Urinary-based infections affect millions of people worldwide. Such bacterial infections are mainly caused by Escherichia coli (E. coli) biofilm formation in the bladder and/or urinary catheters. Herein, the authors present a hybrid enzyme/photocatalytic microrobot, based on urease-immobilized TiO2 /CdS nanotube bundles, that can swim in urea as a biocompatible fuel and respond to visible light. Upon illumination for 2 h, these microrobots are able to remove almost 90% of bacterial biofilm, due to the generation of reactive radicals, while bare TiO2 /CdS photocatalysts (non-motile) or urease-coated microrobots in the dark do not show any toxic effect. These results indicate a synergistic effect between the self-propulsion provided by the enzyme and the photocatalytic activity induced under light stimuli. This work provides a photo-biocatalytic approach for the design of efficient light-driven microrobots with promising applications in microbiology and biomedicine.

Center for Advanced Functional Nanorobots Department of Inorganic Chemistry University of Chemistry and Technology Prague Technická 5 Prague 166 28 Czech Republic

Center of Materials and Nanotechnologies Faculty of Chemical Technology University of Pardubice Náměstí čs Legií 565 Pardubice 530 02 Czech Republic

Central European Institute of Technology Brno University of Technology Purkyňova 123 Brno 612 00 Czech Republic

Department of Biochemistry and Microbiology University of Chemistry and Technology Prague Technická 5 Prague 166 28 Czech Republic

Department of Chemical and Biomolecular Engineering Yonsei University 50 Yonsei ro Seodaemun gu Seoul 03722 Korea

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

See more in PubMed

A. L. Flores-Mireles, J. N. Walker, M. Caparon, S. J. Hultgren, Nat. Rev. Microbiol. 2015, 13, 269.

T. L. Vollmerhausen, A. Conneely, C. Bennett, V. E. Wagner, J. C. Victor, C. P. O'Byrne, J. Photochem. Photobiol. B 2017, 170, 295.

L. E. Nicolle, Antimicrob. Resist. Infect. Control 2014, 3, 23.

G. G. Anderson, J. J. Palermo, J. D. Schilling, R. Roth, J. Heuser, S. J. Hultgren, Science 2003, 301, 105.

J. W. Costerton, P. S. Stewart, E. P. Greenberg, Science 1999, 284, 1318.

a) W. C. de Melo, P. Avci, M. N. de Oliveira, A. Gupta, D. Vecchio, M. Sadasivam, R. Chandran, Y.-Y. Huang, R. Yin, L. R. Perussi, G. P. Tegos, J. R. Perussi, T. Dai, M. R. Hamblin, Expert Rev. Anti-Infect. Ther. 2013, 11, 669;

b) J. Li, C. C. Mayorga-Martinez, C. D. Ohl, M. Pumera, Adv. Funct. Mater. 2021, 32, 2102265.

M. Erriu, C. Blus, S. Szmukler-Moncler, S. Buogo, R. Levi, G. Barbato, D. Madonnaripa, G. Denotti, V. Piras, G. Orrù, Ultrason. Sonochem. 2014, 21, 15.

J. L. Del Pozo, M. S. Rouse, R. Patel, Int. J. Artif. Organs 2008, 31, 786.

a) M. M. Stanton, B.-W. Park, D. Vilela, K. Bente, D. Faivre, M. Sitti, S. Sánchez, ACS Nano 2017, 11, 9968;

b) C. C. Mayorga, J. Zelenka, J. Grmela, H. Michalkova, T. Ruml, J. Mareš, M. Pumera, Adv. Sci. 2021, 8, 2101301.

a) J. Wang, W. Gao, ACS Nano 2012, 6, 5745;

b) K. Villa, J. Viktorova, J. Plutnar, T. Ruml, L. Hoang, M. Pumera, Cell Rep. Phys. Sci. 2020, 1, 100181.

a) M. Ussia, M. Urso, K. Doleželíková, H. Michálková, V. Adam, M. Pumera, Adv. Funct. Mater. 2021, 31, 2101178;

b) D. Vilela, N. Blanco-Cabra, A. Eguskiza, A. C. Hortelao, E. Torrents, S. Sanchez, ACS Appl. Mater. Interfaces 2021, 13, 14964.

Z. Lin, C. Gao, D. Wang, Q. He, Angew. Chem., Int. Ed. 2021, 133, 8832.

T. Cui, S. Wu, Y. Sun, J. Ren, X. Qu, Nano Lett. 2020, 20, 7350.

G. Hwang, A. J. Paula, E. E. Hunter, Y. Liu, A. Babeer, B. Karabucak, K. Stebe, V. Kumar, E. Steager, H. Koo, Sci. Rob. 2019, 4, eaaw2388.

a) Y. Dong, L. Wang, K. Yuan, F. Ji, J. Gao, Z. Zhang, X. Du, Y. Tian, Q. Wang, L. Zhang, ACS Nano 2021, 15, 5056;

b) H. Zhou, C. C. Mayorga-Martinez, S. P., L. Zhang, M. Pumera, Chem. Rev. 2021, 121, 4999.

K. Yuan, B. Jurado-Sánchez, A. Escarpa, Angew. Chem., Int. Ed. 2021, 60, 4915.

a) W. Gao, J. Wang, ACS Nano 2014, 8, 4, 3170;

b) B. Jurando-Sánchez, J. Wang, Environ. Sci.: Nano 2018, 5, 1530;

c) L. Kong, A. Ambrosi, M. Z. M. Nasir, J. Guan, M. Pumera, Adv. Funct. Mater. 2019, 29, 1903872;

d) Y. Ying, M. Pumera, Chem. - Eur. J. 2019, 25, 106;

e) L. Wang, K. Villa, Environ. Sci.: Nano 2021, 8, 3440;

f) C. M. Oral, M. Ussia, D. K. Yavuz, M. Pumera, Small 2022, https://doi.org/10.1002/smll.202106271.

a) M. P. Browne, V. Urbanova, J. Plutnar, F. Novotný, M. Pumera, J. Mater. Chem. A 2020, 8, 1120;

b) K. Villa, J. R. Galán-Mascarós, ChemSusChem 2021, 14, 2023;

c) X. Zhou, I. Hwang, O. Tomanec, D. Fehn, A. Mazare, R. Zboril, K. Meyer, P. Schmuki, Adv. Funct. Mater. 2021, 31, 2102843.

a) K. Villa, J. R. Galán-Mascarós, N. López, E. Palomares, Sustainable Energy Fuels 2021, 5, 4560;

b) S. Hejazi, S. Mohajernia, B. Osuagwu, G. Zoppellaro, P. Andryskova, O. Tomanec, S. Kment, R. Zbořil, P. Schmuki, Adv. Mater. 2020, 32, 1908505.

G. G. Genchi, Y. Cao, T. A. Desai, in Smart Nanoparticles for Biomedicine (Ed: G. Ciofani), Elsevier, New York 2018, pp. 143-157.

M. Kalbacova, J. M. Macak, F. Schmidt-Stein, C. T. Mierke, P. Schmuki, Phys. Status Solidi RRL 2008, 2, 194.

K. Nakata, A. Fujishima, J. Photochem. Photobiol. C 2012, 13, 169.

a) L. Kong, C. C. Mayorga-Martinez, J. Guan, M. Pumera, Small 2020, 16, 1903179;

b) J. Li, M. Pumera, Chem. Soc. Rev. 2021, 50, 2794;

c) J. Zhang, J. Song, F. Mou, J. Guan, A. Sen, Trends Chem. 2021, 3, 387.

a) S. K. Srivastava, M. Guix, O. G. Schmidt, Nano Lett. 2016, 16, 817;

b) R. Dong, Q. Zhang, W. Gao, A. Pei, B. Ren, ACS Nano 2016, 10, 839.

a) G. Zhao, M. Viehrig, M. Pumera, Lab Chip 2013, 13, 1930;

b) Y. Li, F. Mou, C. Chen, M. You, Y. Yin, L. Xu, J. Guan, RSC Adv. 2016, 6, 10697.

E. Karshalev, B. Esteban-Fernández de Ávila, J. Wang, J. Am. Chem. Soc. 2018, 140, 3810.

M. Enachi, M. Guix, V. Postolache, V. Ciobanu, V. M. Fomin, O. G. Schmidt, I. Tiginyanu, Small 2016, 12, 5497.

Y. Wang, Z. Li, A. A. Solovev, G. Huang, Y. Mei, RSC Adv. 2019, 9, 29433.

T. Luttrell, S. Halpegamage, J. Tao, A. Kramer, E. Sutter, M. Batzill, Sci. Rep. 2014, 4, 4043.

K. Villa, A. Black, X. Domènech, J. Peral, Sol. Energy 2012, 86, 558.

K. Huang, L. Chen, J. Deng, J. Xiong, J. Nanomater. 2012, 2012, 11.

K. Almashhori, T. T. Ali, A. Saeed, R. Alwafi, M. Aly, F. E. Al-Hazmi, New J. Chem. 2020, 44, 562.

A. Boonserm, C. Kruehong, V. Seithtanabutara, A. Artnaseaw, P. Kwakhong, Appl. Surf. Sci. 2017, 419, 933.

X. Ma, A. C. Hortelao, A. Miguel-López, S. Sánchez, J. Am. Chem. Soc. 2016, 138, 13782.

S. Tang, F. Zhang, H. Gong, F. Wei, J. Zhuang, E. Karshalev, B. E.-F. de Ávila, C. Huang, Z. Zhou, Z. Li, L. Yin, H. Dong, R. H. Fang, X. Zhang, L. Zhang, J. Wang, Sci. Rob. 2020, 5, eaba6137.

a) H. Choi, S. H. Cho, S. K. Hahn, ACS Nano 2020, 14, 6683;

b) S. Hermanová, M. Pumera, Chem. - Eur. J. 2020, 26, 11085.

V. Vaiano, O. Sacco, G. Di Capua, N. Femia, D. Sannino, Water 2019, 11, 1642.

J. M. Macak, M. Zlamal, J. Krysa, P. Schmuki, Small 2007, 3, 300.

H. Sopha, M. Krbal, S. Ng, J. Prikryl, R. Zazpe, F. K. Yam, J. M. Macak, Appl. Mater. Today 2017, 9, 104.

J. A. Maciá-Agulló, A. Corma, H. Garcia, Chem. - Eur. J. 2015, 21, 10940.

J. Ryu, S. H. Lee, D. H. Nam, C. B. Park, Adv. Mater. 2011, 23, 1883.

A. J. Conneely, C. Bennett, G. M. O'Connor, T. Vollmerhausen, C. O'Byrne, G. Spence, D. Rowe, J. Victor, International Congress on Applications of Lasers & Electro-Optics (ICALEO) 2016, 2016, M604.

Y. Lv, Z. Li, X. Zhou, S. Cheng, L. Zheng, Sci. Total Environ. 2020, 749, 142213.

B. Krajewska, J. Mol. Catal. B: Enzym. 2011, 68, 262.

R. Wu, X. Ou, R. Tian, J. Zhang, H. Jin, M. Dong, J. Li, L. Liu, Nanoscale 2018, 10, 20162.

S. Borse, M. Temgire, A. Khan, S. Joshi, RSC Adv. 2016, 6, 56674.

F. K.-M. Chan, K. Moriwaki, M. J. De Rosa, Methods in Molecular Biology, Humana Press, Totowa, NJ, New York, 2013, Vol. 979, p. 65.

Y. H. Leung, X. Xu, A. P. Y. Ma, F. Liu, A. M. C. Ng, Z. Shen, L. A. Gethings, M. Y. Guo, A. B. Djurišić, P. K. H. Lee, H. K. Lee, W. K. Chan, F. C. C. Leung, Sci. Rep. 2016, 6, 35243.

K. Pathakoti, S. Morrow, C. Han, M. Pelaez, X. He, D. D. Dionysiou, H.-M. Hwang, Environ. Sci. Technol. 2013, 47, 9988.

Y. H. Leung, A. M. C. Ng, X. Xu, Z. Shen, L. A. Gethings, M. T. Wong, C. M. N. Chan, M. Y. Guo, Y. H. Ng, A. B. Djurišić, P. K. H. Lee, W. K. Chan, L. H. Yu, D. L. Phillips, A. P. Y. Ma, F. C. C. Leung, Small 2014, 10, 1171.

Y. Cheng, H. Yang, Y. Yang, J. Huang, K. Wu, Z. Chen, X. Wang, C. Lin, Y. Lai, J. Mater. Chem. B 2018, 6, 1862.

R. Zazpe, M. Knaut, H. Sopha, L. Hromadko, M. Albert, J. Prikryl, V. Gärtnerová, J. W. Bartha, J. M. Macak, Langmuir 2016, 32, 10551.

H. Michalkova, Z. Skubalova, H. Sopha, V. Strmiska, B. Tesarova, S. Dostalova, P. Svec, L. Hromadko, M. Motola, J. M. Macak, V. Adam, Z. Heger, J. Hazard. Mater. 2020, 388, 122054.

H. Yang, N. Fan, W. Luan, S. Tu, Nanoscale Res. Lett. 2009, 4, 344.

N. Li, X. Zhang, S. Chen, X. Hou, Y. Liu, X. Zhai, Mater. Sci. Eng.: B 2011, 176, 688.

A. M. Suhail, M. J. Khalifa, N. M. Saeed, O. A. Ibrahim, Eur. Phys. J. Appl. Phys. 2010, 49, 30601.

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