Developing bioinspired materials to convert sunlight into electricity efficiently is paramount for sustainable energy production. Fluorescent proteins are promising candidates as photoactive materials due to their high fluorescence quantum yield and absorption extinction coefficients in aqueous media. However, developing artificial bioinspired photosynthetic systems requires a detailed understanding of molecular interactions and energy transfer mechanisms in the required operating conditions. Here, the supramolecular self-assembly and photophysical properties of fluorescent proteins complexed with organic dyes are investigated in aqueous media. Supercharged mGreenLantern protein, mutated to have a charge of +22, is complexed together with anionic zinc phthalocyanines having 4 or 16 carboxylate groups. The structural characterization reveals a strong electrostatic interaction between the moieties, accompanied by partial conformational distortion of the protein structure, yet without compromising the mGreenLantern chromophore integrity as suggested by the lack of emission features related to the neutral form of the chromophore. The self-assembled biohybrid shows a total quenching of protein fluorescence, in favor of an energy transfer process from the protein to the phthalocyanine, as demonstrated by fluorescence lifetime and ultrafast transient absorption measurements. These results provide insight into the rich photophysics of fluorescent protein-dye complexes, anticipating their applicability as water-based photoactive materials.

Department of Bioproducts and Biosystems Aalto University Aalto 00076 Finland

Faculty of Engineering and Natural Sciences Tampere University Korkeakoulunkatu 8 Tampere 33720 Finland

Faculty of Pharmacy in Hradec Kralove Charles University Ak Heyrovskeho 1203 Hradec Kralove 50003 Czech Republic

Technical University of Munich Campus Straubing for Biotechnology and Sustainability Chair of Biogenic Functional Materials Schulgasse 22 94315 Straubing Germany

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Gust D., Moore T. A., Science 1989, 244, 35. PubMed

Berardi S., Drouet S., Francas L., Gimbert‐Surinach C., Guttentag M., Richmond C., Stoll T., Llobet A., Chem. Soc. Rev. 2014, 43, 7501. PubMed

Barber J., Chem. Soc. Rev. 2009, 38, 185. PubMed

Barber J., Tran P. D., J. R. Soc. Interface 2013, 10, 20120984. PubMed PMC

Croce R., van Amerongen H., Nat. Chem. Biol. 2014, 10, 492. PubMed

Zhang D., Liu Y., Fan Y., Yu C., Zheng Y., Jin H., Fu L., Zhou Y., Yan D., Adv. Funct. Mater. 2016, 26, 7652.

Bonchio M., Syrgiannis Z., Burian M., Marino N., Pizzolato E., Dirian K., Rigodanza F., Volpato G. A., Ganga G. L.a, Demitri N., Berardi S., Amenitsch H., Guldi D. M., Caramori S., Bignozzi C. A., Sartorel A., Prato M., Nat. Chem. 2019, 11, 146. PubMed

Tian J., Zhang Y., Du L., He Y., Jin X. H., Pearce S., Eloi J. C., Harniman R. L., Alibhai D., Ye R., Phillips D. L., Manners I., Nat. Chem. 2020, 12, 1150. PubMed

Anaya‐Plaza E., Joseph J., Bauroth S., Wagner M., Dolle C., Sekita M., Grohn F., Spiecker E., Clark T., de la Escosura A., Guldi D. M., Torres T., Angew. Chem., Int. Ed. 2020, 59, 18786. PubMed PMC

Chen X. F., Gobeze H. B., D'Souza F., Chem. ‐ Eur. J. 2023, 29, e202300709. PubMed

Hao M., Sun G., Zuo M., Xu Z., Chen Y., Hu X. Y., Wang L., Angew. Chem., Int. Ed. 2020, 59, 10095. PubMed

Fernandez‐Luna V., Coto P. B., Costa R. D., Angew. Chem., Int. Ed. 2018, 57, 8826. PubMed

Pikas D. J., Kirkpatrick S. M., Tewksbury E., Brott L. L., Naik R. R., Stone M. O., Dennis W. M., J. Phys. Chem. B 2002, 106, 4831.

Gather M. C., Yun S. H., Nat. Photonics 2011, 5, 406.

Weber M. D., Niklaus L., Proschel M., Coto P. B., Sonnewald U., Costa R. D., Adv. Mater. 2015, 27, 5493. PubMed

Niklaus L., Tansaz S., Dakhil H., Weber K. T., Pröschel M., Lang M., Kostrzewa M., Coto P. B., Detsch R., Sonnewald U., Wierschem A., Boccaccini A. R., Costa R. D., Adv. Funct. Mater. 2016, 27, 1601792.

Press D. A., Melikov R., Conkar D., Firat‐Karalar E. N., Nizamoglu S., Nanotechnology 2016, 27, 45LT01. PubMed

Nizamoglu S., SDÜ fen bilim. enst. Derg. 2016, 20, 89206.

Thompson D. B., Cronican J. J., Liu D. R., in Methods Enzymol. 2012, 503, 293. PubMed PMC

Patrian M., Shaukat A., Nieddu M., Banda‐Vazquez J. A., Timonen J. V. I., Fuenzalida Werner J. P., Anaya‐Plaza E., Kostiainen M. A., Costa R. D., ACS Nano 2023, 17, 21206. PubMed PMC

Lawrence M. S., Phillips K. J., Liu D. R., J. Am. Chem. Soc. 2007, 129, 10110. PubMed PMC

Chuang W. T., Chen B. S., Chen K. Y., Hsieh C. C., Chou P. T., Chem. Commun. 2009, 6982, 10.1039/b908542d. PubMed DOI

Chowdhury S., Nieddu M., Patrian M., Gutiérrez‐Armayor D., Cavinato L. M., Fuenzalida‐Werner J. P., Lleó M. G., Ligi S., Costa R. D., Adv. Mat. Technol. 2024, 01968.

Sadeghi S., Melikov R., Bahmani Jalali H., Karatum O., Srivastava S. B., Conkar D., Firat‐Karalar E. N., Nizamoglu S., ACS Appl. Mater. Interfaces 2019, 11, 8710. PubMed

Chirgwandi Z., Panas I., Johansson L.‐G., Nordén B., Willander M., Winkler D., Ågren H., J. Phys. Chem. C 2008, 112, 18717.

de la Torre G., Claessens C. G., Torres T., Chem. Commun. 2007, 2000–2015, 4234f. PubMed

Rio Y., Rodriguez‐Morgade M. S., Torres T., Org. Biomol. Chem. 2008, 6, 1877. PubMed

Wang A., Long L., Zhang C., J. Incl. Phenom. Macrocycl. Chem. 2011, 71, 1.

Balcik‐Ercin P., Ekineker G., Salik N., Aydogdu B., Yagci T., Goksel M., Photodiag. Photodyn. Ther. 2023, 43, 103667. PubMed

Lau J. T., Lo P. C., Jiang X. J., Wang Q., Ng D. K., J. Med. Chem. 2014, 57, 4088. PubMed

Lau J. T., Lo P. C., Fong W. P., Ng D. K., Chem. ‐ Eur. J. 2011, 17, 7569. PubMed

Dumoulin F., Durmuş M., Ahsen V., Nyokong T., Coord. Chem. Rev. 2010, 254, 2792.

Rahali A., Shaukat A., Almeida‐Marrero V., Jamoussi B., de la Escosura A., Torres T., Kostiainen M. A., Anaya‐Plaza E., Bioconjug. Chem. 2021, 32, 1123. PubMed PMC

Halaskova M., Rahali A., Almeida‐Marrero V., Machacek M., Kucera R., Jamoussi B., Torres T., Novakova V., de la Escosura A., Zimcik P., ACS Med. Chem. Lett. 2021, 12, 502. PubMed PMC

Halaskova M., Kostelansky F., Demuth J., Hlbocanova I., Miletin M., Zimcik P., Machacek M., Novakova V., ChemPlusChem 2022, 87, 202200133. PubMed

Machacek M., Kollár J., Miletin M., Kučera R., Kubát P., Simunek T., Novakova V., Zimcik P., RSC Adv. 2016, 6, 10064.

Kollar J., Machacek M., Halaskova M., Lenco J., Kucera R., Demuth J., Rohlickova M., Hasonova K., Miletin M., Novakova V., Zimcik P., J. Med. Chem. 2020, 63, 7616. PubMed

Tunç G., Albakour M., Ahsen V., Gürek A. G., J. Porphyr. Phthalocyanines 2019, 23, 1355.

Shaukat A., Anaya‐Plaza E., Julin S., Linko V., Torres T., de la Escosura A., Kostiainen M. A., Chem. Commun. 2020, 56, 7341. PubMed

Anaya‐Plaza E., Aljarilla A., Beaune G., Nonappa, J. V. I. T. , de la Escosura A., Torres T., Kostiainen M. A., Adv. Mater. 2019, 31, 1902582. PubMed

Mikkila J., Anaya‐Plaza E., Liljestrom V., Caston J. R., Torres T., de la Escosura A., Kostiainen M. A., ACS Nano 2016, 10, 1565. PubMed

Almeida‐Marrero V., van de Winckel E., Anaya‐Plaza E., Torres T., de la Escosura A., Chem. Soc. Rev. 2018, 47, 7369. PubMed

Brasch M., de la Escosura A., Ma Y., Uetrecht C., Heck A. J., Torres T., Cornelissen J. J., J. Am. Chem. Soc. 2011, 133, 6878. PubMed

Luque D., Escosura A. d. l., Snijder J., Brasch M., Burnley R. J., Koay M. S. T., Carrascosa J. L., Wuite G. J. L., Roos W. H., Heck A. J. R., Cornelissen J. J. L. M., Torres T., Castón J. R., Chem. Sci. 2014, 5, 575.

Dee D. R., Gupta A. N., Anikovskiy M., Sosova I., Grandi E., Rivera L., Vincent A., Brigley A. M., Petersen N. O., Woodside M. T., Biochim. Biophys. Acta 2012, 1824, 826. PubMed

Li X., Zheng B.‐D., Peng X.‐H., Li S.‐Z., Ying J.‐W., Zhao Y., Huang J.‐D., Yoon J., Coord. Chem. Rev. 2019, 379, 147.

Mejias S. H., Roelfes G., Browne W. R., Phys. Chem. Chem. Phys. 2020, 22, 12228. PubMed

Roguin L. P., Chiarante N., Garcia Vior M. C., Marino J., Int. J. Biochem. Cell Biol. 2019, 114, 105575. PubMed

Bottari G., Trukhina O., Ince M., Torres T., Coord. Chem. Rev. 2012, 256, 2453.

Walter M. G., Rudine A. B., Wamser C. C., J. Porphyrins Phthalocyanines 2012, 14, 759.

Liljestrom V., Mikkila J., Kostiainen M. A., Nat. Commun. 2014, 5, 4445. PubMed PMC

Liljestrom V., Ora A., Hassinen J., Rekola H. T., Nonappa M. H., Hynninen V., Joensuu J. J., Ras R. H. A., Torma P., Ikkala O., Kostiainen M. A., Nat. Commun. 2017, 8, 671. PubMed PMC

Fuenzalida J. P., Nareddy P. K., Moreno‐Villoslada I., Moerschbacher B. M., Swamy M. J., Pan S., Ostermeier M., Goycoolea F. M., Food Hydrocoll 2016, 53, 239.

Bian T., Gardin A., Gemen J., Houben L., Perego C., Lee B., Elad N., Chu Z., Pavan G. M., Klajn R., Nat. Chem. 2021, 13, 940. PubMed PMC

Prelesnik J. L., Alberstein R. G., Zhang S., Pyles H., Baker D., Pfaendtner J., De Yoreo J. J., Tezcan F. A., Remsing R. C., Mundy C. J., Proc. Natl. Acad. Sci. USA 2021, 118, 121118. PubMed PMC

Visser N. V., Hink M. A., Borst J. W., van der Krogt G. N., Visser A. J., FEBS Lett. 2002, 521, 31. PubMed

Svilenov H. L., Menzen T., Richter K., Winter G., Mol. Pharmaceutics 2020, 17, 2638. PubMed

Yuan L., Lin W., Zheng K., Zhu S., Acc. Chem. Res. 2013, 46, 1462. PubMed

Ruckebusch C., Sliwa M., Pernot P., de Juan A., Tauler R., J. Photochem. Photobiol. C 2012, 13, 1.

Berberan‐Santos M. N., Bodunov E. N., Valeur B., Chem. Phys. 2005, 315, 171.

Jurrus E., Engel D., Star K., Monson K., Brandi J., Felberg L. E., Brookes D. H., Wilson L., Chen J., Liles K., Chun M., Li P., Gohara D. W., Dolinsky T., Konecny R., Koes D. R., Nielsen J. E., Head‐Gordon T., Geng W., Krasny R., Wei G. W., Holst M. J., McCammon J. A., Baker N. A., Protein Sci. 2018, 27, 112. PubMed PMC

Khan R., Ali‐Loytty H., Saari J., Valden M., Tukiainen A., Lahtonen K., Tkachenko N. V., Nanomaterials 2020, 10, 10081567. PubMed PMC