Photoinduced hole hopping through tryptophans in proteins
Hole hopping through tryptophan/tyrosine chains enables rapid unidirectional charge transport over long distances. We have elucidated structural and dynamical factors controlling hopping speed and efficiency in two modified azurin constructs that include a rhenium(I) sensitizer, Re(His)(CO) (dmp) ,...
Uložené v:
| Vydané v: | Proceedings of the National Academy of Sciences - PNAS Ročník 118; číslo 11 |
|---|---|
| Hlavní autori: | , , , , , |
| Médium: | Journal Article |
| Jazyk: | English |
| Vydavateľské údaje: |
United States
16.03.2021
|
| Predmet: | |
| ISSN: | 1091-6490, 1091-6490 |
| On-line prístup: | Zistit podrobnosti o prístupe |
| Tagy: |
Pridať tag
Žiadne tagy, Buďte prvý, kto otaguje tento záznam!
|
| Abstract | Hole hopping through tryptophan/tyrosine chains enables rapid unidirectional charge transport over long distances. We have elucidated structural and dynamical factors controlling hopping speed and efficiency in two modified azurin constructs that include a rhenium(I) sensitizer, Re(His)(CO)
(dmp)
, and one or two tryptophans (W
, W
). Experimental kinetics investigations showed that the two closely spaced (3 to 4 Å) intervening tryptophans dramatically accelerated long-range electron transfer (ET) from Cu
to the photoexcited sensitizer. In our theoretical work, we found that time-dependent density-functional theory (TDDFT) quantum mechanics/molecular mechanics/molecular dynamics (QM/MM/MD) trajectories of low-lying triplet excited states of Re
(His)(CO)
(dmp)
-W
(-W
) exhibited crossings between sensitizer-localized (*Re) and charge-separated [Re
(His)(CO)
(dmp
)/(W
or W
)] (CS1 or CS2) states. Our analysis revealed that the distances, angles, and mutual orientations of ET-active cofactors fluctuate in a relatively narrow range in which the cofactors are strongly coupled, enabling adiabatic ET. Water-dominated electrostatic field fluctuations bring *Re and CS1 states to a crossing where *Re(CO)
(dmp)
←W
ET occurs, and CS1 becomes the lowest triplet state. ET is promoted by solvation dynamics around *Re(CO)
(dmp)
(W
); and CS1 is stabilized by Re(dmp
)/W
electron/hole interaction and enhanced W
solvation. The second hop, W
←W
, is facilitated by water fluctuations near the W
/W
unit, taking place when the electrostatic potential at W
drops well below that at W
Insufficient solvation and reorganization around W
make W
←W
ET endergonic, shifting the equilibrium toward W
and decreasing the charge-separation yield. We suggest that multiscale TDDFT/MM/MD is a suitable technique to model the simultaneous evolution of photogenerated excited-state manifolds. |
|---|---|
| AbstractList | Hole hopping through tryptophan/tyrosine chains enables rapid unidirectional charge transport over long distances. We have elucidated structural and dynamical factors controlling hopping speed and efficiency in two modified azurin constructs that include a rhenium(I) sensitizer, Re(His)(CO)3(dmp)+, and one or two tryptophans (W1, W2). Experimental kinetics investigations showed that the two closely spaced (3 to 4 Å) intervening tryptophans dramatically accelerated long-range electron transfer (ET) from CuI to the photoexcited sensitizer. In our theoretical work, we found that time-dependent density-functional theory (TDDFT) quantum mechanics/molecular mechanics/molecular dynamics (QM/MM/MD) trajectories of low-lying triplet excited states of ReI(His)(CO)3(dmp)+-W1(-W2) exhibited crossings between sensitizer-localized (*Re) and charge-separated [ReI(His)(CO)3(dmp•-)/(W1•+ or W2•+)] (CS1 or CS2) states. Our analysis revealed that the distances, angles, and mutual orientations of ET-active cofactors fluctuate in a relatively narrow range in which the cofactors are strongly coupled, enabling adiabatic ET. Water-dominated electrostatic field fluctuations bring *Re and CS1 states to a crossing where *Re(CO)3(dmp)+←W1 ET occurs, and CS1 becomes the lowest triplet state. ET is promoted by solvation dynamics around *Re(CO)3(dmp)+(W1); and CS1 is stabilized by Re(dmp•-)/W1•+ electron/hole interaction and enhanced W1•+ solvation. The second hop, W1•+←W2, is facilitated by water fluctuations near the W1/W2 unit, taking place when the electrostatic potential at W2 drops well below that at W1•+ Insufficient solvation and reorganization around W2 make W1•+←W2 ET endergonic, shifting the equilibrium toward W1•+ and decreasing the charge-separation yield. We suggest that multiscale TDDFT/MM/MD is a suitable technique to model the simultaneous evolution of photogenerated excited-state manifolds.Hole hopping through tryptophan/tyrosine chains enables rapid unidirectional charge transport over long distances. We have elucidated structural and dynamical factors controlling hopping speed and efficiency in two modified azurin constructs that include a rhenium(I) sensitizer, Re(His)(CO)3(dmp)+, and one or two tryptophans (W1, W2). Experimental kinetics investigations showed that the two closely spaced (3 to 4 Å) intervening tryptophans dramatically accelerated long-range electron transfer (ET) from CuI to the photoexcited sensitizer. In our theoretical work, we found that time-dependent density-functional theory (TDDFT) quantum mechanics/molecular mechanics/molecular dynamics (QM/MM/MD) trajectories of low-lying triplet excited states of ReI(His)(CO)3(dmp)+-W1(-W2) exhibited crossings between sensitizer-localized (*Re) and charge-separated [ReI(His)(CO)3(dmp•-)/(W1•+ or W2•+)] (CS1 or CS2) states. Our analysis revealed that the distances, angles, and mutual orientations of ET-active cofactors fluctuate in a relatively narrow range in which the cofactors are strongly coupled, enabling adiabatic ET. Water-dominated electrostatic field fluctuations bring *Re and CS1 states to a crossing where *Re(CO)3(dmp)+←W1 ET occurs, and CS1 becomes the lowest triplet state. ET is promoted by solvation dynamics around *Re(CO)3(dmp)+(W1); and CS1 is stabilized by Re(dmp•-)/W1•+ electron/hole interaction and enhanced W1•+ solvation. The second hop, W1•+←W2, is facilitated by water fluctuations near the W1/W2 unit, taking place when the electrostatic potential at W2 drops well below that at W1•+ Insufficient solvation and reorganization around W2 make W1•+←W2 ET endergonic, shifting the equilibrium toward W1•+ and decreasing the charge-separation yield. We suggest that multiscale TDDFT/MM/MD is a suitable technique to model the simultaneous evolution of photogenerated excited-state manifolds. Hole hopping through tryptophan/tyrosine chains enables rapid unidirectional charge transport over long distances. We have elucidated structural and dynamical factors controlling hopping speed and efficiency in two modified azurin constructs that include a rhenium(I) sensitizer, Re(His)(CO) (dmp) , and one or two tryptophans (W , W ). Experimental kinetics investigations showed that the two closely spaced (3 to 4 Å) intervening tryptophans dramatically accelerated long-range electron transfer (ET) from Cu to the photoexcited sensitizer. In our theoretical work, we found that time-dependent density-functional theory (TDDFT) quantum mechanics/molecular mechanics/molecular dynamics (QM/MM/MD) trajectories of low-lying triplet excited states of Re (His)(CO) (dmp) -W (-W ) exhibited crossings between sensitizer-localized (*Re) and charge-separated [Re (His)(CO) (dmp )/(W or W )] (CS1 or CS2) states. Our analysis revealed that the distances, angles, and mutual orientations of ET-active cofactors fluctuate in a relatively narrow range in which the cofactors are strongly coupled, enabling adiabatic ET. Water-dominated electrostatic field fluctuations bring *Re and CS1 states to a crossing where *Re(CO) (dmp) ←W ET occurs, and CS1 becomes the lowest triplet state. ET is promoted by solvation dynamics around *Re(CO) (dmp) (W ); and CS1 is stabilized by Re(dmp )/W electron/hole interaction and enhanced W solvation. The second hop, W ←W , is facilitated by water fluctuations near the W /W unit, taking place when the electrostatic potential at W drops well below that at W Insufficient solvation and reorganization around W make W ←W ET endergonic, shifting the equilibrium toward W and decreasing the charge-separation yield. We suggest that multiscale TDDFT/MM/MD is a suitable technique to model the simultaneous evolution of photogenerated excited-state manifolds. |
| Author | Záliš, Stanislav Šebesta, Filip Heyda, Jan Winkler, Jay R Gray, Harry B Vlček, Antonín |
| Author_xml | – sequence: 1 givenname: Stanislav orcidid: 0000-0003-4345-3205 surname: Záliš fullname: Záliš, Stanislav email: hbgray@caltech.edu, zalis@jh-inst.cas.cz, a.vlcek@qmul.ac.uk organization: J. Heyrovský Institute of Physical Chemistry, Academy of Sciences of the Czech Republic, CZ-182 23 Prague, Czech Republic; hbgray@caltech.edu zalis@jh-inst.cas.cz a.vlcek@qmul.ac.uk – sequence: 2 givenname: Jan orcidid: 0000-0002-9428-9508 surname: Heyda fullname: Heyda, Jan organization: Department of Physical Chemistry, University of Chemistry and Technology, Prague, CZ-166 28 Prague, Czech Republic – sequence: 3 givenname: Filip orcidid: 0000-0001-6707-8118 surname: Šebesta fullname: Šebesta, Filip organization: School of Biological and Chemical Sciences, Queen Mary University of London, London E1 4NS, United Kingdom – sequence: 4 givenname: Jay R orcidid: 0000-0002-4453-9716 surname: Winkler fullname: Winkler, Jay R organization: Beckman Institute, California Institute of Technology, Pasadena, CA 91125 – sequence: 5 givenname: Harry B orcidid: 0000-0002-7937-7876 surname: Gray fullname: Gray, Harry B email: hbgray@caltech.edu, zalis@jh-inst.cas.cz, a.vlcek@qmul.ac.uk organization: Beckman Institute, California Institute of Technology, Pasadena, CA 91125 hbgray@caltech.edu zalis@jh-inst.cas.cz a.vlcek@qmul.ac.uk – sequence: 6 givenname: Antonín orcidid: 0000-0002-6413-8311 surname: Vlček fullname: Vlček, Antonín email: hbgray@caltech.edu, zalis@jh-inst.cas.cz, a.vlcek@qmul.ac.uk organization: School of Biological and Chemical Sciences, Queen Mary University of London, London E1 4NS, United Kingdom |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33836608$$D View this record in MEDLINE/PubMed |
| BookMark | eNpNjz1PwzAYhC1URD9gZkMZWVJe24ljj6iigFQJBpgjx3nTBCW2iZ2h_55IFInl7oZHd7o1WVhnkZBbClsKBX_wVoctA5YJVlAqL8iKgqKpyBQs_uUlWYfwBQAql3BFlpxLLgTIFVHvrYuus_VksE5a1-Ms3nf2mMR2dNOxTeJ48tH5VtuQdDbxo4vY2XBNLhvdB7w5-4Z87p8-di_p4e35dfd4SE1WqJg2xuRNbbTJQEAmK6GMqg1SSTVQEIiqgVzQitdUSgAsRNVoxgWTslAoJNuQ-9_eefh7whDLoQsG-15bdFMoWU4pyyRwNqN3Z3SqBqxLP3aDHk_l3132AwUmWUk |
| CitedBy_id | crossref_primary_10_1073_pnas_2403324121 crossref_primary_10_1073_pnas_2308286120 crossref_primary_10_1016_j_jhazmat_2023_131027 crossref_primary_10_1016_j_ccr_2024_215878 crossref_primary_10_1073_pnas_2405156121 crossref_primary_10_1002_cssc_202201679 crossref_primary_10_1042_BCJ20250001 |
| ContentType | Journal Article |
| DBID | NPM 7X8 |
| DOI | 10.1073/pnas.2024627118 |
| DatabaseName | PubMed MEDLINE - Academic |
| DatabaseTitle | PubMed MEDLINE - Academic |
| DatabaseTitleList | MEDLINE - Academic PubMed |
| Database_xml | – sequence: 1 dbid: NPM name: PubMed url: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed sourceTypes: Index Database – sequence: 2 dbid: 7X8 name: MEDLINE - Academic url: https://search.proquest.com/medline sourceTypes: Aggregation Database |
| DeliveryMethod | no_fulltext_linktorsrc |
| Discipline | Sciences (General) |
| EISSN | 1091-6490 |
| ExternalDocumentID | 33836608 |
| Genre | Journal Article |
| GrantInformation_xml | – fundername: NIDDK NIH HHS grantid: R01 DK019038 |
| GroupedDBID | --- -DZ -~X .55 0R~ 123 29P 2AX 2FS 2WC 4.4 53G 5RE 5VS 85S AACGO AAFWJ AANCE ABBHK ABOCM ABPLY ABPPZ ABTLG ABXSQ ABZEH ACGOD ACIWK ACNCT ACPRK AENEX AEUPB AEXZC AFFNX AFOSN AFRAH ALMA_UNASSIGNED_HOLDINGS BKOMP CS3 D0L DCCCD DIK DU5 E3Z EBS F5P FRP GX1 H13 HH5 HYE IPSME JAAYA JBMMH JENOY JHFFW JKQEH JLS JLXEF JPM JSG JST KQ8 L7B LU7 N9A NPM N~3 O9- OK1 PNE PQQKQ R.V RHF RHI RNA RNS RPM RXW SA0 SJN TAE TN5 UKR VQA W8F WH7 WOQ WOW X7M XSW Y6R YBH YIF YIN YKV YSK ZCA ~02 ~KM 7X8 |
| ID | FETCH-LOGICAL-c479t-fcc5fdcac406048b69c9dce181a0106ee9f0561b3d18800e76bfa23628879e682 |
| IEDL.DBID | 7X8 |
| ISICitedReferencesCount | 16 |
| ISICitedReferencesURI | http://www.webofscience.com/api/gateway?GWVersion=2&SrcApp=Summon&SrcAuth=ProQuest&DestLinkType=CitingArticles&DestApp=WOS_CPL&KeyUT=000629635100086&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D |
| ISSN | 1091-6490 |
| IngestDate | Thu Oct 02 10:56:39 EDT 2025 Wed Feb 19 02:28:33 EST 2025 |
| IsDoiOpenAccess | false |
| IsOpenAccess | true |
| IsPeerReviewed | true |
| IsScholarly | true |
| Issue | 11 |
| Keywords | electron transfer molecular dynamics hole hopping tryptophan azurin |
| Language | English |
| LinkModel | DirectLink |
| MergedId | FETCHMERGED-LOGICAL-c479t-fcc5fdcac406048b69c9dce181a0106ee9f0561b3d18800e76bfa23628879e682 |
| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 |
| ORCID | 0000-0002-7937-7876 0000-0002-4453-9716 0000-0001-6707-8118 0000-0003-4345-3205 0000-0002-6413-8311 0000-0002-9428-9508 |
| OpenAccessLink | https://www.ncbi.nlm.nih.gov/pmc/articles/7980458 |
| PMID | 33836608 |
| PQID | 2511248032 |
| PQPubID | 23479 |
| ParticipantIDs | proquest_miscellaneous_2511248032 pubmed_primary_33836608 |
| PublicationCentury | 2000 |
| PublicationDate | 2021-03-16 |
| PublicationDateYYYYMMDD | 2021-03-16 |
| PublicationDate_xml | – month: 03 year: 2021 text: 2021-03-16 day: 16 |
| PublicationDecade | 2020 |
| PublicationPlace | United States |
| PublicationPlace_xml | – name: United States |
| PublicationTitle | Proceedings of the National Academy of Sciences - PNAS |
| PublicationTitleAlternate | Proc Natl Acad Sci U S A |
| PublicationYear | 2021 |
| SSID | ssj0009580 |
| Score | 2.4450598 |
| Snippet | Hole hopping through tryptophan/tyrosine chains enables rapid unidirectional charge transport over long distances. We have elucidated structural and dynamical... |
| SourceID | proquest pubmed |
| SourceType | Aggregation Database Index Database |
| Title | Photoinduced hole hopping through tryptophans in proteins |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/33836608 https://www.proquest.com/docview/2511248032 |
| Volume | 118 |
| WOSCitedRecordID | wos000629635100086&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D |
| hasFullText | |
| inHoldings | 1 |
| isFullTextHit | |
| isPrint | |
| link | http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpZ27T8MwEMZPQBlYgPIsLxmJAYaIxHb9mBBCVCxUHUDqVjmOA12S0AQk_nt8iStYkJBYvEWKzmfffbb1-wAuHJrEpdRrk0QMvUDhPFLOishhsXeJL0h53JpNyPFYTad6Eg7c6vCscrkntht1Vlo8I7_GVphyFTN6U71F6BqFt6vBQmMVesy3MpjVcqp-QHdVRyPQSSS4jpdoH8muq8IgrJtyQWWSqN_7y7bOjLb--4fbsBk6THLbpUQfVlyxA_2whmtyGUDTV7ugJ69lU3pR7qc3I2iU6wfkNbyQYN9DmsVnhegBX9DIvCAt1WFe1HvwPLp_unuIgpVCZLnUTZRbO8wzayxHWI5KhbY6s86Xd4Oi0Dmdo5RIWYZ8tthJkeaGMvQiltoJRfdhrSgLdwjEKqlMJvKYacOlTRXLuEnt0EqG9DI6gPNleGY-VfH-wRSufK9n3wEawEEX41nVMTVmqJSFiNXRH74-hg2KL0vwVZ04gV7uF6o7hXX70czrxVmbA34cTx6_AFnvupo |
| linkProvider | ProQuest |
| openUrl | ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Photoinduced+hole+hopping+through+tryptophans+in+proteins&rft.jtitle=Proceedings+of+the+National+Academy+of+Sciences+-+PNAS&rft.au=Z%C3%A1li%C5%A1%2C+Stanislav&rft.au=Heyda%2C+Jan&rft.au=%C5%A0ebesta%2C+Filip&rft.au=Winkler%2C+Jay+R&rft.date=2021-03-16&rft.eissn=1091-6490&rft.volume=118&rft.issue=11&rft_id=info:doi/10.1073%2Fpnas.2024627118&rft_id=info%3Apmid%2F33836608&rft_id=info%3Apmid%2F33836608&rft.externalDocID=33836608 |
| thumbnail_l | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1091-6490&client=summon |
| thumbnail_m | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1091-6490&client=summon |
| thumbnail_s | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1091-6490&client=summon |