1. Key Laboratory of Pollution Control Chemistry and Environmental Functional Materials for Qinghai-Tibet Plateau of the National Ethnic Affairs Commission, School of Chemistry and Environment, Southwest Minzu University, Chengdu 610041, China 2. Institute for Environmental Pollution and Health, School of Environmental and Chemical Engineering, Shanghai University, Shanghai 200444, China 3. School of Life Sciences, Southwest University, Chongqing 400715, China 4. State Environmental Protection Key Laboratory of Environmental Risk Assessment and Control on Chemical Process, School of Resources and Environmental Engineering, East China University of Science and Technology, Shanghai 200237, China 5. Institute of Qinghai-Tibetan Plateau, Southwest Minzu University, Chengdu 610041, China
● Aerobic granular sludge could withstand long-term saline stresses.
● Aerobic granular sludge maintained strength under low-salinity condition.
● Aerobic granular sludge was dominated by halophiles at 50 g/L salinity.
Saline wastewater is regarded as a challenge for wastewater treatment plants because high-salinity conditions negatively affect on traditional biological technologies. Aerobic granular sludge (AGS) has gained attention as a promising technology for saline wastewater treatment because of its compact structure and the ability to withstand toxic loadings. Therefore, this study investigated the salt-resistance performance, sludge properties and microbial community of AGS under low-salinity and high-salinity conditions, with the saline concentrations ranging from 0 to 50 g/L. The results showed that AGS could withstand long-term saline stresses, and the maximum salinity reached 50 g/L within 113 d. Under salinities of 10, 30, and 50 g/L, the chemical oxygen demand (COD) removal efficiencies were 90.3%, 88.0% and 78.0%, respectively. AGS also its maintained strength and aggregation at salinities of 10 and 30 g/L. Overproduction of extracellular polymeric substances (EPS) by non-halophilic bacteria that enhanced sludge aggregation. The compact structure that ensured the microorganisms bioactivity helped to remove organic matters under salinities of 10 and 30 g/L. At a salinity of 50 g/L, moderately halophilic bacteria, including Salinicola, Thioclava, Idiomarina and Albirhodobacter, prevailed in the reactor. The dominant microbial communities shifted to moderately halophilic bacteria, which could maintain aerobic granular stabilization and remove organic matters under 50 g/L salinity. These results in this study provide a further explanation for the long-term operation of AGS for treating saline wastewater at different salinities. It is hoped that this work could bring some clues for the mystery of salt- resistance mechanisms.
APHA (2005). Standard Methods for the Examination of Water and Wastewater, 21st ed. Washington, DC: American Public Health Association/American Water Works Association/Water Environment Federation
2
R Campo, S F Corsino, M Torregrossa, G Di Bella. (2018). The role of extracellular polymeric substances on aerobic granulation with stepwise increase of salinity. Separation and Purification Technology, 195: 12–20 https://doi.org/10.1016/j.seppur.2017.11.074
3
J H Cao, F Z Chen, Z Fang, Y Gu, H Wang, J F Lu, Y M Bi, S P Wang, W L Huang, F S Meng. (2022). Effect of filamentous algae in a microalgal-bacterial granular sludge system treating saline wastewater: assessing stability, lipid production and nutrients removal. Bioresource Technology, 354: 127182 https://doi.org/10.1016/j.biortech.2022.127182
4
P Carrera, T Casero-Díaz, C M Castro-Barros, R Méndez, del Río A Val, A Mosquera-Corral. (2021). Features of aerobic granular sludge formation treating fluctuating industrial saline wastewater at pilot scale. Journal of Environmental Management, 296: 113135 https://doi.org/10.1016/j.jenvman.2021.113135
5
I S Chang, C H Lee. (1998). Membrane filtration characteristics in membrane-coupled activated sludge system: the effect of physiological states of activated sludge on membrane fouling. Desalination, 120(3): 221–233 https://doi.org/10.1016/S0011-9164(98)00220-3
6
L Chen, Y S Gu, C Q Cao, J Zhang, J W Ng, C Y Tang. (2014). Performance of a submerged anaerobic membrane bioreactor with forward osmosis membrane for low-strength wastewater treatment. Water Research, 50: 114–123 https://doi.org/10.1016/j.watres.2013.12.009
7
S F Corsino, M Capodici, M Torregrossa, G Viviani. (2017). Physical properties and extracellular polymeric substances pattern of aerobic granular sludge treating hypersaline wastewater. Bioresource Technology, 229: 152–159 https://doi.org/10.1016/j.biortech.2017.01.024
8
G Di Bella, D Di Trapani, M Torregrossa, G Viviani. (2013). Performance of a MBR pilot plant treating high strength wastewater subject to salinity increase: analysis of biomass activity and fouling behaviour. Bioresource Technology, 147: 614–618 https://doi.org/10.1016/j.biortech.2013.08.025
9
H Dong, K Y Zhang, X Han, B Du, Q Wei, D Wei. (2017). Achievement, performance and characteristics of microbial products in a partial nitrification sequencing batch reactor as a pretreatment for anaerobic ammonium oxidation. Chemosphere, 183: 212–218 https://doi.org/10.1016/j.chemosphere.2017.05.119
10
J W Fan, W Li, B Zhang, W X Shi, P N L Lens. (2022). Unravelling the biodegradation performance and mechanisms of acid orange 7 by aerobic granular sludge at different salinity levels. Bioresource Technology, 357: 127347 https://doi.org/10.1016/j.biortech.2022.127347
11
R D G Franca, H M Pinheiro, M C M van Loosdrecht, N D Lourenco. (2018). Stability of aerobic granules during long-term bioreactor operation. Biotechnology Advances, 36(1): 228–246 https://doi.org/10.1016/j.biotechadv.2017.11.005
12
M T Ghazani, A Taghdisian. (2019). Performance evaluation of a hybrid sequencing batch reactor under saline and hyper saline conditions. Journal of Biological Engineering, 13(1): 64 https://doi.org/10.1186/s13036-019-0192-1
13
S Hamimed, A Gamraoui, A Landoulsi, A Chatti. (2022). Bio-nanocrystallization of NaCl using saline wastewaters through biological treatment by Yarrowia lipolytica. Environmental Technology & Innovation, 26: 102338 https://doi.org/10.1016/j.eti.2022.102338
14
F Han, M R Zhang, Z Liu, Y F Han, Q Li, W Z Zhou. (2022). Enhancing robustness of halophilic aerobic granule sludge by granular activated carbon at decreasing temperature. Chemosphere, 292: 133507 https://doi.org/10.1016/j.chemosphere.2021.133507
15
X D Hao, D Q Wu, J Li, R B Liu, M Van Loosdrecht (2022). Making waves: a sea change in treating wastewater-Why thermodynamics supports resource recovery and recycling? Water Research, 218: 118516
16
H He, Y Chen, X Li, Y Cheng, C Yang, G Zeng. (2017). Influence of salinity on microorganisms in activated sludge processes: a review. International Biodeterioration & Biodegradation, 119: 520–527 https://doi.org/10.1016/j.ibiod.2016.10.007
17
J L Huang, Y W Cui, J L Yan, Y Cui. (2022). Occurrence of heterotrophic nitrification-aerobic denitrification induced by decreasing salinity in a halophilic AGS SBR treating hypersaline wastewater. Chemical Engineering Journal, 431: 134133 https://doi.org/10.1016/j.cej.2021.134133
18
S B Ismail, C J de La Parra, H Temmink, J B van Lier. (2010). Extracellular polymeric substances (EPS) in upflow anaerobic sludge blanket (UASB) reactors operated under high salinity conditions. Water Research, 44(6): 1909–1917 https://doi.org/10.1016/j.watres.2009.11.039
19
E P Ivanova, L A Romanenko, J Chun, M H Matte, G R Matte, V V Mikhailov, V I Svetashev, A Huq, T Maugel, R R Colwell. (2000). Idiomarina gen. nov., comprising novel indigenous deep-sea bacteria from the Pacific Ocean, including descriptions of two species, Idiomarina abyssalis sp. nov and Idiomarina zobellii sp. nov. International Journal of Systematic and Evolutionary Microbiology, 50(2): 901–907 https://doi.org/10.1099/00207713-50-2-901
20
H S Jung, J Lee, J W Hyeon, S Hyun, C O Jeon. (2018). Albirhodobacter confluentis sp. nov., isolated from an estuary. International Journal of Systematic and Evolutionary Microbiology, 68(1): 289–293 https://doi.org/10.1099/ijsem.0.002499
21
Q Lai, S Li, H Xu, L Jiang, R Zhang, Z Shao. (2014). Thioclava atlantica sp. nov., isolated from deep sea sediment of the Atlantic Ocean. Antonie van Leeuwenhoek, 106(5): 919–925 https://doi.org/10.1007/s10482-014-0261-x
22
L Lei, J C Yao, Y D Liu, W Li. (2021). Performance, sludge characteristics and microbial community in a salt-tolerant aerobic granular SBR by seeding anaerobic granular sludge. International Biodeterioration & Biodegradation, 163: 105258 https://doi.org/10.1016/j.ibiod.2021.105258
23
C Li, W Li, H Li, M Hou, X Wu, J L Zhuang, Y D Liu. (2019). The effect of quorum sensing on performance of salt-tolerance aerobic granular sludge: linking extracellular polymeric substances and microbial community. Biodegradation, 30(5-6): 447–456 https://doi.org/10.1007/s10532-019-09886-7
24
J X Li, Z P Ma, M M Gao, Y K Wang, Z J Yang, H Xu, X H Wang. (2020a). Enhanced aerobic granulation at low temperature by stepwise increasing of salinity. Science of the Total Environment, 722: 137660 https://doi.org/10.1016/j.scitotenv.2020.137660
25
W Li, J C Yao, J L Zhuang, Y Y Zhou, J P Shapleigh, Y D Liu. (2020b). Metagenomics revealed the phase-related characteristics during rapid development of halotolerant aerobic granular sludge. Environment International, 137: 105548 https://doi.org/10.1016/j.envint.2020.105548
26
X Y Li, S F Yang. (2007). Influence of loosely bound extracellular polymeric substances (EPS) on the flocculation, sedimentation and dewaterability of activated sludge. Water Research, 41(5): 1022–1030 https://doi.org/10.1016/j.watres.2006.06.037
27
Z Liu, X H Zhang, S M Zhang, H Qi, Y W Hou, M Gao, J X Wang, A Zhang, Y Chen, Y Liu. (2022). A comparison between exogenous carriers enhanced aerobic granulation under low organic loading in the aspect of sludge characteristics, extracellular polymeric substances and microbial communities. Bioresource Technology, 346: 126567 https://doi.org/10.1016/j.biortech.2021.126567
28
W H Luo, H V Phan, M Xie, F I Hai, W E Price, M Elimelech, L D Nghiem. (2017). Osmotic versus conventional membrane bioreactors integrated with reverse osmosis for water reuse: biological stability, membrane fouling, and contaminant removal. Water Research, 109: 122–134 https://doi.org/10.1016/j.watres.2016.11.036
29
M J Martínez-Cánovas, V Bejar, F Martinez-Checa, R Paez, E Quesada. (2004). Idiomarina fontislapidosi sp. nov and Idiomanna ramblicola sp. nov., isolated from inland hypersaline habitats in Spain. International Journal of Systematic and Evolutionary Microbiology, 54(5): 1793–1797 https://doi.org/10.1099/ijs.0.63172-0
30
D Ou, H Li, W Li, X Wu, Y Q Wang, Y D Liu. (2018). Salt-tolerance aerobic granular sludge: formation and microbial community characteristics. Bioresource Technology, 249: 132–138 https://doi.org/10.1016/j.biortech.2017.07.154
31
L Quartaroli, C M Silva, L C F Silva, H S Lima, S O de Paula, R S Dias, K B Carvalho, R S Souza, J P Bassin, C C da Silva. (2019). Effect of the gradual increase of salt on stability and microbial diversity of granular sludge and ammonia removal. Journal of Environmental Management, 248: 109273 https://doi.org/10.1016/j.jenvman.2019.109273
32
Y Sui, Y W Cui, J L Huang, M J Xu. (2024). Feast/famine ratio regulates the succession of heterotrophic nitrification-aerobic denitrification and autotrophic ammonia oxidizing bacteria in halophilic aerobic granular sludge treating saline wastewater. Bioresource Technology, 393: 129995 https://doi.org/10.1016/j.biortech.2023.129995
33
B J Thwaites, B van den Akker, P J Reeve, M D Short, N Dinesh, J P Alvarez-Gaitan, R Stuetz. (2018). Ecology and performance of aerobic granular sludge treating high-saline municipal wastewater. Water Science and Technology, 77(4): 1107–1114 https://doi.org/10.2166/wst.2017.626
34
C L Wan, D J Lee, X Yang, Y Y Wang, X Z Wang, X Liu. (2015). Calcium precipitate induced aerobic granulation. Bioresource Technology, 176: 32–37 https://doi.org/10.1016/j.biortech.2014.11.008
35
F Xiao, S F Yang, X Y Li. (2008). Physical and hydrodynamic properties of aerobic granules produced in sequencing batch reactors. Separation and Purification Technology, 63(3): 634–641 https://doi.org/10.1016/j.seppur.2008.07.002
36
Q Yuan, H Gong, H Xi, K J Wang. (2020). Aerobic granular sludge formation based on substrate availability: effects of flow pattern and fermentation pretreatment. Frontiers of Environmental Science & Engineering, 14(3): 49 https://doi.org/10.1007/s11783-020-1226-0
37
W X Zhang, W Z Liang, Z E Zhang, T W Hao. (2021). Aerobic granular sludge (AGS) scouring to mitigate membrane fouling: performance, hydrodynamic mechanism and contribution quantification model. Water Research, 188: 116518 https://doi.org/10.1016/j.watres.2020.116518