Photosynth Res DOI 10.1007/s11120-013-9948-5

TRIBUTE

Roderick K. Clayton: a life, and some personal recollections Colin A. Wraight

Received: 20 October 2013 / Accepted: 21 October 2013 Ó Springer Science+Business Media Dordrecht 2013

Abstract Roderick K. Clayton passed away on October 23, 2011, at the age of 89, shortly after the plan for this dedicatory issue of Photosynthesis Research had been hatched. I had just written a lengthy letter to him to reestablish contact after a hiatus of 2 or 3 years, and to suggest that I visit him to talk about his life. It isn’t clear whether he saw the letter or not, but it was found at his home in Santa Rosa, California. Fortunately, Rod has written two memoirs for Photosynthesis Research that not only cover much of his research on reaction centers (Photosynth Res 73:63–71, 2002) but also provide a humorous and honest look at his personal life (Photosynth Res 19:207–224, 1988). I cannot hope to improve on these and will try, instead, to fill in some of the gaps that Rod’s own writing has left, and offer some of my own personal recollections over the more recent years. Keywords Roderick K. Clayton
William Arnold
Rhodospirillum rubrum
Rhodobacter sphaeroides
Phototaxis
Photosynthetic reaction center

Family background Roderick Keener Clayton was born in Tallinn, Estonia, on March 29, 1922. His father, John Heber Clayton, was said to be the grandson of William H. Clayton, an early leader in the Mormon Church, and one of the founding fathers of

C. A. Wraight (&) Department of Biochemistry and Center for Biophysics & Computational Biology, University of Illinois at UrbanaChampaign, Urbana, IL 61801, USA e-mail: [email protected]

Salt Lake City. He also wrote ‘‘Come, Come, Ye Saints,’’ a still popular Mormon hymn. John worked as a reporter for the Hearst newspaper group and travelled extensively, especially in the Baltic region from where he covered the Russian revolution. In Estonia he met Rod’s mother, Helena Mullerstein, the daughter of a Lutheran minister who had enlightened ideas about women’s education such that Helena spoke 6 languages by the time she was a teenager. She attended the university in St. Petersburg, but when the revolution broke out, so the story goes, she fled north as the governess for an aristocratic Russian family, eventually crossing the border to Finland and so back to Estonia. John met Helena when she was working in the American Embassy in Tallinn. The family spent time in many places all over Europe, including Italy, where the rise of Mussolini signaled the inevitability of changing times. When the influence of fascism was percolating into the boys’ psyches—Rod was able to sing the fascist Italian anthem all his life—it was decided to move the family back to the U. S., to Chicago. Rod was 6 then, and he has written about the Todd Seminary for Boys (Clayton 1988). However, he did not mention that the Seminary was also attended by Orson Welles who, although a bit older, was friends with Rod and his older brother, Dale. (Fig. 1) In Chicago, John continued to work as a reporter for the Chicago Tribune, until the economy dictated otherwise. In 1935 when Rod was in his early teens, the Claytons moved to Pasadena, California, in part for Helena’s health. For a while his father took to gold mining, at Joshua Tree (Fig. 2), a not uncommon thing to do in the Great Depression, but success was limited to breaking even. Nevertheless, the move was a gold mine for Rod, whose interest in girls, science and nature, especially butterfly collecting, found vastly expanded horizons in this new

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Fig. 2 Rod puts Dale to work hauling him up the Joshua Tree mine track, c.1936

Fig. 1 Top Helena, Rod & Dale shopping in preparation for leaving Tallinn, c.1926. Bottom Rod, Orson Welles and Dale in Chicago, c.1928

found land. He excelled in high school, which was somehow combined with Pasadena Junior College where Jackie Robinson was the star football player (apparently he excelled at all sports). Rod graduated from Pasadena Junior College at about the same time as his parents moved back to Chicago, where Rod worked briefly in James Franck’s lab at the University of Chicago. His father eventually found a stable position as publicity director for the Chicago Opera, but the main breadwinner was Helena who wrote copy for the J. Walter Thomson advertizing agency (Fig. 3).

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Fig. 3 Family portrait, c.1943

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Growing up

Fig. 4 Trainee flight instructor, c.1943

Meanwhile, Rod had already set his sights on the California Institute of Technology and enrolled in chemistry. He excelled there, too, initially, but fell off the wagon in his third year, enticed by the beach, poker, and girls, whom he liked to impress with his considerable gymnastic abilities (he was especially good on the rings), and failed classes miserably. He was advised to take a year off ‘‘to grow up.’’ Whatever he might have done otherwise to recover the situation, the U. S. had already entered the Second World War and Rod enlisted in the U. S. Air Force in the summer of 1943. He trained at Blytheville Army Airfield, Arkansas, first as a flying instructor (Fig. 4) and then as a bomber pilot (Fig. 5). While at Blytheville, he met his future wife, Betty Jean (BJ) Compton, a beauty from Indiana (Fig. 5). She was the youngest of six children. The family suffered sorely in the great depression and BJ and her two sisters, Etha and Mary Beth, were farmed out to local families but later moved to Texas. With the outbreak of World War II, BJ took a job in Blytheville, where she met Rod. When they met, Rod told her he planned to go back to Cal Tech after the war, and she thought, ‘‘How nice, a good vocational school. He’ll have a job.’’ She was always delighted by their

Fig. 5 Roderick K. Clayton, Pilot K30, c.1944, and Betty Jean Clayton, c. 1950

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good fortune and the world travels that came with a successful academic life. They were married in August, 1944. Posted to Guam, Rod enjoyed the exotic nature of his new surroundings, especially the butterflies and other wild life. His active duties took him on sorties over Japan, which he described in some affective accounts. One I have, titled ‘‘Night Mission’’ by Rod Clayton, Pilot K30, and dated June 1945. He also began studying in preparation to recover his status in college. After demobilization, Rod returned to Cal Tech to complete his undergraduate education, switching his major to Physics. The following year, 1947, he entered the graduate program in Physics and was accepted into the lab of Max Delbru¨ck. Delbru¨ck was a renowned physicist who had very successfully transitioned into biology, and had pioneered research on bacteriophage genetics and replication. This set Rod on a career path in ‘‘biophysics,’’ a new sounding field but with deep roots in electrophysiology and photobiology.

Phototaxis and chemotaxis in Rhodospirillum rubrum As a graduate student, Rod’s studies were on phototaxis in the photosynthetic bacterium, Rhodospirillum (Rsp.) rubrum, a relatively large species that could be observed under the optical microscope. As nicely summarized by Armitage and Hellingwerf (2003), he was the indisputable pioneer of quantitative studies of phototaxis. In his thesis work, completed in 1951, he reexamined the action spectrum, refining earlier work by Manten (1948) and Duysens (1951), and firmly established the relationship between phototaxis and photosynthesis (Clayton 1953a, b, c). He also provided the first quantitative data for the ‘‘step-down’’ response, in which phototrophically grown Rsp. rubrum reversed direction repeatedly when the light intensity was reduced. The size and duration of the response depended not only on the size of the step-down, but also on the initial light intensity, in adherence to the Weber–Fechner Law, which was proposed on the basis of psychophysical research in the nineteenth century (Fechner 1860; Weber 1846). In this age of so much available commercial equipment it is always sobering to see the degree to which biophysical studies of the era were totally dependent on the investigator’s ability to construct sophisticated equipment from scratch, including optics, mechanics, and electronics, which, of course, had developed so markedly during the war. Also, in reading the older literature, one is struck by the difficulties presented by the lack of detailed knowledge we enjoy today, such that the conceptualization of underlying mechanisms is achieved only with great care and logical consistency. The arguments are often long, but the outcome is masterful.

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The phototactic responses of Rsp. rubrum turned out to be very dependent on the metabolic state of the cells, as determined by their growth conditions, including light levels, oxygen tension, and carbon source (Clayton 1955a). Rod had unpublished results from his thesis work in which he had measured photosynthesis and respiration simultaneously to monitor the competition between aerobic and anaerobic (phototrophic) metabolism and the effects on taxis. For this he used standard Warburg–Barcroft manometry, but developed a method that allowed discrimination between O2 uptake, CO2 assimilation or evolution, and the transfer of CO2 from gas to liquid phase that accompanies alkalinization. He extended this work at the Hopkins Marine Station, in the lab of Cornelis (Kees) B. van Niel (1951–1952), and subsequently at the U. S. Naval Postgraduate School in Carmel, where he spent 4 years (1952–1956). Like his studies of phototaxis, his investigations were highly quantitative (Clayton 1955b, c), and he provided a critical analysis of problems in experimental studies, including the effects of substrate diffusion, and distinguishing taxis and trapping due to immobility (Clayton 1957, 1958). Examination of the interaction between chemotactic and phototactic responses under complex environmental conditions suggested a strong link to metabolic state and energy source, leading him to suggest that the responses probably depended on changes in the levels of ATP (Clayton 1958). This had been previously proposed by Links (1955), but Rod’s hypothesis was more general. Furthermore, he had earlier been clearly enamored of the research by Hodgkin, Huxley, and others on nerve impulse generation and propagation, and he identified the positive phototactic response of Rsp. rubrum as an example of a general excitatory system. Drawing on the extensive literature on nerve impulse generation and propagation, Rod had elaborated a theoretical description of phototaxis in terms of its ‘‘all-or-none’’ behavior, refractoriness and accommodation, and supported this with elegant experiments on the threshold–strength relationship (Clayton 1953c). This viewpoint led him to suggest that, in addition to the general energy-status regulation of phototaxis, a more central coordination might be involved—as suggested by the occasional coordinated but self-cancelling behavior of the flagella bundles at opposite ends of the cell (Clayton 1958). It is not clear even today how this happens but it is almost certainly not a mechanism based on membrane electrical activity, although Rod did not limit it to such. However, the known basis of diffusion of small signaling molecules inside the cell may achieve something equivalent. It is noteworthy that his work on taxes in Rsp. rubrum was not only ignored when the very simple Escherichia coli motile system was developed, but was largely

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dismissed. However, in the last 25 years it has been substantially rehabilitated by work on other organisms with more complex taxis responses and multiple pathways (Armitage and Hellingwerf 2003; Kojadinovic et al. 2013).

Biochemical digressions: propionate metabolism and catalase Rod’s work on chemotaxis and the influence of growth substrates led to questions concerning the oxidative metabolism of propionate. He discovered that this required CO2 fixation to form an intermediate (Clayton et al. 1957), thereby establishing the pathway in this species as the recently identified methylmalonyl-CoA pathway through succinate (Flavin et al. 1955), rather than direct oxidation via acrylate and pyruvate, which was still favored by some. By now, however, the Claytons had fallen out of love with Carmel-by-the Sea, and Rod conspired to get the family away, with an NSF Senior Postdoctoral Fellowship to join the Microbiology Unit at Oxford University, England, headed by D. D. Wood. The notion was to explore the role of catalase in protecting phototrophic bacteria from oxidative killing, which occurs in the simultaneous presence of light and oxygen. This was primarily undertaken with Rhodobacter (Rba.) sphaeroides1 as he had discovered the species to give a much bigger fizz with hydrogen peroxide. It was a fortuitous choice, but not for his hypothesis concerning catalase. Rod had proposed that catalase would protect cells from photooxidative killing because it was widely believed that hydrogen peroxide was a major factor in this. However, his quantitative measurements of protein levels and the kinetics of induction of catalase—with a typical theoretical analysis—soon indicated that this was not the case (Clayton 1959c, 1960a, b, c, 1961). The work on catalase continued through a half year (1958) in Helge Larsen’s lab, at the Norwegian Institute of Technology, Trondheim, Norway. There, Rod showed by experiment and theory that in situ assays of catalase activity were rate limited, not by the enzyme (which has a very high kcat, but also a very high Km), but by permeation across the cell membrane (Clayton 1959b).

Oak Ridge National Laboratory (1958–1961) Returning to the U.S. in 1958, Rod joined the Biological Division at Oak Ridge National Laboratory, in Tennessee. At first he continued his work on catalase, investigating the

1

Known at that time as Rhodopseudomonas spheroides.

induction of protein synthesis and screening for mutants in Rba. sphaeroides that had high catalase activity, some of which lacked colored carotenoids and were highly susceptible to photooxidative killing (Clayton and Smith 1960). This work finally killed off the original hypothesis that H2O2 was involved, but the blue, carotenoidless mutants that he generated were key to his later success in identifying and isolating the photosynthetic reaction center. In hindsight, the most interesting aspect of the catalase work was that it represented the first round of an enduring intellectual competition between Rod and Britton Chance, who had proposed that catalase in combination with peroxidase could suppress the levels of H2O2 in cells (Chance 1952). However, Rod was able to show on theoretical grounds that peroxidase substrates (hydrogen donors) in such a system actually raised the H2O2 levels under all known enzymatic conditions (Clayton 1959a).

Early biochemical and biophysical work on bacterial photosynthesis For Rod the key event at Oak Ridge was meeting up with William (Bill) Arnold, a plant physiologist with a strong physics background, who had distinctive notions of how photosynthesis worked. Bill Arnold had the distinction of having done (as an undergraduate) one of the most important and best known experiments in photosynthesis— demonstration of the photosynthetic unit (Emerson and Arnold 1932). This experiment could have led to the proposal of the reaction center and it seems strange, now, that this possible implication was not made explicitly. However, Rod’s knowledge of the Emerson and Arnold experiment did prepare him for recognizing the significance of reaction centers in his own work. When Rod met Bill Arnold, the latter was gearing up to do another notable experiment, to see if photosynthetic events occurred at liquid helium temperatures. This was inspired by the notion that the photosynthetic unit behaved like a semiconductor, with light-generated electrons and holes migrating from their sites of separation to trapping sites. The experiments showed that the spectroscopic signatures of light-induced activity in chromatophores were essentially unchanged down to 1.3 K. Rod was hooked. Photosynthetic activity at 1 K could only mean that the events were electronic in nature. The spectral changes, which arose from the bulk BChl, suggested to them that ‘‘the electric field surrounding the separated electrons and holes modifies the energy levels of the bacteriochlorophyll to produce the spectral changes near its absorption bands’’ (Arnold and Clayton 1960). This was a prescient assertion, considering the later identification of spectral bandshifts as arising from both local and transmembrane electric fields.

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Bill Arnold and Rod interpreted their results as indicating excitation and migration of electrons, and concluded that ‘‘the first step in photosynthesis appears to be the separation of an electron and a hole in a chlorophyll semiconductor.’’ Accurate enough, considering that proteins were not even being thought of in this context. However, it was a limited viewpoint as migration of excitation energy itself, with subsequent electron–hole generation (charge separation), was also possible. Indeed, Duysens had earlier shown that under ambient conditions excitation energy transfer was highly efficient (Duysens 1951, 1952). Rod put these two views together in a review and, although unable to choose between three models, sketched out the possibility of a localized site of light energy trapping by charge transfer (Clayton 1962e). In three original papers from Oak Ridge (Clayton 1962b, c, d), he then showed that the major light-induced absorbance changes in chromatophores were of bacteriochlorophyll origin and were very similar in different species (Rba. sphaeroides, Rsp. rubrum, and Chromatium), in mutant strains and in preparations with very different bulk absorbance spectra. These absorbance changes, first observed by Duysens (1952), could have arisen from a small change in many bacteriochlorophylls or a large change in a small subset. In fact, Duysens et al. (1956) had suggested that these represented oxidized BChl as an intermediate in photosynthesis, but Olson and Kok (1959) subsequently concluded that it was not. Rod was able to show that not only did the spectral changes arise from the photooxidation of bacteriochlorophyll but that it was a special component, as proposed for P700 in oxygenic organisms (Kok 1956). For this entity, he coined the term ‘‘photosynthetic reaction center’’2 (Clayton 1962d), although Duysens had earlier used the term ‘‘reaction center’’ in his thesis (Duysens 1952). A particularly convincing demonstration of the special nature of the photoactive BChl was obtained with the blue, carotenoidlesss mutants of Rba. sphaeroides that he had previously isolated (Clayton and Smith 1960). When cultures were left in the light for a few weeks, these strains lost all of the bulk BChl, leaving only the photoactive component, which remained in undiminished amounts. The bulk BChl was substantially converted to bacteriopheophytin (BPhe), which gave the normally blue culture a pink hue. For these blue mutants, he estimated that the number of special BChl was 2–5 % of the total BChl (Clayton 1962b), in rather good agreement with what we know now for these strains, 2

Rod also labeled the special molecule BChl2, but this should not be taken to indicate that he thought it was a dimer, as is now known for the primary donor! However, his spectra, and those of Arnold and Clayton (1960) extended much further into the near infra-red than in previous studies, revealing the absorbance increase at 1250 nm upon oxidation, which is now associated with the dimer nature of P870.

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Fig. 6 Rod warms to his subject—a seminar at the Kettering, c.1963. Note the speculative inclusion of ubiquinone (UQ) as the electron acceptor

which have only one type of light-harvesting pigment complex (B870 or LH1) in their antenna complement. In this early work, comparing chromatophores before and after detergent (deoxycholate) treatment, Rod observed bandshifts in the BChl spectrum that were only seen on light activation, not oxidation, and were abolished by detergent. Similar behavior was seen for the carotenoids in wild-type strains. Following the earlier suggestion of Arnold and Clayton (1960), Rod ascribed them to an

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Fig. 7 The reaction center spectrum in chromatophores of Rba. sphaeroides revealed by destroying bulk BChl by oxidation with K2IrCl6 (Clayton 1966c). The large peak at 680 nm is an oxidized breakdown product of BChl

electric field effect due to light-induced charge separation in the membrane (Clayton 1962b, d).

Toward the isolation of a photosynthetic reaction center In 1961, and at the invitation of Clinton Fuller, Rod moved to Dartmouth Medical School, where he continued his work to characterize and isolate the reaction center (RC). He had already begun fractionating the membranes (chromatophores), using the detergent deoxycholate, following Bril (1958, 1960). With wild-type strains, he obtained a substantial separation of bulk BChl types, with B850 well separated from B870. Both fractions exhibited identical lightinduced spectra but the latter was much enriched. Switching to Triton X-100, he obtained a solubilized fraction from chromatophores from pink cultures of Rba. sphaeroides R26. This preparation allowed a detailed examination of the spectroscopic properties of the reaction center. This included confirmation that P870 was a specialized BChl, likely associated with some BPhe since the latter was more effective at promoting photochemistry (P870 bleaching) than bulk BChl fluorescence (Clayton 1963).

The Charles F. Kettering Research Laboratory (1962–1966) In 1962 the Claytons moved to Yellow Springs, Ohio, where Rod joined the Charles F. Kettering Research Laboratory,

directed by Leo Vernon (Fig. 6). The intellectual environment was very strong, with Anthony San Pietro, Bacon Ke and Gilbert Seely, in addition to Vernon, all working on photosynthesis topics, and a year later Berger Mayne joined the lab. Leo Vernon had had significant experience using Triton X-100 to fractionate chloroplast membranes, but Rod’s progress with isolating a purified bacterial reaction center continued to be elusive. He therefore continued to work primarily with membrane preparations and whole cells, often using various treatments that yielded materials in which the RC was essentially the only spectroscopically intact BChl species. With these, he was able to show unequivocally that the RC spectrum consisted of the three peaks at 870, 800, and 760 nm (Fig. 7). The first two, identifiable with BChl, were designated P870 and P800; the last was identified as BPhe (Clayton 1966c; Clayton and Sistrom 1966). Similar results were also found for Eimhjellen’s Rhodopseudomonas sp. NHTC133,3 which had longer wavelength components, P830 and P980, due to the presence of BChl b in place of BChl a (Holt and Clayton 1965; Olson and Clayton 1966). Rod made considerable efforts to determine the number of BChl responsible for the P800 and P870 absorbance peaks, but concluded that the ratio was most likely 2:1, i.e., 3 BChl per RC, rather than the 1:1 (4 BChl) we know today (Clayton 1966c). On the other hand, he did find that the BPhe:BChl ratio was approximately 1:2, and BPhe was later confirmed as a functional component of the RC by his post-doc Hon Yau (1971). It later became evident that the difficulties in deciding the number of BChl in the RC arose from excitonic splitting of the P870 absorbance, which gave rise to a contribution in the 800 nm band region. A shoulder here was first noticed by Feher in low temperature derivative spectra, but it was not apparent at room temperature. Furthermore, assays of Mg appeared to favor 5 BChl per RC (Feher 1971)! The pigment content was finally established by Straley et al. (1973), but it took dichroic measurements by Verme´glio and Clayton (1976) to firmly establish the excitonic band of P870 in the 800 nm region. Rod also examined the relationship between fluorescence and photochemistry and confirmed the pioneering work of Duysens that implied that fluorescence and photochemistry were competitive and that excitation energy transfer in the light-harvesting pigments served many energy traps (RCs) (Clayton 1966a; Vredenberg and Duysens 1963). A more subtle analysis allowed him to conclude that photochemistry was from the singlet state, as suspected, and that only singlets were involved in energy

3 Later identified as Rhodopseudomonas (now Blastochloris, Blc.) viridis.

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transfer while triplets, for example, were not involved (Clayton 1966b).

Cornell University (1966–1984) Rod’s work in defining the RC was high profile and by 1965 he had caught the attention of several universities. He eventually chose Cornell University, in Ithaca, New York, where he was appointed in both Biological Sciences and Applied Physics in 1966. It was an appropriate juxtaposition, but Rod had no appetite for developing some sort of combined academic program, as had been hoped by the administration. Instead, he finally threw himself full time into trying to isolate the RC in a genuinely purified form. The faltering progress made to that point largely reflected the general state of knowledge of membrane fractionation rather than naivety of biochemical methods. Although Rod claimed to find biochemistry an ‘‘awe-inspiring mystery,’’ his thesis and subsequent work, described above, show him to be a very competent microbiologist and biochemist, and an informed student of metabolism. However, membrane protein purification was still in its infancy with few guidelines, and Rod was not aware of the separation techniques that might have led him to isolate reaction centers much earlier. Even these few years later, with his post-doc Dan Reed also working on the project from 1967, the significant advantages of different detergents were not widely appreciated. Sticking with Triton X-100, Rod and Dan were able to obtain a more refined preparation in which the only BChl was the reaction center (Reed and Clayton 1968), although the spectroscopic definition was not greatly improved over the variously treated membranes of the earlier work (Clayton 1966c). Furthermore, it also contained cytochromes b and c, and further characterization showed it to have an apparent molecular mass of 650,000, several fold larger than what we now know for purified RCs (Reed 1969). It seems likely, now, that it constituted membrane fragments or aggregates, depleted of light-harvesting pigments but containing some bc1 complex. Finally, a tip from Bob Bartsch, kindly passed on by Georger Feher, introduced a new detergent, lauryldimethylamine-N-oxide (LDAO), with which Feher (Feher 1971) and Clayton (Clayton and Wang 1971) were both able to purify the minimal photosynthetic RC we know today (Fig. 8). It had an apparent molecular mass of 70,000, although the true value is 105,000. Throughout his work, but especially in the 60s and early 70s, Rod put a lot of store and effort into measuring quantum yields of photochemical activities and fluorescence emission. Initially this was driven by the need to establish the primary functionality and connectedness of phenomena such as absorption changes and excitation

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Fig. 8 Rod thinks it over—with George Feher, at the International Conference on the Photosynthetic Unit, Gatlinburg, TN, 1970. Photo by Jeanette Brown

energy transfer associated with spectral components whose identity and significance were still unknown. As the photosynthetic reaction center became more of a reality, these measurements assumed more targeted meaning and helped to establish the nature of the RC itself and its immediate light-harvesting environment. The apogee of this work was Ken Zankel’s measurement of the absolute yield of fluorescence from the reaction center, a tiny number that allowed estimation of the rate of the primary photochemical electron transfer event (Zankel et al. 1968). The calculated time constant of 7 ps was in excellent agreement with the later direct measurement of 3–4 ps (Holten et al. 1980). Likewise, Richard Wang measured the absolute yield of fluorescence emission from the bulk BChl (Wang and Clayton 1971), a parameter that had long been needed to obtain absolute values from the many measurements on relative yields and excitation transfer rates. In parallel with ongoing efforts to isolate the reaction center minimal unit, Rod had long been interested in the implications of a photosynthetic unit (PSU) comprising a well-defined trap, the reaction center, with associated lightharvesting antenna. The primary tool for studying this was fluorescence emission, which came from the bulk pigments but was controlled by the activity state of the reaction center, or centers, depending on the extended structure of the PSU. The first descriptions of the energy transfer process necessary for excitation to reach a reaction center had been given by Duysens (Duysens 1952), employing the theoretical grounds provided by Fo¨rster. With the discovery of two photosystems in oxygenic organisms the picture became more complex, but fortunately photosystem II was by far the major emitter. Rod described prompt fluorescence and delayed light emission from the bulk pigments of a wide variety of species of bacteria and plants/algae (Clayton 1965, 1966b). For bacteria he showed that the well-defined relationship between fluorescence and P870

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oxidation, seen by Vredenberg and Duysens (1963), was limited to aerobic conditions, and that under anaerobiosis the fluorescence was controlled by events on the electron acceptor side, in the same manner as in photosystem II where the oxidized acceptor, Q, is a quencher (Clayton 1966b). Rod’s main theoretical contribution was to develop a general model of fluorescence emission and quenching that included heterogeneity in the domain size and connectedness of PSUs (Clayton 1967). From this, other models, such as those of Joliot (Joliot and Joliot 1964; Joliot 1965) and Vredenberg (Vredenberg and Duysens 1963), arose as special cases. For photosystem II, the general model was largely accepted as necessary to account for new experimental data from later work by Joliot and coworkers (Joliot et al. 1973). Rod also embraced the notion of ‘‘dead fluorescence’’ arising from pigments that were not functionally connected to a trap, i.e., domains or PSUs that lacked reaction centers (Clayton 1969; Lavorel 1968). These modifications can cause significant departures from the behavior described by homogeneous models, with special impact on delayed light emission as I had found in my own work (Wraight 1972). Rod especially showed a keen appreciation for the meaning of an ‘‘energy trap’’ with respect to excitation energy migration between antenna complexes and to the RCs. He showed this to be largely unaffected by the energy differences indicated by the long wavelength absorption peaks, in contrast to the popular idea of an energy ‘‘funnel.’’ A striking experimental demonstration of this was the uphill energy transfer from the bulk pigments of Blc. viridis, with a peak absorbance at 1030 nm, to P980 in the RC (Holt and Clayton 1965; Olson and Clayton 1966). Ken Zankel

Fig. 9 BJ, Rod, and Tom Ebrey at the Third International Photosynthesis Congress, Stresa, Italy, 1971

subsequently showed this to be a general phenomenon within antenna pigments, with excitation transfering readily from B870 to B850, e.g., in Rba. sphaeroides (Zankel and Clayton 1969). This emphasized the free reversibility of excitation energy transfer, which later became important for understanding RC function in a well coupled pigment bed.

Some personal recollections from the 1970s I joined Rod’s lab in February, 1972, following a year at the Biophysics Laboratory in Leiden, The Netherlands, headed by Louis N. M. Duysens (I have been very fortunate, therefore, to have a direct line of descent from two of the fathers of the reaction center commemorated in this issue). I had been drawn to Rod’s work because I admired his thinking about fluorescence emission (see above), which pertained to my prior research in Leiden and for my PhD at Bristol University, but was sufficiently different to suggest that my experience would be significantly broadened. I was also drawn to him by an anecdote that he had slept on benches at the Newport Jazz Festival. This turned out to be quite untrue and I have no idea, now, where I heard it. But the real story is that Rod and BJ went to Newport (from Woods Hole) to drag their daughter, Ann, back from the Folk Festival, where she had gone without permission, and it was Ann who had slept rough! Indeed, at that time Rod did not seem to be particularly interested in any form of music, and certainly not jazz, although he was wonderfully enthusiastic about the musical talents of his daughter, who was an excellent pianist with classical training. By Rod’s own admission, few things penetrated his commitment to science, with the exception of skiing— and butterfly collecting, an interest we shared from about the same age. It was deep winter when I arrived and almost the first thing Rod did was to offer to take me skiing at Greek Peak, the nearest ski slopes about half an hour away. I had just started skiing the week before arriving at Ithaca and, while a beginner, I had taken quite well to it and was very enthusiastic to do more. We went regularly throughout the two winters I spent with him. Rod was a strong but journeyman skier and yearned to be able to wedeln. Whatever his technical limitations, however, he was intrepid. He would take on slopes and mogul fields that seemed well beyond his grade and always muddled through. This was fully in character because, at heart, Rod was a serious risk taker who was kept in check only by his wife, BJ, with whom he had a very close and loving relationship (Fig. 9). Rod’s lab was always small in number and much of his work was done alone, or in effective collaboration with BJ, who was an accomplished technician despite no formal

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scientific training. She also acted as lab manager, as well as mother and disciplinarian to other lab members. BJ was solely responsible for maintaining the bacterial cultures in the lab, but gave all new lab members meticulous instructions in the procedures involved, especially sterile technique. BJ never went to college but she was very bright and had been the valedictorian at her High School in Indiana. However, the mores of the time and her rural family meant that college was out of the question for a girl. I had no idea about this and once asked her what she had majored in, to which she answered ‘‘boys.’’ When I arrived, there was only one other post-doc, Lou Sherman, who departed shortly thereafter (now at Purdue University), and a technician, Steve Drews. Steve was a member of a three-person Moog synthesizer group, Mother Mallard’s Portable Masterpiece Company, which was quite well known for the exotic form known as the New York School of the Hyponotic. I greatly enjoyed their music, and Rod and BJ were quietly supportive despite their bewilderment. Post-docs and visiting scientists who overlapped with me were Peter Heathcote, Richard Cogdell, and Dan Brune. Others who came afterward included Andre´ Verme´glio, Chuck Rafferty, and Tomoko Yamamoto. After the experience of the Biophysical Laboratory, which had an extensive and sophisticated team of electronics and machine workshop technicians that produced beautiful, professional-looking apparatus, I was bemused by Rod’s equipment, which was literally held together by something called tacky wax (Fig. 10). The materials were often cardboard and styrofoam, usually sprayed black, but it was highly functional and I doubt if its performance was in any way inferior to the best looking instruments available. In reading the descriptions of the apparatuses that Rod built for his experiments in the 1950s, it amused me to recognize that the instruments he constructed then were almost certainly held together in the same way as those I encountered in Rod’s lab the 1970s! After a short period of orientation in the lab, Rod and I decided that a good project for me was to measure as precisely as possible the quantum yield of charge separation in bacterial photosynthetic reaction centers. Rod had already put a lot of time and effort into determining the quantum yield in many preparations, but with variable results, ranging from 0.4 to 1.0. Paul Loach had reported that cytochrome c was photo-oxidized in Rsp. rubrum chromatophores with a quantum yield of 0.85, leading to an estimate of 0.95 for photooxidation of the reaction center itself (Loach and Sekura 1968). Previous measurements by Rod and coworkers had also yielded values very close to 1 (Bolton et al. 1969). Decisively, however, the fluorescence yields of isolated reaction centers in the open and closed states indicated a value of &0.7 according to the simple relationship, /p = (Fmax - Fmin)/Fmax, where /p is the

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Fig. 10 Rod contemplates the diffusion pump for the helium cryostat, 1973—one of my favorite photos of him. Photo by Colin Wraight

photochemical yield, Fmin is the fluorescence intensity when photochemistry is active, and Fmax is the fluorescence intensity when photochemistry is shut off (Clayton et al. 1972a). We therefore considered it to be an important, open question. The basic measurement was the initial slope of charge separation under illumination by weak light of defined intensity and wavelength. To ensure that the absorbed light energy was well defined, I mapped the intensity over the whole illumination field at the cuvette, and modified the position and angle of the light source to minimize the inhomogeneities. Measuring the initial slope of the charge separation was, of course, key to a valid result and Rod showed me the trick of using a small mirror placed perpendicularly to the trace at the origin, to obtain a smooth, linear transition between the actual trace and its reflection (see Bolton et al. 1969). With this in hand, Rod and I retired to our own desks to measure the slopes independently. The mirror trick was very effective and our values were in extremely good agreement. Using the newly established extinction coefficients for the reaction center (Straley et al. 1973), we concluded that the quantum yield was very high—1.02 ± 0.04, which is generally taken to mean at least 0.98 (Wraight and Clayton

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Fig. 11 The gathering at Cornell 1973. Standing, from left to right: Bob Downs (graduate student), Baz Jackson, Les Dutton, Stewart Lindsay, Colin Wraight, Lou Sherman, Darrell Fleischmann, Berger Mayne; Sitting: Susan Straley, BJ Clayton. Photo by Roderick Clayton

1973). Evidently, any skepticism regarding Paul Loach’s or Rod’s earlier measurements was quite unwarranted! Nevertheless, confirming a value very close to 1 made it clear that the fluorescence yields of RCs in open and closed states could not be used to obtain an absolute value of the photochemical yield, and that other pathways of de-excitation were in play. During my first year with Rod, I became friends with Les Dutton at the Johnson Foundation (JF) at the University of Pennsylvania. This was prompted by visits to the JF by Baz Jackson, who was a fellow graduate student in Tony Crofts’ lab at the University of Bristol. Baz had started visiting the JF a few years earlier, to work with Britton Chance on ion transport and energy coupling in photosynthetic bacteria. At that time, the Bristol groups of Brian Chappell, Peter Garland, and Tony Crofts were the frontline support of Peter Mitchell’s chemiosmotic coupling hypothesis, while Brit was the embodiment of the chemical view. In fact, Brit was almost completely driven by empirical evidence and was so far unpersuaded by experiments supporting the chemiosmotic theory, but he was very keen to see the work done that might resolve the issues. He was also extremely generous in promoting young scientists to visit the JF to do just that. Baz was one of those and was at the JF in the first summer I was in Ithaca, and I took the opportunity to visit him there. This turned out to be a harrowing trip as my newly acquired 1966 Mustang developed an electrical fault in which all the

lights went out intermittently as I drove through the pitch black Catskill Mountains. Nevertheless, thus began a longstanding, enjoyable, and fruitful friendship with Les Dutton and others at the JF, especially Jack Leigh, a master of all things but especially magnetic resonance. Les and Jack had recently identified an EPR signal from illuminated reaction centers, which corresponded to a triplet state (Dutton et al. 1973). It was only seen in samples where the normal electron acceptors (quinones) were already chemically reduced and photochemical activity was blocked. Jack, Les, and I measured the quantum yield of triplet formation, in the process blowing up the laser and setting fire to the dye solvent, and found the yield of triplet in reduced RCs to be indistinguishable from the normal photochemistry, i.e., &1 (Wraight et al. 1974). This could be indicative of the triplet state as a side product or as an intermediate in the active pathway. However, our EPR measurements were done at low temperature, and Bill Parson and Rod subsequently showed that at room temperature the yield was only 0.1 (Parson et al. 1975) ruling it out as an intermediate in functional electron transfer. Rod was actively following this work and thought that a grand meeting of minds would be helpful and fun, and invited Les and Baz to visit. This turned into a small gathering of past and present Clayton lab friends and associates (Fig. 11). As early as 1962, Clayton observed light-induced reduction of ubiquinone in chromatophores in approximately stoichiometric proportion to the photooxidation of

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BChl or cytochrome c, depending on the redox state (Clayton 1962a). He suggested that UQ might correspond to the primary electron acceptor (see Fig. 6), but subsequently backed off from this, considering it to be a secondary acceptor (Reed et al. 1969). Rod and Sue Straley discovered the absorbance band at 450 nm that we now know is characteristic of the ubisemiquinones of QA and QB, and suggested that it most likely represented the primary acceptor (Clayton and Straley 1970). However, the key work of Land and coworkers on the ubisemiquinone spectrum was yet to come (Land et al. 1971; Land and Swallow 1970). Just 2 years later several groups, including Rod’s, published spectroscopic results that supported the identification of a ubisemiquinone anion radical as the reduced primary acceptor (Clayton and Straley 1972; Loach and Hall 1972; Slooten 1972). Simultaneously, this assignment was strongly supported by the Q-band ESR spectrum of a g2 signal in preparations treated to remove an iron atom associated with the RC (Feher 1971). When the iron is present, this signal is broadened so much as to be unrecognizable, but it had been reported by Feher (1971) and by Leigh and Dutton (1972). The activity of ubiquinone as the primary acceptor was confirmed in Rod’s lab by Richard Cogdell, who arrived as a post-doc in 1973. Richard was able to extract the ubiquinone with dry organic solvents, which rendered the RCs in active, and restore photochemical activity by adding ubiquinone back (Cogdell et al. 1974). Rod had earlier found that high detergent depleted the secondary acceptor pool and that the combination of o-phenathroline and high LDAO inhibited photochemistry, suggesting that the primary acceptor was extracted (Clayton et al. 1972b). Mel Okamura, in George Feher’s lab, subsequently developed this into a quantitative approach to show that RCs had two ubiquinones, a primary quinone (QA) essential for photochemistry, and a secondary quinone (QB) (Okamura et al. 1975). At the end of 1973, Rod went to Bill Parson’s lab at the University of Washington, Seattle, for a sabbatical, and Richard Cogdell went with him to continue his post-doc in Bill’s lab. Bill was beginning the first nanosecond kinetic studies of RCs, and the work there led to the discovery of two short-lived intermediate states, termed PF and PR (Parson et al. 1975). PF was suggested to be on the path of electron transfer, and was subsequently identified as P?BPhe-. PR was likely a side reaction, possibly a triplet, but its decay kinetics were much slower than those reported by Dutton et al. (1973) for a triplet EPR signal. However, the EPR signal is strongly spin polarized, accounting for its large size and unusual features and, as shown by Marion Thurnauer and Jim Norris at Argonne National Lab, the fast decay observed is for the polarization, not the triplet state itself (Thurnauer et al. 1975). By this time, I had moved on to get a ‘‘real job’’ at the University of California at Santa Barbara. Setting up my

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lab was slow and, despite occasional visits to Les Dutton at the JF, I became frustrated. Luck would have it that at the Biophysical Society Annual Meeting in the spring of 1975, Govindjee came up to me and asked why I hadn’t applied for a job opening at Illinois! In fact, I had been thinking of looking for a new position but, apart from interviewing at Harvard, I had done nothing systematic about it and was unaware of the post at Illinois. The search was actually closed, but Govindjee and Tom Ebrey (also a former postdoc with Rod, but a couple of years before me) arranged for me to go immediately to Urbana for a job interview. In spite of misjudging the length of my seminar, such that Gregorio Weber left before the end, I got the job and started there in the Fall. Harvard was not pleased. I felt bad about leaving UCSB after only 18 months, but the Chair of the department, George Taborski, was very understanding and wished me well. The spectrophotometer I had been waiting for at UCSB was still not completed but I was allowed to take what was done, plus the blue-prints, for completion at Illinois. I loaded up my VW van with everything I could lay my hands on, such that the wheels looked as if they were buckling, and drove across country. Waiting still for the necessary instrumentation at Illinois, I continued to visit Les Dutton whenever I could, especially because the free-wheeling nature of his lab and Les’s generosity allowed me to do experiments almost unhampered. During one visit there, in November 1975, I observed the characteristic binary oscillations of the semiquinones in RCs for the first time. I recognized them immediately as an electron gating activity, as similar patterns of electron accumulation and release had been seen for Photosystem II by Bernadette Bouges-Bocquet (1973) and Bruno Velthuys (Velthuys and Amesz 1974). However, this was the first observation of the optical spectrum, which showed the oscillations to be a semiquinone and identified the activity of two ubiquinones acting in series as a two-electron gate. Because of delays in my own instrument set-up, it took me a while to bring this to fruition, but it led me to start measurements of the proton uptake that must accompany the full reduction of quinone to quinol, and this became an enduring aspect of my research for many years. At almost the same time, Andre´ Verme´glio, who had come to Rod’s lab after I had left, discovered the same behavior. Having a good grounding in PS II he also immediately recognized the significance of the oscillatory behavior and, according to Rod, exclamations of ‘‘Jesus Christ, just like System Two!’’ could often be heard emanating from the dark room where Andre´ was working. Our parallel work became apparent at a meeting at Brookhaven National Lab, in 1976, and Rod brokered an arrangement whereby Andre´ and I would submit papers simultaneously (Verme´glio 1977; Wraight 1977). Andre´’s

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spectra were beautiful and extended from the UV into the near infra-red, and I regretted holding back my results on the associated proton binding (Wraight 1979). While in Rod’s lab, Andre´ also initiated some very elegant spectroscopic studies on oriented chromatophores and RCs, using linear dichroism to reveal the orientations of the transition moments of various pigments (Clayton et al. 1979; Verme´glio and Clayton 1976). Rod was especially excited by this work, because it involved the application of polar geometry, which he had not used in decades—in fact, since learning it as a student at Cal Tech. This unfettered enthusiasm was typical of him. It was an important part of the inner drive that was apparent in all aspects of his life, as became especially evident later on. Rod’s enthusiasm made him a wonderful teacher oneon-one, but his classroom approach was heavy handed (he described himself as a didactic steamroller), despite lightening the atmosphere by sharing some of his discoveries from playing with words. He delighted in telling his class that ‘‘snot hypothesis’’ was an anagram of photosynthesis, and suggesting that an enzyme, ‘‘transvestase,’’ was responsible for turning the normally blue cultures of Rba. sphaeroides R26 pink, if they were allowed to over-grow. His ability to explain things was especially well illustrated by the books he wrote—‘‘Light and Living Matter, Vols 1 and 2’’ (Clayton 1970a, b) and ‘‘Photosynthesis: physical mechanisms and chemical patterns’’ (Clayton 1980). In both, he was especially effective in bringing simple physical principles alive, and they remain very useful introductions to light measurements and interactions with materials (albeit unfortunately out of print). Rod had a decidedly mischievous streak in him. I remember sitting with him at lunch during a visit to Urbana to deliver a seminar to the Chemistry Department (invited by Ken Kaufman). On the other side was Sam Kaplan, who was telling Rod, with great excitement (and very fast), about the newly discovered cytoplasmic signaling molecules ppGpp and ppGppp, affectionately known as Magic Spot 1 and 2. Rod had lost the thread within a minute or two and suddenly interjected ‘‘Vot is zis pee–pee business?’’ This threw Sam off his stride–but only for a moment. In his opening remarks for his seminar, Rod noted that the name of our local airline, Ozark, spelled krazo backwards and that its logo looked like a headless bird (Fig. 12). Not surprisingly the airline was one of a string of short-lived companies that attempted to make a living serving the Midwest at that time. It is perhaps only coincidence that Rod’s favorite comedian, George Carlin, appeared in advertisements for Ozark in the 1960s. As a more recent example, I tried to find out some current details about Rod on the internet and I came across a social web site called Spokeo. It was evident that he had

Fig. 12 Ozark air lines’ logo, c.1980

started this and almost immediately lost interest in it, and the only significant entries in the template were that he was Male, Aries, in his Late 80’s, and African-American!

Decline and fall: and resurrection Rod’s life took a terrible and unforeseen turn in 1980. In preparation for a visit to France, the necessary health requirements for a visa revealed that BJ had cancer of the lung. Rod and BJ had both been smokers, but he had given up many years earlier while BJ struggled to do so. The cancer was quite far advanced and BJ died in the fall of 1981, shortly after their last joint publication appeared (Clayton and Clayton 1981). In the summer of that year, as she had often in the past, BJ accompanied Rod to the Gordon Research Conference on Biochemical Aspects of Photosynthesis, held at Kimball Union Academy, NH. She was very weak and spent most of her time in their room, but she received visitors when she could. Toward the end of the week, she asked me to visit her, which I did, accompanied by Les Dutton and Bill Parson, and she talked about her concerns for Rod. She knew better than anyone that he had the potential for going off the tracks, and that his curiosity could potentially take him anywhere. His smooth progression through a life in science, so far, was due in part to BJ keeping him focused on his primary love, but she knew, as he did, that he had a propensity for risk taking. BJ’s parting words to us were ‘‘take care of Rod.’’ In this, we and many others were spectacularly unsuccessful. Over the next couple of years, Rod’s life unraveled like a pilot episode for Breaking Bad. Rod was not a total stranger to the counter culture and he and I had occasionally enjoyed smoking pot while I was in Ithaca. BJ did not approve but tolerated it because it clearly released Rod from some of his workaholic demons. In subsequent years, however, he made friends with some who were more invested in it. When BJ died, Rod largely rejected the well meant but staid reactions and condolences of the academic community and sought solace in the hippie-esque values he saw in his new friends. The transition was extraordinarily rapid. In the winter of 1981, he visited us in Illinois on his way to California, where both his children lived. He was quite wild, but truly excited by the new experiences he was feeling and seeing. He was

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discovering, among other things, a newfound delight in popular music, especially of the 1960s and 1970s, and many esthetics that he had not had time or the inclination for before. Unfortunately, this included more extensive and varied drug experiences, including the use of cocaine. At this point, when he returned to Ithaca, his new life merged with the old as he was able to harness his old fashioned, but still very serviceable, chemical knowledge to extracting and refining drugs. Apart from the obvious issues of legality, a major problem was the incongruity and inappropriateness of the youthful environment he had immersed himself in. He was oblivious to fact that, rather than a family of peers, he was surrounded by acolytes and that he had taken on the mantle of a Pied Piper. My family visited him in Ithaca around this time and was dismayed by the unkempt state he was in and the disarray of his house, which BJ had always kept in immaculate condition. It is fortunate that the situation came to the attention of the authorities before anything truly untoward happened. Abrupt events in 1984 shook him awake. He was lucky to escape major criminal consequences, but it was a scandal that Cornell University could not ignore. As Rod has written, Cornell was very generous in their handling of it and he was allowed to retire gracefully as the Liberty Hyde Bailey Professor Emeritus in the Division of Plant Biology. Many people have expressed regret and some guilt at not doing more to steer Rod away from the downward path he took. But it was impossible and, indeed, few were able to even stay in meaningful contact with him. However, from 1985 onwards, he began to recover his life and to undergo a remarkable, second transformation. Typically, he retained what he felt were the good things he had learned as a hippie, and was much more attuned to peoples’ feelings, including his own. In his own words, he was ashamed that as a father he had told his young son, Rick, that his favorite word was ‘‘work’’ not ‘‘love.’’ His discovery of an expansive meaning of love was touching and remained central to his world view for the rest of his life. And he kept the music. He was especially fond of the Grateful Dead and often enjoyed singing their songs to me a cappella, particularly Ripple, which was a talisman for him. Most importantly, he was inspired to develop the creative potential of applying his formidable scientific intellect to the arts and humanities. His first exploration of the art world was through photography, where he delighted in the techniques accessible in developing black and white photos, such as solarization. He sent me several examples and they showed a primitiveness that was partly technical but also reflected the state of his regrowth. It was a pleasure and a relief to see this happening. In 1988 he moved permanently to California, first to Los Angeles where his daughter, Ann, still lives. I was able to maintain sporadic contact through telephone calls and

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occasional visits. He was always full of news of what he was doing. Another source of stability for Rod was his lifelong dedication to butterfly collecting, and he amassed an extraordinary collection. In LA the active collecting took a back seat to a classic Rod enterprise that combined his scientific acumen and curiosity in a survey of the more than 600 North American skippers. Skippers are instantly recognizable by the characteristic way in which they sit with the fore wings perpendicular to the hind wings, but, with generally rather drab coloring, many species are so similar that even experts cannot reliably distinguish them. However, Rod discovered that even the most similar looking species had radically different and exotically shaped genitalia! Over a few years he dissected and examined many of the species and worked on a monograph, illustrated with his own micrographs. Unfortunately, it was probably not finished and its whereabouts are unknown. However, in 2000 his butterfly collection was transferred to the Texas Lepidoptera Survey in Houston, under the care of Dr. Charles Bordelon. Although they only met once, when the collection was moved, they became great friends through their exchanges of lepidopteran specimens. In January 1994, I visited Rod on the way to a winter Gordon Research Conference. It was just days after the Northridge earthquake and Rod’s house, while unaffected, was close to a neighborhood that was hard hit. By this time, Rod had moved on from photography and had taken up ceramics. Here his precise logic and chemical interests meshed with established methods in a stunning way. He had invested in a gas kiln capable of firing reduction, allowing him to use glazes that produced wondrous colors, and he continually experimented with glazes of his own devising. When I saw him he was already extremely adept at the manual handling of clay, and he produced some outstanding pieces of very high quality. Of course, everything was a one-off and he was not interested in developing anything like a product, although he did exhibit and sell his work at local events. He was always eager to give his pieces away and he pressed me to select some to take home. Among other smaller items, I chose a couple of large, thin but extraordinarily flat plates, made by his adaptation of the millefiori technique. Although seemingly fragile, they have survived frequent usage (Fig. 13). Rod enjoyed talking and he would only communicate by phone, but he became increasingly difficult to understand as he got older. He would send me ‘‘care packages’’ with examples of whatever he was working on, including photos and drawings and the occasional one line. Knowing that I preferred writing, he once scribbled ‘‘I don’t write letters ‘cause I’m illiterate.’’ His reluctance to write was both frustrating and surprising, since we know from his papers and very successful books that he was an outstanding writer.

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(Allen et al. 1987a, b) had both been reported by then. Illustrating both his old scientific and new artistic sensibilities, at the conference he gave away several T-shirts that he had designed, with a wonderful representation of the pigments of the RC like burning embers against the black cloth. These were cherished by many, none more than by Arnold Hoff, who was almost overcome by the significance of the gesture. For many participants at that meeting, Rod’s presence was as memorable as the science.

Coda Fig. 13 Two plates by Rod—the larger one is 13’’ in diameter; the smaller one is a classic example of the millefiori technique. Photo by Colin Wraight

In 1999, Rod relocated to a small house in Santa Rosa, CA. He had one old friend nearby and he adapted quickly to his new environment. He had always loved animals, especially dogs, and he was very hard hit when his long-time companion, Tret, died. In Santa Rosa he became involved with a local group that trained service dogs, and he put a lot of time and effort into that. Meanwhile his main artistic outlet became drawing and he sketched his friends, dogs in particular, and some self-portraits (Fig. 14). He was never very interested in landscapes, which was fully consistent with his focus, at least in later life, on people, which evidently included dogs. Rod’s recovery was well underway by 1988, and I invited him to the Gordon Research Conference on Physical Aspects of Photosynthesis at the Holderness School, NH, which I organized. He was thrilled by the prospect, in part because the X-ray structures of reaction centers from Blc. viridis (Deisenhofer et al. 1985) and Rba. sphaeroides

In spite of the traumatic events that ushered in the last part of his life, Rod enthusiastically embraced everything that came his way and I believe he was highly fulfilled in all chapters of his life. In his science career, he was well recognized, being elected to the American Academy of Arts and Sciences in 1975 and to the National Academy of Sciences in 1977. In 1982, he was awarded the Prize in Biological Physics from the American Physical Society (jointly with George Feher). As a scientist, Rod Clayton was a stimulating and challenging colleague to all who knew him, and a wonderful mentor and a very important friend to me. It could be viewed as tragic that his scientific career ended in such a sudden, unnecessary and messy way, but it was inspiring to see how easily and eagerly he applied the creativity that we all saw in his science to the entirely new esthetics of his recovery. Rod had a certain childlike quality about him, which blossomed after he left science behind and was expressed in an excitement and interest in things that I think he was oblivious to before. In his later life, he was

Fig. 14 Left—‘‘Narissa’’ 2000; Right—Self portrait, 2001

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full of wonder at the love and warmth he found in the communities he lived among, and his keen acceptance of new friends and experiences is a lesson for us all. Acknowledgments I am indebted to Mrs. Ann Williams, Rod’s daughter, for all her help in piecing together details of Rod’s early life. It would have been an impoverished version without her willingness to answer so many questions. She was truly a fount of information, as well as the source of many of the photos that I have used in this memoir. Unfortunately, the true provenance of most of the photos is unknown.

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