Please wait a minute...
Frontiers of Environmental Science & Engineering

ISSN 2095-2201

ISSN 2095-221X(Online)

CN 10-1013/X

Postal Subscription Code 80-973

2018 Impact Factor: 3.883

Front. Environ. Sci. Eng.    2022, Vol. 16 Issue (6) : 71    https://doi.org/10.1007/s11783-021-1505-4
RESEARCH ARTICLE
Enhanced methane production during long-term UASB operation at high organic loads as enabled by the immobilized Fungi
Qiong Guo1, Zhichao Yang1, Bingliang Zhang1, Ming Hua1,2, Changhong Liu3, Bingcai Pan1,2()
1. State Key Laboratory of Pollution Control and Resource Reuse, School of Environment, Nanjing University, Nanjing 210023, China
2. Research Center for Environmental Nanotechnology (ReCENT), Nanjing University, Nanjing 210023, China
3. School of Life Sciences, Nanjing University, State Key Laboratory of Pharmaceutical Biotechnology, Nanjing 210023, China
 Download: PDF(2359 KB)   HTML
 Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks
Abstract

• Fungi enable the constant UASB operation even at OLR of 25.0 kg/(m3×d).

• The COD removal of 85.9% and methane production of 5.6 m3/(m3×d) are achieved.

• Fungi inhibit VFAs accumulation and favor EPS generation and sludge granulation.

• Fungi enrich methanogenic archaea and promote methanogenic pathways.

Anaerobic digestion is widely applied in organic wastewater treatment coupled with bioenergy production, and how to stabilize its work at the high organic loading rate (OLR) remains a challenge. Herein, we proposed a new strategy to address this issue via involving the synergetic role of the Aspergillus sydowii 8L-9-F02 immobilized beads (AEBs). A long-term (210-day) continuous-mode operation indicated that the upflow anaerobic sludge bed (UASB) reactor (R1, with AEBs added) could achieve the OLR as high as 25.0 kg/(m3×d), whereas the control reactor (R0, with AEBs free) could only tolerate the maximum OLR of 13.3 kg/(m3×d). Remarkably, much higher COD removal (85.9% vs 23.9%) and methane production (5.4 m3/(m3×d) vs 2.2 m3/(m3×d)) were achieved in R1 than R0 at the OLR of 25.0 kg/(m3×d). Such favorable effect results from the facts that fungi inhibit VFAs accumulation, favor the pH stabilization, promote the generation of more extracellular polymeric substance, and enhance the sludge granulation and settleability. Moreover, fungi may enhance the secretion of acetyl-coenzyme A, a key compound in converting organic matters to CO2. In addition, fungi are favorable to enrich methanogenic archaea even at high OLR, improving the activity of acetate kinase and coenzyme F420 for more efficient methanogenic pathway. This work may shed new light on how to achieve higher OLR and methane production in anaerobic digestion of wastewater.

Keywords Anaerobic digestion      Fungi      Methane production      High OLR      Microbial community     
Corresponding Author(s): Bingcai Pan   
Issue Date: 23 September 2021
 Cite this article:   
Qiong Guo,Zhichao Yang,Bingliang Zhang, et al. Enhanced methane production during long-term UASB operation at high organic loads as enabled by the immobilized Fungi[J]. Front. Environ. Sci. Eng., 2022, 16(6): 71.
 URL:  
https://academic.hep.com.cn/fese/EN/10.1007/s11783-021-1505-4
https://academic.hep.com.cn/fese/EN/Y2022/V16/I6/71
Fig.1  Long-term operation of R0 (control) and R1 (with AEBs addition) in terms of (A) COD removal efficiency, (B) CH4 generation, (C) the produced gas composition (CO2 and CH4 percentage), and (D) effluent VFAs concentration under otherwise identical condition.
Fig.2  (A) Morphology and (B) SEM image of AEBs sampled from R1 on Day 100, and the SEM images of the anaerobic sludge samples from R0 (C, Day 160; E, Day 200) and R1 (D, Day 160; F, Day 200).
Fig.3  (A) Particle size diffusion of granular sludge and (B) its settleability under different OLRs. Samples were collected from R0 and R1 on Day 20, 50, 100, 160 and 200, both featuring different OLRs. (A) Whiskers that protrude out of the box indicate 1.5 × IQR (interquartile range). The boundary of the box indicates the range of 25% and 75%. The line in the middle of the box marks the median and the hollow circle marks the mean. Sample points that fall outside 1.5 × IQR are possible outliers. 50<n<65, ***, p<0.001. (B) 50<n<70.
Fig.4  Variations in the (A) protein and (B) polysaccharides contents in EPS throughout the long-term UASB operation along with the increasing OLR.
Fig.5  FT-IR spectra of sludge mixtures in (A) R0 (control) and (B) R1 (AEBs added) at different OLRs. Significant differences are labeled by shading in the spectra.
Fig.6  Activities of (A) cellulase, (B) acetate kinase, and (C) coenzyme F420 in R0 (control) and R1 (AEBs added) in different operation periods. (Error bars represent standard deviations of triplicate tests).
Fig.7  The distribution of bacteria and archaea abundances at genus level in the seeded sludge, R0 (control) and R1 (AEBs added) at different OLRs. (The dotted line marks the boundary between bacteria and archaea).
1 M Akbar, M F S Khan, L Qian, H Wang (2020). Degradation of polyacrylamide (PAM) and methane production by mesophilic and thermophilic anaerobic digestion: Effect of temperature and concentration. Frontiers of Environmental Science & Engineering, 14(6): 98
https://doi.org/10.1007/s11783-020-1277-2
2 M K H Al-Mashhadani, S J Wilkinson, W B Zimmerman (2016). Carbon dioxide rich microbubble acceleration of biogas production in anaerobic digestion. Chemical Engineering Science, 156: 24–35
https://doi.org/10.1016/j.ces.2016.09.011
3 K Alef, P Nannipieri (1995). Methods in Applied Soil Microbiology and Biochemistry. Alef K and Nannipieri P,eds. London: Academic Press, 311–373
4 J J Ambuchi, Z Zhang, L Shan, D Liang, P Zhang, Y Feng (2017). Response of anaerobic granular sludge to iron oxide nanoparticles and multi-wall carbon nanotubes during beet sugar industrial wastewater treatment. Water Research, 117: 87–94
https://doi.org/10.1016/j.watres.2017.03.050 pmid: 28390238
5 APHA (2005). Standard methods for the examination of water and wastewater. Washington, DC, USA: American Public Health Association (APHA), American Water Works Association(AWWA), Water Environment Federation (AEF)
6 H A Assress, R Selvarajan, H Nyoni, K Ntushelo, B B Mamba, T A M Msagati (2019). Diversity, co-occurrence and implications of fungal communities in wastewater treatment plants. Scientific Reports, 9(1): 14056
https://doi.org/10.1038/s41598-019-50624-z pmid: 31575971
7 Y Bajón Fernández, A Soares, P Vale, K Koch, A L Masse, E Cartmell (2019). Enhancing the anaerobic digestion process through carbon dioxide enrichment: initial insights into mechanisms of utilization. Environmental Technology, 40(13): 1744–1755
https://doi.org/10.1080/09593330.2019.1597173 pmid: 30888257
8 Y Bajón Fernández, A Soares, R Villa, P Vale, E Cartmell (2014). Carbon capture and biogas enhancement by carbon dioxide enrichment of anaerobic digesters treating sewage sludge or food waste. Bioresource Technology, 159: 1–7
https://doi.org/10.1016/j.biortech.2014.02.010 pmid: 24632434
9 P Ceron-Chafla, R Kleerebezem, K Rabaey, J B van Lier, R E F Lindeboom (2020). Direct and indirect effects of increased CO2 partial pressure on the bioenergetics of syntrophic propionate and butyrate conversion. Environmental Science & Technology, 54(19): 12583–12592
https://doi.org/10.1021/acs.est.0c02022 pmid: 32845128
10 H Chen, Z Wang, H Liu, Y Nie, Y Zhu, Q Jia, G Ding, J Ye (2021). Variable sediment methane production in response to different source-associated sewer sediment types and hydrological patterns: Role of the sediment microbiome. Water Research, 190: 116670
https://doi.org/10.1016/j.watres.2020.116670 pmid: 33296733
11 R Chen, Y Nie, N Tanaka, Q Niu, Q Li, Y Y Li (2017). Enhanced methanogenic degradation of cellulose-containing sewage via fungi-methanogens syntrophic association in an anaerobic membrane bioreactor. Bioresource Technology, 245(Pt A): 810–818
https://doi.org/10.1016/j.biortech.2017.09.046 pmid: 28926913
12 W Chen, N Habibul, X Y Liu, G P Sheng, H Q Yu (2015). FTIR and synchronous fluorescence heterospectral two-dimensional correlation analyses on the binding characteristics of copper onto dissolved organic matter. Environmental Science & Technology, 49(4): 2052–2058
https://doi.org/10.1021/es5049495 pmid: 25611159
13 X Dai, F Luo, D Zhang, L Dai, Y Chen, B Dong (2015). Waste-activated sludge fermentation for polyacrylamide biodegradation improved by anaerobic hydrolysis and key microorganisms involved in biological polyacrylamide removal. Scientific Reports, 5(1): 11675
https://doi.org/10.1038/srep11675 pmid: 26144551
14 L D Eirich, G D Vogels, R S Wolfe (1978). Proposed structure for coenzyme F420 from Methanobacterium. Biochemistry, 17(22): 4583–4593
https://doi.org/10.1021/bi00615a002 pmid: 728375
15 S Fukuzaki, N Nishio, S Nagai (1990). Kinetics of the methanogenic fermentation of acetate. Applied and Environmental Microbiology, 56(10): 3158–3163
https://doi.org/10.1128/aem.56.10.3158-3163.1990 pmid: 16348323
16 B Guo, Y Zhang, N Yu, Y Liu (2021a). Impacts of conductive materials on microbial community during syntrophic propionate oxidization for biomethane recovery. Water Environment Research, 93(1): 84–93
https://doi.org/10.1002/wer.1357 pmid: 32391609
17 H Guo, Y Zhang, Z Huang, W Liang, M Urynowicz, M I Ali (2020). High potential of methane production from coal by fungi and hydrogenotrophic methanogens from produced water. Energy & Fuels, 34(9): 10958–10967
https://doi.org/10.1021/acs.energyfuels.0c02265
18 Q Guo, Y Wang, J Qian, B Zhang, M Hua, C Liu, B Pan (2021b). Enhanced production of methane in anaerobic water treatment as mediated by the immobilized fungi. Water Research, 190: 116761
https://doi.org/10.1016/j.watres.2020.116761 pmid: 33360615
19 M Imran, Z Anwar, M Irshad, M J Asad, H Ashfaq (2016). Cellulase production from species of fungi and bacteria from agricultural wastes and its utilization in industry: A review. Advances in Enzyme Research, 4(2): 44–55
https://doi.org/10.4236/aer.2016.42005
20 T Katayama, Y Kamagata (2017). Hydrocarbon and Lipid Microbiology Protocols: Isolation and Cultivation. McGenity T J, Timmis K N, Nogales B, eds. Berlin: Springer Berlin Heidelberg, 177–195
21 J Kim, C Lee (2015). Response of a continuous biomethanation process to transient organic shock loads under controlled and uncontrolled pH conditions. Water Research, 73: 68–77
https://doi.org/10.1016/j.watres.2015.01.015 pmid: 25644629
22 X Kong, Y Wei, S Xu, J Liu, H Li, Y Liu, S Yu (2016). Inhibiting excessive acidification using zero-valent iron in anaerobic digestion of food waste at high organic load rates. Bioresource Technology, 211: 65–71
https://doi.org/10.1016/j.biortech.2016.03.078 pmid: 26998799
23 K Lee, S Lee, S H Lee, S R Kim, H S Oh, P K Park, K H Choo, Y W Kim, J K Lee, C H Lee (2016). Fungal quorum quenching: A paradigm shift for energy savings in membrane bioreactor (MBR) for wastewater treatment. Environmental Science & Technology, 50(20): 10914–10922
https://doi.org/10.1021/acs.est.6b00313 pmid: 27634354
24 Q Li, Y Liu, X Yang, J Zhang, B Lu, R Chen (2020). Kinetic and thermodynamic effects of temperature on methanogenic degradation of acetate, propionate, butyrate and valerate. Chemical Engineering Journal, 396: 125366
https://doi.org/10.1016/j.cej.2020.125366
25 R Li, M Zhou, S He, T Pan, J Liu, J Zhu (2021a). Deciphering the effect of sodium dodecylbenzene sulfonate on up-flow anaerobic sludge blanket treatment of synthetic sulfate-containing wastewater. Frontiers of Environmental Science & Engineering, 15(5): 91
https://doi.org/10.1007/s11783-020-1385-z
26 Y Li, Z Meng, Y Xu, Q Shi, Y Ma, M Aung, Y Cheng, W Zhu (2021b). Interactions between anaerobic fungi and methanogens in the rumen and their biotechnological potential in biogas production from lignocellulosic materials. Microorganisms, 9(1): 190
https://doi.org/10.3390/microorganisms9010190 pmid: 33477342
27 Y Q Liu, Y Liu, J H Tay (2004). The effects of extracellular polymeric substances on the formation and stability of biogranules. Applied Microbiology and Biotechnology, 65(2): 143–148
https://doi.org/10.1007/s00253-004-1657-8 pmid: 15197510
28 C Ma, R C Jin, G F Yang, J J Yu, B S Xing, Q Q Zhang (2012). Impacts of transient salinity shock loads on Anammox process performance. Bioresource Technology, 112: 124–130
https://doi.org/10.1016/j.biortech.2012.02.122 pmid: 22440577
29 D Mayumi, J Dolfing, S Sakata, H Maeda, Y Miyagawa, M Ikarashi, H Tamaki, M Takeuchi, C H Nakatsu, Y Kamagata (2013). Carbon dioxide concentration dictates alternative methanogenic pathways in oil reservoirs. Nature Communications, 4(1): 1998
https://doi.org/10.1038/ncomms2998 pmid: 23759740
30 N H Mohd Yasin, T Maeda, A Hu, C P Yu, T K Wood (2015). CO2 sequestration by methanogens in activated sludge for methane production. Applied Energy, 142: 426–434
https://doi.org/10.1016/j.apenergy.2014.12.069
31 Y S Mostafa, S A Alamri, M Hashem, N A Nafady, K A M Abo-Elyousr, Z A Mohamed (2020). Thermostable cellulase biosynthesis from Paenibacillus alvei and its utilization in lactic acid production by simultaneous saccharification and fermentation. Open Life Sciences, 15(1): 185–197
https://doi.org/10.1515/biol-2020-0019 pmid: 33987475
32 D Nguyen, Z Wu, S Shrestha, P H Lee, L Raskin, S K Khanal (2019). Intermittent micro-aeration: New strategy to control volatile fatty acid accumulation in high organic loading anaerobic digestion. Water Research, 166: 115080
https://doi.org/10.1016/j.watres.2019.115080 pmid: 31541792
33 J L A Pennings, J T Keltjens, G D Vogels (1998). Isolation and characterization of Methanobacteriumthermoautotrophicum ΔH mutants unable to grow under hydrogen-deprived conditions. Journal of Bacteriology, 180(10): 2676–2681
https://doi.org/10.1128/JB.180.10.2676-2681.1998 pmid: 9573152
34 A Rothstein (1971). Current Topics in Membranes and Transport. Bronner F, Kleinzeller A, eds. Washington, DC: Academic Press, 135–176
35 M Sobieraj, D R Boone (2006). The Prokaryotes: Volume 4: Bacteria: Firmicutes, Cyanobacteria. Dworkin M, Falkow S, Rosenberg E, Schleifer K H, Stackebrandt E, eds. New York, NY: Springer US, 1041–1049
36 C Sundberg, W A Al-Soud, M Larsson, E Alm, S S Yekta, B H Svensson, S J Sørensen, A Karlsson (2013). 454 pyrosequencing analyses of bacterial and archaeal richness in 21 full-scale biogas digesters. FEMS Microbiology Ecology, 85(3): 612–626
https://doi.org/10.1111/1574-6941.12148 pmid: 23678985
37 K C Surendra, C Sawatdeenarunat, S Shrestha, S Sung, S K Khanal (2015). Anaerobic digestion-based biorefinery for bioenergy and biobased products. Industrial Biotechnology (New Rochelle, N.Y.), 11(2): 103–112
https://doi.org/10.1089/ind.2015.0001
38 U Tezel, L P Padhye, C H Huang, S G Pavlostathis (2011). Biotransformation of nitrosamines and precursor secondary amines under methanogenic conditions. Environmental Science & Technology, 45(19): 8290–8297
https://doi.org/10.1021/es2005557 pmid: 21863807
39 Z Tian, Y Zhang, Y Li, Y Chi, M Yang (2015). Rapid establishment of thermophilic anaerobic microbial community during the one-step startup of thermophilic anaerobic digestion from a mesophilic digester. Water Research, 69: 9–19
https://doi.org/10.1016/j.watres.2014.11.001 pmid: 25463927
40 K Torres, F J Álvarez-Hornos, P San-Valero, C Gabaldón, P Marzal (2018). Granulation and microbial community dynamics in the chitosan-supplemented anaerobic treatment of wastewater polluted with organic solvents. Water Research, 130: 376–387
https://doi.org/10.1016/j.watres.2017.12.009 pmid: 29258049
41 T H Tsui, G A Ekama, G H Chen (2018). Quantitative characterization and analysis of granule transformations: Role of intermittent gas sparging in a super high-rate anaerobic system. Water Research, 139: 177–186
https://doi.org/10.1016/j.watres.2018.04.002 pmid: 29649702
42 Y Ueno, S Haruta, M Ishii, Y Igarashi (2001). Changes in product formation and bacterial community by dilution rate on carbohydrate fermentation by methanogenic microflora in continuous flow stirred tank reactor. Applied Microbiology and Biotechnology, 57(1-2): 65–73
https://doi.org/10.1007/s002530100760 pmid: 11693936
43 J B Van Lier, N Mahmoud, G Zeeman (2008). Anaerobic Wastewater Treatment. Henze M, van Loosdrecht M C M, Ekama G A, Brdjanovic D, eds. London: IWA Publishing
44 A Vigneron, E B Alsop, B P Lomans, N C Kyrpides, I M Head, N Tsesmetzis (2017). Succession in the petroleum reservoir microbiome through an oil field production lifecycle. The ISME Journal, 11(9): 2141–2154
https://doi.org/10.1038/ismej.2017.78 pmid: 28524866
45 J Wu, Z U R Afridi, Z P Cao, Z L Zhang, S Poncin, H Z Li, J E Zuo, K J Wang (2016). Size effect of anaerobic granular sludge on biogas production: A micro scale study. Bioresource Technology, 202: 165–171
https://doi.org/10.1016/j.biortech.2015.12.006 pmid: 26708484
46 Y C Yang, X Liu, C Wan, S Sun, D J Lee (2014). Accelerated aerobic granulation using alternating feed loadings: Alginate-like exopolysaccharides. Bioresource Technology, 171: 360–366
https://doi.org/10.1016/j.biortech.2014.08.092 pmid: 25218208
47 Y Zhang, W Wei, J Fan, C Jin, L Lu, W Fang (2020). Aspergillus fumigatus mitochondrial acetyl Coenzyme A acetyltransferase as an antifungal target. Applied and Environmental Microbiology, 86(7): e02986–02919
https://doi.org/10.1128/AEM.02986-19 pmid: 32005728
48 W Zhou, T Imai, M Ukita, M Sekine, T Higuchi (2006). Triggering forces for anaerobic granulation in UASB reactors. Process Biochemistry, 41(1): 36–43
https://doi.org/10.1016/j.procbio.2005.02.029
[1] FSE-21084-of-GQ_suppl_1 Download
[1] Cheng Hou, Xinbai Jiang, Na Li, Zhenhua Zhang, Qian Zhang, Jinyou Shen, Xiaodong Liu. Enhanced 4-chlorophenol biodegradation by integrating Fe2O3 nanoparticles into an anaerobic reactor: Long-term performance and underlying mechanism[J]. Front. Environ. Sci. Eng., 2022, 16(8): 98-.
[2] Zecong Yu, Keke Xiao, Yuwei Zhu, Mei Sun, Sha Liang, Jingping Hu, Huijie Hou, Bingchuan Liu, Jiakuan Yang. Comparison of different valent iron on anaerobic sludge digestion: Focusing on oxidation reduction potential, dissolved organic nitrogen and microbial community[J]. Front. Environ. Sci. Eng., 2022, 16(6): 80-.
[3] Lei Li, Shijie Yuan, Chen Cai, Xiaohu Dai. Developing “precise-acting” strategies for improving anaerobic methanogenesis of organic waste: Insights from the electron transfer system of syntrophic partners[J]. Front. Environ. Sci. Eng., 2022, 16(6): 74-.
[4] Yanan Bai, Xiuning Wang, Fang Zhang, Raymond Jianxiong Zeng. Acid Orange 7 degradation using methane as the sole carbon source and electron donor[J]. Front. Environ. Sci. Eng., 2022, 16(3): 34-.
[5] Zaishan Wei, Meiru Tang, Zhenshan Huang, Huaiyong Jiao. Mercury removal from flue gas using nitrate as an electron acceptor in a membrane biofilm reactor[J]. Front. Environ. Sci. Eng., 2022, 16(2): 20-.
[6] Yifan Liu, Qiongfang Zhang, Ainiwaer Sidike, Nuerla Ailijiang, Anwar Mamat, Guangxiao Zhang, Miao Pu, Wenhu Cheng, Zhengtao Pang. The impact of different voltage application modes on biodegradation of chloramphenicol and shift of microbial community structure[J]. Front. Environ. Sci. Eng., 2022, 16(11): 141-.
[7] Shuhan Li, Xin Zhou, Xiwei Cao, Jiabo Chen. Insights into simultaneous anammox and denitrification system with short-term pyridine exposure: Process capability, inhibition kinetics and metabolic pathways[J]. Front. Environ. Sci. Eng., 2021, 15(6): 139-.
[8] Qinxue Wen, Shuo Yang, Zhiqiang Chen. Mesophilic and thermophilic anaerobic digestion of swine manure with sulfamethoxazole and norfloxacin: Dynamics of microbial communities and evolution of resistance genes[J]. Front. Environ. Sci. Eng., 2021, 15(5): 94-.
[9] Ruijie Li, Mengmeng Zhou, Shilong He, Tingting Pan, Jing Liu, Jiabao Zhu. Deciphering the effect of sodium dodecylbenzene sulfonate on up-flow anaerobic sludge blanket treatment of synthetic sulfate-containing wastewater[J]. Front. Environ. Sci. Eng., 2021, 15(5): 91-.
[10] Ying Xu, Hui Gong, Xiaohu Dai. High-solid anaerobic digestion of sewage sludge: achievements and perspectives[J]. Front. Environ. Sci. Eng., 2021, 15(4): 71-.
[11] Weichuan Qiao, Rong Li, Tianhao Tang, Achuo Anitta Zuh. Removal, distribution and plant uptake of perfluorooctane sulfonate (PFOS) in a simulated constructed wetland system[J]. Front. Environ. Sci. Eng., 2021, 15(2): 20-.
[12] Yanqing Duan, Aijuan Zhou, Xiuping Yue, Zhichun Zhang, Yanjuan Gao, Yanhong Luo, Xiao Zhang. Acceleration of the particulate organic matter hydrolysis by start-up stage recovery and its original microbial mechanism[J]. Front. Environ. Sci. Eng., 2021, 15(1): 12-.
[13] Mona Akbar, Muhammad Farooq Saleem Khan, Ling Qian, Hui Wang. Degradation of polyacrylamide (PAM) and methane production by mesophilic and thermophilic anaerobic digestion: Effect of temperature and concentration[J]. Front. Environ. Sci. Eng., 2020, 14(6): 98-.
[14] Yuhan Zheng, Zhiguo Su, Tianjiao Dai, Feifei Li, Bei Huang, Qinglin Mu, Chuanping Feng, Donghui Wen. Identifying human-induced influence on microbial community: A comparative study in the effluent-receiving areas in Hangzhou Bay[J]. Front. Environ. Sci. Eng., 2019, 13(6): 90-.
[15] Aoshuang Jing, Tao Liu, Xie Quan, Shuo Chen, Yaobin Zhang. Enhanced nitrification in integrated floating fixed-film activated sludge (IFFAS) system using novel clinoptilolite composite carrier[J]. Front. Environ. Sci. Eng., 2019, 13(5): 69-.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed