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Frontiers of Environmental Science & Engineering

ISSN 2095-2201

ISSN 2095-221X(Online)

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Front. Environ. Sci. Eng.    2024, Vol. 18 Issue (11) : 142    https://doi.org/10.1007/s11783-024-1902-6
Enhancing biofilm formation in the hydrogen-based membrane biofilm reactor through bacterial Acyl-homoserine lactones
Yuchao Chen1, Kun Dong1, Yiming Zhang1, Junjian Zheng3, Minmin Jiang3, Dunqiu Wang1, Xuehong Zhang1, Xiaowu Huang4,5, Lijie Zhou2(), Haixiang Li1()
1. College of Environmental Science and Engineering, Guilin University of Technology, Guilin 541006, China
2. College of Chemistry and Environmental Engineering, Shenzhen University, Shenzhen 518060, China
3. College of Life and Environmental Sciences, Guilin University of Electronic Technology, Guilin 541004, China
4. Department of Environmental Science and Engineering, Guangdong Technion-Israel Institute of Technology, Shantou 515063, China
5. Guangdong Provincial Key Laboratory of Materials and Technologies for Energy Conversion, Guangdong Technion-Israel Institute of Technology, Shantou 515063, China
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Abstract

● AHL-mediated quorum sensing is widely observed in H2-denitrification systems.

● Inclusion of an external AHL source can enhance the induction of QS.

● C14-HSL and C4-HSL, especially C14-HSL, can enhance biofilm formation.

● Tech to expedite autochthonous microbial biofilm formation has been proposed.

The slow growth rate of autotrophic bacteria and regulation of biofilm thickness are critical factors that limit the development of a hydrogen-based membrane biofilm reactor (H2-MBfR). The acyl-homoserine lactone (AHL) mediated quorum sensing (QS) system is a crucial mechanism regulating biofilm behavior. However, the AHLs that promote biofilm formation in autotrophic denitrification systems and their underlying mechanisms, remain unclear. This study explored the impact of AHL-mediated QS signaling molecules on biofilm development in H2-MBfR. This study revealed that C14-HSL and C4-HSL are potential signaling molecules that enhanced biofilm formation in long-term stable operating H2-MBfR. Subsequent short-term experiments with C14-HSL and C4-HSL confirmed their ability to increase bacterial adhesion to carrier surfaces by promoting the production of extracellular polymeric substances (EPS). Functional gene annotation indicated that exogenous C14-HSL and C4-HSL increased the abundance of signal transduction (increased by 0.250%–0.375%), strengthening the inter bacterial QS response while enhancing cell motility (increased by 0.24% and 0.21%, respectively) and biological adhesion (increased by 0.044% and 0.020%, respectively), thereby accelerating the initial bacterial attachment to hollow fiber membranes and facilitating biofilm development. These findings contribute to the understanding of microbial community interactions in H2-MBfRs and provide novel approaches for biofilm management in wastewater treatment systems.
Keywords Hydrogen-based membrane biofilm reactor (H2-MBfR)      Acyl-homoserine lactones (AHLs)      Quorum sensing (QS)      Biofilm enhancement     
Corresponding Author(s): Lijie Zhou,Haixiang Li   
Issue Date: 20 September 2024
 Cite this article:   
Yuchao Chen,Kun Dong,Yiming Zhang, et al. Enhancing biofilm formation in the hydrogen-based membrane biofilm reactor through bacterial Acyl-homoserine lactones[J]. Front. Environ. Sci. Eng., 2024, 18(11): 142.
 URL:  
https://academic.hep.com.cn/fese/EN/10.1007/s11783-024-1902-6
https://academic.hep.com.cn/fese/EN/Y2024/V18/I11/142
Fig.1  Schematic of the H2-MBfR.
Fig.2  Types and contents of AHLs in different periods, (a) in biofilms and (b) in bulk liquids; percentage of AHLs, (c) C4-HSL, (d) C6-HSL, (e) C7-HSL, (f) C8-HSL, (g) C10-HSL, (h) C12-HSL, (i) C14-HSL, (j) 3-oxo-C10-HSL, and (k) 3-oxo-C14-HSL at different periods (The inner circle represents the content in biofilm, while the outer circle represents the content in bulk liquid. The two signaling molecules in Figures (d) and (e) were not detected in the bulk liquid).
Fig.3  Concentrations of (a) PS and PN in SMP and (b) PS and PN in EPS in different periods of long-term experiments; (c) is the correlation coefficients of AHLs with SMP and EPS in biofilm samples, and (d) is the correlation coefficients of AHLs with SMP and EPS in bulk liquids.
Fig.4  Effects of exogenous C4-HSL and C14-HSL on (a) biofilm thickness, (b) biofilm metabolites, (c) biofilm enrichment rate, and (d) AHLs content in the biofilm were investigated. R1: Blank control, R2: 1 μg/L C14-HSL, R3: 1 μg/L C4-HSL, T1: 0–15 d, T2: 15–35 d, T3: 35–65 d. The biofilm thickness was measured using SEM after dehydration.
Fig.5  In the short-term experiments (a) species enrichment leads to variations in relative abundance and impacts the presence of key functional genes, including those encoding AHL and those involved in denitrification processes (relative abundance > 1%), (b) relative gene abundance of AHL, and (c) relative gene abundance of denitrification.
Fig.6  Metagenomic analysis results utilized to evaluate: (a) the relative abundance of the top 30 metabolic pathways, (b) the impact of exogenous AHLs on these pathways, with positive numbers indicating a decrease in abundance from 15 to 65 d, (c) the genes regulating biofilm formation, and (d) the relative abundance of key metabolic pathways essential for biofilm formation.
1 A M Bolger, M Lohse, B Usadel. (2014). Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics, 30(15): 2114–2120
https://doi.org/10.1093/bioinformatics/btu170
2 T R Cataldi, G Bianco, L Palazzo, V Quaranta. (2007). Occurrence of N-acyl-L-homoserine lactones in extracts of some Gram-negative bacteria evaluated by gas chromatography–mass spectrometry. Analytical Biochemistry, 361(2): 226–235
https://doi.org/10.1016/j.ab.2006.11.037
3 A Elsayed, M Hurdle, Y Kim. (2021). Comprehensive model applications for better understanding of pilot-scale membrane-aerated biofilm reactor performance. Journal of Water Process Engineering, 40: 101894
https://doi.org/10.1016/j.jwpe.2020.101894
4 Q Feng, L Luo, X Chen, K Zhang, F Fang, Z Xue, C Li, J Cao, J Luo. (2021). Facilitating biofilm formation of Pseudomonas aeruginosa via exogenous N-Acy-L-homoserine lactones stimulation: regulation on the bacterial motility, adhesive ability and metabolic activity. Bioresource Technology, 341: 125727
https://doi.org/10.1016/j.biortech.2021.125727
5 Z Feng, X Lu, C Chen, Y Huo, D Zhou. (2022). Transboundary intercellular communications between Penicillium and bacterial communities during sludge bulking: inspirations on quenching fungal dominance. Water Research, 221: 118829
https://doi.org/10.1016/j.watres.2022.118829
6 Z Feng, Y Sun, T Li, F Meng, G Wu. (2019). Operational pattern affects nitritation, microbial community and quorum sensing in nitrifying wastewater treatment systems. Science of the Total Environment, 677: 456–465
https://doi.org/10.1016/j.scitotenv.2019.04.371
7 M Gao, Y Peng, Y Shen, F Tan. (2023). Study of the biofilm mechanism of C4-HSL and C6-HSL in the degradation of quinoline. Journal of Biotechnology, 376: 53–63
https://doi.org/10.1016/j.jbiotec.2023.10.002
8 A González, S Bellenberg, S Mamani, L Ruiz, A Echeverría, L Soulère, A Doutheau, C Demergasso, W Sand, Y Queneau. et al.. (2013). AHL signaling molecules with a large acyl chain enhance biofilm formation on sulfur and metal sulfides by the bioleaching bacterium Acidithiobacillus ferrooxidans. Applied Microbiology and Biotechnology, 97(8): 3729–3737
https://doi.org/10.1007/s00253-012-4229-3
9 F Hou, T Zhang, Y Peng, X Cao, H Pang, Y Shao, X Lu, J Yuan, X Chen, J Zhang. (2022). Partial anammox achieved in full scale biofilm process for typical domestic wastewater treatment. Frontiers of Environmental Science & Engineering, 16(3): 33
https://doi.org/10.1007/s11783-021-1467-6
10 H Hu, J He, J Liu, H Yu, J Zhang. (2016). Biofilm activity and sludge characteristics affected by exogenous N-acyl homoserine lactones in biofilm reactors. Bioresource Technology, 211: 339–347
https://doi.org/10.1016/j.biortech.2016.03.068
11 J Huang, Y Shi, G Zeng, Y Gu, G Chen, L Shi, Y Hu, B Tang, J Zhou. (2016). Acyl-homoserine lactone-based quorum sensing and quorum quenching hold promise to determine the performance of biological wastewater treatments: an overview. Chemosphere, 157: 137–151
https://doi.org/10.1016/j.chemosphere.2016.05.032
12 W Huang, B Gong, L He, Y Wang, J Zhou. (2020). Intensified nutrients removal in a modified sequencing batch reactor at low temperature: metagenomic approach reveals the microbial community structure and mechanisms. Chemosphere, 244: 125513
https://doi.org/10.1016/j.chemosphere.2019.125513
13 B K Hwang, W N Lee, P K Park, C H Lee, I S Chang. (2007). Effect of membrane fouling reducer on cake structure and membrane permeability in membrane bioreactor. Journal of Membrane Science, 288(1−2): 149–156
https://doi.org/10.1016/j.memsci.2006.11.032
14 M Jiang, Y Zhang, J Zheng, H Li, J Ma, X Zhang, Q Wei, X Wang, X Zhang, Z Wang. (2022). Mechanistic insights into CO2 pressure regulating microbial competition in a hydrogen-based membrane biofilm reactor for denitrification. Chemosphere, 303: 134875
https://doi.org/10.1016/j.chemosphere.2022.134875
15 M Jiang, J Zheng, P Perez-Calleja, C Picioreanu, H Lin, X Zhang, Y Zhang, H Li, R Nerenberg. (2020). New insight into CO2-mediated denitrification process in H2-based membrane biofilm reactor: an experimental and modeling study. Water Research, 184: 116177
https://doi.org/10.1016/j.watres.2020.116177
16 C Y Lai, L Zhong, Y Zhang, J X Chen, L L Wen, L D Shi, Y P Sun, F Ma, B E Rittmann, C Zhou. et al.. (2016). Bioreduction of chromate in a methane-based membrane biofilm reactor. Environmental Science & Technology, 50(11): 5832–5839
https://doi.org/10.1021/acs.est.5b06177
17 K Lee, H Yu, X Zhang, K H Choo. (2018). Quorum sensing and quenching in membrane bioreactors: opportunities and challenges for biofouling control. Bioresource Technology, 270: 656–668
https://doi.org/10.1016/j.biortech.2018.09.019
18 H Li, Y Han, Y Zhang, X Mi, D Wang, Y Xu, K Dong. (2024). Optimization of nitrogen removal and microbial mechanism of a hydrogen-based membrane biofilm reactor. Environmental Technology, 46: 1–17
https://doi.org/10.1080/09593330.2024.2317817
19 J Li, J Ma, L Sun, X Liu, H Liao, D He. (2022). Mechanistic insight into the biofilm formation and process performance of a passive aeration ditch (PAD) for decentralized wastewater treatment. Frontiers of Environmental Science & Engineering, 16(7): 86
https://doi.org/10.1007/s11783-021-1494-3
20 T Li, F Guo, Y Lin, Y Li, G Wu. (2019). Metagenomic analysis of quorum sensing systems in activated sludge and membrane biofilm of a full-scale membrane bioreactor. Journal of Water Process Engineering, 32: 100952
https://doi.org/10.1016/j.jwpe.2019.100952
21 T Li, B Yang, X Li, J Li, G Zhao, J Kan. (2018). Quorum sensing system and influence on food spoilage in Pseudomonas fluorescens from turbot. Journal of Food Science and Technology, 55(8): 3016–3025
https://doi.org/10.1007/s13197-018-3222-y
22 Y Li, H Xia, F Bai, X Song, L Zhuang, H Xu, X Zhang, X Zhang, M Qiao. (2020). PA5001 gene involves in swimming motility and biofilm formation in Pseudomonas aeruginosa. Microbial Pathogenesis, 144: 103982
https://doi.org/10.1016/j.micpath.2020.103982
23 Q Liu, J Wang, R He, H Hu, B Wu, H Ren. (2020). Bacterial assembly during the initial adhesion phase in wastewater treatment biofilms. Water Research, 184: 116147
https://doi.org/10.1016/j.watres.2020.116147
24 X Lu, G Yan, L Fu, B Cui, J Wang, D Zhou. (2023). A review of filamentous sludge bulking controls from conventional methods to emerging quorum quenching strategies. Water Research, 236: 119922
https://doi.org/10.1016/j.watres.2023.119922
25 M J Lynch, S Swift, D F Kirke, C W Keevil, C E Dodd, P Williams. (2002). The regulation of biofilm development by quorum sensing in Aeromonas hydrophila. Environmental Microbiology, 4(1): 18–28
https://doi.org/10.1046/j.1462-2920.2002.00264.x
26 S Mukherjee, B L Bassler. (2019). Bacterial quorum sensing in complex and dynamically changing environments. Nature Reviews. Microbiology, 17(6): 371–382
https://doi.org/10.1038/s41579-019-0186-5
27 S Q Ni, N Sun, H Yang, J Zhang, H H Ngo. (2015). Distribution of extracellular polymeric substances in anammox granules and their important roles during anammox granulation. Biochemical Engineering Journal, 101: 126–133
https://doi.org/10.1016/j.bej.2015.05.014
28 H S Oh, C H Lee. (2018). Origin and evolution of quorum quenching technology for biofouling control in MBRs for wastewater treatment. Journal of Membrane Science, 554: 331–345
https://doi.org/10.1016/j.memsci.2018.03.019
29 Y Pang, S Wang, J Tao, J Wang, Z Xue, R Wang. (2022). Mechanism of berberine hydrochloride interfering with biofilm formation of Hafnia alvei. Archives of Microbiology, 204(2): 126–134
https://doi.org/10.1007/s00203-021-02617-8
30 B E Rittmann. (2018). Biofilms, active substrata, and me. Water Research, 132: 135–145
https://doi.org/10.1016/j.watres.2017.12.043
31 Y Sun, Y Guan, D Zeng, K He, G Wu. (2018). Metagenomics-based interpretation of AHLs-mediated quorum sensing in anammox biofilm reactors for low-strength wastewater treatment. Chemical Engineering Journal, 344: 42–52
https://doi.org/10.1016/j.cej.2018.03.047
32 Z Sun, J Xi, C Yang, W Cong. (2022). Quorum sensing regulation methods and their effects on biofilm in biological waste treatment systems: a review. Frontiers of Environmental Science & Engineering, 16(7): 87
https://doi.org/10.1007/s11783-021-1495-2
33 Z Sun, B Yang, M Yeung, J Xi. (2023). Effects of exogenous acylated homoserine lactones on biofilms in biofilters for gaseous toluene treatment. Frontiers of Environmental Science & Engineering, 17(2): 17
https://doi.org/10.1007/s11783-023-1617-0
34 C H Tan, Y P Yeo, M Hafiz, N K J Ng, S Subramoni, S Taj, M Tay, X Chao, S Kjelleberg, S A Rice (2021). Functional metagenomic analysis of quorum sensing signaling in a nitrifying community. npj Biofilms and Microbiomes, 7(1): 79
35 K L Tomlin, R J Malott, G Ramage, D G Storey, P A Sokol, H Ceri. (2005). Quorum-sensing mutations affect attachment and stability of Burkholderia cenocepacia biofilms. Applied and Environmental Microbiology, 71(9): 5208–5218
https://doi.org/10.1128/AEM.71.9.5208-5218.2005
36 J Wang, Z Jiang, W Wang, H Wang, Y Zhang, Y Wang. (2021a). The connection between aeration regimes and EPS composition in nitritation biofilm. Chemosphere, 265: 129–141
https://doi.org/10.1016/j.chemosphere.2020.129141
37 J Wang, Q Liu, D Dong, H Hu, B Wu, H Ren. (2021b). AHLs-mediated quorum sensing threshold and its response towards initial adhesion of wastewater biofilms. Water Research, 194: 116925
https://doi.org/10.1016/j.watres.2021.116925
38 J Wang, H Ren, X Li, J Li, L Ding, J Geng, K Xu, H Huang, H Hu. (2018). In situ monitoring of wastewater biofilm formation process via ultrasonic time domain reflectometry (UTDR). Chemical Engineering Journal, 334: 2134–2141
https://doi.org/10.1016/j.cej.2017.11.043
39 X Wang, C Jiang, D Wang, Y Yang, L Fan, S Xu, X Zhuang. (2023). Quorum sensing responses of activated sludge to free nitrous acid: Zoogloea deformation, AHL redistribution, and microbiota acclimatization. Water Research, 238: 119993
https://doi.org/10.1016/j.watres.2023.119993
40 B Wu, X Chai, Y Zhao. (2016). Enhanced dewatering of waste-activated sludge by composite hydrolysis enzymes. Bioprocess and Biosystems Engineering, 39(4): 627–639
https://doi.org/10.1007/s00449-016-1544-6
41 B Wu, H Wang, X Dai, X Chai. (2021). Influential mechanism of water occurrence states of waste-activated sludge: specifically focusing on the roles of EPS micro-spatial distribution and cation-dominated interfacial properties. Water Research, 202: 117461
https://doi.org/10.1016/j.watres.2021.117461
42 Y Wu, Y Li, A Ontiveros-Valencia, L Ordaz-Díaz, J Liu, C Zhou, B E Rittmann. (2017). Enhancing denitrification using a novel in situ membrane biofilm reactor (isMBfR). Water Research, 119: 234–241
https://doi.org/10.1016/j.watres.2017.04.054
43 H Yu, G Xu, F Qu, G Li, H Liang. (2016). Effect of solid retention time on membrane fouling in membrane bioreactor: from the perspective of quorum sensing and quorum quenching. Applied Microbiology and Biotechnology, 100(18): 7887–7897
https://doi.org/10.1007/s00253-016-7496-6
44 Z Yue, P Li, L Bin, S Huang, F Fu, Z Yang, B Qiu, B Tang. (2020). N-Acyl-homoserine lactone-mediated quorum sensing of aerobic granular sludge system in a continuous-flow membrane bioreactor. Biochemical Engineering Journal, 164: 107801
https://doi.org/10.1016/j.bej.2020.107801
45 Y Zhang, J X Chen, L L Wen, Y Tang, H P Zhao. (2016). Effects of salinity on simultaneous reduction of perchlorate and nitrate in a methane-based membrane biofilm reactor. Environmental Science and Pollution Research International, 23(23): 24248–24255
https://doi.org/10.1007/s11356-016-7678-x
46 Y Zhang, M Jiang, J Ma, Y Wang, X Zhang, Q Wei, X Wang, X Zhang, J Zheng. (2023a). Development of a novel periodic venting-controlled membrane biofilm reactor for hydrogenotrophic denitrification: process performance and microbial mechanism. Chemical Engineering Journal, 463: 142529
https://doi.org/10.1016/j.cej.2023.142529
47 Y Zhang, H Yu, Y Xie, Y Guo, Y Cheng, W Yao. (2023b). Inhibitory effects of hexanal on acylated homoserine lactones (AHLs) production to disrupt biofilm formation and enzymes activity in Erwinia carotovora and Pseudomonas fluorescens. Journal of Food Science and Technology, 60(1): 372–381
https://doi.org/10.1007/s13197-022-05624-9
[1] FSE-24082-OF-CYC_suppl_1 Download
[1] Zhuoying WU, Qing WANG, Feng GUO, Shenghua ZHANG, Qipei JIANG, Xin YU. Responses of bacterial strains isolated from drinking water environments to N-acyl-L-homoserine lactones and their analogs during biofilm formation[J]. Front Envir Sci Eng, 2014, 8(2): 205-214.
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