Multimodal Biofilm Inactivation Using a Photocatalytic Bismuth Perovskite-TiO2-Ru(II)polypyridyl-Based Multisite Heterojunction

Noufal Kandoth; Sonu Pratap Chaudhary; Shresth Gupta; Kumari Raksha; Atin Chatterjee; Shresth Gupta; Safakath Karuthedath; Catherine S.P. De Castro; Frédéric Laquai; Sumit Kumar Pramanik; Sayan Bhattacharyya; Amirul Islam Mallick; Amitava Das

doi:10.1021/acsnano.3c01064

Multimodal Biofilm Inactivation Using a Photocatalytic Bismuth Perovskite-TiO₂-Ru(II)polypyridyl-Based Multisite Heterojunction

Noufal Kandoth^*, Sonu Pratap Chaudhary, Shresth Gupta, Kumari Raksha, Atin Chatterjee, Shresth Gupta, Safakath Karuthedath, Catherine S.P. De Castro, Frédéric Laquai, Sumit Kumar Pramanik, Sayan Bhattacharyya^*, Amirul Islam Mallick^*, Amitava Das^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

12 Scopus citations

Abstract

Infectious bacterial biofilms are recalcitrant to most antibiotics compared to their planktonic version, and the lack of appropriate therapeutic strategies for mitigating them poses a serious threat to clinical treatment. A ternary heterojunction material derived from a Bi-based perovskite-TiO₂hybrid and a [Ru(2,2′-bpy)₂(4,4′-dicarboxy-2,2′-bpy)]²⁺(2,2′-bpy, 2,2′-bipyridyl) as a photosensitizer (RuPS) is developed. This hybrid material is found to be capable of generating reactive oxygen species (ROS)/reactive nitrogen species (RNS) upon solar light irradiation. The aligned band edges and effective exciton dynamics between multisite heterojunctions are established by steady-state/time-resolved optical and other spectroscopic studies. Proposed mechanistic pathways for the photocatalytic generation of ROS/RNS are rationalized based on a cascade-redox processes arising from three catalytic centers. These ROS/RNS are utilized to demonstrate a proof-of-concept in treating two elusive bacterial biofilms while maintaining a high level of biocompatibility (IC₅₀> 1 mg/mL). The in situ generation of radical species (ROS/RNS) upon photoirradiation is established with EPR spectroscopic measurements and colorimetric assays. Experimental results showed improved efficacy toward biofilm inactivation of the ternary heterojunction material as compared to their individual/binary counterparts under solar light irradiation. The multisite heterojunction formation helped with better exciton delocalization for an efficient catalytic biofilm inactivation. This was rationalized based on the favorable exciton dissociation followed by the onset of multiple oxidation and reduction sites in the ternary heterojunction. This together with exceptional photoelectric features of lead-free halide perovskites outlines a proof-of-principle demonstration in biomedical optoelectronics addressing multimodal antibiofilm/antimicrobial modality.

Original language	English (US)
Pages (from-to)	10393-10406
Number of pages	14
Journal	ACS Nano
Volume	17
Issue number	11
DOIs	https://doi.org/10.1021/acsnano.3c01064
State	Published - Jun 13 2023

Bibliographical note

Funding Information:
A.D. acknowledges SERB (India) Grants CRG/2020/000492 and JCB/2017/000004 for supporting this research. S.B. acknowledges SERB (India) Grants CRG/2020/000084 and STR/2021/00000 for supporting this research. N.K. acknowledges the SRA-CSIR scientist pool scheme (13/9144-A/2020-pool). S.P.C. thanks CSIR for a Research Fellowship (File No-09/921(0180)/2017-EMR-I). K.R. acknowledges the DST/INSPIRE program for a Ph.D. fellowship (IF170004). S.K.P. acknowledges DBT Grant BT/PR22251/NNT/28/1274/2017. Su.G. and Sh.G acknowledge MoE, Government of India, IISER Kolkata and Prime Ministers Research Fellowship, respectively, for their fellowships. The research reported in this publication was also partially supported by the King Abdullah University of Science and Technology (KAUST). N.K. and S.K. acknowledge FIRST India scientific outreach forum.

Publisher Copyright:
© 2023 American Chemical Society. All rights reserved.

Keywords

bacterial biofilm
bismuth perovskite halides
multiheterojunction
ruthenium polypyridyl complex
TiO

ASJC Scopus subject areas

General Materials Science
General Engineering
General Physics and Astronomy

Access to Document

10.1021/acsnano.3c01064

Cite this

Kandoth, N., Chaudhary, S. P., Gupta, S., Raksha, K., Chatterjee, A., Gupta, S., Karuthedath, S., De Castro, C. S. P., Laquai, F., Pramanik, S. K., Bhattacharyya, S., Mallick, A. I., & Das, A. (2023). Multimodal Biofilm Inactivation Using a Photocatalytic Bismuth Perovskite-TiO₂-Ru(II)polypyridyl-Based Multisite Heterojunction. ACS Nano, 17(11), 10393-10406. https://doi.org/10.1021/acsnano.3c01064

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title = "Multimodal Biofilm Inactivation Using a Photocatalytic Bismuth Perovskite-TiO2-Ru(II)polypyridyl-Based Multisite Heterojunction",

abstract = "Infectious bacterial biofilms are recalcitrant to most antibiotics compared to their planktonic version, and the lack of appropriate therapeutic strategies for mitigating them poses a serious threat to clinical treatment. A ternary heterojunction material derived from a Bi-based perovskite-TiO2hybrid and a [Ru(2,2′-bpy)2(4,4′-dicarboxy-2,2′-bpy)]2+(2,2′-bpy, 2,2′-bipyridyl) as a photosensitizer (RuPS) is developed. This hybrid material is found to be capable of generating reactive oxygen species (ROS)/reactive nitrogen species (RNS) upon solar light irradiation. The aligned band edges and effective exciton dynamics between multisite heterojunctions are established by steady-state/time-resolved optical and other spectroscopic studies. Proposed mechanistic pathways for the photocatalytic generation of ROS/RNS are rationalized based on a cascade-redox processes arising from three catalytic centers. These ROS/RNS are utilized to demonstrate a proof-of-concept in treating two elusive bacterial biofilms while maintaining a high level of biocompatibility (IC50> 1 mg/mL). The in situ generation of radical species (ROS/RNS) upon photoirradiation is established with EPR spectroscopic measurements and colorimetric assays. Experimental results showed improved efficacy toward biofilm inactivation of the ternary heterojunction material as compared to their individual/binary counterparts under solar light irradiation. The multisite heterojunction formation helped with better exciton delocalization for an efficient catalytic biofilm inactivation. This was rationalized based on the favorable exciton dissociation followed by the onset of multiple oxidation and reduction sites in the ternary heterojunction. This together with exceptional photoelectric features of lead-free halide perovskites outlines a proof-of-principle demonstration in biomedical optoelectronics addressing multimodal antibiofilm/antimicrobial modality.",

keywords = "bacterial biofilm, bismuth perovskite halides, multiheterojunction, ruthenium polypyridyl complex, TiO",

author = "Noufal Kandoth and Chaudhary, {Sonu Pratap} and Shresth Gupta and Kumari Raksha and Atin Chatterjee and Shresth Gupta and Safakath Karuthedath and {De Castro}, {Catherine S.P.} and Fr{\'e}d{\'e}ric Laquai and Pramanik, {Sumit Kumar} and Sayan Bhattacharyya and Mallick, {Amirul Islam} and Amitava Das",

note = "Funding Information: A.D. acknowledges SERB (India) Grants CRG/2020/000492 and JCB/2017/000004 for supporting this research. S.B. acknowledges SERB (India) Grants CRG/2020/000084 and STR/2021/00000 for supporting this research. N.K. acknowledges the SRA-CSIR scientist pool scheme (13/9144-A/2020-pool). S.P.C. thanks CSIR for a Research Fellowship (File No-09/921(0180)/2017-EMR-I). K.R. acknowledges the DST/INSPIRE program for a Ph.D. fellowship (IF170004). S.K.P. acknowledges DBT Grant BT/PR22251/NNT/28/1274/2017. Su.G. and Sh.G acknowledge MoE, Government of India, IISER Kolkata and Prime Ministers Research Fellowship, respectively, for their fellowships. The research reported in this publication was also partially supported by the King Abdullah University of Science and Technology (KAUST). N.K. and S.K. acknowledge FIRST India scientific outreach forum. Publisher Copyright: {\textcopyright} 2023 American Chemical Society. All rights reserved.",

year = "2023",

month = jun,

day = "13",

doi = "10.1021/acsnano.3c01064",

language = "English (US)",

volume = "17",

pages = "10393--10406",

journal = "ACS Nano",

issn = "1936-0851",

publisher = "American Chemical Society",

number = "11",

}

Kandoth, N, Chaudhary, SP, Gupta, S, Raksha, K, Chatterjee, A, Gupta, S, Karuthedath, S, De Castro, CSP, Laquai, F, Pramanik, SK, Bhattacharyya, S, Mallick, AI & Das, A 2023, 'Multimodal Biofilm Inactivation Using a Photocatalytic Bismuth Perovskite-TiO₂-Ru(II)polypyridyl-Based Multisite Heterojunction', ACS Nano, vol. 17, no. 11, pp. 10393-10406. https://doi.org/10.1021/acsnano.3c01064

TY - JOUR

T1 - Multimodal Biofilm Inactivation Using a Photocatalytic Bismuth Perovskite-TiO2-Ru(II)polypyridyl-Based Multisite Heterojunction

AU - Kandoth, Noufal

AU - Chaudhary, Sonu Pratap

AU - Gupta, Shresth

AU - Raksha, Kumari

AU - Chatterjee, Atin

AU - Gupta, Shresth

AU - Karuthedath, Safakath

AU - De Castro, Catherine S.P.

AU - Laquai, Frédéric

AU - Pramanik, Sumit Kumar

AU - Bhattacharyya, Sayan

AU - Mallick, Amirul Islam

AU - Das, Amitava

N1 - Funding Information: A.D. acknowledges SERB (India) Grants CRG/2020/000492 and JCB/2017/000004 for supporting this research. S.B. acknowledges SERB (India) Grants CRG/2020/000084 and STR/2021/00000 for supporting this research. N.K. acknowledges the SRA-CSIR scientist pool scheme (13/9144-A/2020-pool). S.P.C. thanks CSIR for a Research Fellowship (File No-09/921(0180)/2017-EMR-I). K.R. acknowledges the DST/INSPIRE program for a Ph.D. fellowship (IF170004). S.K.P. acknowledges DBT Grant BT/PR22251/NNT/28/1274/2017. Su.G. and Sh.G acknowledge MoE, Government of India, IISER Kolkata and Prime Ministers Research Fellowship, respectively, for their fellowships. The research reported in this publication was also partially supported by the King Abdullah University of Science and Technology (KAUST). N.K. and S.K. acknowledge FIRST India scientific outreach forum. Publisher Copyright: © 2023 American Chemical Society. All rights reserved.

PY - 2023/6/13

Y1 - 2023/6/13

N2 - Infectious bacterial biofilms are recalcitrant to most antibiotics compared to their planktonic version, and the lack of appropriate therapeutic strategies for mitigating them poses a serious threat to clinical treatment. A ternary heterojunction material derived from a Bi-based perovskite-TiO2hybrid and a [Ru(2,2′-bpy)2(4,4′-dicarboxy-2,2′-bpy)]2+(2,2′-bpy, 2,2′-bipyridyl) as a photosensitizer (RuPS) is developed. This hybrid material is found to be capable of generating reactive oxygen species (ROS)/reactive nitrogen species (RNS) upon solar light irradiation. The aligned band edges and effective exciton dynamics between multisite heterojunctions are established by steady-state/time-resolved optical and other spectroscopic studies. Proposed mechanistic pathways for the photocatalytic generation of ROS/RNS are rationalized based on a cascade-redox processes arising from three catalytic centers. These ROS/RNS are utilized to demonstrate a proof-of-concept in treating two elusive bacterial biofilms while maintaining a high level of biocompatibility (IC50> 1 mg/mL). The in situ generation of radical species (ROS/RNS) upon photoirradiation is established with EPR spectroscopic measurements and colorimetric assays. Experimental results showed improved efficacy toward biofilm inactivation of the ternary heterojunction material as compared to their individual/binary counterparts under solar light irradiation. The multisite heterojunction formation helped with better exciton delocalization for an efficient catalytic biofilm inactivation. This was rationalized based on the favorable exciton dissociation followed by the onset of multiple oxidation and reduction sites in the ternary heterojunction. This together with exceptional photoelectric features of lead-free halide perovskites outlines a proof-of-principle demonstration in biomedical optoelectronics addressing multimodal antibiofilm/antimicrobial modality.

AB - Infectious bacterial biofilms are recalcitrant to most antibiotics compared to their planktonic version, and the lack of appropriate therapeutic strategies for mitigating them poses a serious threat to clinical treatment. A ternary heterojunction material derived from a Bi-based perovskite-TiO2hybrid and a [Ru(2,2′-bpy)2(4,4′-dicarboxy-2,2′-bpy)]2+(2,2′-bpy, 2,2′-bipyridyl) as a photosensitizer (RuPS) is developed. This hybrid material is found to be capable of generating reactive oxygen species (ROS)/reactive nitrogen species (RNS) upon solar light irradiation. The aligned band edges and effective exciton dynamics between multisite heterojunctions are established by steady-state/time-resolved optical and other spectroscopic studies. Proposed mechanistic pathways for the photocatalytic generation of ROS/RNS are rationalized based on a cascade-redox processes arising from three catalytic centers. These ROS/RNS are utilized to demonstrate a proof-of-concept in treating two elusive bacterial biofilms while maintaining a high level of biocompatibility (IC50> 1 mg/mL). The in situ generation of radical species (ROS/RNS) upon photoirradiation is established with EPR spectroscopic measurements and colorimetric assays. Experimental results showed improved efficacy toward biofilm inactivation of the ternary heterojunction material as compared to their individual/binary counterparts under solar light irradiation. The multisite heterojunction formation helped with better exciton delocalization for an efficient catalytic biofilm inactivation. This was rationalized based on the favorable exciton dissociation followed by the onset of multiple oxidation and reduction sites in the ternary heterojunction. This together with exceptional photoelectric features of lead-free halide perovskites outlines a proof-of-principle demonstration in biomedical optoelectronics addressing multimodal antibiofilm/antimicrobial modality.

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KW - bismuth perovskite halides

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KW - ruthenium polypyridyl complex

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