Single-photon microscopy to study biomolecular condensates

Eleonora Perego, Sabrina Zappone, Francesco Castagnetti, Davide Mariani, Erika Vitiello, Jakob Rupert, Elsa Zacco, Gian Gaetano Tartaglia, Irene Bozzoni, Eli Slenders and Giuseppe Vicidomini ()
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Eleonora Perego: Istituto Italiano di Tecnologia
Sabrina Zappone: Istituto Italiano di Tecnologia
Francesco Castagnetti: Istituto Italiano di Tecnologia
Davide Mariani: Istituto Italiano di Tecnologia
Erika Vitiello: Istituto Italiano di Tecnologia
Jakob Rupert: Istituto Italiano di Tecnologia
Elsa Zacco: Istituto Italiano di Tecnologia
Gian Gaetano Tartaglia: Istituto Italiano di Tecnologia
Irene Bozzoni: Istituto Italiano di Tecnologia
Eli Slenders: Istituto Italiano di Tecnologia
Giuseppe Vicidomini: Istituto Italiano di Tecnologia

Nature Communications, 2023, vol. 14, issue 1, 1-14

Abstract: Abstract Biomolecular condensates serve as membrane-less compartments within cells, concentrating proteins and nucleic acids to facilitate precise spatial and temporal orchestration of various biological processes. The diversity of these processes and the substantial variability in condensate characteristics present a formidable challenge for quantifying their molecular dynamics, surpassing the capabilities of conventional microscopy. Here, we show that our single-photon microscope provides a comprehensive live-cell spectroscopy and imaging framework for investigating biomolecular condensation. Leveraging a single-photon detector array, single-photon microscopy enhances the potential of quantitative confocal microscopy by providing access to fluorescence signals at the single-photon level. Our platform incorporates photon spatiotemporal tagging, which allowed us to perform time-lapse super-resolved imaging for molecular sub-diffraction environment organization with simultaneous monitoring of molecular mobility, interactions, and nano-environment properties through fluorescence lifetime fluctuation spectroscopy. This integrated correlative study reveals the dynamics and interactions of RNA-binding proteins involved in forming stress granules, a specific type of biomolecular condensates, across a wide range of spatial and temporal scales. Our versatile framework opens up avenues for exploring a broad spectrum of biomolecular processes beyond the formation of membrane-less organelles.

Date: 2023
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DOI: 10.1038/s41467-023-43969-7

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