TRIBUTE

Warwick Hillier: a tribute

Johannes Messinger • Richard Debus •

G. Charles Dismukes

Received: 9 June 2014 / Accepted: 30 June 2014

� Springer Science+Business Media Dordrecht 2014

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 collabo-

rators and colleagues.

Keywords Bicarbonate � FTIR � Isotopes � Mass

spectrometry � Oxygenic photosynthesis � Photosystem II

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 Warwick Hillier (Fig. 1) was born on October 18, 1967 and

died on January 10, 2014. He is survived by his wife Sari, son

Henry Oscar and daughter Stella Amelia. As a child, family

vacations were invariably spent camping, an activity that

gave Warwick a great appreciation for nature, both its living

and non-living forms. This gift from his parents later became

a dominant influence in his adult life, expressed in both his

hobbies and his profession. His mother—who was trained as

a midwife and nurse—imparted Warwick with a great

awareness of the gift of life which was revealed in his sen-

sitivity to others. As a child and teenager, Warwick learned

from his father how to take things apart, put them back

together and to modify them to suit his needs. Together they

built a beautiful treehouse from driftwood found on the

beach. This lofty treehouse had a fold down table, working

Fig. 1 Warwick Hillier, September 2007

J. Messinger

Department of Chemistry, Chemical Biological Centre (KBC),

Umea University, Linnaeus vag 6, 90187 Umea, Sweden

R. Debus

Department of Biochemistry, University of California at

Riverside, Riverside, CA 92521-0129, USA

G. C. Dismukes (&)

Department of Chemistry & Chemical Biology, Rutgers, The

State University of New Jersey, Piscataway, NJ 08854, USA

e-mail: dismukes@rutgers.edu

123

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DOI 10.1007/s11120-014-0025-5

telephone to the garage, a trap door and a flying fox (zipline)

which would hurtle you across the back yard at an alarming

speed. It was the perfect escape and command center for

future discoveries. This skill was refined as a teenager as he

became a builder of telescopes and an avid star gazer. Among

the telescopes that he built, one featured a 20-inch mirror that

he ground himself. Warwick’s fascination with stars and the

light they radiate extended to how photosynthetic life uti-

lized this energy source. This avocation eventually led him to

university training and became his main interest and area of

his greatest professional contributions. Warwick was a

graduate of the Australian National University (ANU; BSc

(Honors), 1991; MSc, 1994; PhD, 1999) (Fig. 2). He was a

perpetual tinkerer who shared his passion for astronomy and

the building of instruments with his scientific collaborators.

He developed close working relationships and friendships

with others who, like him, enjoyed building unique

instruments.

Beyond his scientific impact, outlined below, those who

knew him well describe him as an exceptional human being

(see personal recollections at end). The sentiments expressed

by his students and colleagues emphasized his warm per-

sonal character, unpretentious self-image, eager sharing of

experience, generous giving of time, and playful mischie-

vousness. Warwick’s strong sense of humanity was made

evident following his PhD training while at Michigan State

University (MSU, 1999–2003). When his postdoctoral

mentor, Gerald (Jerry) T. Babcock, was diagnosed with lung

cancer and died soon thereafter, everyone expected Warwick

would move on to complete his postdoctoral training else-

where. Instead, Warwick stayed on for another 36 months to

guide several pre-doctoral candidates in the Babcock labo-

ratory to complete their PhD theses.

His fun loving mischievousness infiltrated both his sci-

entific interests in photosynthetic water splitting and

astronomy and his personal life. When Sari’s and War-

wick’s first child arrived, Henry Oscar Hillier, none of us

could believe that the initials were a mere coincidence

(HOH or H2O !). But he never admitted otherwise. Later

when their second child arrived, Stella(r), there could be no

denying it. We all knew what playfulness he was up to.

Sharon, Warwick’s sister, noted that his enthusiasm for

astronomy and all aspects of science defined him as a

father. He encouraged Henry and Stella to do photography

and got them into stargazing—including keeping them

home from school to observe the transit of Venus in

Australia (on June 6, 2012). Warwick’s colleagues from the

ANU honored him by naming a star in the constellation of

Telescopium (star 607417 in the Sydney Southern Star

Catalogue) after him.

Hillier’s scientific impact

Warwick dedicated his scientific career to understanding

photosynthesis—the fundamental process whereby green

plants and all phototrophs capture sunlight and convert it

into chemical energy that sustains all life on Earth. Spe-

cifically, he was interested in the mechanism by which

photosystem II (PSII) oxidizes water for delivering the

electrons and protons required for the conversion of carbon

dioxide into carbohydrates, and in the process releases

oxygen forming the atmosphere essential for aerobic

respiration.

Substrate water exchange experiments (1995–1999;

2003–2014)

Warwick was Thomas (Tom) J. Wydrzynski’s first Mas-

ter’s student. He joined Tom’s group in 1990 shortly after

Tom had started his new position at the Research School of

Biological Sciences at the ANU in Canberra, Australia. He

helped Tom to set up his lab and worked during his Mas-

ter’s thesis among others on light-induced peroxide for-

mation by salt-washed PSII preparations and on the effects

of high concentrations of ethylene glycol on PSII (Hillier

et al. 1992; Hillier and Wydrzynski 1993; Wydrzynski

et al. 1996; Hillier et al. 1997). In 1993 Johannes Mes-

singer joined Tom’s lab as a postdoc and established with

the help of Murray Badger the instrumentation and the

protocol for the measurement and analysis of the binding

affinity of the two water molecules (substrate water) that

are bound to the Mn4CaO5 cluster in PSII in order to be

oxidized to molecular oxygen (Messinger et al. 1995a). In

these experiments, which significantly improved previous

attempts (Radmer and Ollinger 1986; Bader et al. 1993),

the binding affinity of the two substrate waters to the

Fig. 2 BSc honors graduation day at the Australian National

University (ANU), 1991. Warwick Hillier with Barry Osmond,

Director of the Research School of Biology. Photo by Duncan

Fitzpatrick

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Mn4CaO5 cluster is probed by measuring the rate of

exchange with bulk water after short-time incubations of

PSII with H218O. The isotopic composition of the oxygen

generated after a series of different incubation times is then

assayed by isotope-ratio membrane inlet mass spectrome-

try (Fig. 3) (Konermann et al. 2008; Beckmann et al. 2009;

Cox and Messinger 2013). Warwick was immediately

fascinated by these experiments and decided to make them

the subject of his PhD thesis. Thus, he took over the

instrumentation from Johannes after he left for London in

1995 (Fig. 4), and further reduced the time required for

complete mixing of the PSII sample with H218O (from 30 to

10 ms). This additional improvement was critical to allow

resolving the exchange kinetics of the fast exchanging

(more loosely bound) substrate water in the S3 state

(Messinger et al. 1995b; Hillier et al. 1998a). He then

extended the experiments to the S2, S1, and S0 states

(Messinger et al. 1995b; Hillier et al. 1998b; Hillier and

Wydrzynski 2000), which he studied not only under one

experimental condition, but also at several temperatures

and pH values. This was a formidable achievement con-

sidering that the determination of each exchange kinetic

requires the collection of 20–30 individual measurements

that take about 1 h each and completely stable instru-

mentation over this period. Curious as he was, he studied

the water exchange not only in spinach thylakoids, but also

in various other PSII preparations from spinach,

Thermosynechococcus elongatus and Synechocystis sp.

PCC6803 (Hillier et al. 2001). To gain even deeper insight,

he also determined the substrate water exchange rates after

removing or substituting the Ca2? or Cl- cofactors. Many

of the results he obtained during his PhD thesis (Hillier

1999) were published only several years later.

After completion of his PhD (1999), he took a post-

doctoral position at Michigan State University with Jerry

Babcock to learn Fourier transform infrared (FTIR) spec-

troscopy (see below). In 2003 he returned to ANU and re-

joined the Photobioenergetics group at the RSBS as a

postdoc funded by the Human Frontier Science Program.

He continued the substrate water exchange experiments

and obtained a permanent position in RSBS (now Research

School of Biology, RSB) in May 2007. In order to localize

the substrate water binding sites on the Mn4CaO5 cluster he

started, in collaboration with Richard (Rick) Debus (Singh

et al. 2008; Hillier et al. 2008; Service et al. 2011) and

others (Sugiura et al. 2009) to map the effects of PSII point

mutations on the substrate water exchange rates. Warwick

and Tom Wydrzynski have summarized their seminal work

on substrate water binding in several excellent reviews

(Hillier and Wydrzynski 2001, 2004; Hillier and Messinger

2005; Hillier and Wydrzynski 2008) (see also Cox and

Messinger 2013). The importance of Warwick’s substrate

water-exchange measurements for the understanding of the

mechanism of water oxidation in PSII lies in the fact that

this technique is the only one that directly reports on the

properties of the substrate water molecules in the different

oxidation states of PSII. In 2007 Warwick shared the Robin

Hill Award, given at the 14th International Photosynthesis

Congress, for his seminal work on the mechanism of water

oxidation (Fig. 5). In 2009, he won an Australian Future

Fellowship for research in this area and at the time of his

Fig. 3 Membrane inlet mass spectrometer (MIMS) set up in the lab

of Murray Badger in 1995. The MIMS cell (black) for the substrate-

water exchange experiments is located underneath the table on top of

the white box

Fig. 4 Thomas (Tom) J. Wydrzynski’s group at the ANU in 1995

(from left to right): Warwick Hillier, Tom Wydrzynski, Johannes

Messinger and Haoming Zhang. Picture was taken during a stroll in

the Botanical Garden in Canberra

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death was a Laboratory Leader in the Division of Plant

Sciences in the RSB (Fig. 6).

In search of the fingerprints of water oxidation

by infrared spectroscopy (1999–2014)

Warwick sought to obtain more detailed information about

the chemical bonds and atomic vibrations of the substrate

water molecules and the atoms they interacted with in the

water oxidizing complex (WOC) and so turned to vibra-

tional spectroscopy for answers. After completing his PhD

dissertation in 1999 in Wydrzynski’s laboratory, Warwick

joined Jerry Babcock’s laboratory at MSU as a postdoctoral

fellow (Fig. 7). At this time the Babcock’s laboratory was

beginning to apply FTIR difference spectroscopy to study

the structural changes that accompany the S state transi-

tions in PSII. Jerry, graduate student Matt Gardner, and

postdoctoral fellows Hsiu-An (Andy) Chu, and John

O’Brien were developing FTIR instrumentation capable of

measuring spectra between 1,000 and 350 cm-1 (Chu et al.

1999). Jerry was particularly interested in this region

because metal–ligand vibrations appear here and the Mn-

ligand and Mn-substrate modes of the Mn4CaO5 cluster of

PSII were expected to be found between 200 and

900 cm-1. The technical obstacles to measuring FTIR

spectra in this spectral region are formidable, including

strong absorption from water, few materials for optical

windows and low detector sensitivity.

Warwick helped develop the group’s ‘‘third generation’’

spectrometer, pushing the lower frequency limit from

550 cm-1 down to 350 cm-1 (Chu et al. 2000a, b). Also,

before 2000, only the S2-minus-S1 FTIR difference spec-

trum of PSII had been reported (Noguchi et al. 1992,

1995a, b; Zhang et al. 1998; Chu et al. 1999). Warwick’s

specific task was to extend the application of FTIR dif-

ference spectroscopy to the study of ALL of the S state

transitions in the mid-frequency region

(2,000–1,000 cm-1), where vibrations from amino acid

side chains and the polypeptide backbone appear. He

assisted with the first report of a S3-minus-S2 FTIR dif-

ference spectrum in this region (Chu et al. 2000c), then

developed the methodology for recording all of the Sn?1-

minus-Sn FTIR difference spectra in this region in spinach

PSII core complexes (Hillier and Babcock 2001). This was

a landmark publication that was published alongside an

equally significant publication from Takumi Noguchi and

Miwa Sugiura, who developed the methodology indepen-

dently and simultaneously for PSII core complexes from T.

elongatus (Noguchi and Sugiura 2001). For this work,

Warwick designed the sample compartment and cryostat

for a new spectrometer that Babcock’s laboratory had

Fig. 5 2007 Robin Hill Award winners, Warwick Hillier and Junko

Yano (left and front), and Melvin Calvin-Andrew Benson Award

winner Julian Hibberd (center, back)

Fig. 6 Warwick’s research group in 2011(from left to right):

Sikander Ali, Duncan Fitzpatrick, Riichi Oguchi, Nicholas Zehm,

Warwick Hillier and Alison Winger. (Source: Research School of

Biology, ANU)

Fig. 7 Warwick wearing his favorite red shirt during a hiking trip in

Arches National Park, USA, in 2001. Photo by Sari Hillier

Photosynth Res

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recently acquired, configured the FTIR spectrometer and

Nd:YAG laser system, and developed software that would

allow actinic laser illumination and data collection to occur

automatically. Warwick loved to tinker and developed

numerous ‘‘bits’’ and jigs for helping prepare samples for

FTIR measurement.

After Jerry Babcock passed away in December 2000,

Warwick remained at MSU for three years to help guide

students (Fig. 8). During this time, he built a sample cell

for generating electrochemically induced FTIR difference

spectra, then employed it, in combination with global 15N

labeling and 15N-labeling of histidine, to assign heme and

histidine peaks in an electrochemically induced FTIR dif-

ference spectrum of cytochrome c oxidase (Schmidt et al.

2004). Also during this time, Warwick began collaboration

with Rick Debus, who had just acquired a new FTIR

spectrometer at The University of California (UC) River-

side (Fig. 9). During a visit by Rick to MSU in 2002,

Warwick taught Rick how to prepare samples for FTIR

analysis and to record spectra. Soon after, Warwick trav-

eled to UC Riverside to help set up Rick’s new spec-

trometer, configuring it with a new laser system and writing

software that would allow actinic laser illumination and

data collection to occur automatically. For the next eleven

years, Warwick would become an almost annual visitor to

Rick’s laboratory where he would update the spectrome-

ter’s configuration and software and discuss new types of

experiments. When Rick acquired a newer spectrometer in

2007, Warwick configured it, wrote its software, and

designed its cryostat and sample compartment. For most of

the decade between 2003 and 2013, the collaboration

focused on the ligands of the Mn4CaO5 cluster. The first

product of this collaboration provided evidence that the

C-terminal carboxylate group of the D1 polypeptide at Ala-

344 ligates a Mn ion in the Mn4CaO5 cluster (Chu et al.

2004; Strickler et al. 2005). Subsequent publications (De-

bus et al. 2005; Strickler et al. 2006, 2007; Service et al.

2011, 2013) provided the unexpected result that the indi-

vidual mutation of four of the Mn4CaO5 cluster’s six car-

boxylate ligands produces no significant changes in the

Sn?1-minus-Sn FTIR difference spectra. Not only do

mutations of D1-Asp170, D1-Glu189, D1-Glu333, and D1-

Asp342 fail to eliminate carboxylate vibrational modes,

they fail to produce significant changes in the response of

the protein’s polypeptide backbone to the oxidations of the

Mn4CaO5 cluster during the individual S state transitions.

The realization that the wealth of features in the Sn?1-

minus-Sn FTIR difference spectra must reflect changes in

the Mn4CaO5 cluster’s second coordination and beyond,

led the collaboration into studies of the hydrogen-bonding

networks surrounding the Mn4CaO5 cluster (Service et al.

2010, 2014) and the water reactions that accompany the S

state transitions. The latter include the region between

3,600 and 2,000 cm-1 where the vibrational modes of

hydrogen bonded OH groups and delocalized protons in

highly polarizable hydrogen bonds appear (Service et al.

2013; Debus 2014). Most of the mutants examined during

this collaboration were also examined by Warwick for their

effects on the exchange of substrate water molecules

(Singh et al. 2008; Hillier et al. 2008; Service et al. 2011).

One of Warwick’s goals was to configure FTIR spec-

trometers for technically daunting time-resolved measure-

ments. Towards that goal, Warwick developed sample

compartments fitted with computer-controlled sample

wheels that would increase sample throughput many-fold.

He was still working on this goal at the time of his passing.

Fig. 8 Gerald T. Babcock group at MSU, *2001 (from left to right).

Back row: Denis Proshlyakov, Bryan Schmidt, Neil Law, Steve

Seibold, Warwick Hillier; Front row: Hsiu-An Chu, Vada O’Donnell,

Jose Cerda, and Shannon Haymond

Fig. 9 FTIR mini-summit in Tokagawa Garden, Nagoya, Japan,

2010. Front to back: Takumi Noguchi, Warwick Hillier, Rick Debus.

Photo provided by Takumi Noguchi

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Chasing bicarbonate and the evolution of oxygenic

photosynthesis (2003–2006)

Warwick researched the biogenesis of oxygenic photo-

synthesis, the process by which it came to exist following

accretion of the Earth at the beginning of life. His iconic

images of cyanobacterial stromatolites from Shark Bay,

Australia (http://www.photosynthesisresearch.org/resour

ces/Theme/images/Warwick%20st4250L.jpg), and ‘‘cham-

pagne bubbles’’ video of oxygen gas fizzing from blades of

underwater grass at Ewens Pond, Australia, are examples

of his outstanding amateur photography skills that have

inspired us all and been sought after by textbook writers.

During his postdoctoral research at MSU, Warwick

visited Charles (Chuck) Dismukes’ laboratory at Princeton

University to present his research on substrate water

exchange and FTIR of intermediates during photoassembly

(biosynthesis) of the PSII-WOC. Discussions on interpre-

tation of these data led to the literature on the chemical

speciation of water as substrate for O2 evolution. Earlier

mass spectrometric work by Ruben et al. (1941) using 18O

enriched water had demonstrated that under equilibrium

conditions water, not CO2 alone, is the ultimate source of

O2. Because water can rapidly and reversibly hydrolyze

CO2 to give ionized forms of carbonic acid (H2CO3,

HCO3- and CO3

2-) in excess water, it was unclear whether

these species needed to be considered as potential candi-

dates for the active form of substrate water molecules.

Hartmut Metzner’s group had provided time-resolved mass

spectrometric evidence implicating bicarbonate as a pos-

sible directly oxidizable electron donor to PSII (Metzner

1978; Metzner et al. 1979). This work has been mostly

overlooked, having appeared mainly in conference pro-

ceedings. The rapid mixing mass spectrometry system

developed at the ANU looked to be the best tool for

answering this question and Warwick was eager for the

challenge. These experiments began after Warwick fin-

ished his work at MSU and returned to the ANU to take a

postdoctoral position funded by the Human Frontier Sci-

ence Program. There was already strong evidence dem-

onstrating that bicarbonate influenced the steady-state rate

of water oxidation by intact plant PSIIs and that at least two

effects where involved, the so-called acceptor and donor

sites (Stemler et al. 1974). Govindjee’s group at the Uni-

versity of Illinois Urbana-Champaign originated this ter-

minology based on work done by Govindjee’s then PhD

students, first Alan Stemler and later Tom Wydrzynski

(Shevela et al. 2012). They established clear evidence for

bicarbonate binding to the acceptor side at the non-heme

iron and showed that removal resulted in slowing of elec-

tron transfer QA-QB ? QAQB

-. A postulated functional

consequence for regulation is appealing. First Govindjee’s

group, and later Metzner’s (Metzner 1978; Metzner et al.

1979), Stemler’s (Stemler 2002) and Klimov’s group

(Klimov et al. 1995) provided evidence for bicarbonate

stimulation of PSII activity on the donor side of PSII. The

donor side effects of bicarbonate have been far more spe-

cies dependent and difficult to pin down. One of the

hypotheses was that bicarbonate might serve as the sub-

strate for O2 evolution as it is energetically easier to dis-

sociate CO2 from bicarbonate to give hydroxide than it is to

dissociate a proton from water. This hypothesis implied

that the contemporary oxygenic reaction center could have

evolved from a bicarbonate oxidizing prokaryotic reaction

center (Dismukes et al. 2001).

Warwick reckoned that the rapid mixing isotope ratio

MS instrument that he helped to develop at the ANU

could answer this question by using 13C/18O-labeled

bicarbonate to measure both the potential flux of oxygen

from bicarbonate into O2, while monitoring the self-

exchange reaction of labeled bicarbonate with unlabeled

water. He used an inhibitor of carbonic anhydrase to slow

the latter reaction. The measurements were made with

both plant and cyanobacterial sources of PSII prepared

from spinach and T. elongatus in order to examine the

earlier evolving prokaryotes, and from Arthrospira max-

ima which grows naturally in alkaline soda lakes at high

(bi)carbonate levels. Warwick’s data showed that bicar-

bonate is not the substrate for O2 production in any of

these contemporary oxygenic photoautotrophs when

assayed under single turnover conditions (Hillier et al.

2006). Clausen had independently reached similar con-

clusions on plant PSII by showing the absence of an

effect from high CO2 pressure on the UV absorbance

changes of manganese (Clausen et al. 2005). Warwick’s

work provided strong evidence and stimulated subsequent

studies which have been interpreted in favor of bicar-

bonate acting as mobile proton acceptor for water oxi-

dation (Carrieri et al. 2007; Koroidov et al. 2014).

Personal accounts

Tom Wydrzynski, ANU (PhD Mentor)

It is with great sadness in my heart that I write these few

words for my beloved mate and friend, Warwick Hillier.

We met when I joined the RSBS in October, 1990. A few

days later, he joined me as my first master student (see

Fig. 2).

Warwick revealed himself to be a true scientist and

naturalist in the genre of Alexander von Humboldt. He

displayed a curiosity in many different areas—he cared for

the small wonders of nature as well as the vastness of the

universe. So keen was his interest in astronomy, that he

even built his own telescope.

Photosynth Res

123

The first time Warwick came to the USA with me was in

1993. It was summer here and we set out to make a cross-

country trip to San Francisco, California from St. Louis,

Missouri. As we were driving through Missouri, we hap-

pened upon the world’s largest fireworks stand. Since it

was around the Fourth of July (America’s Independence

Day), we bought some fireworks to ‘‘shoot off’’ later. As

we were camping just outside of Flagstaff, Arizona, we

heard fireworks being shot off, so we decided to ‘‘shoot

off’’ the ones we had purchased. The very first firecracker

we shot off caught fire about 50 feet away from our

campsite. Warwick quickly ran over to put out the flames,

and then we realized how easily we could have burnt the

San Francisco mountains!

On our second trip to the USA a year later, Warwick and

I decided to visit Mike Siebert (Fig. 10) at National

Renewal Energy Laboratory (NREL) in Denver, Colorado.

While we were driving across the loneliest road in the

USA, the engine in the Jeep failed. We continued driving,

inch by inch, to the next town where we spent the night.

The next morning the service man told us the engine was

damaged because there were filings in the motor. He said it

was possible that we could make it to Denver but we had to

cross a ridge of mountains. Warwick was ready to meet the

next challenge with me, so we decided to try it. About

20 min into our drive, the engine quit again. As we made a

U-turn to head back to town to buy a refurbished engine,

we got stuck in the snow. At this point, it was decided I

would hitch a ride back to town and Warwick would stay

with the Jeep. I picked up a ride and, as we were turning

into the gas station, I was surprised to see Warwick drive

past us in the Jeep! He had managed to get the Jeep out of

the rut and driving again! End of story, we rented a car and

made it to Denver on time.

After Warwick graduated with his PhD, he did a post-

doc at the Department of Chemistry at MSU where he

developed a keen sense of doing FTIR spectroscopy. At

one time I asked him why he was doing a post-doc and he

replied that he wanted to become the world’s expert in

FTIR spectroscopy. Warwick developed many new tech-

niques in FTIR spectroscopy, which are covered by Rick

Debus (also see the main text). After his post-doc, War-

wick returned to the ANU. During this time, he continued

mass spectrometry experiments which led to information

that has been critical for understanding the oxygen evolu-

tion mechanism.

I will always remember Warwick. He was my colleague

and best friend in the truest sense of the word. I will miss

him dearly.

Hsiu-An Chu, Institute of Plant and Microbial Biology,

Academia Sinica, Taiwan

It was my privilege to work with Warwick during

1999–2001 in the late Professor Jerry Babcock’s Lab at

MSU (see Fig. 8). At that time, Warwick was a young post-

doc but already famous for his work with Tom Wydrzynski

on measuring water exchange rates of the oxygen-evolving

complex (OEC) in PSII. He was extremely talented and

creative. He built a very useful FTIR instrumental setup to

measure structural changes of the OEC during the entire S

state cycle. His innovation was published as the back-to-

back Biochemistry papers in 2001 independently with

Professor Takumi Noguchi’s work. It was a significant

breakthrough in our research field. In addition, we

accomplished several publications on FTIR studies of the

OEC with Jerry and other colleagues. Warwick also built a

setup to measure electrochemically induced FTIR differ-

ence spectra of cytochrome c oxidase. Furthermore,

through collaborations with Rick Debus at UC Riverside,

Warwick contributed many insightful FTIR papers in

understanding mechanism of photosynthetic water oxida-

tion. Moreover, he had made numerous other important

scientific innovations and inspired many people around

him. His death is a great loss to our research community.

He will be greatly missed by all of us.

Rick Debus, UC Riverside

Warwick was my friend and closest scientific colleague.

Most of what I know about FTIR spectroscopy, I learned

from Warwick, including how to collect FTIR data

(Fig. 11). I always looked forward to discussing research

with Warwick via Skype (sometimes for an hour at a time)

and treasured his nearly annual visits to my laboratory,

usually for several days before or after a Gordon Confer-

ence. During these trips he would update my equipment

and reconfigure it for additional experiments that we then

proceeded to try. He was always remarkably calm, even

Fig. 10 Enjoying an afternoon break during the 1994 Gordon

Research Conference on Photosynthesis in New Hamsphire (from

left to right): Johannes Messinger, Michael (Mike) Seibert, Warwick

Hillier, Ronald (Ron) Pace and Tom Wydrzynski

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when critical components failed. One highlight of these

visits was a night or two of stargazing. We have a local

astronomy club, so I was able to take Warwick to star

parties in the desert or mountains or to the club’s dark site

east of Riverside near Joshua Tree National Park.

Observing the northern sky was a particular treat for

Warwick. Shortly before one of Warwick’s visits, I

acquired an integrating video camera for viewing particu-

larly dim deep sky objects. It was Warwick’s tinkering with

the camera that first allowed us to see objects with clarity

and colors rivaling those of published astrophotos. The

night of our last outing together, clouds rolled in about 11

PM and I retreated to the warmth of the club’s nearby

clubhouse. When I returned 30 min later, I was greeted by a

seated and smiling Warwick. ‘‘Look what I did!’’ he

exclaimed proudly. I looked up and saw that the clouds had

disappeared. We continued to observe galaxies and nebulae

past dawn. I greatly valued our conversations about data

and interpretations and about science and other things. I

will miss him greatly.

Barry Osmond, ANU

To most of us, his coworkers, Warwick was such an

unassuming, low-key guy who achieved great things.

Those closer to him clearly admired his warm and sym-

pathetic support in all aspects of life. His can-do attitude

came to the fore a few years back as we helped Tom

Wydrzynski move from his lovely hillside home to an

apartment in the city. At a particularly critical moment of

the move Warwick arrived in his trusty Brumby (vintage

Subaru mini-pickup) to take on an amazing last load of

gear that enabled Tom to settle immediately at his new

address.

Kastoori Hingorani (PhD student 2008–2013)

Warwick was my PhD mentor for the five years that I was

at ANU (Fig. 12). It was a pleasure for me to work with

him and learn from him. Warwick stepped up to the role of

my PhD supervisor seamlessly, when my primary super-

visor Tom Wydrzysnki had to take an early retirement. He

was my supervisor, friend and an inspiration from then on.

I will ever be so grateful to Warwick for leading by

example as an excellent scientist and an exceptional human

being. His calm and gentle demeanor and that kind smile

on his face has touched many hearts. While a great loss to

his family, friends and the scientific community, we have

his teachings to live up to and the wonderful memories to

keep. There are numerous valuable lessons he taught to

those around him (unknowingly), simply through his

actions and carefully selected words. For example, he

inspired his students to never stop questioning, and to keep

an eye out for the ‘black swan.’ He taught us to believe in

ourselves, and that there is nothing that we cannot learn to

do. In Warwick’s lab, a molecular biologist could be found

troubleshooting a complex multipart spectrometer, disas-

sembling, changing parts and reassembling, using a user’s

manual and minimal guidance. In other words, with his

mentoring ‘we learnt—how to learn, anything.’ Lastly I

would like to share what he told me once when I was

writing my thesis –‘‘Stress, is a wasted emotion.’’ I don’t

recall ever seeing him stressed.

Fig. 11 Warwick Hillier in front of his new Bruker Vertex 80 FTIR

spectrometer in the lab of Rick Debus at UC Riverside, September

2007

Fig. 12 Graduation day at the ANU, December 12, 2013. Left to

right: Warwick Hillier, Kastoori Hingorani, and Ron Pace

Photosynth Res

123

Tom Faunce, ANU

I came to know my colleague Warwick through his joint

editing of the Royal Society Molecular Solar Fuels volume

(Wydrzynski and Hillier 2012) in which I contributed

Chapter 18 ‘Future Directions on Solar Fuels.’ Warwick

was very encouraging on the idea of globalizing artificial

photosynthesis and gave a presentation at the Lord Howe

Island conference on that theme I had organized. He was

also a joint author on our Energy and Environmental Sci-

ence paper (Faunce et al. 2013) making the case for a

global project on artificial photosynthesis. He once had

made this suggestion in an e-mail to me that I still strive to

keep in mind: ‘‘I make a comment that if you are planting a

seed then the idea might be more important than the

individual.’’ But this is style perhaps that I am not accus-

tomed to and it stumps me at times. Our family interacted

closely with his throughout his final illness. He wrote a

diary and left videos to celebrate the milestones to come in

the lives of his children. He accepted and kept trying to

share.

Robert (Rob) Burnap, Oklahoma State University

My earliest recollections of Warwick date to my six week

visit to Tom Wydryzynski’s lab at ANU in 1996 to study

the effects of the extrinsic proteins on water exchange. The

extrinsic proteins of PSII are known to control the acces-

sibility of ions to the manganese cluster and we were

testing the effects of genetic removal of PsbO protein in

the cyanobacterium Synechocystis. At the time, Warwick

was working on his PhD under Tom’s supervision and he

was asked to guide me in the lab and to work out how to

apply the water exchange techniques to cyanobacterial

preparations. The technique had been worked out for

spinach thylakoids and core preparations while Johannes

Messinger had been in the lab, but it was unclear how to

best apply the techniques to the cyanobacterial prepara-

tions including those from site-directed mutants. Warwick

was wonderful to work with—enthusiastic and an irre-

pressible problem solver. He was also very sharp and open

minded when experiments began producing exactly the

opposite results as we initially had anticipated. We had

hypothesized that the genetic removal of PsbO would

increase the exchange rates due to increased accessibility

of the substrate water to the Mn cluster. What we observed

was the opposite–water exchange was diminished. At the

moment the calculations were completed, Warwick

cheerfully announced something to the effect ‘‘So Science

can work just as they tell us it is supposed to—Rob, I

believe we have just rejected your hypothesis.’’ Of course

it didn’t end at that, since the result told us that the

exchange rates reflected chemical binding characteristics at

the Mn cluster as opposed to diffusion to and from the

catalytic site (Hillier et al. 2001).

Ronald (Ron)Pace, ANU

He was, in local Australian usage, simply a really nice

bloke, really nice, as well as a first rate scientist. The

substrate water exchange work, with Johannes and Tom,

was ground-breaking. We refer to it constantly; that is at

least an outstanding scientific legacy. See sketch of War-

wick Hillier (Fig. 13).

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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