Ultrafast Collective Excited-State Dynamics of a Virus-Supported Fluorophore Antenna

Holmes, Joseph; Sushma, Arathi Anil; Tsvetkova, Irina B.; Schaich, William L.; Schaller, Richard D.; Dragnea, Bogdan

doi:10.1021/acs.jpclett.2c00262

Title: Ultrafast Collective Excited-State Dynamics of a Virus-Supported Fluorophore Antenna

Journal Article · 04 April 2022 · Journal of Physical Chemistry Letters

DOI: https://doi.org/10.1021/acs.jpclett.2c00262 · OSTI ID:1898640

Holmes, Joseph ^[1]; Sushma, Arathi Anil ^[1]; Tsvetkova, Irina B. ^[1]; Schaich, William L. ^[1];

^[2];

^[1]

Indiana Univ., Bloomington, IN (United States)
Argonne National Lab. (ANL), Argonne, IL (United States)

Radiation brightening was recently observed in a multifluorophore-conjugated brome mosaic virus (BMV) particle at room temperature under pulsed excitation. On the basis of its nonlinear dependence on the number of chromophores, the origins of the phenomenon were attributed to a collective relaxation. However, the mechanism remains unknown. Here, we present ultrafast transient absorption and fluorescence spectroscopic studies which shed new light on the collective nature of the relaxation dynamics in such radiation-brightened, multifluorophore particles. Our findings indicate that the emission dynamics is consistent with a superradiance mechanism. The ratio between the rates of competing radiative and nonradiative relaxation pathways depends on the number of chromophores per virus. The findings suggest that small icosahedral virus shells provide a unique biological scaffold for developing nonclassical, deep subwavelength light sources and may open new avenues for the development of photonic probes for medical imaging applications.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Argonne National Laboratory (ANL)

Sponsoring Organization:: USDOE Office of Science; US Army Research Office (ARO); National Science Foundation (NSF)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1898640

Journal Information:: Journal of Physical Chemistry Letters, Journal Name: Journal of Physical Chemistry Letters Journal Issue: 14 Vol. 13; ISSN 1948-7185

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

References (43)

Single-Photon Superradiance from a Quantum Dot Tighineanu, Petru; Daveau, Raphaël S.; Lehmann, Tau B. Physical Review Letters, Vol. 116, Issue 16 https://doi.org/10.1103/PhysRevLett.116.163604	journal	April 2016
Picosecond coherence coupling in the pump and probe technique Vardeny, Z.; Tauc, J. Optics Communications, Vol. 39, Issue 6 https://doi.org/10.1016/0030-4018(81)90231-5	journal	November 1981
Photobleaching of organic fluorophores: quantitative characterization, mechanisms, protection Demchenko, Alexander P. Methods and Applications in Fluorescence, Vol. 8, Issue 2 https://doi.org/10.1088/2050-6120/ab7365	journal	February 2020
Raman spectra in spectrofluorimetry Parker, C. A. The Analyst, Vol. 84, Issue 1000 https://doi.org/10.1039/an9598400446	journal	January 1959
Laser characteristics of KCL:O-2 Wilk, Stephen R.; Boyd, Robert W.; Teegarden, Kenneth J. Optics Communications, Vol. 47, Issue 6 https://doi.org/10.1016/0030-4018(83)90316-4	journal	October 1983
Transition from superfluorescence to amplified spontaneous emission Malcuit, Michelle S.; Maki, Jeffery J.; Simkin, David J. Physical Review Letters, Vol. 59, Issue 11 https://doi.org/10.1103/PhysRevLett.59.1189	journal	September 1987
Superradiance: An essay on the theory of collective spontaneous emission Gross, M.; Haroche, S. Physics Reports, Vol. 93, Issue 5 https://doi.org/10.1016/0370-1573(82)90102-8	journal	December 1982
Tunable and ultra-stable UV light-switchable fluorescent composites for information hiding and storage Li, Mengxiao; Feng, Yu; Tian, Qingyong Dalton Transactions, Vol. 47, Issue 32 https://doi.org/10.1039/C8DT02475H	journal	January 2018
Superradiance and Exciton (De)localization in Light-Harvesting Complex II from Green Plants? ^† Palacios, Miguel A.; de Weerd, Frank L.; Ihalainen, Janne A. The Journal of Physical Chemistry B, Vol. 106, Issue 22 https://doi.org/10.1021/jp014078t	journal	June 2002
Dicke superradiance in solids [Invited] Cong, Kankan; Zhang, Qi; Wang, Yongrui Journal of the Optical Society of America B, Vol. 33, Issue 7 https://doi.org/10.1364/JOSAB.33.000C80	journal	January 2016
Superradiance in molecular aggregates Spano, Frank C.; Mukamel, Shaul The Journal of Chemical Physics, Vol. 91, Issue 2 https://doi.org/10.1063/1.457174	journal	July 1989
Radiation Brightening from Virus-like Particles Tsvetkova, Irina B.; Anil Sushma, Arathi; Wang, Joseph Che-Yen ACS Nano, Vol. 13, Issue 10 https://doi.org/10.1021/acsnano.9b04786	journal	July 2019
Fluorescent probes for bioimaging of potential biomarkers in Parkinson's disease Gao, Liqian; Wang, Wei; Wang, Xuan Chemical Society Reviews, Vol. 50, Issue 2 https://doi.org/10.1039/D0CS00115E	journal	January 2021
Fluorescent Biosensors for Neurotransmission and Neuromodulation: Engineering and Applications Leopold, Anna V.; Shcherbakova, Daria M.; Verkhusha, Vladislav V. Frontiers in Cellular Neuroscience, Vol. 13 https://doi.org/10.3389/fncel.2019.00474	journal	October 2019
Effect of concentration quenching on fluorescence recovery after photobleaching measurements Robeson, J. L.; Tilton, R. D. Biophysical Journal, Vol. 68, Issue 5 https://doi.org/10.1016/S0006-3495(95)80397-8	journal	May 1995
Near Infrared Fluorescence Imaging in Nano-Therapeutics and Photo-Thermal Evaluation Vats, Mukti; Mishra, Sumit; Baghini, Mahdieh International Journal of Molecular Sciences, Vol. 18, Issue 5 https://doi.org/10.3390/ijms18050924	journal	April 2017
Near-infrared fluorescent probes in cancer imaging and therapy: an emerging field Yi, Xiaomin; Wang, Fuli; Qin, Weijun International Journal of Nanomedicine https://doi.org/10.2147/IJN.S60206	journal	March 2014
Exploiting Chromophore–Protein Interactions through Linker Engineering To Tune Photoinduced Dynamics in a Biomimetic Light-Harvesting Platform Delor, Milan; Dai, Jing; Roberts, Trevor D. Journal of the American Chemical Society, Vol. 140, Issue 20 https://doi.org/10.1021/jacs.7b13598	journal	May 2018
Concentration quenching in chlorophyll Beddard, G. S.; Porter, G. Nature, Vol. 260, Issue 5549 https://doi.org/10.1038/260366a0	journal	March 1976
Photoluminescent and Chromic Nanomaterials for Anticounterfeiting Technologies: Recent Advances and Future Challenges Abdollahi, Amin; Roghani-Mamaqani, Hossein; Razavi, Bahareh ACS Nano, Vol. 14, Issue 11 https://doi.org/10.1021/acsnano.0c07289	journal	October 2020
Brief comment: Dicke Superradiance and Superfluorescence Find Application for Remote Sensing in Air Dai, D. C. arXiv https://doi.org/10.48550/arXiv.1108.5360	preprint	January 2011
Influence of collisional dephasing processes on superfluorescence Maki, Jeffery J.; Malcuit, Michelle S.; Raymer, Michael G. Physical Review A, Vol. 40, Issue 9 https://doi.org/10.1103/PhysRevA.40.5135	journal	November 1989
Amplified Spontaneous Emission and External Signal Amplification in an Inverted Medium Allen, L.; Peters, G. I. Physical Review A, Vol. 8, Issue 4 https://doi.org/10.1103/PhysRevA.8.2031	journal	October 1973
New red-fluorescent calcium indicators for optogenetics, photoactivation and multi-color imaging Oheim, Martin; van 't Hoff, Marcel; Feltz, Anne Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1843, Issue 10 https://doi.org/10.1016/j.bbamcr.2014.03.010	journal	October 2014
Subset of Fluorophores Is Responsible for Radiation Brightening in Viromimetic Particles Anil Sushma, Arathi; Zhao, Bingqing; Tsvetkova, Irina B. The Journal of Physical Chemistry B, Vol. 125, Issue 37 https://doi.org/10.1021/acs.jpcb.1c06395	journal	September 2021
Ultrashort Radiation of Biexcitonic Superfluorescence from High-Density Assembly of Semiconductor Quantum Dots Miyajima, Kensuke; Kumagai, Yuki; Ishikawa, Akira The Journal of Physical Chemistry C, Vol. 121, Issue 49 https://doi.org/10.1021/acs.jpcc.7b09795	journal	December 2017
How to recognize lasing Samuel, Ifor D. W.; Namdas, Ebinazar B.; Turnbull, Graham A. Nature Photonics, Vol. 3, Issue 10 https://doi.org/10.1038/nphoton.2009.173	journal	October 2009
Superfluorescence from lead halide perovskite quantum dot superlattices Rainò, Gabriele; Becker, Michael A.; Bodnarchuk, Maryna I. Nature, Vol. 563, Issue 7733 https://doi.org/10.1038/s41586-018-0683-0	journal	November 2018
An overview of nanoparticles commonly used in fluorescent bioimaging Wolfbeis, Otto S. Chemical Society Reviews, Vol. 44, Issue 14 https://doi.org/10.1039/C4CS00392F	journal	January 2015
Quantum-statistical analysis of superfluorescence and amplified spontaneous emission in dense media Rai, Jagdish; Bowden, Charles M. Physical Review A, Vol. 46, Issue 3 https://doi.org/10.1103/PhysRevA.46.1522	journal	August 1992
Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems Engel, Gregory S.; Calhoun, Tessa R.; Read, Elizabeth L. Nature, Vol. 446, Issue 7137 https://doi.org/10.1038/nature05678	journal	April 2007
Correlated Protein Environments Drive Quantum Coherence Lifetimes in Photosynthetic Pigment-Protein Complexes Rolczynski, Brian S.; Zheng, Haibin; Singh, Ved P. Chem, Vol. 4, Issue 1 https://doi.org/10.1016/j.chempr.2017.12.009	journal	January 2018
Elimination of the Coherent Artifact in a Pump-Probe Experiment by Directly Detecting the Background-Free Diffraction Signal Liu, Hui; Zhang, Hang; Si, Jin-Hai Chinese Physics Letters, Vol. 28, Issue 8 https://doi.org/10.1088/0256-307X/28/8/086602	journal	August 2011
Monodisperse Long-Chain Sulfobetaine-Capped CsPbBr ₃ Nanocrystals and Their Superfluorescent Assemblies Krieg, Franziska; Sercel, Peter C.; Burian, Max ACS Central Science, Vol. 7, Issue 1 https://doi.org/10.1021/acscentsci.0c01153	journal	December 2020
Superradiance of bacteriochlorophyll c aggregates in chlorosomes of green photosynthetic bacteria Malina, Tomáš; Koehorst, Rob; Bína, David Scientific Reports, Vol. 11, Issue 1 https://doi.org/10.1038/s41598-021-87664-3	journal	April 2021
Superradiant Emission from Coherent Excitons in van Der Waals Heterostructures Haider, Golam; Sampathkumar, Krishna; Verhagen, Tim Advanced Functional Materials, Vol. 31, Issue 29 https://doi.org/10.1002/adfm.202102196	journal	May 2021
Superradiance of J-aggregates: correspondence between an infinite disordered chain and a regular finite chain Ratner, M. A. Low Temperature Physics, Vol. 29, Issue 7 https://doi.org/10.1063/1.1596593	journal	July 2003
Superradiance and Exciton Delocalization in Bacterial Photosynthetic Light-Harvesting Systems Monshouwer, René; Abrahamsson, Malin; van Mourik, Frank The Journal of Physical Chemistry B, Vol. 101, Issue 37 https://doi.org/10.1021/jp963377t	journal	September 1997
Manipulating Excited-State Dynamics of Individual Light-Harvesting Chromophores through Restricted Motions in a Hydrated Nanoscale Protein Cavity Noriega, Rodrigo; Finley, Daniel T.; Haberstroh, John The Journal of Physical Chemistry B, Vol. 119, Issue 23 https://doi.org/10.1021/acs.jpcb.5b03784	journal	June 2015
Fluorescent probes for sensing and imaging Ueno, Tasuku; Nagano, Tetsuo Nature Methods, Vol. 8, Issue 8 https://doi.org/10.1038/nmeth.1663	journal	July 2011
Coherence in Spontaneous Radiation Processes Dicke, R. H. Physical Review, Vol. 93, Issue 1 https://doi.org/10.1103/PhysRev.93.99	journal	January 1954
Artifacts in femtosecond transient absorption spectroscopy Lorenc, M.; Ziolek, M.; Naskrecki, R. Applied Physics B: Lasers and Optics, Vol. 74, Issue 1 https://doi.org/10.1007/s003400100750	journal	January 2002
Superradiance in Molecular H Aggregates Meinardi, F.; Cerminara, M.; Sassella, A. Physical Review Letters, Vol. 91, Issue 24 https://doi.org/10.1103/PhysRevLett.91.247401	journal	December 2003

Similar Records

Possible replicative form of brome mosaic virus RNA 4

Journal Article · 1976 · Virology; (United States) · OSTI ID:7346972

Bastin, M; Kaesberg, P

Packaging and structural phenotype of brome mosaic virus capsid protein with altered N-terminal {beta}-hexamer structure

Journal Article · 2011 · Virology · OSTI ID:21587893

Wispelaere, Melissanne de; Chaturvedi, Sonali; Wilkens, Stephan; +1 more

Live cell imaging of interactions between replicase and capsid protein of Brome mosaic virus using Bimolecular Fluorescence Complementation: Implications for replication and genome packaging

Journal Article · 2014 · Virology · OSTI ID:22435054

Chaturvedi, Sonali; Rao, A. L.N.,

Related Subjects

37
Amplified Spontaneous Emission
Coherence
Radiation
Superfluorescence
Superradiance

Title: Ultrafast Collective Excited-State Dynamics of a Virus-Supported Fluorophore Antenna

Citation Formats

References (43)

Similar Records

Related Subjects