Naþ which led to lower intracellular Naþ (Srivastava et al.,2014). However, if sulfate reducing bacteria could not adapt to highsalinity condition, under the inhibitory salt condition (in SBR_SR3),a contrary effect of salinity on fatty acid desaturase took place(Srivastava et al., 2014), which led to decline of unsaturated fattyacids and down-regulated expression of desaturase.

After treatment of FGD wastewater, up-regulated expression ofsulfate (ABC) transporter genes and (di)sulfite reductase genes,were consistence with the observed high sulfate reducing activityin SBR_BY7 and SBR_SR10, which was not observed in SBR_SR3. Alarge number of genes related to carbohydrate and energy meta-bolism were differentially expressed after treatment of FGDwastewater. For instance, genes of formate dehydrogenase andsuccinate dehydrogenase were decreased expression, which mightindicate carbon source limitation during treatment of FGD waste-water (Park et al., 2010). Up-regulated expression of NADP(H)related genes might enhance refractory organic compound degra-dation during treatment of FGD wastewater.

5. Conclusion

In this study, an integrated process of chemical precipitation andsulfate reduction (CP-SR) was established, for treatment of coal-fired power plant FGD wastewater. Chemical precipitation wasperformed as pre-treatment for removal of suspended solid (97%)in raw FGD wastewater. Strain BY7 and SR10 sulfate reducingbacteria were able to adapted to high-salinity FGD wastewater inSBRs, with extremely high efficiencies of sulfate reduction, metalsand refractory organic compounds removal. A sustainable removalof chloride and fluoride was achieved, which probably relate to co-precipitation or biosorption processes. Up to 14 out of 25 refractoryorganic compounds in FGD wastewater could be completelyremoved after integrated treatment process. To adapt to highsalinity FGD wastewater, increasing abundance of mono-unsaturated fatty acids, and upregulated gene expression related tosalt detoxification sulfate reducing bacteria were observed. There-fore, this study provided a potential low-cost FGD wastewaterrecycling technology with simultaneously removal of sulfate, re-fractory organic compounds, heavy metal and salts.

Declarations of interest

None.

Acknowledgements

The authors would like to thank the members of the Analysisand test center of Guangzhou University for their invaluable anddedicated assistance. The work was supported by National NaturalScience Foundation of China (51708142, 51208122, and 51778156),Science and Technology Program of Guangzhou (201707010256),and Pearl River S and T Nova Program of Guangzhou(201806010191).

Appendix A. Supplementary data

Supplementary data to this article can be found online athttps://doi.org/10.1016/j.jclepro.2019.04.227.

Compliance with ethical standards

Conflict of interest The authors declare that they have no conflictof interest. Human and animal rights and informed consent. Thisarticle does not contain any studies with human participants oranimals performed by any of the authors.

References

Alexandrino, F., Macías, R., Costa, N.C., Gomes, A.V., Can�ario, M.C., Costa, A., 2011.Bacterial consortium isolated from an Icelandic fumarole displays exceptionallyhigh levels of sulfate reduction and metals resistance. J. Hazard Mater. 187,362e370.

An, S., Gong, Q., Huang, Y., 2016. Promotive effect of zinc ions on the vitality,migration, and osteogenic differentiation of human dental pulp cells. Biol. TraceElem. Res. 175 (1), 1e10.

APHA, 2005. Standard Methods for the Examination of Water and Wastewater,21thed. American Public Health Association, American Water Works Associa-tion, Water Environment Federation, Washington, DC.

Chen, F., Xie, S., Zhang, J., Liu, R., 2013. Synthesis of spherical Fe3O4 magneticnanoparticles by co-precipitation in choline chloride/urea deep eutectic sol-vent. Mater. Lett. 112, 177e179.

C�ordoba, P., 2015. Status of Flue Gas Desulphurisation (FGD) systems from coal-firedpower plants: overview of the physic-chemical control processes of wet lime-stone FGDs. Fuel 144, 274e286.

Cui, L., Li, Y., Tang, Y.Z., Shi, Y.F., Wang, Q.S., Yuan, X.L., Kellett, J., 2018. Integratedassessment of the environmental and economic effects of an ultra-clean fluegas treatment process in coal-fired power plant. J. Clean. Prod. 199, 359e368.

Elsener, B., Angst, U., 2007. Mechanism of electrochemical chloride removal. Corros.Sci. 49 (12), 0e4522.

Ghanbari, R., Molaee Aghaee, E., Rezaie, S., Jahed Khaniki, G., Alimohammadi, M.,Soleimani, M., Noorbakhsh, F., 2017. The inhibitory effect of lactic acid bacteriaon aflatoxin production and expression of aflR gene in\r, Aspergillus parasiticus.J. Food Saf., e12413

H€aggblom, M.M., 1998. Reductive dechlorination of halogenated phenols by a sul-fate-reducing consortium. FEMS Microbiol. Ecol. 26 (1), 35e41.

Hahne, H., M€ader, U., Otto, A., Bonn, F., Steil, L., Bremer, E., Hecker, M., Becher, D.,2010. A comprehensive proteomics and transcriptomics analysis of bacillussubtilis salt stress adaptation. J. Bacteriol. 192 (3), 870e882.

Huang, Y., Hou, X., Liu, S., Ni, J., 2016. Correspondence analysis of bio-refractorycompounds degradation and microbiological community distribution inanaerobic filter for coking wastewater treatment. Chem. Eng. J. 304, 864e872.

Hutson, N.D., Krzyzynska, R., Srivastava, R.K., 2008. Simultaneous removal of SO2,NOx, and Hg from coal flue gas using a NaClO2-enhanced wet scrubber. Ind. Eng.Chem. Res. 47 (16).

Jia, F., Wang, J., 2017. Treatment of flue gas desulfurization wastewater with near-zero liquid discharge by nanofiltration-membrane distillation process. Separ.Sci. Technol. 1e8.

Jiang, F., Zhang, L., Peng, G.L., Liang, S.Y., Qian, J., Chen, G.H., 2013. A novel approachto realize sani process in freshwater sewage treatment e use of wet flue gasdesulfurization waste streams as sulfur source. Water Research 47 (15),5773e5782.

Kieu, H.T.Q., Müller, E., Horn, H., 2011. Heavy metal removal in anaerobic semi-continuous stirred tank reactors by a consortium of sulfate-reducing bacteria.Water Res. 45 (13), 3863e3870.

Lee, K.S., Myung, S.T., Bang, H.J., Chung, S., Sun, Y.K., 2007. Co-precipitation synthesisof spherical Li1.05M0.05Mn1.9O4 (m ¼ Ni, Mg, Al) spinel and its application forlithium secondary battery cathode. Electrochim. Acta 52 (16), 5201e5206.

Lee, S., Kim, Y., Hong, S., 2018. Treatment of industrial wastewater produced bydesulfurization process in a coal-fired power plant via FO-MD hybrid process.Chemosphere 210, 44e51.

Li, R., Yu, C., Li, Y., Lam, T.W., Yiu, S.M., Kristiansen, K., Wang, J., 2009. SOAP2: animproved ultrafast tool for short read alignment. Bioinformatics 25 (15),1966e1967.

Liu, Y., Li, J., Zhou, B., Lv, S., Li, X., Chen, H., Chen, Q., Cai, W., 2012. Photo-electrocatalytic degradation of refractory organic compounds enhanced by aphotocatalytic fuel cell. Appl. Catal. B Environ. 111e112, 485e491.

Ma, S., Jin, C., Chen, G., Yu, W., Zhu, S., 2016. Research on desulfurization wastewaterevaporation: present and future perspectives. Renew. Sustain. Energy Rev. 58,1143e1151.

Mohan, S.V., Ramanaiah, S.V., Rajkumar, B., Sarma, P.N., 2007. Removal of fluoridefrom aqueous phase by biosorption onto algal biosorbent spirogyra sp.-TiO2:sorption mechanism elucidation. J. Hazard Mater. 141 (3), 465e474.

Mortazavi, A., Williams, B.A., Mccue, K., Schaeffer, L., Wold, B., 2008. Mapping andquantifying mammalian transcriptomes by RNA-seq. Nat. Methods 5 (7),621e628.

Müller, A.L.H., Müller, C.C., Antes, F.G., Barin, J.S., Dressler, V.L., Flores, E.M.M.,Müller, A.E.I., 2012. Determination of bromide, chloride, and fluoride in ciga-rette tobacco by ion chromatography after microwave-induced combustion.Anal. Lett. 45 (9), 1004e1015.

Muyzer, G., Stams, A., 2008. The ecology and biotechnology of sulphate-reducingbacteria. Nat. Rev. Microbiol. 6, 441e454.

J. Yan et al. / Journal of Cleaner Production 228 (2019) 63e7272

Nie, Y., Zhang, L., Li, Y.Y., Hu, C., 2015. Enhanced Fenton-like degradation of re-fractory organic compounds by surface complex formation of LaFeO3 and H2O2.J. Hazard Mater. 294, 195e200.

Park, S.J., Tseng, C.P., Gunsalus, R.P., 2010. Regulation of succinate dehydrogenase(sdhCDAB) operon expression in Escherichia coli in response to carbon supplyand anaerobiosis: role of ArcA and Fnr. Mol. Microbiol. 15 (3), 473e482.

Park, J., Joo, H., Noh, M., Namkoong, Y., Lee, S., Jung, K.H., Ahn, H.R., Kim, S., Lee, J.C.,Yoon, J., Lee, Y., 2017. Systematic structure control of ammonium iodide salts asfeasible UCST-type forward osmosis draw solutes for the treatment of highlyconcentrated wastewater. J. Mater. Chem. A. 10.1039.C7TA09741G.

Peterson, B.V., Hummerick, M., Roberts, M.S., Krumins, V., Kish, A.L., Garland, J.L.,Maxwell, S., Mills, A., 2004. Characterization of microbial and chemicalcomposition of shuttle wet waste with permanent gas and volatile organiccompound analyses. Adv. Space Res. 34 (7), 1470e1476.

Qian, J., Liu, R., Wei, L., Lu, H., Chen, G.H., 2015. System evaluation and microbialanalysis of a sulfur cycle-based wastewater treatment process for co-treatmentof simple wet flue gas desulfurization wastes with freshwater sewage. WaterResearch 80, 189e199.

Sahan, Y., Basoglu, F., Seref, Gücer, 2007. ICP-MS analysis of a series of metals(namely: Mg, Cr, Co, Ni, Fe, Cu, Zn, Sn, Cd and Pb) in black and green olivesamples from bursa, Turkey. Food Chem. 105 (1), 395e399.

Sakamoto, T., Murata, N., 2002. Regulation of the desaturation of fatty acids and itsrole in tolerance to cold and salt stress. Curr. Opin. Microbiol. 5 (2), 206e210.

Saroj, D.P., Kumar, A., Bose, P., Tare, V., Dhopavkar, Y., 2005. Mineralization of somenatural refractory organic compounds by biodegradation and ozonation. WaterRes. 39 (9), 1921e1933.

Shaw, W.A., 2008. Benefits of evaporating FGD purge water. J. Power 152 (3), 59e66.Srivastava, A., Singh, S.S., Mishra, A.K., 2014. Modulation in fatty acid composition

influences salinity stress tolerance in Frankia strains. Ann. Microbiol. 64 (3),1315e1323.

Theiss, F.L., Ayoko, G.A., Frost, R.L., 2016. Synthesis of layered double hydroxidescontaining Mg2þ, Zn2þ, Ca2þ and Al3þ layer cations by co-precipitation meth-odsda review. Appl. Surf. Sci. 383 (33), 200e213.

Tong, T., Elimelech, M., 2016. The global rise of zero liquid discharge for wastewatermanagement: drivers, technologies, and future directions. Environ. Sci. Technol.50 (13), 6846e6855.

Vallero, M.V.G., Pol, L.W.H., Lettinga, G., Lens, P.N.L., 2003. Effect of NaCl on ther-mophilic (55�C) methanol degradation in sulfate reducing granular sludge

reactors. Water Res. 37 (10), 2269e2280.Vallero, M.V.G., Lettinga, G., Lens, P.N.L., 2005. High rate sulfate reduction in a

submerged anaerobic membrane bioreactor (SAMBR) at high salinity. J. Membr.Sci. 253 (1e2), 217e232.

Vainshtein, M., Hippe, H., Kroppenstedt, R.M., 1992. Cellular fatty acid compositionof Desulfovibrio species and its use in classification of sulfate-reducing bacteria.Syst. Appl. Microbiol. 15 (4), 554e566.

Wang, S., Xing, J., Jang, C., Zhu, Y., Fu, J.S., Hao, J., 2011. Impact assessment ofammonia emissions on inorganic aerosols in east China using response surfacemodeling technique. Environ. Sci. Technol. 45 (21), 9293e9300.

Wang, J.T., Zhang, L., Kang, Y., Chen, G., Jiang, F., 2018. Long-term feeding ofelemental sulfur alters microbial community structure and eliminates mercurymethylation potential in sulfate-reducing bacteria abundant activated sludge.Environ. Sci. Technol. 52 (8) acs.est.7b06399.

Yan, J., Zhong, K.Q., Wang, S.J., Chen, Z.X., Hu, H.S., Jian, Z.Y., Wen, H.J., Zhang, H.G.,2018a. Carbon metabolism and sulfate respiration by a non-conventional Cit-robacter freundii strain SR10 with potential application in removal of metals andmetalloids. Int. Biodeterior. Biodegrad. 133, 238e246.

Yan, J., Ye, W.Z., Jian, Z.Y., Xie, J.H., Zhong, K.Q., Wang, S.J., Hu, H.S., Chen, Z.X.,Wen, H.J., Zhang, H.G., 2018b. Enhanced sulfate and metal removal by reducedgraphene oxide self-assembled, Enterococcus avium, sulfate-reducing bacteriaparticles. Bioresour. Technol. 266, 447e453.

Ying, H., Xiang, X., Wang, F.P., 2013. Metagenome reveals potential microbialdegradation of hydrocarbon coupled with sulfate reduction in an oil-immersedchimney from Guaymas basin. Front. Microbiol. 4.

Zhang, H.G., Li, M., Yang, Z., Sun, Y., Yan, J., Chen, D.Y., Chen, Y.H., 2017. Isolation of anon-traditional sulfate reducing-bacteria Citrobacter freundii sp. and bioremovalof thallium and sulfate. Ecol. Eng. 102, 397e403.

Zhang, J., Wu, K., Zeng, S., Silva, J.A.T.D., Zhao, X., Tian, C.E., Xia, H.Q., Duan, J., 2013.Transcriptome analysis of Cymbidium sinense and its application to the identi-fication of genes associated with floral development. BMC Genomics 14 (1),279-279.

Zhang, L., Lin, X., Wang, J., Jiang, F., Wei, L., Chen, G., Hao, X., 2016. Effects of lead andmercury on sulfate-reducing bacterial activity in a biological process for flue gasdesulfurization wastewater treatment. Sci. Rep.-UK 6, 30455.

Zhao, X., Yu, H., Kong, L., Li, Q., 2012. Transcriptomic responses to salinity stress inthe pacific oyster Crassostrea gigas. PLoS One 7 (9), e46244.