Collective buoyancy-driven dynamics in swarming enzymatic nanomotors.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
29 Oct 2024
29 Oct 2024
Historique:
received:
29
02
2024
accepted:
15
10
2024
medline:
30
10
2024
pubmed:
30
10
2024
entrez:
30
10
2024
Statut:
epublish
Résumé
Enzymatic nanomotors harvest kinetic energy through the catalysis of chemical fuels. When a drop containing nanomotors is placed in a fuel-rich environment, they assemble into ordered groups and exhibit intriguing collective behaviour akin to the bioconvection of aerobic microorganismal suspensions. This collective behaviour presents numerous advantages compared to individual nanomotors, including expanded coverage and prolonged propulsion duration. However, the physical mechanisms underlying the collective motion have yet to be fully elucidated. Our study investigates the formation of enzymatic swarms using experimental analysis and computational modelling. We show that the directional movement of enzymatic nanomotor swarms is due to their solutal buoyancy. We investigate various factors that impact the movement of nanomotor swarms, such as particle concentration, fuel concentration, fuel viscosity, and vertical confinement. We examine the effects of these factors on swarm self-organization to gain a deeper understanding. In addition, the urease catalysis reaction produces ammonia and carbon dioxide, accelerating the directional movement of active swarms in urea compared with passive ones in the same conditions. The numerical analysis agrees with the experimental findings. Our findings are crucial for the potential biomedical applications of enzymatic nanomotor swarms, ranging from enhanced diffusion in bio-fluids and targeted delivery to cancer therapy.
Identifiants
pubmed: 39472587
doi: 10.1038/s41467-024-53664-w
pii: 10.1038/s41467-024-53664-w
doi:
Substances chimiques
Urease
EC 3.5.1.5
Carbon Dioxide
142M471B3J
Ammonia
7664-41-7
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
9315Subventions
Organisme : EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council)
ID : 866348
Organisme : Departament d'Innovació, Universitats i Empresa, Generalitat de Catalunya (Department of Innovation, Education and Enterprise, Government of Catalonia)
ID : 2021 SGR 01606
Organisme : Departament d'Innovació, Universitats i Empresa, Generalitat de Catalunya (Department of Innovation, Education and Enterprise, Government of Catalonia)
ID : 2023 FI-1 00654
Organisme : Ministry of Economy and Competitiveness | Agencia Estatal de Investigación (Spanish Agencia Estatal de Investigación)
ID : CEX2018-000789-S
Informations de copyright
© 2024. The Author(s).
Références
Wang, H. & Pumera, M. Coordinated behaviors of artificial micro/nanomachines: From mutual interactions to interactions with the environment. Chem. Soc. Rev. 49, 3211–3230 (2020).
pubmed: 32307471
doi: 10.1039/C9CS00877B
Shim, G., Devenport, D. & Cohen, D. J. Overriding native cell coordination enhances external programming of collective cell migration. Proc. Natl Acad. Sci. USA. 118, e2101352118 (2021).
pubmed: 34272284
pmcid: 8307614
doi: 10.1073/pnas.2101352118
Peleg, O., Peters, J. M., Salcedo, M. K. & Mahadevan, L. Collective mechanical adaptation of honeybee swarms. Nat. Phys. 14, 1193–1198 (2018).
doi: 10.1038/s41567-018-0262-1
Zitterbart, D. P., Wienecke, B., Butler, J. P. & Fabry, B. Coordinated movements prevent jamming in an emperor penguin huddle. PLoS One 6, e20260 (2011).
pubmed: 21673816
pmcid: 3106014
doi: 10.1371/journal.pone.0020260
Yang, M. et al. Swarming magnetic nanorobots bio-interfaced by heparinoid-polymer brushes for in vivo safe synergistic thrombolysis. Sci. Adv. 9, eadk7251 (2023).
pubmed: 38019908
pmcid: 10686566
doi: 10.1126/sciadv.adk7251
Yu, J. et al. Active generation and magnetic actuation of microrobotic swarms in bio-fluids. Nat. Commun. 10, 5631–5642 (2019).
pubmed: 31822669
pmcid: 6904566
doi: 10.1038/s41467-019-13576-6
Xie, H. et al. Reconfigurable magnetic microrobot swarm: multimode transformation, locomotion, and manipulation. Sci. Robot. 4, eaav8006 (2019).
pubmed: 33137748
doi: 10.1126/scirobotics.aav8006
Bente, K. et al. Selective actuation and tomographic imaging of swarming magnetite nanoparticles. ACS Appl. Mater. Interfaces 4, 6752–6759 (2021).
Chen, M. et al. Programmable dynamic shapes with a swarm of light-powered colloidal motors. Angew. Chem. Int. Ed. 60, 16674–16679 (2021).
doi: 10.1002/anie.202105746
Aubret, A., Youssef, M., Sacanna, S. & Palacci, J. Targeted assembly and synchronization of self-spinning microgears. Nat. Phy. 14, 1114–1118 (2018).
doi: 10.1038/s41567-018-0227-4
Xu, T. et al. Reversible swarming and separation of self-propelled chemically powered nanomotors under acoustic fields. J. Am. Chem. Soc. 137, 2163–2166 (2015).
pubmed: 25634724
doi: 10.1021/ja511012v
Tang, S. et al. Structure-dependent optical modulation of propulsion and collective behavior of acoustic/light-driven hybrid microbowls. Adv. Funct. Mater. 29, 1809003–1809009 (2019).
doi: 10.1002/adfm.201809003
Leunissen, M. E., Vutukuri, H. R. & Van Blaaderen, A. Directing colloidal self-assembly with biaxial electric fields. Adv. Mater. 21, 3116–3120 (2009).
doi: 10.1002/adma.200900640
Ma, F., Wang, S., Wu, D. T. & Wu, N. Electric-field-induced assembly and propulsion of chiral colloidal clusters. Proc. Natl Acad. Sci. USA. 112, 6307–6312 (2015).
pubmed: 25941383
pmcid: 4443365
doi: 10.1073/pnas.1502141112
Duan, W., Liu, R. & Sen, A. Transition between collective behaviors of micromotors in response to different stimuli. J. Am. Chem. Soc. 135, 1280–1283 (2013).
pubmed: 23301622
doi: 10.1021/ja3120357
Gentile, K., Somasundar, A., Bhide, A. & Sen, A. Chemically powered synthetic “living” systems. Chem 6, 2174–2185 (2020).
doi: 10.1016/j.chempr.2020.08.010
Ziepke, A., Maryshev, I., Aranson, I. S. & Frey, E. Multi-scale organization in communicating active matter. Nat. Commun. 13, 6727–6736 (2022).
Zhang, F. et al. Extremophile-based biohybrid micromotors for biomedical operations in harsh acidic environments. Sci. Adv. 8, eade645 (2022).
doi: 10.1126/sciadv.ade6455
Chen, H. et al. An engineered bacteria-hybrid microrobot with the magnetothermal bioswitch for remotely collective perception and imaging-guided cancer treatment. ACS Nano 16, 6118–6133 (2022).
pubmed: 35343677
doi: 10.1021/acsnano.1c11601
Zhuang, J. & Sitti, M. Chemotaxis of bio-hybrid multiple bacteria-driven microswimmers. Sci. Rep. 6, 32135–32144 (2016).
pubmed: 27555465
pmcid: 4995368
doi: 10.1038/srep32135
Akter, M. et al. Cooperative cargo transportation by a swarm of molecular machines. Sci. Robot. 7, eabm0677 (2022).
pubmed: 35442703
doi: 10.1126/scirobotics.abm0677
Keya, J. J. et al. DNA-assisted swarm control in a biomolecular motor system. Nat. Commun. 9, 453–460 (2018).
pubmed: 29386522
pmcid: 5792447
doi: 10.1038/s41467-017-02778-5
Chen, S. et al. Dual-source powered nanomotor with integrated functions for cancer photo-theranostics. Biomaterials 288, 121744–121753 (2022).
pubmed: 35999081
doi: 10.1016/j.biomaterials.2022.121744
Chen, S. et al. Active nanomotors surpass passive nanomedicines: current progress and challenges. J. Mater. Chem. B 10, 7099–7107 (2022).
pubmed: 35543361
doi: 10.1039/D2TB00556E
Ma, X. et al. Enzyme-powered hollow mesoporous Janus nanomotors. Nano Lett. 15, 7043–7050 (2015).
pubmed: 26437378
doi: 10.1021/acs.nanolett.5b03100
Ma, X., Hortelao, A. C., Miguel-López, A. & Sánchez, S. Bubble-free propulsion of ultrasmall tubular nanojets powered by biocatalytic reactions. J. Am. Chem. Soc. 138, 13782–13785 (2016).
pubmed: 27718566
pmcid: 5228068
doi: 10.1021/jacs.6b06857
Arqué, X. et al. Intrinsic enzymatic properties modulate the self-propulsion of micromotors. Nat. Commun. 10, 2826–2837 (2019).
pubmed: 31249381
pmcid: 6597730
doi: 10.1038/s41467-019-10726-8
Ma, X. & Sanchez, S. A bio-catalytically driven Janus mesoporous silica cluster motor with magnetic guidance. Chem. Commun. 51, 5467–5470 (2015).
doi: 10.1039/C4CC08285K
Hortelão, A. C., Patiño, T., Perez-Jiménez, A., Blanco, À. & Sánchez, S. Enzyme-powered nanobots enhance anticancer drug delivery. Adv. Funct. Mater. 28, 1705086–1705095 (2018).
doi: 10.1002/adfm.201705086
Llopis-Lorente, A. et al. Enzyme-powered gated mesoporous silica nanomotors for on-command intracellular payload delivery. ACS Nano 13, 12171–12183 (2019).
pubmed: 31580642
doi: 10.1021/acsnano.9b06706
Hortelao, A. C., Carrascosa, R., Murillo-Cremaes, N., Patino, T. & Sánchez, S. Targeting 3D bladder cancer spheroids with urease-powered nanomotors. ACS Nano 13, 429–439 (2019).
pubmed: 30588798
doi: 10.1021/acsnano.8b06610
Tang, S. et al. Enzyme-powered Janus platelet cell robots for active and targeted drug delivery. Sci. Robot. 5, eaba6137 (2020).
pubmed: 33022613
doi: 10.1126/scirobotics.aba6137
Choi, H., Cho, S. H. & Hahn, S. K. Urease-powered polydopamine nanomotors for intravesical therapy of bladder diseases. ACS Nano 14, 6683–6692 (2020).
pubmed: 32491832
doi: 10.1021/acsnano.9b09726
Patino, T. et al. Self-sensing enzyme-powered micromotors equipped with pH-responsive DNA nanoswitches. Nano Lett. 19, 3440–3447 (2019).
pubmed: 30704240
doi: 10.1021/acs.nanolett.8b04794
Liu, X. et al. Urease-powered micromotors with spatially selective distribution of enzymes for capturing and sensing exosomes. ACS Nano 17, 24343–24354 (2023).
pubmed: 38038995
doi: 10.1021/acsnano.3c10405
Hortelao, A. C. et al. Swarming behavior and in vivo monitoring of enzymatic nanomotors within the bladder. Sci. Robot. 6, eabd2823 (2021).
pubmed: 34043548
doi: 10.1126/scirobotics.abd2823
Simó, C. et al. Urease-powered nanobots for radionuclide bladder cancer therapy. Nat. Nanotechnol. 19, 554–564 (2024).
pubmed: 38225356
pmcid: 11026160
doi: 10.1038/s41565-023-01577-y
Serra-Casablancas, M. et al. Catalase-powered nanobots for overcoming the mucus barrier. ACS Nano 18, 16701–16714 (2024).
pubmed: 38885185
pmcid: 11223492
doi: 10.1021/acsnano.4c01760
Ruiz-González, N. et al. Swarms of enzyme-powered nanomotors enhance the diffusion of macromolecules in viscous media. Small 20, 2309387–2309403 (2024).
doi: 10.1002/smll.202309387
Ramos-Docampo, M. A., Wang, N., Pendlmayr, S. & Städler, B. Self-propelled collagenase-powered nano/micromotors. ACS Appl. Nano Mater. 5, 14622–14629 (2022).
doi: 10.1021/acsanm.2c02989
Ramos-Docampo, M. A. et al. Microswimmers with heat delivery capacity for 3D cell spheroid penetration. ACS Nano 13, 12192–12205 (2019).
pubmed: 31502822
doi: 10.1021/acsnano.9b06869
Fraire, J. C. et al. Light-triggered mechanical disruption of extracellular barriers by swarms of enzyme-powered nanomotors for enhanced delivery. ACS Nano 17, 7180–7193 (2023).
pubmed: 37058432
pmcid: 10134497
doi: 10.1021/acsnano.2c09380
Kessler, J. O. & Hill, N. A. The growth of bioconvection patterns in a uniform suspension of gyrotactic micro-organisms. J. Fluid Mech. 195, 223–237 (1988).
pubmed: 11543357
doi: 10.1017/S0022112088002393
Bodenschatz, E., Pesch, W. & Ahlers, G. Recent developments in Rayleigh-Bénard Convection. Annu. Rev. Fluid Mech. 32, 709–778 (2000).
doi: 10.1146/annurev.fluid.32.1.709
Bees, M. A. Advances in bioconvection. Annu. Rev. Fluid Mech. 52, 449–476 (2020).
doi: 10.1146/annurev-fluid-010518-040558
Metcalfe, A. M. & Pedley, T. J. Falling plumes in bacterial bioconvection. J. Fluid Mech. 445, 121–149 (2001).
doi: 10.1017/S0022112001005547
Zhang, J. et al. Light-powered, fuel-Free oscillation, migration, and reversible manipulation of multiple cargo types by micromotor swarms. ACS Nano 17, 251–262 (2023).
pubmed: 36321936
doi: 10.1021/acsnano.2c07266
Sun, M. et al. Bioinspired self-assembled colloidal collectives drifting in three dimensions underwater. Sci. Adv. 9, eadj4201 (2023).
pubmed: 37948530
pmcid: 10637755
doi: 10.1126/sciadv.adj4201
Kumar, B. V. V. S. P., Patil, A. J. & Mann, S. Enzyme-powered motility in buoyant organoclay/DNA protocells. Nat. Chem. 10, 1154–1163 (2018).
pubmed: 30127511
doi: 10.1038/s41557-018-0119-3
Song, J., Shklyaev, O. E., Sapre, A., Balazs, A. C. & Sen, A. Self‐propelling macroscale sheets powered by enzyme pumps. Angew. Chem. Int. Ed. 63, e202311556 (2023).
doi: 10.1002/anie.202311556
Sapre, A. et al. Enzyme catalysis causes fluid flow, motility, and directional transport on supported lipid bilayers. ACS Appl. Mater. Interfaces 16, 9380–9387 (2024).
pubmed: 38319873
doi: 10.1021/acsami.3c15383
Patiño, T. et al. Influence of enzyme quantity and distribution on the self-propulsion of non-Janus urease-powered micromotors. J. Am. Chem. Soc. 140, 7896–7903 (2018).
pubmed: 29786426
doi: 10.1021/jacs.8b03460
Patiño, T., Llacer-Wintle, J., Pujals, S., Albertazzi, L. & Sánchez, S. Unveiling protein corona formation around self-propelled enzyme nanomotors by nanoscopy. Nanoscale 16, 2904–2912 (2023).
doi: 10.1039/D3NR03749E
De Corato, M. et al. Self-propulsion of active colloids via ion release: theory and experiments. Phys. Rev. Lett. 124, 108001–108006 (2020).
pubmed: 32216443
doi: 10.1103/PhysRevLett.124.108001
De Corato, M., Pagonabarraga, I., Abdelmohsen, L. K. E. A., Sánchez, S. & Arroyo, M. Spontaneous polarization and locomotion of an active particle with surface-mobile enzymes. Phys. Rev. Fluids 5, 122001–122011 (2020).
doi: 10.1103/PhysRevFluids.5.122001
Arqué, X. et al. Ionic species affect the self-propulsion of urease-powered micromotors. Research 2020, 1–14 (2020).
Simmchen, J. et al. Topographical pathways guide chemical microswimmers. Nat. Commun. 7, 10598–10606 (2016).
pubmed: 26856370
pmcid: 4748132
doi: 10.1038/ncomms10598
Katuri, J., Uspal, W. E., Popescu, M. N. & Sánchez, S. Inferring non-equilibrium interactions from tracer response near confined active Janus particles. Sci. Adv. 7, eabd0719 (2021).
pubmed: 33931441
pmcid: 8087409
doi: 10.1126/sciadv.abd0719
Katuri, J., Caballero, D., Voituriez, R., Samitier, J. & Sanchez, S. Directed flow of micromotors through alignment interactions with micropatterned ratchets. ACS Nano 12, 7282–7291 (2018).
pubmed: 29949338
doi: 10.1021/acsnano.8b03494
Feng, Y. et al. Self-adaptive enzyme-powered micromotors with switchable propulsion mechanism and motion directionality. Appl. Phys. Rev. 8, 011406–011413 (2021).
doi: 10.1063/5.0029060
Hales, J. M. & Drewes, D. R. Solubility of ammonia in water at low concentrations. Atmos. Environ. 13, 1133–1147 (1979).
doi: 10.1016/0004-6981(79)90037-4
Gottwald, F. et al. Physical properties of ammonia solutions. Ammonium nitrate-ammonia-water and urea-ammonia-water. Ind. Eng. Chem. 44, 910–913 (1952).
doi: 10.1021/ie50508a054
Wang, X., Conway, W., Burns, R., McCann, N. & Maeder, M. Phys. Chem. A 114, 1734–1740 (2010).
doi: 10.1021/jp909019u
Estiu, G. & Merz, K. M. Catalyzed decomposition of urea. Molecular dynamics simulations of the binding of urea to urease. Biochemistry 45, 4429–4443 (2006).
pubmed: 16584179
doi: 10.1021/bi052020p
Sarigul, N., Korkmaz, F. & Kurultak, İ. A new artificial urine protocol to better imitate human urine. Sci. Rep. 9, 20159–20169 (2019).
pubmed: 31882896
pmcid: 6934465
doi: 10.1038/s41598-019-56693-4
Ishii, M. & Mishima, K. Two-fluid model and hydrodynamic constitutive relations. Nucl. Eng. Des. 82, 107–126 (1984).
doi: 10.1016/0029-5493(84)90207-3
Valdez, L., Shum, H., Ortiz-Rivera, I., Balazs, A. C. & Sen, A. Solutal and thermal buoyancy effects in self-powered phosphatase micropumps. Soft Matter 13, 2800–2807 (2017).
pubmed: 28345091
doi: 10.1039/C7SM00022G
Aranson, I. S. & Sapozhnikov, M. V. Theory of pattern formation of metallic microparticles in poorly conducting liquids. Phys. Rev. Lett. 92, 234301–234304 (2004).
pubmed: 15245160
doi: 10.1103/PhysRevLett.92.234301
Chen, S. et al. Collective buoyancy-driven dynamics of enzymatic nanomotors. Figshare, https://doi.org/10.6084/m9.figshare.27134523.v1 (2024).
Chen, S. et al. Collective buoyancy-driven dynamics of enzymatic nanomotors. Github, https://doi.org/10.5281/zenodo.13842706 (2024).