Bacterial biofilms are complex multicellular communities that adhere firmly to solid surfaces. They are widely recognized as major threats to human health, contributing to issues such as persistent infections on medical implants and severe contamination in drinking water systems. As a potential treatment for biofilms, this work proposes two strategies: (i) light-driven ZnFe2O4 (ZFO)/Pt microrobots for photodegradation of biofilms and (ii) magnetically driven ZFO microrobots for mechanical removal of biofilms from surfaces. Magnetically driven ZFO microrobots were realized by synthesizing ZFO microspheres through a low-cost and large-scale hydrothermal synthesis, followed by a calcination process. Then, a Pt layer was deposited on the surface of the ZFO microspheres to break their symmetry, resulting in self-propelled light-driven Janus ZFO/Pt microrobots. Light-driven ZFO/Pt microrobots exhibited active locomotion under UV light irradiation and controllable motion in terms of "stop and go" features. Magnetically driven ZFO microrobots were capable of maneuvering precisely when subjected to an external rotating magnetic field. These microrobots could eliminate Gram-negative Escherichia coli (E. coli) biofilms through photogenerated reactive oxygen species (ROS)-related antibacterial properties in combination with their light-powered active locomotion, accelerating the mass transfer to remove biofilms more effectively in water. Moreover, the actuation of magnetically driven ZFO microrobots allowed for the physical disruption of biofilms, which represents a reliable alternative to photocatalysis for the removal of strongly anchored biofilms in confined spaces. With their versatile characteristics, the envisioned microrobots highlight a significant potential for biofilm removal with high efficacy in both open and confined spaces, such as the pipelines of industrial plants.

Advanced Nanorobots and Multiscale Robotics Laboratory Faculty of Electrical Engineering and Computer Science VSB─Technical University of Ostrava 17 Listopadu 2172 15 70800 Ostrava Czech Republic

Department of Medical Research China Medical University Hospital China Medical University No 91 Hsueh Shih Road TW 40402 Taichung Taiwan

Future Energy and Innovation Laboratory Central European Institute of Technology Brno University of Technology Purkynova 123 61200 Brno Czech Republic

Zobrazit více v PubMed

Blair K. M.; Turner L.; Winkelman J. T.; Berg H. C.; Kearns D. B. A Molecular Clutch Disables Flagella in the Bacillus Subtilis Biofilm. Science 2008, 320, 1636–1638. 10.1126/science.1157877. PubMed DOI

Mah T. F.; Pitts B.; Pellock B.; Walker G. C.; Stewart P. S.; O’Toole G. A. A Genetic Basis for Pseudomonas Aeruginosa Biofilm Antibiotic Resistance. Nature 2003, 426, 306–310. 10.1038/nature02122. PubMed DOI

Arnaouteli S.; Bamford N. C.; Stanley-Wall N. R.; Kovács Á. T. Bacillus Subtilis Biofilm Formation and Social Interactions. Nat. Rev. Microbiol. 2021, 19, 600–614. 10.1038/s41579-021-00540-9. PubMed DOI

Liu Y.; Shi L.; Su L.; Van der Mei H. C.; Jutte P. C.; Ren Y.; Busscher H. J. Nanotechnology-Based Antimicrobials and Delivery Systems for Biofilm-Infection Control. Chem. Soc. Rev. 2019, 48, 428–446. 10.1039/C7CS00807D. PubMed DOI

Peterson B. W.; He Y.; Ren Y.; Zerdoum A.; Libera M. R.; Sharma P. K.; van Winkelhoff A. J.; Neut D.; Stoodley P.; van der Mei H. C.; Busscher H. J. Viscoelasticity of Biofilms and Their Recalcitrance to Mechanical and Chemical Challenges. FEMS Microbiol. Rev. 2015, 39, 234–245. 10.1093/femsre/fuu008. PubMed DOI PMC

Dieltjens L.; Appermans K.; Lissens M.; Lories B.; Kim W.; Van der Eycken E. V.; Foster K. R.; Steenackers H. P. Inhibiting Bacterial Cooperation Is an Evolutionarily Robust Anti-Biofilm Strategy. Nat. Commun. 2020, 11, 10710.1038/s41467-019-13660-x. PubMed DOI PMC

Chauhan A.; Ghigo J. M.; Beloin C. Study of in Vivo Catheter Biofilm Infections Using Pediatric Central Venous Catheter Implanted in Rat. Nat. Protoc. 2016, 11, 525–541. 10.1038/nprot.2016.033. PubMed DOI

Arciola C. R.; Campoccia D.; Montanaro L. Implant Infections: Adhesion, Biofilm Formation and Immune Evasion. Nat. Rev. Microbiol. 2018, 16, 397–409. 10.1038/s41579-018-0019-y. PubMed DOI

Sun M.; Chan K. F.; Zhang Z.; Wang L.; Wang Q.; Yang S.; Chan S. M.; Chiu P. W. Y.; Sung J. J. Y.; Zhang L. Magnetic Microswarm and Fluoroscopy-Guided Platform for Biofilm Eradication in Biliary Stents. Adv. Mater. 2022, 34, 220188810.1002/adma.202201888. PubMed DOI

Ussia M.; Urso M.; Dolezelikova K.; Michalkova H.; Adam V.; Pumera M. Active Light-Powered Antibiofilm ZnO Micromotors with Chemically Programmable Properties. Adv. Funct. Mater. 2021, 31, 210117810.1002/adfm.202101178. DOI

Chan S.; Pullerits K.; Keucken A.; Persson K. M.; Paul C. J.; Rådström P. Bacterial Release from Pipe Biofilm in a Full-Scale Drinking Water Distribution System. npj Biofilms Microbiomes 2019, 5, 910.1038/s41522-019-0082-9. PubMed DOI PMC

Farh H. M. H.; El Amine Ben Seghier M.; Taiwo R.; Zayed T. Analysis and Ranking of Corrosion Causes for Water Pipelines: A Critical Review. npj Clean Water 2023, 6, 6510.1038/s41545-023-00275-5. DOI

Gomes I. B.; Simões M.; Simões L. C. An Overview on the Reactors to Study Drinking Water Biofilms. Water Res. 2014, 62, 63–87. 10.1016/j.watres.2014.05.039. PubMed DOI

Villa K.; Sopha H.; Zelenka J.; Motola M.; Dekanovsky L.; Beketova D. C.; Macak J. M.; Ruml T.; Pumera M. Enzyme-Photocatalyst Tandem Microrobot Powered by Urea for Escherichia coli Biofilm Eradication. Small 2022, 18, 210661210.1002/smll.202106612. PubMed DOI

Urso M.; Ussia M.; Pumera M. Smart Micro- and Nanorobots for Water Purification. Nat. Rev. Bioeng. 2023, 1, 236–251. 10.1038/s44222-023-00025-9. PubMed DOI PMC

Liu Y.; Naha P. C.; Hwang G.; Kim D.; Huang Y.; Simon-Soro A.; Jung H. I.; Ren Z.; Li Y.; Gubara S.; Alawi F.; Zero D.; Hara A. T.; Cormode D. P.; Koo H. Topical Ferumoxytol Nanoparticles Disrupt Biofilms and Prevent Tooth Decay in Vivo via Intrinsic Catalytic Activity. Nat. Commun. 2018, 9, 292010.1038/s41467-018-05342-x. PubMed DOI PMC

Chen Z.; Wang Z.; Ren J.; Qu X. Enzyme Mimicry for Combating Bacteria and Biofilms. Acc. Chem. Res. 2018, 51, 789–799. 10.1021/acs.accounts.8b00011. PubMed DOI

Benoit D. S. W.; Sims K. R.; Fraser D. Nanoparticles for Oral Biofilm Treatments. ACS Nano 2019, 13, 4869–4875. 10.1021/acsnano.9b02816. PubMed DOI PMC

Hu Y.; Ruan X.; Lv X.; Xu Y.; Wang W.; Cai Y.; Ding M.; Dong H.; Shao J.; Yang D.; Dong X. Biofilm Microenvironment-Responsive Nanoparticles for the Treatment of Bacterial Infection. Nano Today 2022, 46, 10160210.1016/j.nantod.2022.101602. DOI

Wang Z.; Klingner A.; Magdanz V.; Misra S.; Khalil I. S. M. Soft Bio-Microrobots: Toward Biomedical Applications. Adv. Intell. Syst. 2023, 6, 230009310.1002/aisy.202300093. DOI

Soto F.; Wang J.; Ahmed R.; Demirci U. Medical Micro/Nanorobots in Precision Medicine. Adv. Sci. 2020, 7, 200220310.1002/advs.202002203. PubMed DOI PMC

Zhang Z.; Wang L.; Chan T. K. F.; Chen Z.; Ip M.; Chan P. K. S.; Sung J. J. Y.; Zhang L. Micro-/Nanorobots in Antimicrobial Applications: Recent Progress, Challenges, and Opportunities. Adv. Healthcare Mater. 2022, 11, 210199110.1002/adhm.202101991. PubMed DOI

Wu R.; Zhu Y.; Cai X.; Wu S.; Xu L.; Yu T. Recent Process in Microrobots: From Propulsion to Swarming for Biomedical Applications. Micromachines 2022, 13, 147310.3390/mi13091473. PubMed DOI PMC

Zhang F.; Zhuang J.; Li Z.; Gong H.; de Ávila B. E. F.; Duan Y.; Zhang Q.; Zhou J.; Yin L.; Karshalev E.; Gao W.; Nizet V.; Fang R. H.; Zhang L.; Wang J. Nanoparticle-Modified Microrobots for in Vivo Antibiotic Delivery to Treat Acute Bacterial Pneumonia. Nat. Mater. 2022, 21, 1324–1332. 10.1038/s41563-022-01360-9. PubMed DOI PMC

Liu D.; Wang T.; Lu Y. Untethered Microrobots for Active Drug Delivery: From Rational Design to Clinical Settings. Adv. Healthcare Mater. 2022, 11, 210225310.1002/adhm.202102253. PubMed DOI

Rojas D.; Kuthanova M.; Dolezelikova K.; Pumera M. Facet Nanoarchitectonics of Visible-Light Driven Ag3PO4 Photocatalytic Micromotors: Tuning Motion for Biofilm Eradication. NPG Asia Mater. 2022, 14, 6310.1038/s41427-022-00409-0. DOI

Ussia M.; Urso M.; Kment S.; Fialova T.; Klima K.; Dolezelikova K.; Pumera M. Light-Propelled Nanorobots for Facial Titanium Implants Biofilms Removal. Small 2022, 18, 220070810.1002/smll.202200708. PubMed DOI

Guix M.; Mayorga-martinez C. C.; Merkoc A. Nano/Micromotors in (Bio) Chemical Science Applications. Chem. Rev. 2014, 114, 6285–6322. 10.1021/cr400273r. PubMed DOI

Hu D.; Li H.; Wang B.; Ye Z.; Lei W.; Jia F.; Jin Q.; Ren K. F.; Ji J. Surface-Adaptive Gold Nanoparticles with Effective Adherence and Enhanced Photothermal Ablation of Methicillin-Resistant Staphylococcus Aureus Biofilm. ACS Nano 2017, 11, 9330–9339. 10.1021/acsnano.7b04731. PubMed DOI

Villa K.; Viktorova J.; Plutnar J.; Ruml T.; Hoang L.; Pumera M. Chemical Microrobots as Self-Propelled Microbrushes against Dental Biofilm. Cell Rep. Phys. Sci. 2020, 1, 10018110.1016/j.xcrp.2020.100181. DOI

Yuan K.; Jurado-Sánchez B.; Escarpa A. Dual-Propelled Lanbiotic Based Janus Micromotors for Selective Inactivation of Bacterial Biofilms. Angew. Chem., Int. Ed. 2021, 60, 4915–4924. 10.1002/anie.202011617. PubMed DOI

Mayorga-Martinez C. C.; Zelenka J.; Klima K.; Mayorga-Burrezo P.; Hoang L.; Ruml T.; Pumera M. Swarming Magnetic Photoactive Microrobots for Dental Implant Biofilm Eradication. ACS Nano 2022, 16, 8694–8703. 10.1021/acsnano.2c02516. PubMed DOI

Dong Y.; Wang L.; Zhang Z.; Ji F.; Chan T. K. F.; Yang H.; Chan C. P. L.; Yang Z.; Chen Z.; Chang W. T.; Chan J. Y. K.; Sung J. J. Y.; Zhang L. Endoscope-Assisted Magnetic Helical Micromachine Delivery for Biofilm Eradication in Tympanostomy Tube. Sci. Adv. 2022, 8, eabq857310.1126/sciadv.abq8573. PubMed DOI PMC

Zhou H.; Mayorga-Martinez C. C.; Pané S.; Zhang L.; Pumera M. Magnetically Driven Micro and Nanorobots. Chem. Rev. 2021, 121, 4999–5041. 10.1021/acs.chemrev.0c01234. PubMed DOI PMC

Wang L.; Meng Z.; Chen Y.; Zheng Y. Engineering Magnetic Micro/Nanorobots for Versatile Biomedical Applications. Adv. Intell. Syst. 2021, 3, 200026710.1002/aisy.202000267. DOI

Hwang G.; Paula A. J.; Hunter E. E.; Liu Y.; Babeer A.; Karabucak B.; Stebe K.; Kumar V.; Steager E.; Koo H. Catalytic Antimicrobial Robots for Biofilm Eradication. Sci. Robot. 2019, 4, eaaw238810.1126/scirobotics.aaw2388. PubMed DOI PMC

Dong Y.; Wang L.; Yuan K.; Ji F.; Gao J.; Zhang Z.; Du X.; Tian Y.; Wang Q.; Zhang L. Magnetic Microswarm Composed of Porous Nanocatalysts for Targeted Elimination of Biofilm Occlusion. ACS Nano 2021, 15, 5056–5067. 10.1021/acsnano.0c10010. PubMed DOI

Sun B.; Sun M.; Zhang Z.; Jiang Y.; Hao B.; Wang X.; Cao Y.; Chan T. K. F.; Zhang L. Magnetic Hydrogel Micromachines with Active Release of Antibacterial Agent for Biofilm Eradication. Adv. Intell. Syst. 2023, 6, 230009210.1002/aisy.202300092. DOI

Huang S.; Gao Y.; Lv Y.; Wang Y.; Cao Y.; Zhao W.; Zuo D.; Mu H.; Hua Y. Applications of Nano/Micromotors for Treatment and Diagnosis in Biological Lumens. Micromachines 2022, 13, 178010.3390/mi13101780. PubMed DOI PMC

Ji H.; Hu H.; Tang Q.; Kang X.; Liu X.; Zhao L.; Jing R.; Wu M.; Li G.; Zhou X.; Liu J.; Wang Q.; Cong H.; Wu L.; Qin Y. Precisely Controlled and Deeply Penetrated Micro-Nano Hybrid Multifunctional Motors with Enhanced Antibacterial Activity against Refractory Biofilm Infections. J. Hazard. Mater. 2022, 436, 12921010.1016/j.jhazmat.2022.129210. PubMed DOI

Urso M.; Ussia M.; Pumera M. Breaking Polymer Chains with Self-Propelled Light-Controlled Navigable Hematite Microrobots. Adv. Funct. Mater. 2021, 91, 210151010.1002/adfm.202101510. DOI

Urso M.; Ussia M.; Novotný F.; Pumera M. Trapping and detecting nanoplastics by MXene-derived oxide microrobots. Nat. Commun. 2022, 13, 357310.1038/s41467-022-31161-2. PubMed DOI PMC

Manjura Hoque S.; Sazzad Hossain Md.; Choudhury S.; Akhter S.; Hyder F. Synthesis and Characterization of ZnFe2O4 Nanoparticles and its Biomedical Applications. Mater. Lett. 2016, 162, 60–63. 10.1016/j.matlet.2015.09.066. PubMed DOI PMC

Huang Y.; Liang Y.; Rao Y.; Zhu D.; Cao J.; Shen Z.; Ho W.; Lee S. C. Environment-Friendly Carbon Quantum Dots/ZnFe2O4 Photocatalysts: Characterization, Biocompatibility, and Mechanisms for NO Removal. Environ. Sci. Technol. 2017, 51, 2924–2933. 10.1021/acs.est.6b04460. PubMed DOI

F Fang Z.; Zhang L.; Qi H.; Yue H.; Zhang T.; Zhao X.; Chen G.; Wei Y.; Wang C.; Zhang D. Nanosheet Assembled Hollow ZnFe2O4 Microsphere as Anode for Lithium-Ion Batteries. J. Alloys Compd. 2018, 762, 480–487. 10.1016/j.jallcom.2018.05.259. DOI

Köseoğlu Y.; Baykal A.; Toprak M. S.; Gözüak F.; Başaran A. C.; Aktaş B. Synthesis and Characterization of ZnFe2O4 Magnetic Nanoparticles via a PEG-Assisted Route. J. Alloys Compd. 2008, 462, 209–213. 10.1016/j.jallcom.2007.07.121. DOI

Manohar A.; Vijayakanth V.; Kim K. H. Influence of Ca Doping on ZnFe2O4 Nanoparticles Magnetic Hyperthermia and Cytotoxicity Study. J. Alloys Compd. 2021, 886, 16127610.1016/j.jallcom.2021.161276. DOI

Sundararajan M.; Sukumar M.; Dash C. S.; Sutha A.; Suresh S.; Ubaidullah M.; Al-Enizi A. M.; Raza M. K.; Kumar D. A Comparative Study on NiFe2O4 and ZnFe2O4 Spinel Nanoparticles: Structural, Surface Chemistry, Optical, Morphology and Magnetic Studies. Phys. B 2022, 644, 41423210.1016/j.physb.2022.414232. DOI

Khezri B.; Villa K. Hybrid Photoresponsive/Biocatalytic Micro- and Nanoswimmers. Chem. - Asian J. 2022, 17, e20220059610.1002/asia.202200596. PubMed DOI

Villa K.; Novotný F.; Zelenka J.; Browne M. P.; Ruml T.; Pumera M. Visible-Light-Driven Single-Component BiVO4 Micromotors with the Autonomous Ability for Capturing Microorganisms. ACS Nano 2019, 13, 8135–8145. 10.1021/acsnano.9b03184. PubMed DOI

Peng X.; Urso M.; Pumera M. Photo-Fenton Degradation of Nitroaromatic Explosives by Light-Powered Hematite Microrobots: When Higher Speed Is Not What We Go For. Small Methods 2021, 5, 210061710.1002/smtd.202100617. PubMed DOI

Lyu X.; Liu X.; Zhou C.; Duan S.; Xu P.; Dai J.; Chen X.; Peng Y.; Cui D.; Tang J.; Ma X.; Wang W. Active, Yet Little Mobility: Asymmetric Decomposition of H2O2 Is Not Sufficient in Propelling Catalytic Micromotors. J. Am. Chem. Soc. 2021, 143, 12154–12164. 10.1021/jacs.1c04501. PubMed DOI

Brooks A. M.; Tasinkevych M.; Sabrina S.; Velegol D.; Sen A.; Bishop K. J. M. Shape-Directed Rotation of Homogeneous Micromotors via Catalytic Self-Electrophoresis. Nat. Commun. 2019, 10, 49510.1038/s41467-019-08423-7. PubMed DOI PMC

Navidpour A. H.; Fakhrzad M. Photocatalytic and Magnetic Properties of ZnFe2O4 Nanoparticles Synthesised by Mechanical Alloying. Int. J. Environ. Anal. Chem. 2022, 102, 690–706. 10.1080/03067319.2020.1726331. DOI

Lin Z.; Fan X.; Sun M.; Gao C.; He Q.; Xie H. Magnetically Actuated Peanut Colloid Motors for Cell Manipulation and Patterning. ACS Nano 2018, 12, 2539–2545. 10.1021/acsnano.7b08344. PubMed DOI

Oral C. M.; Ussia M.; Urso M.; Salat J.; Novobilsky A.; Stefanik M.; Ruzek D.; Pumera M. Radiopaque Nanorobots as Magnetically Navigable Contrast Agents for Localized In Vivo Imaging of the Gastrointestinal Tract. Adv. Healthcare Mater. 2023, 12, 220268210.1002/adhm.202202682. PubMed DOI

Jurado-Sánchez B.; Wang J. Micromotors for Environmental Applications: A Review. Environ. Sci. Nano 2018, 5, 1530–1544. 10.1039/C8EN00299A. DOI

Shen H.; Cai S.; Wang Z.; Ge Z.; Yang W. Magnetically Driven Microrobots: Recent Progress and Future Development. Mater. Des. 2023, 227, 11173510.1016/j.matdes.2023.111735. DOI

Fu D.; Jiang J.; Fu S.; Xie D.; Gao C.; Feng Y.; Liu S.; Ye Y.; Liu L.; Tu Y.; Peng F. Real-Time Micromotor Probe for Immune Neutrophil Activation State. Adv. Healthcare Mater. 2023, 12, 230073710.1002/adhm.202300737. PubMed DOI

Valdez-Garduño M.; Leal-Estrada M.; Oliveros-Mata E. S.; Sandoval-Bojorquez D. I.; Soto F.; Wang J.; Garcia-Gradilla V. Density Asymmetry Driven Propulsion of Ultrasound-Powered Janus Micromotors. Adv. Funct. Mater. 2020, 30, 200404310.1002/adfm.202004043. DOI

Muhammad M. H.; Idris A. L.; Fan X.; Guo Y.; Yu Y.; Jin X.; Qiu J.; Guan X.; Huang T. Beyond Risk: Bacterial Biofilms and Their Regulating Approaches. Front. Microbiol. 2020, 11, 92810.3389/fmicb.2020.00928. PubMed DOI PMC

Wasiński B. Extra-Intestinal Pathogenic Escherichia Coli – Threat Connected with Food-Borne Infections. Ann. Agric. Environ. Med. 2019, 26, 532–537. 10.26444/aaem/111724. PubMed DOI

Zhang S.; Abbas M.; Rehman M. U.; Wang M.; Jia R.; Chen S.; Liu M.; Zhu D.; Zhao X.; Gao Q.; Tian B.; Cheng A. Updates on the Global Dissemination of Colistin-Resistant Escherichia Coli: An Emerging Threat to Public Health. Sci. Total Environ. 2021, 799, 14928010.1016/j.scitotenv.2021.149280. PubMed DOI