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Warwick Hillier: a tribute

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Abstract

Warwick Hillier (October 18, 1967–January 10, 2014) made seminal contributions to our understanding of photosynthetic water oxidation employing membrane inlet mass spectrometry and FTIR spectroscopy. This article offers a collection of historical perspectives on the scientific impact of Warwick Hillier’s work and tributes to the personal impact his life and ideas had on his collaborators and colleagues.

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Abbreviations

ANU:

Australian National University

FTIR:

Fourier transform infrared spectroscopy

MSU:

Michigan State University

OEC:

Oxygen evolving complex of PSII, also known as WOC

PsbO:

Manganese stabilizing protein of PSII

PSII-WOC:

Photosystem II water oxidizing complex

RSB:

Research School of Biology

References

  • Bader KP, Renger G, Schmid GH (1993) A mass spectrometric analysis of the water-splitting reaction. Photosynth Res 38:355–361

    Article  PubMed  CAS  Google Scholar 

  • Beckmann K, Messinger J, Badger MR, Wydrzynski T, Hillier W (2009) On-line mass spectrometry: membrane inlet sampling. Photosynth Res 102:511–522

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Carrieri D, Ananyev G, Brown T, Dismukes GC (2007) In vivo bicarbonate requirement for water oxidation by photosystem II in the hypercarbonate-requiring cyanobacterium Arthrospira maxima. J Inorg Biochem 101:1865–1874

    Article  PubMed  CAS  Google Scholar 

  • Chu H-A, Gardner MT, O’Brien JP, Babcock GT (1999) Low-frequency Fourier transform infrared spectroscopy of the oxygen-evolving and quinone acceptor complexes in photosystem II. Biochemistry 38:4533–4541

    Article  PubMed  CAS  Google Scholar 

  • Chu H-A, Sackett H, Babcock GT (2000a) Identification of a Mn-O-Mn cluster vibrational mode of the oxygen-evolving complex in photosystem II by low-frequency FTIR spectroscopy. Biochemistry 39:14371–14376

    Article  PubMed  CAS  Google Scholar 

  • Chu H-A, Gardner MT, Hillier W, Babcock GT (2000b) Low-frequency Fourier transform infrared spectroscopy of the oxygen-evolving complexes in photosystem II. Photosyn Res 66:57–63

    Article  PubMed  CAS  Google Scholar 

  • Chu H-A, Hillier W, Law NA, Sackett H, Haymond S, Babcock GT (2000c) Light-induced FTIR difference spectroscopy of the S2 to S3 transitions of the oxygen-evolving complex in photosystem II. Biochim Biophys Acta 1459:528–532

    Article  PubMed  CAS  Google Scholar 

  • Chu H-A, Hillier W, Debus RJ (2004) Evidence that the C-terminus of the D1 polypeptide is ligated to the manganese ion that undergoes oxidation during the S1 to S2 transition: an isotope-edited FTIR study. Biochemistry 43:3152–3166

    Article  PubMed  CAS  Google Scholar 

  • Clausen J, Beckmann K, Junge W, Messinger J (2005) Evidence that bicarbonate is not the substrate in photosynthetic oxygen evolution. Plant Physiol 139:1444–1450

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Cox N, Messinger J (2013) Reflections on substrate water and dioxygen formation. Biochim Biophys Acta 1827:1020–1030

    Article  PubMed  CAS  Google Scholar 

  • Debus RJ (2014) Evidence from FTIR difference spectroscopy that D1-Asp61 influences the water reactions of the oxygen-evolving Mn4CaO5 cluster of photosystem II. Biochemistry 53:2941–2955

    Article  PubMed  CAS  Google Scholar 

  • Debus RJ, Strickler MA, Walker LM, Hillier W (2005) No evidence from FTIR difference spectroscopy that aspartate-170 of the D1 polypeptide ligates a manganese ion that undergoes oxidation during the S0 to S1, S1 to S2, or S2 to S3 transitions in photosystem II. Biochemistry 44:1367–1374

    Article  PubMed  CAS  Google Scholar 

  • Dismukes GC, Klimov VV, Baranov SV, Kozlov YN, DasGupta J, Tyryshkin A (2001) The origin of atmospheric oxygen on Earth: the innovation of oxygenic photosynthesis. Proc Natl Acad Sci USA 98:2170–2175

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Faunce T, Styring S, Wasielewski MR, Brudvig GW, Rutherford AW, Messinger J, Lee AF, Hill CL, deGroot H, Fontecave M, MacFarlane DR, Hankamer B, Nocera DG, Tiede DM, Dau H, Hillier W, Wang L, Amal R (2013) Artificial photosynthesis as a frontier technology for energy sustainability. Energy Environ Sci 6:1074–1076

    Article  Google Scholar 

  • Hillier W (1999) Substrate exchange in the water oxidising complex of photosystem II, Dissertation, The Australian National University

  • Hillier W, Babcock GT (2001) S-State dependent FTIR difference spectra for the photosystem II oxygen evolving complex. Biochemistry 40:1503–1509

    Article  PubMed  CAS  Google Scholar 

  • Hillier W, Messinger J (2005) Mechanism of photosynthetic oxygen production. In: Wydrzynski T, Satoh Ki (eds) Photosystem II: the light-driven water: plastoquinone oxidoreductase. Springer, Dordrecht, pp 567–608

    Google Scholar 

  • Hillier W, Wydrzynski T (1993) Increases in peroxide formation by the photosystem II oxygen evolving reactions upon removal of the extrinsic 16, 22, and 33 kDa proteins are reversed by CaCl2 addition. Photosynth Res 38:417–423

    Article  PubMed  CAS  Google Scholar 

  • Hillier W, Wydrzynski T (2000) The affinities for the two substrate water binding sites in the O2 evolving complex of photosystem II vary independently during S-state turnover. Biochemistry 39:4399–4405

    Article  PubMed  CAS  Google Scholar 

  • Hillier W, Wydrzynski T (2001) Oxygen ligand exchange at metal sites - implications for the O2 evolving mechanism of photosystem II. Biochim Biophys Acta 1503:197–209

    Article  PubMed  CAS  Google Scholar 

  • Hillier W, Wydrzynski T (2004) Substrate water interactions within the photosystem II oxygen evolving complex. Phys Chem Chem Phys 6:4882–4889

    Article  CAS  Google Scholar 

  • Hillier W, Wydrzynski T (2008) 18O-water exchange in photosystem II: substrate binding and intermediates of the water splitting cycle. Coord Chem Rev 252:306–317

    Article  CAS  Google Scholar 

  • Hillier W, Wydrzynski T, Seibert M (1992) Biochemical characterization of photosystem II in the non-aqueous solvent ethylene glycol. In: Murata N (ed) Research in photosynthesis. Kluwer Academic Publishers, Dordrecht, pp 167–170

    Google Scholar 

  • Hillier W, Lukins P, Seibert M, Wydrzynski T (1997) Photochemical reactions of photosystem II in ethylene glycol. Biochemistry 36:76–85

    Article  PubMed  CAS  Google Scholar 

  • Hillier W, Messinger J, Wydrzynski T (1998a) Kinetic determination of the fast exchanging substrate water molecule in the S3 state of photosystem II. Biochemistry 37:16908–16914

    Article  PubMed  CAS  Google Scholar 

  • Hillier W, Messinger J, Wydrzynski T (1998b) Substrate water 18O exchange kinetics in the S2 state of photosystem II. In: Garab G (ed) Photosynthesis: mechanisms and effects. Kluwer Academic Publishers, Dordrecht, pp 1307–1310

    Google Scholar 

  • Hillier W, Hendry G, Burnap RL, Wydrzynski T (2001) Substrate water exchange in photosystem II depends on the peripheral proteins. J Biol Chem 276:46917–46924

    Article  PubMed  CAS  Google Scholar 

  • Hillier W, McConnell I, Badger MR, Boussac A, Klimov VV, Dismukes GC, Wydrzynski T (2006) Quantitative assessment of intrinsic carbonic anhydrase activity and the capacity for bicarbonate oxidation in photosystem II. Biochemistry 45:2094–2102

    Article  PubMed  CAS  Google Scholar 

  • Hillier W, McConnell I, Singh S, Debus RJ, Boussac A, Wydrzynski T (2008) Substrate water exchange in photosystem II: insights from mutants and Ca vs. Sr substitution. In: Allen JF, Gantt E, Golbeck JH, Osmond B (eds) Photosynthesis. Energy from the sun. Springer, Dordrecht, pp 427–430

    Chapter  Google Scholar 

  • Klimov VV, Allakhverdiev SI, Feyziev Y, Baranov SV (1995) Bicarbonate requirement for the donor side of photosystem II. FEBS Lett 363(3):251–255

    Article  PubMed  CAS  Google Scholar 

  • Konermann L, Messinger J, Hillier W (2008) Mass spectrometry-based methods for studying kinetics and dynamics in biological systems. In: Aartsma TJ, Matysik J (eds) Biophysical techniques in photosynthesis II. Springer, Dordrecht, pp 167–190

    Chapter  Google Scholar 

  • Koroidov S, Shevela D, Shutova T, Samuelsson G, Messinger J (2014) Mobile hydrogen carbonate acts as a proton acceptor in photosynthetic water oxidation. Proc Natl Acad Sci USA 111:6299–6304

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Messinger J, Badger M, Wydrzynski T (1995a) Detection of one slowly exchanging substrate water molecule in the S3 state of photosystem II. Proc Natl Acad Sci USA 92:3209–3213

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Messinger J, Hillier W, Badger MR, Wydrzynski T (1995b) Heterogeneity in substrate water binding to photosystem II. In: Mathis P (ed) Photosynthesis: from light to biosphere. Kluwer Academic Publishers, Dordrecht, pp 283–286

    Google Scholar 

  • Metzner H (1978) Oxygen evolution as energetic problem. In: Metzner HE (ed) Photosynthetic oxygen evolution. Academic Press, London, pp 59–76

    Google Scholar 

  • Metzner H, Fischer K, Bazlen O (1979) Isotope ratios in photosynthetic oxygen. Biochim Biophys Acta 548:287–295

    Article  PubMed  CAS  Google Scholar 

  • Noguchi T, Sugiura M (2001) Flash-induced Fourier transform infrared detection of the structural changes during the S-state cycle of the oxygen-evolving complex in photosystem II. Biochemistry 40:1497–1502

    Article  PubMed  CAS  Google Scholar 

  • Noguchi T, Ono T-A, Inoue Y (1992) Detection of structural changes upon S1-to-S2 transition in the oxygen-evolving manganese cluster in photosystem II by light-induced Fourier transform infrared difference spectroscopy. Biochemistry 31:5953–5956

    Article  PubMed  CAS  Google Scholar 

  • Noguchi T, Ono T-A, Inoue Y (1995a) A carboxylate ligand interacting with water in the oxygen-evolving center of photosystem II as revealed by Fourier transform infrared spectroscopy. Biochim Biophys Acta 1232:59–66

    Article  Google Scholar 

  • Noguchi T, Ono T-A, Inoue Y (1995b) Direct detection of a carboxylate bridge between Mn and Ca2+ in the photosynthetic oxygen-evolving center by means of Fourier transform infrared spectroscopy. Biochim Biophys Acta 1228:189–200

    Article  Google Scholar 

  • Radmer R, Ollinger O (1986) Do the higher oxidation states of the photosynthetic O2-evolving system contain bound H2O? FEBS Lett 195:285–289

    Article  PubMed  CAS  Google Scholar 

  • Ruben S, Randall M, Kamen MD, Hyde JL (1941) Heavy oxygen (O18) as a tracer in the study of photosynthesis. J Am Chem Soc 63:877–879

    Article  CAS  Google Scholar 

  • Schmidt B, Hillier W, McCracken J, Ferguson-Miller S (2004) The use of stable isotopes and spectroscopy to investigate the energy transducing function of cytochrome c oxidase. Biochim Biophys Acta 1655:248–255

    Article  PubMed  CAS  Google Scholar 

  • Service RJ, Hillier W, Debus RJ (2010) Evidence from FTIR difference spectroscopy of an extensive network of hydrogen bonds near the oxygen-evolving Mn4Ca cluster of photosystem II involving D1-Glu65, D2-Glu312, and D1-Glu329. Biochemistry 49:6655–6669

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Service RJ, Hillier W, Debus RJ (2014) A network of hydrogen bonds near the oxygen-evolving Mn4CaO5 cluster of photosystem II probed with FTIR difference spectroscopy. Biochemistry 53:1001–1017

    Article  PubMed  CAS  Google Scholar 

  • Service RJ, Yano J, Dilbeck DL, Burnap RL, Hillier W, Debus RJ (2013) Participation of glutamate-333 of the D1 polypeptide in the ligation of the Mn4CaO5 cluster in photosystem II. Biochemistry 52:8452–8464

    Article  PubMed  CAS  Google Scholar 

  • Service RJ, Yano J, McConnell I, Hwang HJ, Niks D, Hille R, Wydrzynski T, Burnap RL, Hillier W, Debus RJ (2011) Participation of glutamate-354 of the CP43 polypeptide in the ligation of manganese and the binding of substrate water in photosystem II. Biochemistry 50:63–81

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Shevela D, Eaton-Rye JJ, Shen J-R, Govindjee (2012) Photosystem II and the unique role of bicarbonate: a historical perspective. Biochim Biophys Acta 1817:1134–1151

    Article  PubMed  CAS  Google Scholar 

  • Singh S, Debus RJ, Wydrzynski T, Hillier W (2008) Investigation of substrate water interactions at the high-affinity Mn site in the photosystem II oxygen-evolving complex. Phil Trans R Soc London, Ser B 363:1229–1235

    Article  CAS  Google Scholar 

  • Stemler AJ (2002) The bicarbonate effect, oxygen evolution, and the shadow of Otto Warburg. Photosynth Res 73:177–183

    Article  PubMed  CAS  Google Scholar 

  • Stemler AJ, Babcock GT, Govindjee (1974) The effect of bicarbonate on photosynthetic oxygen evolution in flashing light in chloroplast fragments. Proc Nat Acad Sci USA 71:4679–4683

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Strickler MA, Walker LM, Hillier W, Debus RJ (2005) Evidence from biosynthetically incorporated strontium and FTIR difference spectroscopy that the C-terminus of the D1 polypeptide of photosystem II does not ligate calcium. Biochemistry 44:8571–8577

    Article  PubMed  CAS  Google Scholar 

  • Strickler MA, Hillier W, Debus RJ (2006) No evidence from FTIR difference spectroscopy that glutamate-189 of the D1 polypeptide ligates a Mn ion that undergoes oxidation during the S0 to S1, S1 to S2, or S2 to S3 transitions in photosystem II. Biochemistry 45:8801–8811

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Strickler MA, Walker LM, Hillier W, Britt RD, Debus RJ (2007) No evidence from FTIR difference spectroscopy that aspartate-342 of the D1 polypeptide ligates a Mn ion That undergoes oxidation during the S0 to S1, S1 to S2, or S2 to S3 transitions in photosystem II. Biochemistry 46:3151–3160

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Sugiura M, Rappaport F, Hillier W, Dorlet P, Ohno Y, Hayashi H, Boussac A (2009) Evidence that D1-His332 in photosystem II from Thermosynechococcus elongatus interacts with the S3-state and not with the S2-State. Biochemistry 48:7856–7866

    Article  PubMed  CAS  Google Scholar 

  • Wydrzynski T, Hillier W (eds) (2012) Molecular solar fuels. Royal Society of Chemistry, London

    Google Scholar 

  • Wydrzynski T, Hillier W, Messinger J (1996) On the functional significance of substrate accessibility in the photosynthetic water oxidation mechanism. Physiol Plant 96:342–350

    Article  CAS  Google Scholar 

  • Zhang HM, Fischer G, Wydrzynski T (1998) Room-temperature vibrational difference spectrum for S2Q B /S1QB of photosystem II determined by time-resolved Fourier transform infrared spectroscopy. Biochemistry 37:5511–5517

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We sincerely thank all colleagues, Sari Hillier, and the Hillier family for contributing recollections and photographs, and Govindjee for the invitation to prepare this tribute and for his editing the final draft.

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Correspondence to G. Charles Dismukes.

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Messinger, J., Debus, R. & Dismukes, G.C. Warwick Hillier: a tribute. Photosynth Res 122, 1–11 (2014). https://doi.org/10.1007/s11120-014-0025-5

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