1. College of Environmental and Resource Sciences, Zhejiang University, Hangzhou 310058, China 2. Innovation Center of Yangtze River Delta, Zhejiang University, Jiashan 314100, China 3. Department of Civil and Environmental Engineering, The George Washington University, Washington, DC 20052, USA
● The milestones underlying studies and mechanisms are summarized.
● Problematic biofilms can be removed by nanozymes through multiple strategies.
● Surface reactivity regulation can improve the antibiofilm efficiency of nanozymes.
● Machine learning-assisted nanozyme design can help improve treatment efficiency.
Current microbial control strategies face challenges in keeping up with the escalation of microbial problems due to the presence of biofilms. Therefore, there is an urgent need to develop effective and robust strategies to control problematic biofilms in water treatment and reuse systems. Nanozymes, which have intrinsic biocatalytic activity and broad antibacterial spectra, hold promise for controlling resilient biofilms. This review summarizes the milestones of nanozyme studies and their applications as antibiofilm agents. The mechanisms behind the antibacterial, quorum quenching, and depolymerizing properties of nanozymes with different enzyme activities are discussed. Notably, the surface and composition of nanozymes are crucial for their efficacy in biofilm control; thus, rationally designed nanozymes can increase their effectiveness. Additionally, the challenges of nanozymes as antibiofilm agents in realistic scenarios are investigated along with proposed strategies to overcome these challenges. Prospects of nanozyme-based biofilm control, such as machine learning-assisted nanozyme design, are also discussed. Overall, this review highlights the potential of nanozymes as antibiofilm agents and provides insights into the future design of nanozymes for biofilm control.
Generation of •OH and change the cell membrane permeability
Pan et al. (2022)
Zn-Nx-C
Lactonase
P. aeruginosa
Hydrolyzing QS signaling compound
Gao et al. (2023a)
CeO2–x nanorods
Haloperoxidase
E. coli
Oxidative quorum sensing signal compounds
Hu et al. (2018)
CeO2
Haloperoxidase
P. aeruginosa
Oxidative quorum sensing signal compounds
Jegel et al. (2022)
Cu–Fe3O4
Horseradish peroxidas, Superoxide dismutase and Catalase
MRSA
Interfere with metabolic and quorum sensing processes
Jin et al. (2024)
MoS2/rGO
Oxidase, peroxidase and catalase
E. coli, S. aureus
Elevated bacterial capture capacity and ROS destruction
Wang et al. (2020a)
Defect-richCu-nanowire
Peroxidase
E. coli, S. aureus
Enhanced bacteria binding capacity and Generation of •OH
Cao et al. (2019)
MOF@Au NPs
DNase
S. aureus
Hydrolyzing eDNA and enhanced penetration of nanozyme
Guo et al. (2023)
Pd@Ir
Oxidase, peroxidase and catalase
MRSA, E. coli
Enhanced generated of •OH and 1O2
Ye et al. (2022)
Tab.1
Fig.2
Fig.3
Fig.4
Fig.5
Fig.6
Fig.7
Fig.8
1
D T Ahneman, J G Estrada, S Lin, S D Dreher, A G Doyle. (2018). Predicting reaction performance in C–N cross-coupling using machine learning. Science, 360(6385): 186–190 https://doi.org/10.1126/science.aar5169
2
A Ali, M Ovais, H Zhou, Y Rui, C Chen. (2021). Tailoring metal-organic frameworks-based nanozymes for bacterial theranostics. Biomaterials, 275: 120951 https://doi.org/10.1016/j.biomaterials.2021.120951
3
S Ali, S Sikdar, S Basak, M Mondal, K Mallick, M Salman Haydar, S Ghosh, M Nath Roy. (2023). Assemble multi-enzyme mimic tandem Mn3O4@ g-C3N4 for augment ROS elimination and label free detection. Chemical Engineering Journal, 463: 142355 https://doi.org/10.1016/j.cej.2023.142355
F Attar, M G Shahpar, B Rasti, M Sharifi, A A Saboury, S M Rezayat, M Falahati. (2019). Nanozymes with intrinsic peroxidase-like activities. Journal of Molecular Liquids, 278: 130–144 https://doi.org/10.1016/j.molliq.2018.12.011
6
N Augustine, P Kumar, S Thomas. (2010). Inhibition of Vibrio cholerae biofilm by AiiA enzyme produced from Bacillus spp. Archives of Microbiology, 192(12): 1019–1022 https://doi.org/10.1007/s00203-010-0633-1
7
I Banerjee, R C Pangule, R S Kane. (2011). Antifouling coatings: recent developments in the design of surfaces that prevent fouling by proteins, bacteria, and marine organisms. Advanced Materials, 23(6): 690–718 https://doi.org/10.1002/adma.201001215
8
A Butler, M Sandy. (2009). Mechanistic considerations of halogenating enzymes. Nature, 460(7257): 848–854 https://doi.org/10.1038/nature08303
9
F Cao, L Zhang, H Wang, Y You, Y Wang, N Gao, J Ren, X Qu. (2019). Defect-rich adhesive nanozymes as efficient antibiotics for enhanced bacterial inhibition. Angewandte Chemie International Edition, 58(45): 16236–16242 https://doi.org/10.1002/anie.201908289
10
Y Chen, C Rong, W Gao, S Luo, Y Guo, Y Gu, G Yang, W Xu, C Zhu, L L Qu. (2024). Ag-MXene as peroxidase-mimicking nanozyme for enhanced bacteriocide and cholesterol sensing. Journal of Colloid and Interface Science, 653: 540–550 https://doi.org/10.1016/j.jcis.2023.09.097
11
Y Chen, Q Sheng, J Wei, Q Wen, D Ma, J Li, Y Xie, J Shen, X Sun. (2022). Novel strategy for membrane biofouling control in MBR with nano-MnO2 modified PVDF membrane by in-situ ozonation. Science of the Total Environment, 808: 151996 https://doi.org/10.1016/j.scitotenv.2021.151996
12
Z Chen, H Ji, C Liu, W Bing, Z Wang, X Qu. (2016). A multinuclear metal complex based DNase-mimetic artificial enzyme: matrix cleavage for combating bacterial biofilms. Angewandte Chemie International Edition, 55(36): 10732–10736 https://doi.org/10.1002/anie.201605296
O Ciofu, C Moser, P Ø Jensen, N Høiby. (2022). Tolerance and resistance of microbial biofilms. Nature Reviews. Microbiology, 20(10): 621–635 https://doi.org/10.1038/s41579-022-00682-4
15
O Ciofu, E Rojo-Molinero, M D Macià, A Oliver. (2017). Antibiotic treatment of biofilm infections. Acta Pathologica et Microbiologica Scandinavica. Supplement, 125(4): 304–319 https://doi.org/10.1111/apm.12673
16
A Cornelissen, P J Ceyssens, V N Krylov, J P Noben, G Volckaert, R Lavigne. (2012). Identification of EPS-degrading activity within the tail spikes of the novel Pseudomonas putida phage AF. Virology, 434(2): 251–256 https://doi.org/10.1016/j.virol.2012.09.030
17
J W Costerton, P S Stewart, E P Greenberg. (1999). Bacterial biofilms: a common cause of persistent infections. Science, 284(5418): 1318–1322 https://doi.org/10.1126/science.284.5418.1318
18
Y Dang, G Wang, G Su, Z Lu, Y Wang, T Liu, X Pu, X Wang, C Wu, C Song. et al.. (2022). Rational construction of a Ni/CoMoO4 heterostructure with strong Ni–O–Co bonds for improving multifunctional nanozyme activity. ACS Nano, 16(3): 4536–4550 https://doi.org/10.1021/acsnano.1c11012
T Das, B P Krom, H C Van Der Mei, H J Busscher, P K Sharma. (2011). DNA-mediated bacterial aggregation is dictated by acid–base interactions. Soft Matter, 7(6): 2927–2935 https://doi.org/10.1039/c0sm01142h
21
D Davies. (2003). Understanding biofilm resistance to antibacterial agents. Nature Reviews. Drug Discovery, 2(2): 114–122 https://doi.org/10.1038/nrd1008
22
D G Davies, M R Parsek, J P Pearson, B H Iglewski, J W Costerton, E P Greenberg. (1998). The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science, 280(5361): 295–298 https://doi.org/10.1126/science.280.5361.295
23
Q Deng, P Sun, L Zhang, Z Liu, H Wang, J Ren, X Qu. (2019). Porphyrin MOF dots–based, function-adaptive nanoplatform for enhanced penetration and photodynamic eradication of bacterial biofilms. Advanced Functional Materials, 29(30): 1903018 https://doi.org/10.1002/adfm.201903018
24
N Derlon, A Grutter, F Brandenberger, A Sutter, U Kuhlicke, T R Neu, E Morgenroth. (2016). The composition and compression of biofilms developed on ultrafiltration membranes determine hydraulic biofilm resistance. Water Research, 102: 63–72 https://doi.org/10.1016/j.watres.2016.06.019
25
P Desmond, J P Best, E Morgenroth, N Derlon. (2018). Linking composition of extracellular polymeric substances (EPS) to the physical structure and hydraulic resistance of membrane biofilms. Water Research, 132: 211–221 https://doi.org/10.1016/j.watres.2017.12.058
26
Q Dong, Z Li, J Xu, Q Yuan, L Chen, Z Chen. (2022). Versatile graphitic nanozymes for magneto actuated cascade reaction-enhanced treatment of S. mutans biofilms. Nano Research, 15(11): 9800–9808 https://doi.org/10.1007/s12274-022-4258-x
27
T Du, Z Xiao, G Zhang, L Wei, J Cao, Z Zhang, X Li, Z Song, W Wang, J Liu. et al.. (2023). An injectable multifunctional hydrogel for eradication of bacterial biofilms and wound healing. Acta Biomaterialia, 161: 112–133 https://doi.org/10.1016/j.actbio.2023.03.008
28
L Eberl, M K Winson, C Sternberg, G S Stewart, G Christiansen, S R Chhabra, B Bycroft, P Williams, S Molin, M Givskov. (1996). Involvement of N-acyl-L-hormoserine lactone autoinducers in controlling the multicellular behaviour of Serratia liquefaciens. Molecular Microbiology, 20(1): 127–136 https://doi.org/10.1111/j.1365-2958.1996.tb02495.x
29
M J Eickhoff, B L Bassler (2018). SnapShot: bacterial quorum sensing. Cell, 174(5): 1328–1328 e.1
30
K Fan, L Gao, H Wei, B Jiang, D Wang, R Zhang, J He, X Meng, Z Wang, H Fan, et al. (2023). Nanozymes. Progress in Chemistry, 35(1): 1–8787
31
G Fang, R Kang, S Cai, C Ge. (2023). Insight into nanozymes for their environmental applications as antimicrobial and antifouling agents: progress, challenges and prospects. Nano Today, 48: 101755 https://doi.org/10.1016/j.nantod.2023.101755
32
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
33
H C Flemming, E D Van Hullebusch, T R Neu, P H Nielsen, T Seviour, P Stoodley, J Wingender, S Wuertz. (2023). The biofilm matrix: multitasking in a shared space. Nature Reviews Microbiology, 21(2): 70–86 https://doi.org/10.1038/s41579-022-00791-0
34
K Forier, A S Messiaen, K Raemdonck, H Nelis, S De Smedt, J Demeester, T Coenye, K Braeckmans. (2014). Probing the size limit for nanomedicine penetration into Burkholderia multivorans and Pseudomonas aeruginosa biofilms. Journal of Controlled Release, 195: 21–28 https://doi.org/10.1016/j.jconrel.2014.07.061
35
S Fulaz, S Vitale, L Quinn, E Casey. (2019). Nanoparticle–biofilm interactions: the role of the EPS matrix. Trends in Microbiology, 27(11): 915–926 https://doi.org/10.1016/j.tim.2019.07.004
36
F Gao, T Shao, Y Yu, Y Xiong, L Yang. (2021). Surface-bound reactive oxygen species generating nanozymes for selective antibacterial action. Nature Communications, 12(1): 745 https://doi.org/10.1038/s41467-021-20965-3
37
L Gao, Y Liu, D Kim, Y Li, G Hwang, P C Naha, D P Cormode, H Koo. (2016). Nanocatalysts promote Streptococcus mutans biofilm matrix degradation and enhance bacterial killing to suppress dental caries in vivo. Biomaterials, 101: 272–284 https://doi.org/10.1016/j.biomaterials.2016.05.051
38
L Gao, J Zhuang, L Nie, J Zhang, Y Zhang, N Gu, T Wang, J Feng, D Yang, S Perrett, X Yan. (2007). Intrinsic peroxidase-like activity of ferromagnetic nanoparticles. Nature Nanotechnology, 2(9): 577–583 https://doi.org/10.1038/nnano.2007.260
39
M Gao, B Xu, Y Huang, J Cao, L Yang, X Liu, A Djumaev, D Wu, M Shoxiddinova, X Cai. et al.. (2023a). Nano-enabled quenching of bacterial communications for the prevention of biofilm formation. Angewandte Chemie International Edition, 62: e202305485 https://doi.org/10.1002/anie.202305485
40
X Gao, Y Liu, Y Li, B Jin, P Jiang, X Chen, C Wei, J Sheng, Y N Liu, J Li. et al.. (2023b). Piezoelectric nanozyme for dual-driven catalytic eradication of bacterial biofilms. ACS Applied Materials & Interfaces, 15(11): 14690–14703 https://doi.org/10.1021/acsami.2c21901
41
S Ghosh, P Roy, N Karmodak, E D Jemmis, G Mugesh. (2018). Nanoisozymes: crystal-facet-dependent enzyme-mimetic activity of V2O5 nanomaterials. Angewandte Chemie International Edition, 57(17): 4510–4515 https://doi.org/10.1002/anie.201800681
42
J J Green, J H Elisseeff. (2016). Mimicking biological functionality with polymers for biomedical applications. Nature, 540(7633): 386–394 https://doi.org/10.1038/nature21005
43
W Guo, Y Wang, K Zhang, X Dai, Z Qiao, Z Liu, B Yu, N Zhao, F J Xu. (2023). Near-infrared light-propelled MOF@Au nanomotors for enhanced penetration and sonodynamic therapy of bacterial biofilms. Chemistry of Materials, 35(17): 6853–6864 https://doi.org/10.1021/acs.chemmater.3c01140
44
A Gupta, R Das, J M Makabenta, A Gupta, X Zhang, T Jeon, R Huang, Y Liu, S Gopalakrishnan, R C Milán. et al.. (2021). Erythrocyte-mediated delivery of bioorthogonal nanozymes for selective targeting of bacterial infections. Materials Horizons, 8(12): 3424–3431 https://doi.org/10.1039/D1MH01408K
45
A Gupta, R Das, G Yesilbag Tonga, T Mizuhara, V M Rotello. (2018). Charge-switchable nanozymes for bioorthogonal imaging of biofilm-associated infections. ACS Nano, 12(1): 89–94 https://doi.org/10.1021/acsnano.7b07496
46
K Habiba, D P Bracho-Rincon, J A Gonzalez-Feliciano, J C Villalobos-Santos, V I Makarov, D Ortiz, J A Avalos, C I Gonzalez, B R Weiner, G Morell. (2015). Synergistic antibacterial activity of PEGylated silver–graphene quantum dots nanocomposites. Applied Materials Today, 1(2): 80–87 https://doi.org/10.1016/j.apmt.2015.10.001
47
K Herget, P Hubach, S Pusch, P Deglmann, H Götz, T E Gorelik, I Y A Gural’skiy, F Pfitzner, T Link, S Schenk. et al.. (2017). Haloperoxidase mimicry by CeO2−x nanorods combats biofouling. Advanced Materials, 29(4): 1603823 https://doi.org/10.1002/adma.201603823
48
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
49
J Hou, Y Xianyu. (2023). Tailoring the surface and composition of nanozymes for enhanced bacterial binding and antibacterial activity. Small, 19(42): 2302640 https://doi.org/10.1002/smll.202302640
50
D Hu, Y Deng, F Jia, Q Jin, J Ji. (2020). Surface charge switchable supramolecular nanocarriers for nitric oxide synergistic photodynamic eradication of biofilms. ACS Nano, 14(1): 347–359 https://doi.org/10.1021/acsnano.9b05493
51
H Hu, X Kang, Z Shan, X Yang, W Bing, L Wu, H Ge, H Ji. (2022). A DNase-mimetic artificial enzyme for the eradication of drug-resistant bacterial biofilm infections. Nanoscale, 14(7): 2676–2685 https://doi.org/10.1039/D1NR07629A
52
M Hu, K Korschelt, M Viel, N Wiesmann, M Kappl, J Brieger, K Landfester, H Therien-Aubin, W Tremel. (2018). Nanozymes in nanofibrous mats with haloperoxidase-like activity to combat biofouling. ACS Applied Materials & Interfaces, 10(51): 44722–44730 https://doi.org/10.1021/acsami.8b16307
R Huang, C H Li, R Cao-Milán, L D He, J M Makabenta, X Zhang, E Yu, V M Rotello. (2020). Polymer-based bioorthogonal nanocatalysts for the treatment of bacterial biofilms. Journal of the American Chemical Society, 142(24): 10723–10729 https://doi.org/10.1021/jacs.0c01758
55
T Huang, Z Yu, B Yuan, L Jiang, Y Liu, X Sun, P Liu, W Jiang, J Tang. (2022). Synergy of light-controlled Pd nanozymes with NO therapy for biofilm elimination and diabetic wound treatment acceleration. Materials Today. Chemistry, 24: 100831 https://doi.org/10.1016/j.mtchem.2022.100831
56
Y Huang, J Ren, X Qu. (2019b). Nanozymes: classification, catalytic mechanisms, activity regulation, and applications. Chemical Reviews, 119(6): 4357–4412 https://doi.org/10.1021/acs.chemrev.8b00672
57
O Jegel, F Pfitzner, A Gazanis, J Oberländer, E Pütz, M Lange, Der Au M Von, B Meermann, V Mailänder, A Klasen. et al.. (2022). Transparent polycarbonate coated with CeO2 nanozymes repel Pseudomonas aeruginosa PA14 biofilms. Nanoscale, 14(1): 86–98 https://doi.org/10.1039/D1NR03320D
58
H Ji, H Hu, Q Tang, X Kang, X Liu, L Zhao, R Jing, M Wu, G Li, X Zhou. et al.. (2022). Precisely controlled and deeply penetrated micro-nano hybrid multifunctional motors with enhanced antibacterial activity against refractory biofilm infections. Journal of Hazardous Materials, 436: 129210 https://doi.org/10.1016/j.jhazmat.2022.129210
59
B Jiang, D Duan, L Gao, M Zhou, K Fan, Y Tang, J Xi, Y Bi, Z Tong, G F Gao. et al.. (2018). Standardized assays for determining the catalytic activity and kinetics of peroxidase-like nanozymes. Nature Protocols, 13(7): 1506–1520 https://doi.org/10.1038/s41596-018-0001-1
60
L Jiao, H Yan, Y Wu, W Gu, C Zhu, D Du, Y Lin. (2020). When nanozymes meet single-atom catalysis. Angewandte Chemie International Edition, 59(7): 2565–2576 https://doi.org/10.1002/anie.201905645
61
L Jin, F Cao, Y Gao, C Zhang, Z Qian, J Zhang, Z Mao. (2023). Microenvironment-activated nanozyme-armed bacteriophages efficiently combat bacterial infection. Advanced Materials, 35(30): 2301349 https://doi.org/10.1002/adma.202301349
62
X Jin, J Shan, J Zhao, T Wang, W Zhang, S Yang, H Qian, L Cheng, X L Chen, X Wang. (2024). Bimetallic oxide Cu–Fe3O4 nanoclusters with multiple enzymatic activities for wound infection treatment and wound healing. Acta Biomaterialia, 173: 403–419 https://doi.org/10.1016/j.actbio.2023.10.028
63
Y Jin, B Zhao, W Guo, Y Li, J Min, W Miao. (2022). Penetration and photodynamic ablation of drug-resistant biofilm by cationic iron oxide nanoparticles. Journal of Controlled Release, 348: 911–923 https://doi.org/10.1016/j.jconrel.2022.06.038
64
L R Johnson. (2008). Microcolony and biofilm formation as a survival strategy for bacteria. Journal of Theoretical Biology, 251(1): 24–34 https://doi.org/10.1016/j.jtbi.2007.10.039
65
T Kilic, E B Bali. (2023). Biofilm control strategies in the light of biofilm-forming microorganisms. World Journal of Microbiology & Biotechnology, 39(5): 131 https://doi.org/10.1007/s11274-023-03584-6
66
J H Kim, D C Choi, K M Yeon, S R Kim, C H Lee. (2011). Enzyme-immobilized nanofiltration membrane to mitigate biofouling based on quorum quenching. Environmental Science & Technology, 45(4): 1601–1607 https://doi.org/10.1021/es103483j
67
U Kim, J H Kim, S W Oh. (2022). Review of multi-species biofilm formation from foodborne pathogens: multi-species biofilms and removal methodology. Critical Reviews in Food Science and Nutrition, 62(21): 5783–5793 https://doi.org/10.1080/10408398.2021.1892585
68
R Kolter, E P Greenberg. (2006). The superficial life of microbes. Nature, 441(7091): 300–302 https://doi.org/10.1038/441300a
69
B Lee, K M Yeon, J Shim, S R Kim, C H Lee, J Lee, J Kim. (2014). Effective antifouling using quorum-quenching acylase stabilized in magnetically-separable mesoporous silica. Biomacromolecules, 15(4): 1153–1159 https://doi.org/10.1021/bm401595q
70
S Li, Z Zhou, Z Tie, B Wang, M Ye, L Du, R Cui, W Liu, C Wan, Q Liu. et al.. (2022a). Data-informed discovery of hydrolytic nanozymes. Nature Communications, 13(1): 827 https://doi.org/10.1038/s41467-022-28344-2
71
W Li, Y Tian, J Chen, X Wang, Y Zhou, N Shi. (2022b). Synergistic effects of sodium hypochlorite disinfection and iron-oxidizing bacteria on early corrosion in cast iron pipes. Frontiers of Environmental Science & Engineering, 16(6): 72 https://doi.org/10.1007/s11783-021-1506-3
72
X Li, L Wang, D Du, L Ni, J Pan, X Niu. (2019a). Emerging applications of nanozymes in environmental analysis: Opportunities and trends. Trends in Analytical Chemistry, 120: 115653 https://doi.org/10.1016/j.trac.2019.115653
73
X Li, X Wang, D J Lee, W M Yan. (2019b). Highly heterogeneous interior structure of biofilm wastewater for enhanced pollutant removals. Bioresource Technology, 291: 121919 https://doi.org/10.1016/j.biortech.2019.121919
74
Y Li, R Zhang, X Yan, K Fan. (2023). Machine learning facilitating the rational design of nanozymes. Journal of Materials Chemistry. B, 11(28): 6466–6477 https://doi.org/10.1039/D3TB00842H
75
P Ling, P Yang, X Gao, X Sun, F Gao. (2022). ROS generation strategy based on biomimetic nanosheets by self-assembly of nanozymes. Journal of Materials Chemistry. B, 10(46): 9607–9612 https://doi.org/10.1039/D2TB01639G
D Liu, Y Xi, S Yu, K Yang, F Zhang, Y Yang, T Wang, S He, Y Zhu, Z Fan. et al.. (2023a). A polypeptide coating for preventing biofilm on implants by inhibiting antibiotic resistance genes. Biomaterials, 293: 121957 https://doi.org/10.1016/j.biomaterials.2022.121957
78
G Liu, Y Zhang, X Liu, F Hammes, W T Liu, G Medema, P Wessels, W Van Der Meer. (2020). 360-degree distribution of biofilm quantity and community in an operational unchlorinated drinking water distribution pipe. Environmental Science & Technology, 54(9): 5619–5628 https://doi.org/10.1021/acs.est.9b06603
79
H Liu, D Zhao, C Zhang, M Li, S Zhang, X Xiao. (2023b). One-step preparation of MnO2 nanozyme by PS-CDs for antibacterial, inhibition of S. aureus biofilm growth and colorimetric assay of tiopronin. Journal of Industrial and Engineering Chemistry, 125: 127–135 https://doi.org/10.1016/j.jiec.2023.05.021
80
P Liu, Y Wu, B Mehrjou, K Tang, G Wang, P K Chu. (2022). Versatile phenol-incorporated nanoframes for in situ antibacterial activity based on oxidative and physical damages. Advanced Functional Materials, 32(17): 2110635 https://doi.org/10.1002/adfm.202110635
81
Q Liu, A Kuzuya, Z G Wang. (2023c). Supramolecular enzyme-mimicking catalysts self-assembled from peptides. iScience, 26(1): 105831 https://doi.org/10.1016/j.isci.2022.105831
82
W Liu, S Jacquiod, A Brejnrod, J Russel, M Burmølle, S J Sørensen. (2019a). Deciphering links between bacterial interactions and spatial organization in multispecies biofilms. ISME Journal, 13(12): 3054–3066 https://doi.org/10.1038/s41396-019-0494-9
83
Y Liu, H J Busscher, B Zhao, Y Li, Z Zhang, H C Van Der Mei, Y Ren, L Shi. (2016). Surface-adaptive, antimicrobially loaded, micellar nanocarriers with enhanced penetration and killing efficiency in Staphylococcal biofilms. ACS Nano, 10(4): 4779–4789 https://doi.org/10.1021/acsnano.6b01370
84
Y Liu, L Shi, L Su, H C Van Der Mei, P C Jutte, Y Ren, H J Busscher. (2019b). Nanotechnology-based antimicrobials and delivery systems for biofilm-infection control. Chemical Society Reviews, 48(2): 428–446 https://doi.org/10.1039/C7CS00807D
85
Z Liu, F Wang, J Ren, X Qu. (2019c). A series of MOF/Ce-based nanozymes with dual enzyme-like activity disrupting biofilms and hindering recolonization of bacteria. Biomaterials, 208: 21–31 https://doi.org/10.1016/j.biomaterials.2019.04.007
86
M Livieri, F Mancin, G Saielli, J Chin, U Tonellato. (2007). Mimicking enzymes: cooperation between organic functional groups and metal ions in the cleavage of phosphate diesters. Chemistry, 13(8): 2246–2256 https://doi.org/10.1002/chem.200600672
87
M B Lohse, M Gulati, A D Johnson, C J Nobile. (2018). Development and regulation of single- and multi-species Candida albicans biofilms. Nature Reviews Microbiology, 16(1): 19–31 https://doi.org/10.1038/nrmicro.2017.107
88
C Lu, M Zandieh, J Zheng, J Liu. (2023). Comparison of the peroxidase activities of iron oxide nanozyme with DNAzyme and horseradish peroxidase. Nanoscale, 15(18): 8189–8196 https://doi.org/10.1039/D3NR01098H
89
J Lu, X Hu, L Ren. (2022). Biofilm control strategies in food industry: inhibition and utilization. Trends in Food Science & Technology, 123: 103–113 https://doi.org/10.1016/j.tifs.2022.03.007
90
Q Luo, J Li, W Wang, Y Li, Y Li, X Huo, J Li, N Wang. (2022). Transition metal engineering of molybdenum disulfide nanozyme for biomimicking anti-biofouling in seawater. ACS Applied Materials & Interfaces, 14(12): 14218–14225 https://doi.org/10.1021/acsami.2c00172
91
M Ma, R Wang, L Xu, J Du, M Xu, S Liu. (2021). Emerging investigator series: enhanced peroxidase-like activity and improved antibacterial performance of palladium nanosheets by an alginate-corona. Environmental Science: Nano, 8(12): 3511–3523 https://doi.org/10.1039/D1EN00485A
92
K U Mahto, M Vandana, D P Priyadarshanee, S Samantaray. (2022). Bacterial biofilm and extracellular polymeric substances in the treatment of environmental pollutants: beyond the protective role in survivability. Journal of Cleaner Production, 379: 134759 https://doi.org/10.1016/j.jclepro.2022.134759
93
J Mathieu, P Yu, P Zuo, M L B Da Silva, P J J Alvarez. (2019). Going viral: emerging opportunities for phage-based bacterial control in water treatment and reuse. Accounts of Chemical Research, 52(4): 849–857 https://doi.org/10.1021/acs.accounts.8b00576
94
R R Matias, A M G Sepúlveda, B N Batista, Lucena J M V M De, P M Albuquerque. (2021). Degradation of Staphylococcus aureus biofilm using hydrolytic enzymes produced by amazonian endophytic fungi. Applied Biochemistry and Biotechnology, 193(7): 2145–2161 https://doi.org/10.1007/s12010-021-03542-8
L Mei, S Zhu, Y Liu, W Yin, Z Gu, Y Zhao. (2021). An overview of the use of nanozymes in antibacterial applications. Chemical Engineering Journal, 418: 129431 https://doi.org/10.1016/j.cej.2021.129431
97
R J Melander, A K Basak, C Melander. (2020). Natural products as inspiration for the development of bacterial antibiofilm agents. Natural Product Reports, 37(11): 1454–1477 https://doi.org/10.1039/D0NP00022A
98
K E Murray, E I Manitou-Alvarez, E C Inniss, F G Healy, A A Bodour. (2015). Assessment of oxidative and UV-C treatments for inactivating bacterial biofilms from groundwater wells. Frontiers of Environmental Science & Engineering, 9(1): 39–49 https://doi.org/10.1007/s11783-014-0699-0
M D Nothling, Z Xiao, A Bhaskaran, M T Blyth, C W Bennett, M L Coote, L A Connal. (2019). Synthetic catalysts inspired by hydrolytic enzymes. ACS Catalysis, 9(1): 168–187 https://doi.org/10.1021/acscatal.8b03326
101
T Pan, H Chen, X Gao, Z Wu, Y Ye, Y Shen. (2022). Engineering efficient artificial nanozyme based on chitosan grafted Fe-doped-carbon dots for bacteria biofilm eradication. Journal of Hazardous Materials, 435: 128996 https://doi.org/10.1016/j.jhazmat.2022.128996
102
Y Pechaud, N Derlon, I Queinnec, Y Bessiere, E Paul. (2024). Modelling biofilm development: The importance of considering the link between EPS distribution, detachment mechanisms and physical properties. Water Research, 250: 120985 https://doi.org/10.1016/j.watres.2023.120985
103
T O Peulen, K J Wilkinson. (2011). Diffusion of nanoparticles in a biofilm. Environmental Science & Technology, 45(8): 3367–3373 https://doi.org/10.1021/es103450g
E Pütz, A Gazanis, N G Keltsch, O Jegel, F Pfitzner, R Heermann, T A Ternes, W Tremel. (2022). Communication breakdown: into the molecular mechanism of biofilm inhibition by CeO2 nanocrystal enzyme mimics and how it can be exploited. ACS Nano, 16(10): 16091–16108 https://doi.org/10.1021/acsnano.2c04377
107
R Qi, Y Cui, J Liu, X Wang, H Yuan. (2023). Recent advances of composite nanomaterials for antibiofilm application. Nanomaterials, 13(19): 2725 https://doi.org/10.3390/nano13192725
108
Y Qi, J Li, R Liang, S Ji, J Li, M Liu. (2017). Chemical additives affect sulfate reducing bacteria biofilm properties adsorbed on stainless steel 316L surface in circulating cooling water system. Frontiers of Environmental Science & Engineering, 11(2): 14 https://doi.org/10.1007/s11783-017-0917-7
109
P S Rajesh, V R Rai. (2015). Purification and antibiofilm activity of AHL-lactonase from endophytic Enterobacter aerogenes VT66. International Journal of Biological Macromolecules, 81: 1046–1052 https://doi.org/10.1016/j.ijbiomac.2015.09.048
K Sauer, P Stoodley, D M Goeres, L Hall-Stoodley, M Burmolle, P S Stewart, T Bjarnsholt. (2022). The biofilm life cycle: expanding the conceptual model of biofilm formation. Nature Reviews Microbiology, 20(10): 608–620 https://doi.org/10.1038/s41579-022-00767-0
Y Shen, C Nie, T Pan, W Zhang, H Yang, Y Ye, X Wang. (2023). A multifunctional cascade nanoreactor based on Fe-driven carbon nanozymes for synergistic photothermal/chemodynamic antibacterial therapy. Acta Biomaterialia, 168: 580–592 https://doi.org/10.1016/j.actbio.2023.07.006
114
X Si, X Quan. (2017). Prevention of multi-species wastewater biofilm formation using vanillin and EPS disruptors through non-microbicidal mechanisms. International Biodeterioration & Biodegradation, 116: 211–218 https://doi.org/10.1016/j.ibiod.2016.11.009
115
S Silva, M Negri, M Henriques, R Oliveira, D W Williams, J Azeredo. (2011). Adherence and biofilm formation of non-Candida albicans Candida species. Trends in Microbiology, 19(5): 241–247 https://doi.org/10.1016/j.tim.2011.02.003
116
S V Somerville, Q Li, J Wordsworth, S Jamali, M R Eskandarian, R D Tilley, J J Gooding. (2024). Approaches to improving the selectivity of nanozymes. Advanced Materials, 36: 2211288 https://doi.org/10.1002/adma.202211288
H Sun, A Zhao, N Gao, K Li, J Ren, X Qu. (2015). Deciphering a nanocarbon-based artificial peroxidase: chemical identification of the catalytically active and substrate-binding sites on graphene quantum dots. Angewandte Chemie International Edition, 54(24): 7176–7180 https://doi.org/10.1002/anie.201500626
119
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
120
Y Tao, E Ju, J Ren, X Qu. (2015). Bifunctionalized mesoporous silica-supported gold nanoparticles: intrinsic oxidase and peroxidase catalytic activities for antibacterial applications. Advanced Materials, 27(6): 1097–1104 https://doi.org/10.1002/adma.201405105
121
E Teirlinck, R Xiong, T Brans, K Forier, J Fraire, Acker H Van, N Matthijs, Rycke R De, Smedt S C De, T Coenye. et al.. (2018). Laser-induced vapour nanobubbles improve drug diffusion and efficiency in bacterial biofilms. Nature Communications, 9(1): 4518 https://doi.org/10.1038/s41467-018-06884-w
122
R Tian, Y Li, J Xu, C Hou, Q Luo, J Liu. (2022). Recent development in the design of artificial enzymes through molecular imprinting technology. Journal of Materials Chemistry. B, 10(35): 6590–6606 https://doi.org/10.1039/D2TB00276K
123
P Urban, G Truan, D Pompon. (2015). Access channels to the buried active site control substrate specificity in CYP1A P450 enzymes. Biochimica et Biophysica Acta, 1850(4): 696–707 https://doi.org/10.1016/j.bbagen.2014.12.015
124
A Vishwakarma, F Dang, A Ferrell, H A Barton, A Joy. (2021). Peptidomimetic polyurethanes inhibit bacterial biofilm formation and disrupt surface established biofilms. Journal of the American Chemical Society, 143(25): 9440–9449 https://doi.org/10.1021/jacs.1c02324
125
V Vishwakarma. (2020). Impact of environmental biofilms: Industrial components and its remediation. Journal of Basic Microbiology, 60(3): 198–206 https://doi.org/10.1002/jobm.201900569
126
A Wang, P J Weldrick, L A Madden, V N Paunov. (2021a). Biofilm-infected human clusteroid three-dimensional coculture platform to replace animal models in testing antimicrobial nanotechnologies. ACS Applied Materials & Interfaces, 13(19): 22182–22194 https://doi.org/10.1021/acsami.1c02679
127
F Wang, J Tan, S Zhang, Y Zhou, D He, L Deng. (2021b). Efficient eradication of bacterial biofilms with highly specific graphene-based nanocomposite sheets. ACS Biomaterials Science & Engineering, 7(11): 5118–5128 https://doi.org/10.1021/acsbiomaterials.1c00575
128
H Wang, C Hu, X Hu, M Yang, J Qu. (2012). Effects of disinfectant and biofilm on the corrosion of cast iron pipes in a reclaimed water distribution system. Water Research, 46(4): 1070–1078 https://doi.org/10.1016/j.watres.2011.12.001
L Wang, F Gao, A Wang, X Chen, H Li, X Zhang, H Zheng, R Ji, B Li, X Yu. et al.. (2020a). Defect-rich adhesive molybdenum disulfide/rGO vertical heterostructures with enhanced nanozyme activity for smart bacterial killing application. Advanced Materials, 32(48): 2005423 https://doi.org/10.1002/adma.202005423
131
W Wang, Q Luo, J Li, L Li, Y Li, X Huo, X Du, Z Li, N Wang. (2022a). Photothermal-amplified single atom nanozyme for biofouling control in seawater. Advanced Functional Materials, 32(36): 2205461 https://doi.org/10.1002/adfm.202205461
132
W Wang, Q Luo, J Li, Y Li, R Wu, Y Li, X Huo, N Wang. (2022b). Single-atom tungsten engineering of MOFs with biomimetic antibiofilm activity toward robust uranium extraction from seawater. Chemical Engineering Journal, 431: 133483 https://doi.org/10.1016/j.cej.2021.133483
133
W Wang, Q Luo, L Li, S Chen, Y Wang, X Du, N Wang. (2023). Hybrid nickel-molybdenum bimetallic sulfide nanozymes for antibacterial and antibiofouling applications. Advanced Composites and Hybrid Materials, 6(4): 139 https://doi.org/10.1007/s42114-023-00718-0
134
Z Wang, K Dong, Z Liu, Y Zhang, Z Chen, H Sun, J Ren, X Qu. (2017). Activation of biologically relevant levels of reactive oxygen species by Au/g-C3N4 hybrid nanozyme for bacteria killing and wound disinfection. Biomaterials, 113: 145–157 https://doi.org/10.1016/j.biomaterials.2016.10.041
135
Z Wang, R Zhang, X Yan, K Fan. (2020b). Structure and activity of nanozymes: Inspirations for de novo design of nanozymes. Materials Today, 41: 81–119 https://doi.org/10.1016/j.mattod.2020.08.020
136
Z Wang, Y Zhang, S Chen, Y Qu, M Tang, W Wang, W Li, L Gu. (2024). Multifunctional CeO2 nanozymes for mitigating high-glucose induced senescence and enhancing bone regeneration in type 2 diabetes mellitus. Chemical Engineering Journal, 485: 149842 https://doi.org/10.1016/j.cej.2024.149842
H Wei, L Gao, K Fan, J Liu, J He, X Qu, S Dong, E Wang, X Yan. (2021). Nanozymes: a clear definition with fuzzy edges. Nano Today, 40: 101269 https://doi.org/10.1016/j.nantod.2021.101269
139
J N Wei, D Duvenaud, A Aspuru-Guzik. (2016). Neural networks for the prediction of organic chemistry reactions. ACS Central Science, 2(10): 725–732 https://doi.org/10.1021/acscentsci.6b00219
140
Y Wei, J Wu, Y Wu, H Liu, F Meng, Q Liu, A C Midgley, X Zhang, T Qi, H Kang. et al.. (2022). Prediction and design of nanozymes using explainable machine learning. Advanced Materials, 34(27): 2201736 https://doi.org/10.1002/adma.202201736
141
B Wu, E F Haney, N Akhoundsadegh, D Pletzer, M J Trimble, A E Adriaans, P H Nibbering, R E W Hancock. (2021). Human organoid biofilm model for assessing antibiofilm activity of novel agents. NPJ Biofilms and Microbiomes, 7(1): 8 https://doi.org/10.1038/s41522-020-00182-4
142
H Wu, M Wei, S Hu, P Cheng, S Shi, F Xia, L Xu, L Yin, G Liang, F Li. et al.. (2023). A photomodulable bacteriophage-spike nanozyme enables dually enhanced biofilm penetration and bacterial capture for photothermal-boosted catalytic therapy of mrsa infections. Advanced Science, 10(24): 2301694 https://doi.org/10.1002/advs.202301694
143
J Wu, S Li, H Wei. (2018). Multifunctional nanozymes: enzyme-like catalytic activity combined with magnetism and surface plasmon resonance. Nanoscale Horizons, 3(4): 367–382 https://doi.org/10.1039/C8NH00070K
144
J Wu, X Wang, Q Wang, Z Lou, S Li, Y Zhu, L Qin, H Wei. (2019a). Nanomaterials with enzyme-like characteristics (nanozymes): next-generation artificial enzymes (II). Chemical Society Reviews, 48(4): 1004–1076 https://doi.org/10.1039/C8CS00457A
145
Y K Wu, N C Cheng, C M Cheng. (2019b). Biofilms in chronic wounds: pathogenesis and diagnosis. Trends in Biotechnology, 37(5): 505–517 https://doi.org/10.1016/j.tibtech.2018.10.011
146
Z Xi, K Wei, Q Wang, M J Kim, S Sun, V Fung, X Xia. (2021). Nickel–platinum nanoparticles as peroxidase mimics with a record high catalytic efficiency. Journal of the American Chemical Society, 143(7): 2660–2664 https://doi.org/10.1021/jacs.0c12605
147
Y Xiao, H Zou, J Li, T Song, W Lv, W Wang, Z Wang, S Tao. (2022). Impact of quorum sensing signaling molecules in gram-negative bacteria on host cells: current understanding and future perspectives. Gut Microbes, 14(1): 2039048 https://doi.org/10.1080/19490976.2022.2039048
D Xu, L Wu, H Yao, L Zhao. (2022). Catalase-like nanozymes: classification, catalytic mechanisms, and their applications. Small, 18(37): 2203400 https://doi.org/10.1002/smll.202203400
150
Y Xu, Y Luo, Z Weng, H Xu, W Zhang, Q Li, H Liu, L Liu, Y Wang, X Liu. et al.. (2023b). Microenvironment-responsive metal-phenolic nanozyme release platform with antibacterial, ROS scavenging, and osteogenesis for periodontitis. ACS Nano, 17(19): 18732–18746 https://doi.org/10.1021/acsnano.3c01940
151
X Yan, J Sun, Y Wang, Z Zhang, C Zhang, W Li, J Xu, X Dai, B J Ni. (2023). Low-rate ferrate dosing damages the microbial biofilm structure through humic substances destruction and facilitates the sewer biofilm control. Water Research, 235: 119834 https://doi.org/10.1016/j.watres.2023.119834
152
W Yang, X Yang, L Zhu, H Chu, X Li, W Xu. (2021). Nanozymes: activity origin, catalytic mechanism, and biological application. Coordination Chemistry Reviews, 448: 214170 https://doi.org/10.1016/j.ccr.2021.214170
153
Y R Yang, X D Wang, J S Chang, D J Lee. (2022). Homogeneously and heterogeneously structured biofilm models for wastewater treatment. Bioresource Technology, 362: 127763 https://doi.org/10.1016/j.biortech.2022.127763
154
Z Ye, Y Fan, T Zhu, D Cao, X Hu, S Xiang, J Li, Z Guo, X Chen, K Tan. et al.. (2022). Preparation of two-dimensional Pd@Ir nanosheets and application in bacterial infection treatment by the generation of reactive oxygen species. ACS Applied Materials & Interfaces, 14(20): 23194–23205 https://doi.org/10.1021/acsami.2c03952
155
W Yin, S Xu, Y Wang, Y Zhang, S H Chou, M Y Galperin, J He. (2021). Ways to control harmful biofilms: prevention, inhibition, and eradication. Critical Reviews in Microbiology, 47(1): 57–78 https://doi.org/10.1080/1040841X.2020.1842325
156
J P Yuan, Z J Guan, H Y Lin, B Yan, K K Liu, H C Zhou, Y Fang. (2023). Modeling the enzyme specificity by molecular cages through regulating reactive oxygen species evolution. Angewandte Chemie International Edition, 62(31): e202303896 https://doi.org/10.1002/anie.202303896
157
A F Zahrt, J J Henle, B T Rose, Y Wang, W T Darrow, S E Denmark. (2019). Prediction of higher-selectivity catalysts by computer-driven workflow and machine learning. Science, 363(6424): eaau5631 https://doi.org/10.1126/science.aau5631
158
P Zhang, Y P Chen, J H Qiu, Y Z Dai, B Feng. (2019). Imaging the microprocesses in biofilm matrices. Trends in Biotechnology, 37(2): 214–226 https://doi.org/10.1016/j.tibtech.2018.07.006
159
R Zhang, B Xue, Y Tao, H Zhao, Z Zhang, X Wang, X Zhou, B Jiang, Z Yang, X Yan. et al.. (2022). Edge-site engineering of defective Fe-N4 nanozymes with boosted catalase-like performance for retinal vasculopathies. Advanced Materials, 34(39): 2205324 https://doi.org/10.1002/adma.202205324
160
X Zhao, X Liu, X Xu, Y V Fu. (2017). Microbe social skill: the cell-to-cell communication between microorganisms. Science Bulletin, 62(7): 516–524 https://doi.org/10.1016/j.scib.2017.02.010
161
C Zhou, Q Wang, J Jiang, L Gao. (2022a). Nanozybiotics: nanozyme-based antibacterials against bacterial resistance. Antibiotics, 11(3): 390 https://doi.org/10.3390/antibiotics11030390
162
Z Zhou, W He, H Chao, H Wang, P Su, J Song, Y Yang. (2022b). Insertion of hemin into metal–organic frameworks: mimicking natural peroxidase microenvironment for the rapid ultrasensitive detection of uranium. Analytical Chemistry, 94(18): 6833–6841 https://doi.org/10.1021/acs.analchem.2c00661
163
G Zhu, P Zheng, M Wang, W Chen, C Li. (2022). A novel CuCoS nanozyme for synergistic photothermal and chemodynamic therapy of tumors. Inorganic Chemistry Frontiers, 9(5): 1006–1015 https://doi.org/10.1039/D1QI01563J
164
Z Zhu, L Wang, Q Li. (2018). A bioactive poly (vinylidene fluoride)/graphene oxide@acylase nanohybrid membrane: Enhanced anti-biofouling based on quorum quenching. Journal of Membrane Science, 547: 110–122 https://doi.org/10.1016/j.memsci.2017.10.041
165
J Zhuang, A C Midgley, Y Wei, Q Liu, D Kong, X Huang. (2024). Machine-learning-assisted nanozyme design: lessons from materials and engineered enzymes. Advanced Materials, 36(10): 2210848 https://doi.org/10.1002/adma.202210848