Abstract
During the early- to mid-twentieth century, a bitter controversy raged among researchers on photosynthesis regarding the minimum number of light quanta required for the evolution of one molecule of oxygen. From 1923 until his death in 1970, Otto Warburg insisted that this value was about three or four quanta. Beginning in the late 1930s, Robert Emerson and others on the opposing side consistently obtained a value of 8–12 quanta. Warburg changed the protocols of his experiments, sometimes in unexplained ways, yet he almost always arrived at a value of four or less, except eight in carbonate/bicarbonate buffer, which he dismissed as “unphysiological”. This paper is largely an abbreviated form of the detailed story on the minimum quantum requirement of photosynthesis, as told by Nickelsen and Govindjee (The maximum quantum yield controversy: Otto Warburg and the “Midwest-Gang”, 2011); we provide here a scientific thread, leaving out the voluminous private correspondence among the principal players that Nickelsen and Govindjee (2011) examined in conjunction with their analysis of the principals’ published papers. We explore the development and course of the controversy and the ultimate resolution in favor of Emerson’s result as the phenomenon of the two-light-reaction, two-pigment-system scheme of photosynthesis came to be understood. In addition, we include a brief discussion of the discovery by Otto Warburg of the requirement for bicarbonate in the Hill reaction.
Similar content being viewed by others
Notes
John F. Allen told us about his recollection of an exchange at a Photochemistry Discussion Group meeting at London's Royal Institution in 1975. Sir George Porter was organizer and chair. Helmut Metzner had just given a talk on the possible role of bicarbonate/CO2 in the Hill reaction. Porter addressed Robin Hill in the audience, “But, CO 2 is not required for your reaction; is it? Robin replied “Yes, it is.” (See Shevela et al. 2012 for a complete perspective on this issue.)
References
Arnold W (1935) Investigations on photosynthesis. PhD Thesis, Harvard University, Cambridge, Massachusetts, USA
Arnold W (1949) A calorimetric determination of the quantum yield in photosynthesis. In: Franck J, Loomis WE (eds) Photosynthesis in plants. Iowa State College Press, Ames, pp 273–276
Arnon DI, Barber J (1990) Photoreduction of NADP+ by isolated reaction centers of photosystem II: requirement for plastocyanin. Proc Natl Acad Sci USA 87:5930–5934
Arnon DI, Knaff DB, McSwain BD, Chain RK, Tsujimoto HY (1971) Three light reactions and the two photosystems of plant photosynthesis. Photochem Photobiol 14:397–425
Baker NR, Bradbury M, Farage PK, Ireland CR, Long S (1989) Measurements of quantum yield of carbon assimilation and chlorophyll fluorescence for assessment of photosynthetic performance of crop plants in the field. Phil Trans Royal Soc B 323: 295–308
Bannister TT (1972) The careers and contributions of Eugene Rabinowitch. Biophys J 12:707–718
Bassham JA (2003) Mapping the carbon reduction cycle: a personal retrospective. Photosynth Res 76:35–52
Bassham JA, Benson AA, Kay LD, Harris AZ, Wilson AT, Calvin M (1954) The path of carbon in photosynthesis. XXI. The cyclic regeneration of carbon dioxide acceptor. J Am Chem Soc 76:1760–1770
BBC movie “Botany: a Blooming History, Episode 2, The Power of Plants” (2010) http://www.bbc.co.uk/programmes/b011wz4q (Not currently available on BBC iplayer); contact Govindjee (e-mail: gov@illinois.edu) for further information
Benson AA (2002) Following the path of carbon in photosynthesis: a personal story. Photosynth Res 73:29–49
Benson AA (2010) Last days in the old radiation laboratory (ORL), Berkeley, California, 1954. Photosynth Res 105:209–212
Blackman FF (1905) Optima and limiting factors. Ann Bot 19:281–296
Blankenship RE (2014) Molecular mechanisms of photosynthesis, 2nd edn. Wiley-Blackwell, Oxford
Blankenship RE, Tiede DM, Barber J, Brudvig GW, Fleming G, Ghirardi M, Gunner MR, Junge W, Kramer DM, Melis A, Moore TA, Moser CC, Nocera DG, Nozik AJ, Ort DR, Parson WW, Prince RC, Sayre RT (2011) Comparing photosynthetic and photovoltaic efficiencies and recognizing the potential for improvement. Science 332:805–809
Bolton JR, Hall D (1991) The maximum efficiency of photosynthesis. Photochem Photobiol 53:545–548
Brown HT, Escombe F (1905) Researches on some of the physiological processes of green leaves, with special reference to the interchange of energy between the leaf and its surroundings. Proc R Soc Lond Ser B 76:29–111
Buchanan BB (2012) A conversation with Andrew Benson: reflections on the discovery of the Calvin-Benson Cycle. YouTube video http://www.youtube.com/watch?v=GfQQJ2vR_xE. Accessed 1 March 2014
Buchanan BB, Wong JH (2013) A conversation with Andrew Benson: reflections on the discovery of the Calvin-Benson cycle. Photosynth Res 114:207–214
Bücher T (1983) Otto Warburg: a personal recollection. In: Sund H, Ullrich V (eds) Biological oxidations. Springer, Berlin, pp 1–29
Burk D, Hendricks S, Korzenovsky M, Schocken V, Warburg O (1949) The maximum efficiency of photosynthesis: a rediscovery. Science 110:225–229
Burk D, Cornfield J, Schwartz M (1951) The efficient transformation of light into chemical energy in photosynthesis: an application of the Einstein law of photochemical equivalence to living organisms. Sci Mon 73:213–223
Calvin M, Bassham JA, Benson AA (1950) Chemical transformations of carbon in photosynthesis. Proc Fed Am Soc Exp Biol 9:524–534
Duysens LNM (1952) Transfer of excitation energy in photosynthesis. Doctoral thesis, University of Utrecht, The Netherlands
Duysens LNM (1958) The path of light in photosynthesis. Brookhaven Symp Biol 11:18–25
Duysens LNM (1962) A note on efficiency for conversion of light energy. Plant Physiol 37:407–408
Einstein A (1912a) Thermodynamische Begründung des photochemischen Aequivalentgesetzes. Ann Physik 37:832–838
Einstein A (1912b) Nachtrag zu meiner Arbeit: thermodynamische Begründung des photochemischen Aequivalentgesetzes. Ann Physik 38:881–884
El-Shintinawy F, Govindjee (1990) Bicarbonate effect in leaf discs from spinach. Photosynth Res 24:189–200
Emerson R (1958) The quantum yield of photosynthesis. Annu Rev Plant Physiol 9:1–24
Emerson R, Arnold W (1932) The photochemical reaction in photosynthesis. J Gen Physiol 16:191–205
Emerson R, Chalmers R (1955) Transient changes in cellular gas exchange and the problem of maximum efficiency of photosynthesis. Plant Physiol 30:504–529
Emerson R, Chalmers R (1958) Speculations concerning the function and phylogenetic significance of the accessory pigments of algae. Phycol Soc News Bull 11:51–56
Emerson R, Lewis CM (1939) Factors influencing the efficiency of photosynthesis. Am J Bot 26(10):808–822
Emerson R, Lewis CM (1941) Carbon dioxide exchange and the measurement of the quantum yield of photosynthesis. Am J Bot 28:789–804
Emerson R, Lewis CM (1943) The dependence of the quantum yield of Chlorella photosynthesis on wave length of light. Am J Bot 30:165–178
Emerson R, Rabinowitch E (1960) Red drop and role of auxiliary pigments in photosynthesis. Plant Physiol 35:477–485
Emerson R, Chalmers R, Cederstrand CN (1957) Some factors influencing the long-wave limit of photosynthesis. Proc Natl Acad Sci USA 43:133–143
Franck J (1949) An interpretation of the contradictory results in measurements of the photosynthetic quantum yields and related phenomena. Arch Biochem 23:297–314
Gaffron H, Wohl K (1936) Zur Theorie der Assimilation. Naturwissenschaften 24(81–90):103–107
Golbeck JH (ed) (2006) Photosystem I: the light-driven plastocyanin:ferredoxin oxidoreductase. Advances in photosynthesis and respiration, vol 24. Springer, Dordrecht
Govindjee (1999) On the requirement of minimum number of four versus eight quanta of light for the evolution of one molecule of oxygen in photosynthesis: a historical note. Photosynth Res 59:249–254
Govindjee (2001) Lighting the path: a tribute to Robert Emerson (1903–1959). In: Proceedings of the 12th international congress on photosynthesis (PS2001), Brisbane. CSIRO Publishing
Govindjee (2004) Robert Emerson and Eugene Rabinowitch: understanding photosynthesis. In: Hoddeson L (ed) No boundaries: University of Illinois Vignettes. University of Illinois Press, Urbana/Chicago, pp 181–194
Govindjee (2010) Celebrating Andrew Alm Benson’s 93rd birthday. Photosynth Res 105:201–208
Govindjee, Bjorn LO (2012) Dissecting oxygenic photosynthesis: the evolution of the Z-scheme for thylakoid membranes. In: Itoh S, Mohanty S, Guruprasad KN (eds) Photosynthesis: overviews on recent progress and future perspective. I. K. International Publishers, New Delhi, pp 1–27
Govindjee, Krogmann D (2004) Discoveries in oxygenic photosynthesis (1727–2003): a perspective. Photosynth Res 80:15–57
Govindjee, Rabinowitch E (1960) Two forms of chlorophyll a in vivo with distinct photochemical functions. Science 132:355–356
Govindjee, Srivastava N (2014) William Archibald Arnold (December 6, 1904–October 26, 2001) Biographical Memoirs of the National Academy of Sciences, USA, Washington, DC. http://www.nasonline.org/publications/biographical-memoirs/memoir-pdfs/arnold-william.pdf
Govindjee, van Rensen JJ (1978) Bicarbonate effects on the electron flow in isolated broken chloroplasts. Biochim Biophys Acta 505:183–213
Govindjee, Owens OvH, Hoch G (1963) A mass spectroscopic study of the Emerson enhancement effect. Biochim Biophys Acta 75:281–284
Govindjee, Munday JC Jr., Papageorgiou GC (1967) Fluorescence studies with algae: Changes with time and preillumination. In: Olson, JM (ed.) Energy Conversion by the Photosynthetic Apparatus, Brookhaven Symposia in Biology 19:434–445
Govindjee, Knox RS, Amesz J (eds) (1996) Photosynthetic unit: antenna and reaction centers, a special issue dedicated to William A. Arnold. Photosynth Res 48 (1 and 2):1–319
Govindjee, Beatty JT, Gest H, Allen JF (eds) (2005) Discoveries in photosynthesis. Advances in photosynthesis and respiration, vol 20. Springer, Dordrecht
Govindjee R(ajni), Thomas JB, Rabinowitch EI (1960) “Second Emerson effect” in the Hill reaction of Chlorella cells with quinine as oxidant. Science 132:421
Govindjee R(ajni), Govindjee, Hoch G (1962) The Emerson enhancement effect in TPN-photoreduction by spinach chloroplasts. Biochem Biophys Res Commun 9:222–225
Govindjee R(ajni), Govindjee, Hoch G (1964) Emerson enhancement effect in chloroplast reactions. Plant Physiol 39:10–14
Govindjee R(ajni), Rabinowitch EI, Govindjee (1968) Maximum quantum yield and action spectrum of photosynthesis and fluorescence in Chlorella. Biochim Biophys Acta 162:539–544
Greenbaum E, Lee JW, Tevault CV, Blankinship SL, Mets LJ (1995) CO2 fixation and photoevolution of H2 and O2 in a mutant of Chlamydomonas lacking photosystem I. Nature 376:438–441
Hendricks SB (1953) A discussion of photosynthesis. Science 117:370–373
Hill R (1937) Oxygen evolved by isolated chloroplasts. Nature 139:881–882
Hill R (1939) Oxygen produced by isolated chloroplasts. Proc R Soc Lond Ser B 127:192–210
Hill JF (2012) Early pioneers of photosynthesis research. In: Eaton-Rye JJ, Sharkey TD, Tripathy BC (eds) Photosynthesis: perspectives on plastid biology, energy conversion and carbon metabolism. Advances in photosynthesis and respiration, vol 34. Springer, Dordrecht, pp 771–800
Hill R, Bendall F (1960) Function of the two cytochrome components in chloroplasts: a working hypothesis. Nature 186:136–137
Höxtermann E (1992) Fundamental discoveries in the history of photosynthesis research. Photosynthetica 26:485–502
Höxtermann E (2007) A comment on Warburg’s early understanding of biocatalysis. Photosynth Res 92:121–127
Höxtermann E, Sucker U (1989) Otto Warburg (Biographien hervorragender Naturwissenschaftler, Techniker und Mediziner) (Book 91) Vieweg + Teubner Verlag, Springer Fachmedien Wiesbaden GmbH
Huzisige H, Ke B (1993) Dynamics of the history of photosynthesis research. Photosynth Res 38:185–209
Kamen MD (1989) Onward into a fabulous half-century. Photosynth Res 21:139–144
Kamen MD (1995) Liebling’s law (“ILL”). Proc Am Philos Soc 139:358–367
Klimov V, Allakhverdiev SI, Feyziev YM, Baranov SV (1995) Bicarbonate requirement for the donor side of photosystem II. FEBS Lett 363:251–255
Knox RS (1969) Thermodynamics and the primary processes of photosynthesis. Biophys J 9:1351–1362
Kok B (1948) A critical consideration of the quantum yield of Chlorella-photosynthesis. Enzymologia 13:1–5
Koroidov S, Shevela D, Shutova T, Samuelsson G, Messinger J (2014) Mobile hydrogen carbonate acts as proton acceptor in photosynthetic water oxidation. Proc Natl Acad Sci USA 111(17):6299–6304
Krebs HA (1972) Otto Heinrich Warburg. Biogr Mem Fellows R Soc 18:628–699
Krebs HA (1981) Otto Warburg: cell physiologist, biochemist, and eccentric. Clarendon Press, Oxford
Ley AC, Mauzerall DC (1982) Absolute absorption cross-sections for photosystem II and the minimum quantum requirement for photosynthesis in Chlorella vulgaris. Biochim Biophys Acta 680:95–106
Magee JL, de Witt TW, Smith EC, Daniels F (1939) A photocalorimeter: the quantum efficiency of photosynthesis in algae. J Am Chem Soc 61:3529–3533
Manning WM, Stauffer JF, Duggar BM, Daniels F (1938) Quantum efficiency of photosynthesis in Chlorella. J Am Chem Soc 60:266–274
Mauzerall D (2013) Thermodynamics of primary photosynthesis. Photosynth Res 116:363–366
McGrath JM, Long SP (2014) Can the cyanobacterial carbon-concentrating mechanism increase photosynthesis in crop species? A theoretical analysis. Plant Physiol. doi:10.1104/pp.113.232611
Mohr H, Schopfer P (1995) Plant physiology (Translated from the German by Lawlor G, Lawlor DW). Springer, Berlin
Myers J (1974) Conceptual developments in photosynthesis, 1924–1974. Plant Physiol 54:420–426
Ng K-S, Bassham JA (1968) The quantum requirement of photosynthesis in Chlorella. Biochim Biophys Acta 162:254–264
Nickelsen K (2007) Otto Warburg’s first approach to photosynthesis. Photosynth Res 92:109–120
Nickelsen K (2009a) Of light and darkness: modeling photosynthesis 1840–1960. Habilitation. University of Bern, Bern, Switzerland
Nickelsen K (2009b) The construction of a scientific model: Otto Warburg and the building block strategy. Stud Hist Philos Biol Biomed Sci 40:73–86
Nickelsen K (2012) From the red drop to the Z-scheme of photosynthesis. Ann Phys (Berlin) 524:A157–A160
Nickelsen K (2014) Explaining photosynthesis: models of biochemical mechanisms. Springer, Dordrecht, pp 1840–1960 (Series: history, philosophy and theory of the life sciences)
Nickelsen K, Govindjee (2011) The maximum quantum yield controversy: Otto Warburg and the “Midwest-Gang.” Bern studies in the history and philosophy of science, University of Bern, Bern, Switzerland
Nishimura MS, Whittingham CP, Emerson R (1951) The maximum efficiency of photosynthesis: a critique of certain manometric techniques used for measuring rates of photosynthesis. Carbon dioxide fixation and photosynthesis: symposia of society for experimental biology 5. Cambridge University Press, Cambridge, pp 176–210
Orr L, Govindjee (2013) Photosynthesis web resources. Photosynth Res 115:179–214
Osborne BA, Geider RJ (1987) The minimum photon requirement for photosynthesis. New Phytol 106:631–644
Parson WW (1978) Thermodynamics of the primary reactions of photosynthesis. Photochem Photobiol 28:389–393
Pirt SJ (1986) The thermodynamic efficiency (quantum demand) and dynamics of photosynthetic growth. New Phytol 102:3–37
Rabinowitch EI (1945) Photosynthesis and related processes, vol I: chemistry of photosynthesis, chemosynthesis and related processes in vitro and in vivo. Interscience Publishers, New York. http://www.life.illinois.edu/govindjee/g/Books.html. Accessed 1 March 2014
Rabinowitch EI (1951) Photosynthesis and related processes, vol II, Part 1. Interscience Publishers, New York. http://www.life.illinois.edu/govindjee/g/Books.html. Accessed 1 March 2014
Rabinowitch EI (1959) Robert Emerson, 1903–1959. Plant Physiol 34:179–184
Rabinowitch EI (1961) Robert Emerson (1903–1959). Biogr Mem Natl Acad Sci USA 25:112–131
Rabinowitch E, Govindjee (1961) Different forms of chlorophyll a in vivo and their photochemical function. In: McElroy WD, Glass B (eds) A symposium on light and life. The Johns Hopkins Press, Baltimore, pp 378–386
Rabinowitch E, Govindjee (1969) Photosynthesis. Wiley, New York. http://www.life.illinois.edu/govindjee/g/Books.html; and http://www.life.illinois.edu/govindjee/photosynBook.html. Accessed 1 March 2014
Rieke FF (1939) On the quantum efficiency of photosynthesis. J Chem Phys 7:238–244
Rieke FF (1949) Quantum efficiencies for photosynthesis and photoreduction in green plants. In: Franck J, Loomis WE (eds) Photosynthesis in plants. Iowa State College Press, Ames, pp 251–272
Ross RT, Calvin M (1967) Thermodynamics of light emission and free energy storage in photosynthesis. Biophys J 7:595–614
Ruben S, Randall M, Kamen M, Hyde JL (1941) Heavy oxygen (18O) as a tracer in the study of photosynthesis. J Am Chem Soc 63:877–879
Ryder AW (1957) The Panchatantra (of India), English translation, University of Chicago Press, 1957, p 9
Senger H, Bishop NI (1967) Quantum yield of photosynthesis in synchronous Scenedesmus cultures. Nature 214:140–142
Sharp RE, Matthews MA, Boyer JS (1984) Kok effect and the quantum yield of photosynthesis: light partially inhibits dark respiration. Plant Physiol 75:95–101
Shevela D, Eaton-Rye JJ, Shen JR, Govindjee (2012) Photosystem II and unique role of bicarbonate: A historical perspective. Biochim Biophys Acta 1817:1134–1151
Skillman JB (2008) Quantum yield variation across the three pathways of photosynthesis: not yet out of the dark. J Exp Bot 59:1647–1661
Stemler A (1982) The functional role of bicarbonate in photosynthetic light reaction II. In: Govindjee (ed) Photosynthesis. Academic Press, New York, pp 513–538
Stemler A, Babcock GT, Govindjee (1974) The effect of bicarbonate on photosynthetic oxygen evolution in flashing light in chloroplast fragments. Proc Natl Acad Sci USA 71:4679–4683
The Nobel Prize in Physiology or Medicine (1931). Nobelprize.org. Nobel Media AB 2013. http://www.nobelprize.org/nobel_prizes/medicine/laureates/1931/. Accessed 30 Apr 2014
Umbreit WW, Burris RH, Stauffer JF (1957) Manometric techniques: a manual describing methods applicable to the study of tissue metabolism. Burgess Publ Co, Minneapolis
Van Niel CB (1932) On the morphology and physiology of the purple and green sulphur bacteria. Arch Mikrobiol 3:1–112
Van Niel CB (1941) The bacterial photosyntheses and their importance for the general problem of photosynthesis. Adv Enzymol Relat Areas Microbiol 1:263–328
Van Rensen JJS, Xu C, Govindjee (1999) Role of bicarbonate in photosystem II, the water-plastoquinone oxido-reductase of plant photosynthesis. Physiol Plant 105:585–592
Vander Heiden MG, Cantley LC, Thompson CB (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324(5930):1029–1033
Walker D (1992) Energy, plants and man. Oxygraphics, East Sussex
Wang QJ, Singh A, Li H, Nedbal L, Sherman LA, Govindjee, Whitmarsh JC (2012) Net light-induced oxygen evolution in photosystem I deletion mutants of the cyanobacterium Synechocystis sp. PCC 6803. Biochim Biophys Acta 1817:792–801
Warburg E (1917) Über die anwendung der Quantenhypothese auf de photochemie. Naturwissenschaften 5(30):489–494
Warburg O (1919) Über die Geschwindigkeit der photochemischen Kohlensäurezersetzung in lebenden Zellen I. Biochem Zeitschrift 100:230–270
Warburg O (1920) Über die Geschwindigkeit der photochemischen Kohlensäurezersetzung in lebenden Zellen II. Biochem Zeitschrift 103:188–217
Warburg O (1921) Theorie der Kohlensäureassimilation. Naturwissenschaften 9:354–358
Warburg O (1928) Uber die Katalytischen Wirkungen der Lebendigen Substanz: Arbeiten aus dem Kaiser Wilhelm-Institut für Biologie Berlin-Dahlem. Springer, Berlin
Warburg O (1945) Über den Quantenbedarf der Kohlensäureassimilation. Naturwissenschaften 33:122
Warburg O (1948) Assimilatory quotient and photochemical yield. Am J Bot 35:194–204
Warburg O (1958) Photosynthesis. Science 128:68–73
Warburg O, Burk D (1950) The maximum efficiency of photosynthesis. Arch Biochem 25:410–443
Warburg O, Krippahl G (1958) Hill-Reakionen. Z Naturforsch 13b:509–514
Warburg O, Negelein E (1922) Über den Energieumsatz bei der Kohlensäureassimilation. Z Phys Chem 102:235–266
Warburg O, Negelein E (1923) Über den Einfluss der Wellenlänge auf den Energieumsatz bei der Kohlensäureassimilation. Z Phys Chem 106:191–218
Warburg O, Burk D, Schocken V, Hendricks SB (1950) The quantum efficiency of photosynthesis. Biochim Biophys Acta 4:335–348
Warburg O, Krippahl G, Schröder W (1954) Katalytische Wirkung des blaugrünen Lichts auf den Energieumsatz bei der Photosynthese. Z Naturforsch 9b:667–675
Warburg O, Krippahl G, Schröder W (1955) Wirkungsspektrum eines Photosynthese-Fermentes. Z Naturforsch 10b:631–639
Warburg O, Krippahl G, Lehman A (1969) Chlorophyll catalysis and Einstein’s law of photochemical equivalence in photosynthesis. Am J Bot 56:961–971
Willstätter R, Stoll A (1918) Untersuchungen über die assimilation der kohlensäure. Sieben Abhandlungen, Springer, Berlin
Wydrzynski TJ, Satoh K (eds) (2005) Photosystem II—the light-driven water: plastoquinone oxidoreductase. Advances in photosynthesis and respiration, vol 22. Springer, Dordrecht
Acknowledgments
J. F. Hill thanks William A. Hill and Anita Baker-Blocker for invaluable comments on early drafts of this paper. J. F. Hill and Govindjee are thankful to Ekkehard Höxtermann for help with the figures and to Kärin Nickelsen, Ekkehard Höxtermann, and John F. Allen for reading and making valuable comments and suggestions on an earlier version of this Historical Corner paper. We are highly thankful to Alexendrina (Sandra) Stirbet for Figs. 1, 6, and 7, used in this paper.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hill, J.F., Govindjee The controversy over the minimum quantum requirement for oxygen evolution. Photosynth Res 122, 97–112 (2014). https://doi.org/10.1007/s11120-014-0014-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-014-0014-8