Dual-Propelled Lanbiotic Based Janus Micromotors for Selective Inactivation of Bacterial Biofilms
Kaisong Yuan
Department of Analytical Chemistry, Physical Chemistry, and Chemical Engineering, University of Alcala, Alcala de Henares, 28871 Madrid, Spain
Institute of Pharmaceutical Analysis, College of Pharmacy, Jinan University, Guangzhou, China
Search for more papers by this authorCorresponding Author
Beatriz Jurado-Sánchez
Department of Analytical Chemistry, Physical Chemistry, and Chemical Engineering, University of Alcala, Alcala de Henares, 28871 Madrid, Spain
Chemical Research Institute “Andres M. del Rio”, University of Alcala, 28871 Madrid, Spain
Search for more papers by this authorCorresponding Author
Alberto Escarpa
Department of Analytical Chemistry, Physical Chemistry, and Chemical Engineering, University of Alcala, Alcala de Henares, 28871 Madrid, Spain
Chemical Research Institute “Andres M. del Rio”, University of Alcala, 28871 Madrid, Spain
Search for more papers by this authorKaisong Yuan
Department of Analytical Chemistry, Physical Chemistry, and Chemical Engineering, University of Alcala, Alcala de Henares, 28871 Madrid, Spain
Institute of Pharmaceutical Analysis, College of Pharmacy, Jinan University, Guangzhou, China
Search for more papers by this authorCorresponding Author
Beatriz Jurado-Sánchez
Department of Analytical Chemistry, Physical Chemistry, and Chemical Engineering, University of Alcala, Alcala de Henares, 28871 Madrid, Spain
Chemical Research Institute “Andres M. del Rio”, University of Alcala, 28871 Madrid, Spain
Search for more papers by this authorCorresponding Author
Alberto Escarpa
Department of Analytical Chemistry, Physical Chemistry, and Chemical Engineering, University of Alcala, Alcala de Henares, 28871 Madrid, Spain
Chemical Research Institute “Andres M. del Rio”, University of Alcala, 28871 Madrid, Spain
Search for more papers by this authorAbstract
Graphene oxide/PtNPs/Fe2O3 “dual-propelled” catalytic and fuel-free rotary actuated magnetic Janus micromotors modified with the lanbiotic Nisin are used for highly selective capture/inactivation of gram-positive bacteria units and biofilms. Specific interaction of Nisin with the Lipid II unit of Staphylococcus Aureus bacteria in connection with the enhanced micromotor movement and generated fluid flow result in a 2-fold increase of the capture/killing ability (both in bubble and magnetic propulsion modes) as compared with free peptide and static counterparts. The high stability of Nisin along with the high towing force of the micromotors allow for efficient operation in untreated raw media (tap water, juice and serum) and even in blood and in flowing blood in magnetic mode. The high selectivity of the approach is illustrated by the dramatically lower interaction with gram-negative bacteria (Escherichia Coli). The double-propulsion (catalytic or fuel-free magnetic) mode of the micromotors and the high biocompatibility holds considerable promise to design micromotors with tailored lanbiotics that can response to the changes that make the bacteria resistant in a myriad of clinical, environmental remediation or food safety applications.
Conflict of interest
The authors declare no conflict of interest.
Supporting Information
As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials are peer reviewed and may be re-organized for online delivery, but are not copy-edited or typeset. Technical support issues arising from supporting information (other than missing files) should be addressed to the authors.
Filename | Description |
---|---|
ange202011617-sup-0001-misc_information.pdf4.8 MB | Supplementary |
ange202011617-sup-0001-Video_S1.avi819.6 KB | Supplementary |
ange202011617-sup-0001-Video_S2.avi2.8 MB | Supplementary |
ange202011617-sup-0001-Video_S3.avi746.8 KB | Supplementary |
ange202011617-sup-0001-Video_S4.avi1.2 MB | Supplementary |
ange202011617-sup-0001-Video_S5.avi8.2 MB | Supplementary |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- 1
- 1aH. F. Chambers, F. R. Deleo, Nat. Rev. Microbiol. 2009, 7, 629–641;
- 1bR. Laxminarayan, A. Duse, C. Wattal, A. K. M. Zaidi, H. F. L. Wertheim, N. Sumpradit, E. Vlieghe, G. L. Hara, I. M. Gould, H. Goossens, C. Greko, A. D. So, M. Bigdeli, G. Tomson, W. Woodhouse, E. Ombaka, A. Q. Peralta, F. N. Qamar, F. Mir, S. Kariuki, Z. A. Bhutta, A. Coates, R. Bergstrom, G. D. Wright, E. D. Brown, O. Cars, Lancet Infect. Dis. 2013, 13, 1057–1098.
- 2G. Mi, D. Shi, M. Wang, T. J. Webster, Adv. Healthcare Mater. 2018, 7, 1800103.
- 3S. Qayyum, A. U. Khan, MedChemComm 2016, 7, 1479–1498.
- 4K. L. Chen, G. D. Bothun, Environ. Sci. Technol. 2014, 48, 873–880.
- 5
- 5aP. C. Ray, S. A. Khan, A. K. Singh, D. Senapati, Z. Fan, Chem. Soc. Rev. 2012, 41, 3193–3209;
- 5bL. Mei, S. Zhu, W. Yin, C. Chen, G. Nie, Z. Gu, Y. Zhao, Theranostics 2020, 10, 757–781.
- 6
- 6aY. Wang, Y. Yang, Y. Shi, H. Song, C. Yu, Adv. Mater. 2019, 0, 1904106;
- 6bX. Fan, F. Yang, J. Huang, Y. Yang, C. Nie, W. Zhao, L. Ma, C. Cheng, C. Zhao, R. Haag, Nano Lett. 2019, 19, 5885–5896.
- 7
- 7aG. A. Ozin, I. Manners, S. Fournier-Bidoz, A. Arsenault, Adv. Mater. 2005, 17, 3011–3018;
- 7bS. Sánchez, M. Pumera, Chem. Asian J. 2009, 4, 1402–1410;
- 7cS. J. Ebbens, J. R. Howse, Soft Matter 2010, 6, 726–738;
- 7dW. Wang, T. Y. Chiang, D. Velegol, T. E. Mallouk, J. Am. Chem. Soc. 2013, 135, 10557–10565;
- 7eJ. Li, I. Rozen, J. Wang, ACS Nano 2016, 10, 5619–5634;
- 7fE. Karshalev, B. Esteban-Fernández de Ávila, J. Wang, J. Am. Chem. Soc. 2018, 140, 3810–3820;
- 7gY. Mei, A. A. Solovev, S. Sanchez, O. G. Schmidt, Chem. Soc. Rev. 2011, 40, 2109–2119;
- 7hJ. Wang, Biosens. Bioelectron. 2016, 76, 234–242.
- 8H. Wang, M. Pumera, Chem. Rev. 2015, 115, 8704–8735.
- 9V. V. Singh, B. Jurado-Sánchez, S. Sattayasamitsathit, J. Orozco, J. Li, M. Galarnyk, Y. Fedorak, J. Wang, Adv. Funct. Mater. 2015, 25, 2147–2155.
- 10Y. Ge, M. Liu, L. Liu, Y. Sun, H. Zhang, B. Dong, Nano-Micro Lett. 2016, 8, 157–164.
- 11D. Vilela, M. M. Stanton, J. Parmar, S. Sánchez, ACS Appl. Mater. Interfaces 2017, 9, 22093–22100.
- 12J. Simmchen, A. Baeza, A. Miguel-Lopez, M. M. Stanton, M. Vallet-Regi, D. Ruiz-Molina, S. Sánchez, ChemNanoMat 2017, 3, 65–71.
- 13F. Soto, D. Kupor, M. A. Lopez-Ramirez, F. Wei, E. Karshalev, S. Tang, F. Tehrani, J. Wang, Angew. Chem. Int. Ed. 2020, 59, 3480–3485; Angew. Chem. 2020, 132, 3508–3513.
- 14J. Li, V. V. Singh, S. Sattayasamitsathit, J. Orozco, K. Kaufmann, R. Dong, W. Gao, B. Jurado-Sanchez, Y. Fedorak, J. Wang, ACS Nano 2014, 8, 11118–11125.
- 15G. Hwang, A. J. Paula, E. E. Hunter, Y. Liu, A. Babeer, B. Karabucak, K. Stebe, V. Kumar, E. Steager, H. Koo, Sci. Robot. 2019, 4, eaaw2388.
- 16J. A. M. Delezuk, D. E. Ramírez-Herrera, B. Esteban-Fernández de Ávila, J. Wang, Nanoscale 2017, 9, 2195–2200.
- 17M. Hoop, Y. Shen, X.-Z. Chen, F. Mushtaq, L. M. Iuliano, M. S. Sakar, A. Petruska, M. J. Loessner, B. J. Nelson, S. Pané, Adv. Funct. Mater. 2016, 26, 1063–1069.
- 18L. Xie, X. Pang, X. Yan, Q. Dai, H. Lin, J. Ye, Y. Cheng, Q. Zhao, X. Ma, X. Zhang, G. Liu, X. Chen, ACS Nano 2020, 14, 2880–2893.
- 19M. Kiristi, V. V. Singh, B. Esteban-Fernández de Ávila, M. Uygun, F. Soto, D. A. Uygun, J. Wang, ACS Nano 2015, 9, 9252–9259.
- 20B. Esteban-Fernández de Ávila, P. Angsantikul, J. Li, M. A. Lopez-Ramirez, D. E. Ramirez-Herrera, S. Thamphiwatana, C. Chen, J. Delezuk, R. Samakapiruk, V. Ramez, M. Obonyo, L. Zhang, J. Wang, Nat. Commun. 2017, 8, 272.
- 21M. M. Stanton, B. W. Park, D. Vilela, K. Bente, D. Faivre, M. Sitti, S. Sanchez, ACS Nano 2017, 11, 9968–9978.
- 22
- 22aB. Esteban-Fernández de Ávila, P. Angsantikul, D. E. Ramírez-Herrera, F. Soto, H. Teymourian, D. Dehaini, Y. Chen, L. Zhang, J. Wang, Sci. Robot. 2018, 3, eaat0485;
- 22bJ. Li, P. Angsantikul, W. Liu, B. Esteban-Fernandez de Avila, X. Chang, E. Sandraz, Y. Liang, S. Zhu, Y. Zhang, C. Chen, W. Gao, L. Zhang, J. Wang, Adv. Mater. 2018, 30, 1704800.
- 23
- 23aB. Khezri, S. M. Beladi Mousavi, Z. Sofer, M. Pumera, Nanoscale 2019, 11, 8825–8834;
- 23bB. Khezri, S. M. Beladi Mousavi, L. Krejčová, Z. Heger, Z. Sofer, M. Pumera, Adv. Funct. Mater. 2019, 29, 1806696;
- 23cV. V. Singh, K. Kaufmann, B. Esteban Fernández de Ávila, E. Karshalev, J. Wang, Adv. Funct. Mater. 2016, 26, 6270–6278;
- 23dT. Maric, J. G. S. Moo, B. Khezri, Z. Sofer, M. Pumera, Appl. Mater. Today 2017, 9, 289–291;
- 23eT. Maric, S. M. Beladi-Mousavi, B. Khezri, J. Sturala, M. Z. M. Nasir, R. D. Webster, Z. Sofer, M. Pumera, Small 2020, 16, 1902365.
- 24
- 24aJ. M. Shin, J. W. Gwak, P. Kamarajan, J. C. Fenno, A. H. Rickard, Y. L. Kapila, J. Appl. Microbiol. 2016, 120, 1449–1465;
- 24bQ. Li, M. Montalban-Lopez, O. P. Kuipers, Appl. Environ. Microbiol. 2018, 84, e0052-18;
- 24cM. Vukomanovic, V. Zunic, S. Kunej, B. Jancar, S. Jeverica, R. Podlipec, D. Suvorov, Sci. Rep. 2017, 7, 4324;
- 24dS. J. Lam, N. M. O'Brien-Simpson, N. Pantarat, A. Sulistio, E. H. H. Wong, Y.-Y. Chen, J. C. Lenzo, J. A. Holden, A. Blencowe, E. C. Reynolds, G. G. Qiao, Nat. Microbiol. 2016, 1, 16162.
- 25K. Yuan, V. de la Asunción-Nadal, B. Jurado-Sánchez, A. Escarpa, Chem. Mater. 2020, 32, 1983–1992.
- 26
- 26aZ. Liang, D. Fan, Sci. Adv. 2018, 4, eaau0981;
- 26bK. Kim, J. Guo, X. Xu, D. Fan, ACS Nano 2015, 9, 548–554.
- 27Z. Li, J. Ma, J. Ruan, X. Zhuang, Nanoscale Res. Lett. 2019, 14, 195.
- 28K. Villa, J. Viktorova, J. Plutnar, T. Ruml, L. Hoang, M. Pumera, Cell Rep. Phys. Sci. 2020, 1, 100181.
- 29T. Cui, S. Wu, Y. Sun, J. Ren, X. Qu, Nanolett. 2020, 10, 7350–7358.
- 30T. Bhuyan, A. T. Simon, S. Maity, A. K. Singh, S. S. Ghosh, D. Bandyopadhyay, ACS Appl. Mater. Interfaces 2020, 12, 43352–43364.
- 31
- 31aE. Breukink, I. Wiedemann, C. van Kraaij, O. P. Kuipers, H.-G. Sahl, B. de Kruijff, Science 1999, 286, 2361–2364;
- 31bK.-i. Okuda, T. Zendo, S. Sugimoto, T. Iwase, A. Tajima, S. Yamada, K. Sonomoto, Y. Mizunoe, Antimicrob. Agents Chemother. 2013, 57, 5572–5579.
- 32
- 32aA. Aziz, M. Medina-Sánchez, N. Koukourakis, J. Wang, R. Kuschmierz, H. Radner, J. W. Czarske, O. G. Schmidt, Adv. Funct. Mater. 2019, 29, 1905272;
- 32bD. Vilela, U. Cossío, J. Parmar, A. M. Martínez-Villacorta, V. Gómez-Vallejo, J. Llop, S. Sánchez, ACS Nano 2018, 12, 1220–1227;
- 32cZ. Wu, L. Li, Y. Yang, P. Hu, Y. Li, S.-Y. Yang, L. V. Wang, W. Gao, Sci. Robot. 2019, 4, eaax0613;
- 32dA. Aziz, S. Pane, V. Iacovacci, N. Koukourakis, J. Czarske, A. Menciassi, M. Medina-Sánchez, O. G. Schmidt, ACS Nano 2020, 14, 10865–10893;
- 32eA. Aziz, M. Medina-Sánchez, J. Claussen, O. G. Schmidt, Nano Lett. 2019, 19, 6612–6620.
Citing Literature
This is the
German version
of Angewandte Chemie.
Note for articles published since 1962:
Do not cite this version alone.
Take me to the International Edition version with citable page numbers, DOI, and citation export.
We apologize for the inconvenience.