Enhancing biofilm formation in the hydrogen-based membrane biofilm reactor through bacterial Acyl-homoserine lactones

Yuchao Chen, Kun Dong, Yiming Zhang, Junjian Zheng, Minmin Jiang, Dunqiu Wang, Xuehong Zhang, Xiaowu Huang, Lijie Zhou, Haixiang Li

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Front. Environ. Sci. Eng. ›› 2024, Vol. 18 ›› Issue (11) : 142. DOI: 10.1007/s11783-024-1902-6
RESEARCH ARTICLE

Enhancing biofilm formation in the hydrogen-based membrane biofilm reactor through bacterial Acyl-homoserine lactones

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Highlights

● 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.

Abstract

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.

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Keywords

Hydrogen-based membrane biofilm reactor (H2-MBfR) / Acyl-homoserine lactones (AHLs) / Quorum sensing (QS) / Biofilm enhancement

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Yuchao Chen, Kun Dong, Yiming Zhang, Junjian Zheng, Minmin Jiang, Dunqiu Wang, Xuehong Zhang, Xiaowu Huang, Lijie Zhou, Haixiang Li. Enhancing biofilm formation in the hydrogen-based membrane biofilm reactor through bacterial Acyl-homoserine lactones. Front. Environ. Sci. Eng., 2024, 18(11): 142 https://doi.org/10.1007/s11783-024-1902-6

References

[1]
Bolger A M, Lohse M, Usadel B. (2014). Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics, 30(15): 2114–2120
CrossRef Google scholar
[2]
Cataldi T R, Bianco G, Palazzo L, Quaranta V. (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
CrossRef Google scholar
[3]
Elsayed A, Hurdle M, Kim Y. (2021). Comprehensive model applications for better understanding of pilot-scale membrane-aerated biofilm reactor performance. Journal of Water Process Engineering, 40: 101894
CrossRef Google scholar
[4]
Feng Q, Luo L, Chen X, Zhang K, Fang F, Xue Z, Li C, Cao J, Luo J. (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
CrossRef Google scholar
[5]
Feng Z, Lu X, Chen C, Huo Y, Zhou D. (2022). Transboundary intercellular communications between Penicillium and bacterial communities during sludge bulking: inspirations on quenching fungal dominance. Water Research, 221: 118829
CrossRef Google scholar
[6]
Feng Z, Sun Y, Li T, Meng F, Wu G. (2019). Operational pattern affects nitritation, microbial community and quorum sensing in nitrifying wastewater treatment systems. Science of the Total Environment, 677: 456–465
CrossRef Google scholar
[7]
Gao M, Peng Y, Shen Y, Tan F. (2023). Study of the biofilm mechanism of C4-HSL and C6-HSL in the degradation of quinoline. Journal of Biotechnology, 376: 53–63
CrossRef Google scholar
[8]
González A, Bellenberg S, Mamani S, Ruiz L, Echeverría A, Soulère L, Doutheau A, Demergasso C, Sand W, Queneau Y. . (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
CrossRef Google scholar
[9]
Hou F, Zhang T, Peng Y, Cao X, Pang H, Shao Y, Lu X, Yuan J, Chen X, Zhang J. (2022). Partial anammox achieved in full scale biofilm process for typical domestic wastewater treatment. Frontiers of Environmental Science & Engineering, 16(3): 33
CrossRef Google scholar
[10]
Hu H, He J, Liu J, Yu H, Zhang J. (2016). Biofilm activity and sludge characteristics affected by exogenous N-acyl homoserine lactones in biofilm reactors. Bioresource Technology, 211: 339–347
CrossRef Google scholar
[11]
Huang J, Shi Y, Zeng G, Gu Y, Chen G, Shi L, Hu Y, Tang B, Zhou J. (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
CrossRef Google scholar
[12]
Huang W, Gong B, He L, Wang Y, Zhou J. (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
CrossRef Google scholar
[13]
Hwang B K, Lee W N, Park P K, Lee C H, Chang I S. (2007). Effect of membrane fouling reducer on cake structure and membrane permeability in membrane bioreactor. Journal of Membrane Science, 288(1−2): 149–156
CrossRef Google scholar
[14]
Jiang M, Zhang Y, Zheng J, Li H, Ma J, Zhang X, Wei Q, Wang X, Zhang X, Wang Z. (2022). Mechanistic insights into CO2 pressure regulating microbial competition in a hydrogen-based membrane biofilm reactor for denitrification. Chemosphere, 303: 134875
CrossRef Google scholar
[15]
Jiang M, Zheng J, Perez-Calleja P, Picioreanu C, Lin H, Zhang X, Zhang Y, Li H, Nerenberg R. (2020). New insight into CO2-mediated denitrification process in H2-based membrane biofilm reactor: an experimental and modeling study. Water Research, 184: 116177
CrossRef Google scholar
[16]
Lai C Y, Zhong L, Zhang Y, Chen J X, Wen L L, Shi L D, Sun Y P, Ma F, Rittmann B E, Zhou C. . (2016). Bioreduction of chromate in a methane-based membrane biofilm reactor. Environmental Science & Technology, 50(11): 5832–5839
CrossRef Google scholar
[17]
Lee K, Yu H, Zhang X, Choo K H. (2018). Quorum sensing and quenching in membrane bioreactors: opportunities and challenges for biofouling control. Bioresource Technology, 270: 656–668
CrossRef Google scholar
[18]
Li H, Han Y, Zhang Y, Mi X, Wang D, Xu Y, Dong K. (2024). Optimization of nitrogen removal and microbial mechanism of a hydrogen-based membrane biofilm reactor. Environmental Technology, 46: 1–17
CrossRef Google scholar
[19]
Li J, Ma J, Sun L, Liu X, Liao H, He D. (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
CrossRef Google scholar
[20]
Li T, Guo F, Lin Y, Li Y, Wu G. (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
CrossRef Google scholar
[21]
Li T, Yang B, Li X, Li J, Zhao G, Kan J. (2018). Quorum sensing system and influence on food spoilage in Pseudomonas fluorescens from turbot. Journal of Food Science and Technology, 55(8): 3016–3025
CrossRef Google scholar
[22]
Li Y, Xia H, Bai F, Song X, Zhuang L, Xu H, Zhang X, Zhang X, Qiao M. (2020). PA5001 gene involves in swimming motility and biofilm formation in Pseudomonas aeruginosa. Microbial Pathogenesis, 144: 103982
CrossRef Google scholar
[23]
Liu Q, Wang J, He R, Hu H, Wu B, Ren H. (2020). Bacterial assembly during the initial adhesion phase in wastewater treatment biofilms. Water Research, 184: 116147
CrossRef Google scholar
[24]
Lu X, Yan G, Fu L, Cui B, Wang J, Zhou D. (2023). A review of filamentous sludge bulking controls from conventional methods to emerging quorum quenching strategies. Water Research, 236: 119922
CrossRef Google scholar
[25]
Lynch M J, Swift S, Kirke D F, Keevil C W, Dodd C E, Williams P. (2002). The regulation of biofilm development by quorum sensing in Aeromonas hydrophila. Environmental Microbiology, 4(1): 18–28
CrossRef Google scholar
[26]
Mukherjee S, Bassler B L. (2019). Bacterial quorum sensing in complex and dynamically changing environments. Nature Reviews. Microbiology, 17(6): 371–382
CrossRef Google scholar
[27]
Ni S Q, Sun N, Yang H, Zhang J, Ngo H H. (2015). Distribution of extracellular polymeric substances in anammox granules and their important roles during anammox granulation. Biochemical Engineering Journal, 101: 126–133
CrossRef Google scholar
[28]
Oh H S, Lee C H. (2018). Origin and evolution of quorum quenching technology for biofouling control in MBRs for wastewater treatment. Journal of Membrane Science, 554: 331–345
CrossRef Google scholar
[29]
Pang Y, Wang S, Tao J, Wang J, Xue Z, Wang R. (2022). Mechanism of berberine hydrochloride interfering with biofilm formation of Hafnia alvei. Archives of Microbiology, 204(2): 126–134
CrossRef Google scholar
[30]
Rittmann B E. (2018). Biofilms, active substrata, and me. Water Research, 132: 135–145
CrossRef Google scholar
[31]
Sun Y, Guan Y, Zeng D, He K, Wu G. (2018). Metagenomics-based interpretation of AHLs-mediated quorum sensing in anammox biofilm reactors for low-strength wastewater treatment. Chemical Engineering Journal, 344: 42–52
CrossRef Google scholar
[32]
Sun Z, Xi J, Yang C, Cong W. (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
CrossRef Google scholar
[33]
Sun Z, Yang B, Yeung M, Xi J. (2023). Effects of exogenous acylated homoserine lactones on biofilms in biofilters for gaseous toluene treatment. Frontiers of Environmental Science & Engineering, 17(2): 17
CrossRef Google scholar
[34]
TanC H, Yeo Y P, HafizM, NgN K J, Subramoni S, TajS, TayM, ChaoX, KjellebergS, Rice S A (2021). Functional metagenomic analysis of quorum sensing signaling in a nitrifying community. npj Biofilms and Microbiomes, 7(1): 79
[35]
Tomlin K L, Malott R J, Ramage G, Storey D G, Sokol P A, Ceri H. (2005). Quorum-sensing mutations affect attachment and stability of Burkholderia cenocepacia biofilms. Applied and Environmental Microbiology, 71(9): 5208–5218
CrossRef Google scholar
[36]
Wang J, Jiang Z, Wang W, Wang H, Zhang Y, Wang Y. (2021a). The connection between aeration regimes and EPS composition in nitritation biofilm. Chemosphere, 265: 129–141
CrossRef Google scholar
[37]
Wang J, Liu Q, Dong D, Hu H, Wu B, Ren H. (2021b). AHLs-mediated quorum sensing threshold and its response towards initial adhesion of wastewater biofilms. Water Research, 194: 116925
CrossRef Google scholar
[38]
Wang J, Ren H, Li X, Li J, Ding L, Geng J, Xu K, Huang H, Hu H. (2018). In situ monitoring of wastewater biofilm formation process via ultrasonic time domain reflectometry (UTDR). Chemical Engineering Journal, 334: 2134–2141
CrossRef Google scholar
[39]
Wang X, Jiang C, Wang D, Yang Y, Fan L, Xu S, Zhuang X. (2023). Quorum sensing responses of activated sludge to free nitrous acid: Zoogloea deformation, AHL redistribution, and microbiota acclimatization. Water Research, 238: 119993
CrossRef Google scholar
[40]
Wu B, Chai X, Zhao Y. (2016). Enhanced dewatering of waste-activated sludge by composite hydrolysis enzymes. Bioprocess and Biosystems Engineering, 39(4): 627–639
CrossRef Google scholar
[41]
Wu B, Wang H, Dai X, Chai X. (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
CrossRef Google scholar
[42]
Wu Y, Li Y, Ontiveros-Valencia A, Ordaz-Díaz L, Liu J, Zhou C, Rittmann B E. (2017). Enhancing denitrification using a novel in situ membrane biofilm reactor (isMBfR). Water Research, 119: 234–241
CrossRef Google scholar
[43]
Yu H, Xu G, Qu F, Li G, Liang H. (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
CrossRef Google scholar
[44]
Yue Z, Li P, Bin L, Huang S, Fu F, Yang Z, Qiu B, Tang B. (2020). N-Acyl-homoserine lactone-mediated quorum sensing of aerobic granular sludge system in a continuous-flow membrane bioreactor. Biochemical Engineering Journal, 164: 107801
CrossRef Google scholar
[45]
Zhang Y, Chen J X, Wen L L, Tang Y, Zhao H P. (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
CrossRef Google scholar
[46]
Zhang Y, Jiang M, Ma J, Wang Y, Zhang X, Wei Q, Wang X, Zhang X, Zheng J. (2023a). Development of a novel periodic venting-controlled membrane biofilm reactor for hydrogenotrophic denitrification: process performance and microbial mechanism. Chemical Engineering Journal, 463: 142529
CrossRef Google scholar
[47]
Zhang Y, Yu H, Xie Y, Guo Y, Cheng Y, Yao W. (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
CrossRef Google scholar

CRediT Authorship Contribution Statement

Yuchao Chen: Conceptualization, Formal analysis, Writing – original draft, Writing – review and editing. Kun Dong: Methodology. Yiming Zhang: Resources. Junjian Zheng: Investigation. Minmin Jiang: Writing – review and editing. Dunqiu Wang: Methodology. Xuehong Zhang: Conceptualization. Xiaowu Huang: Validation. Lijie Zhou: Visualization, Conceptualization. Haixiang Li: Methodology, Project administration, Funding acquisition, Supervision.

Acknowledgements

The authors gratefully acknowledge the financial support of this work by the Guangxi Natural Science Foundation (China) (No. 2022GXNSFFA035033), the National Natural Science Foundation of China (Grant No. 51878197), the Research funds of the Guangxi Key Laboratory of Theory and Technology for Environmental Pollution Control (China) (No. 2301Z003).

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Data Availability

Data will be made available on request.

Electronic Supplementary Material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s11783-024-1902-6 and is accessible for authorized users.

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2024 Higher Education Press 2024
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