Covalent Immobilization of Oriented Photosystem II on a

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Covalent Immobilization of Oriented Photosystem II on a Nanostructured Electrode for Solar Water Oxidation Masaru Kato, Tanai Cardona, Alfred William Rutherford, and Erwin Reisner J. Am. Chem. Soc., Just Accepted Manuscript • DOI: 10.1021/ja404699h • Publication Date (Web): 05 Jul 2013 Downloaded from http://pubs.acs.org on July 10, 2013

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Journal of the American Chemical Society

Covalent Immobilization of Oriented Photosystem II on a Nanostructured Electrode for Solar Water Oxidation Masaru  Kato,† Tanai  Cardona,‡  A.  William  Rutherford‡  and  Erwin  Reisner†*   †

Department  of  Chemistry,  University  of  Cambridge,  Lensfield  Road,  Cambridge  CB2  1EW,  U.K.  



Department  of  Life  Sciences,  Imperial  College  London,  London  SW7  2AZ,  U.K.  

Supporting  Information  Placeholder   ABSTRACT:   Photosystem   II   (PSII)   offers   a   biological   and   sustainable   route   of   photochemical   water   oxidation   to   O2   and  can  provide  protons  and  electrons  for  the  generation  of   solar  fuels  such  as  H2.  We  present  a  rational  strategy  to  elec-­‐ trostatically   improve   the   orientation   of   PSII   from   a   thermo-­‐ philic  cyanobacterium,  Thermosynechococcus   elongatus,  on  a   nanostructured   indium   tin   oxide   (ITO)   electrode   and  to   co-­‐ valently   immobilize   PSII   on   the   electrode.   The   ITO   electrode   was   modified   with   a   self-­‐assembled   monolayer   (SAM)   of   phosphonic   acid   ITO   linkers   with   a   dangling   carboxylate   moiety.  The  negatively  charged  carboxylate  attracts  the  posi-­‐ tive  dipole  on  the  electron  acceptor  side  of  PSII   via  Coulomb   interactions.   Covalent   attachment   of   PSII   in   its   electrostati-­‐ cally   improved   orientation   to   the   SAM-­‐modified   ITO   elec-­‐ trode   was   accomplished   via   an   amide   bond   to   further   en-­‐ hance   red-­‐light   driven,   direct   electron   transfer   and   stability   of  the  PSII  hybrid  photoelectrode.  

Solar   light   driven   splitting   of   water   into   its   elements   is   a   1 sustainable  route  to  generate  hydrogen-­‐based  fuels.  A  major   challenge  in  water  splitting  is  the  thermodynamically  up-­‐hill   reaction   of   water   oxidation   to   O2,   which   involves   a   four-­‐ electron   and   four-­‐proton   transfer   process.   Photosystem   II   (PSII)  is  the  natural  water  oxidation  enzyme  managing  light   absorption,  charge  separation  and  the  extraction  of  electrons   and   protons   through   the   oxidation   of   water   in   a   pH   neutral   2 aqueous   solution.   PSII   operates   at   a   high   rate   −   it   oxidizes   approximately   100   water   molecules   per   second   during   full   sunlight  irradiation  with  an  upper  turnover  number  estimat-­‐ ed  to  be  approximately  one  million  within  the  lifetime  of  the   3   [Mn4Ca]   water   oxidation   catalyst. PSII   therefore   serves   as   the   unchallenged   benchmark   and   an   inspiration   in   photo-­‐ 4 catalytic  water  oxidation.   Protein   film   photoelectrochemistry   (PF-­‐PEC),   the   photo-­‐ 5   chemical   analogue   to   protein   film   electrochemistry, is   cur-­‐ rently  in  its  infancy  as  a  probe  to  study  the  function  of  pho-­‐ 6 tosynthetic   enzymes   such   as   photosystem   I   and   PSII.   PF-­‐ PEC   is   thereby   a   promising   technique   to   study   the   photo-­‐ catalytic   rates   and   performance   of   photosynthetic   enzymes   under   different   conditions.   We   have   recently   reported   on   direct   electron   transfer   (DET)   from   PSII   to   a   mesoporous   6c indium   tin   oxide   (mesoITO)   electrode.   PSII   was   adsorbed   to   the   bare   ITO   surface   in   a   random   orientation   and   the  

three-­‐dimensional   and   transparent   mesoITO   electrode   al-­‐ lowed   for   good   electrical   conductivity   and   high   PSII   6c loading.  Several  redox  enzymes  with  biotechnological  rele-­‐ 7 8 vance   such   as   hydrogenases   and   laccases   were   previously   immobilized  on  electrodes  in  a  controlled  orientation  to  im-­‐ prove  DET  and  the  electrostability  of  the  enzyme  in  protein   film  electrochemistry.  Compared  to  these  enzymes,  the  con-­‐ trolled   immobilization   of   PSII   on   electrodes   is   not   straight-­‐ forward:  PSII  is  photoactive  and  relatively  huge  (a  molecular   weight  of  approximately  700  kDa  and  a  size  of  10.5×20.5×11.0   3 2a,b nm  for  cyanobacterial  PSII  dimers),  and  its  electron  dona-­‐ tion  sites  to  electrodes  are  placed  on  one  region  at  the  stro-­‐ mal  side  of  PSII  (Figure  1).   In  this  communication,  we  report  on  a  rational  protocol  to   improve   the   orientation   of   a   cyanobacterial   PSII   on   a   self-­‐ assembled   monolayer   (SAM)-­‐functionalized   mesoITO   elec-­‐ trode   resulting   in   improved   interfacial   electronic   communi-­‐ cation   between   ITO   and   PSII.   Covalent   immobilization   of   oriented  PSII  to  the  electrode  surface  further  improved  DET   and  the  stability  of  the  enzyme  (Figure  1).  

  Figure   1.   Schematic   representation   for   the   assembly   of   (A)   mesoITO|SAM-­‐CO2–,  (B)  electrostatic  immobilization  of  PSII   (e-­‐mesoITO|SAM-­‐CO2–|PSII)   and   (C)   covalent   bonding   (c-­‐ mesoITO|SAM-­‐CO2–|PSII).   (D)   Red   light-­‐driven   DET   and   2,6-­‐dichloro-­‐1,4-­‐benzoquinone-­‐mediated   electron   transfer   (MET)   resulting   in   photocurrents   with   c-­‐mesoITO|SAM-­‐ CO2–|PSII.  

 

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Chart  1.  Compounds  used  for  SAMs  on  mesoITO.   SAM  

R  

n  

Abbreviation  

 

CO2H   NH2   CO2H   CO2H  

2   2   5   15  

SAM-­‐C2CO2   + SAM-­‐C2NH3   − SAM-­‐C5CO2   − SAM-­‐C15CO2  

H2O3P

n

R

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diffusional   redox   mediator,   2,6-­‐dichloro-­‐1,4-­‐benzoquinone,   was   used.   This   observation   suggests   that   the   negatively   charged  mesoITO|SAM-­‐C2CO2–  surface  resulted  in  improved   orientation   of   PSII   on   ITO   and,   consequently,   enhanced   in-­‐ terfacial   electronic   communication   between   PSII   and   ITO.   No   photocurrent   was   observed   in   the   absence   of   PSII   for   mesoITO|SAM-­‐C2CO2–.   PSII   in   the   absence   of   the   [Mn4Ca]   11 water   oxidation   catalyst   (Mn-­‐depleted   PSII)   on   mesoI-­‐ – TO|SAM-­‐C2CO2 resulted   in   only   a   minor   photocurrent   (<   0.02   µA   cm–2),   demonstrating   that   the   photocurrent   respons-­‐ es  resulted  from  water  oxidation.  



  MesoITO  electrodes  with  a  geometrical  surface  area  of  0.25   2   cm were  synthesized  by  annealing  a  paste  of  ITO  nanoparti-­‐ cles   (