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Forty years of microbial photosynthesis research: Where it came from and what it led to

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Abstract

What follows is a very personal account of my professional life and the early years that preceded it. I have described the social and economic conditions in America and how the nineteen twenties and thirties nurtured our scientific future. The description of the early part of post-World War II research covers my experience in the areas of nutritional biochemistry, biochemical genetics and proceeds to photosynthesis. The latter era lasted around 35 years. For me the most memorable research accomplishments in which I was a participant during this period was the first demonstration of the primary carboxylation enzyme in an in vitro system in algal and higher plants as well to show that it was structurally associated with the chloroplast.Our group while at Oak Ridge and the University of Massachusetts assembled data that described the complete macromolecular assembly of the photosynthetic apparatus of the unusual photosynthetic green bacterium Chloroflexus aurantiacus and created a model of that system which differed greatly from the chomatophore system for the purple bacteria. For the last decade, my scientific journey, with numerous new colleagues has turned to the exciting area of biomaterials.We characterized and modeled the completely new bacterial intracellular inclusions responsible for the synthesis and degredation of biosynthetic, biodegradable and biocompatible bacterial polyesters in the cytoplasm of Pseudomonads.

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References

  • Anderson AJ and Dawes EA (1990) Occurrence, metabolism, metabolic role and industrial uses of bacterial polyhydroxyalkanoates. Microbiol Rev 54: 450–472

    Google Scholar 

  • Anderson L and Fuller RC (1967a) Photosynthesis in Rhodospirillum rubrum. II. Phototheterotrophic carbon dioxide fixation. Plant Physiol 42: 491–496

    Google Scholar 

  • Anderson L and Fuller RC (1967b) Photosynthesis in Rhodospirillum rubrum. III. Metabolic control of reductive pentose phosphate and tricarboxylic acid cycle enzymes. Plant Physiol 42: 497–503

    Google Scholar 

  • Anderson L and Fuller RC (1967c) Photosynthesis in Rhodospirillum rubrum. I. Autotrophic carbon dioxide fixation. Plant Physiol 42: 487–490

    Google Scholar 

  • Anderson L and Fuller RC (1967d) The rapid appearance of glycolate during photosynthesis in Rhodospirillum rubrum. Biochim Biophys Acta 131: 198–201

    Google Scholar 

  • Anderson L, Price GB and Fuller RC (1968) Molecular diversity of the ribulose-1,5-diphosphate carboxylase from photosynthetic microorganisms. Science 161: 482–484

    Google Scholar 

  • Arnold WA (1949) A calorimetric determination of the quantum yield inphotosynthesis. In: Franck J and Loomis WE (eds) Photosynthesis in Plants, pp 273–276. The Iowa State Press, Ames, IA

    Google Scholar 

  • Beatty T and Gest H (1981) Biosynthesis and bioenergetic functions of citric-acid cycle reactions in Rhodopseudomonas capsulata. J Bacteriol 148: 484–503

    Google Scholar 

  • Benson AA (1995) Saga of a great theory of photosynthesis. Am Soc Plant Physiol Newsletter 22(6): 5–6

    Google Scholar 

  • Benson AA and Calvin M (1947) The dark reductions of photosynthesis. Science 106: 648–652

    Google Scholar 

  • Blankenship RE and Fuller RC (1985) Membrane topology and photochemistry of the green bacterium Chloroflexus. In: Staehelin LA and Arntzen CJ (eds) Photosynthetic Membranes, pp 293–303. Springer-Verlag, Heidelberg

    Google Scholar 

  • Brandl, H, Gross RA, Lenz RW and Fuller RC (1988) Pseudomonas oleovorans as a source of poly(β-hydroxyalanoates) for potential applications as biodegradable polyesters. Appl Environ Microbiol 54: 1977–1982

    Google Scholar 

  • Brandl H, Knee EJ, Fuller RC Gross RA and Lenz RW (1989) The ability of the phototrophic bacterium Rhodospirillum rubrum to produce various poly(β-hydroxyalanoates): Potential sources for biodegradable polyesters. Int J Biol Macromol 11: 49–56

    Google Scholar 

  • Brandl H, Gross RA Lenz RW, Lloyd R and Fuller RC (1991) The accumulation of poly (3-hydroxyalkanoates) in Rhodobacter sphaeroides. Arch Microbiol 155: 337–340

    Google Scholar 

  • Bruce B, Blankenship RE and Fuller RC (1982) Primary photochemistry in the facultatively aerobic green photosynthetic bacterium Chloroflexus aurantiacus. Proc Natl Acad Sci USA 79: 6532–6536

    Google Scholar 

  • Calvin M(1992) Following the trail of light: a scientific odyssey. In: Seeman JE (ed) Profiles, Pathways and Dreams, pp 3–178. Am Chem Soc, Washington, DC

  • Calvin M and Benson AA (1948) The path of carbon in photosynthesis. Science 107: 476–480

    Google Scholar 

  • Calvin M, Bassham JA, Benson AA, Kay LD, Harris AZ and Wilson AT (1954) The Path of Carbon in Photosynthesis XXI The cyclic regeneration of carbon dioxide acceptor in photosynthesis. J Am Chem Soc 76: 1760–1770

    Google Scholar 

  • Curley JM, Hazer B, Lenz RW and Fuller RC (1996) Production of poly(3-hydroxyalkanoates) containing aromatic substituents by Pseudomonas oleovorans. Macromolecules 29: 1762–1766

    Google Scholar 

  • Curley JM, Lenz RW, Fuller RC, Browne SE, Gabriel CB and Panday S (1997) 13C n.m.r. spectroscopy in living cells of Pseudomonas oleovorans. Polymer 38: 5313–5319

    Google Scholar 

  • Doi Y (1990) Microbial Polyesters. VCH Publishers, Inc., Yokohama, Japan

    Google Scholar 

  • Doi Y (1995) Microbial synthesis, physical properties and biodegradability of polyhydroxyalkanoates. Macromol Symp 98: 585–599

    Google Scholar 

  • Doi Y, Tamaki A, Kunioka M and Soga K (1987) Biosynthesis of terpolyesters of 3-hydroxybutyrate, 3-hydroxyvalerate and 5-hydroxyvalerate in Alcaligenes eutrophus from 5-chloropentanoic and pentanoic acids. Makromol Chem Rapid Commun 8: 631–635

    Google Scholar 

  • Doi Y, Tamaki A, Kunioka M and Soga K (1988) Production of copolyesters of 3-hydroxybutyrate and 3-hydroxyvalerate by Alcaligenes eutrophus from butyric and pentanoic acids. Appl Microbiol Biotechnol 28: 330–334

    Google Scholar 

  • Doudoroff M and Stanier RY (1959) Role of poly-β-hydroxybutyric acid in assimilation of organic carbon by bacteria. Nature 183: 1440

    Google Scholar 

  • Drews G (1996) Forty-five years of developmental biology of photosynthetic bacteria. Photosynth Res 48: 327–351

    Google Scholar 

  • Duysens WA (1996 ) Arnold's inspiring experiments. Photosynth Res 48: 25–29

    Google Scholar 

  • Emerson R and Lewis CM (1943a) Factors influencing the efficiency of photosynthesis. Am J Bot 26: 808–822

    Google Scholar 

  • Emerson R and Lewis CM (1943b) The dependence of quantum yield of Chlorella photosynthesis on wavelength of light. Am J Bot: 165–175

  • Feher G (1998) Three decades of research in bacterial photosynthesis and the road leading to it: A personal account. Photosynth Res 55: 3–40

    Google Scholar 

  • Feick RG and Fuller RC (1984) The macromolecular structure of the photochemical apparatus of Chloroflexus. Biochemistry 233: 3693–3701

    Google Scholar 

  • Feick R, Fitzpatrick M and Fuller RC (1982) Chemical and physical characteristics of the photochemical membrane system in Chloroflexus aurantiacus. J Bacteriol 150: 905–915

    Google Scholar 

  • Foster LJR, Lenz RW and Fuller RC (1994) Quantitative determination of intracellular depolymerase activity in Pseudomonas oleovorans inclusions containing poly-3-hydroxyalkanoates with long alkyl sustituents. 118: 279–282

    Google Scholar 

  • Foster LJR, Stuart ES, Tehrani A, Lenz RW and Fuller RC (1996) Intracellular depolymerase functionality and location in Pseudomonas oleovorans inclusions containing polyhydroxyoctanoate. Int J Biol Macromol 19: 177–183

    Google Scholar 

  • Foster LJR, Lenz RW and Fuller RC (1999) Intracellular depolymerase activity in isolated inclusion bodies containing polyhydroxyalkanoates with long alkyl and functional substituents in the side chain. Int J Biol Macromol (in press)

  • Fritzsche K, Lenz RW and Fuller RC (1990a) An unusual bacterial polyester with a phenyl pendant group. Makromol Chem 191: 1957–1965

    Google Scholar 

  • Fritzsche K, Lenz RW and Fuller RC (1990b) Bacterial polyesters containing branched poly(β-hydroxyalkanoate) units. Int J Biol Macromol 12: 92–101

    Google Scholar 

  • Fritzsche K, Lenz RW and Fuller RC (1990c) Production of unsaturated polyesters by Pseudomonas oleovorans. Int J Biol Macromol. 12: 85–91

    Google Scholar 

  • Fuller RC (1978) Photosynthetic carbon metabolism in the green and purple bacteria. In: Clayton RK and Sistrom WR (eds) The Photosynthetic Bacteria, pp 691–705. Plenum Press, New York

    Google Scholar 

  • Fuller RC (1995) Polyesters and photosynthetic bacteria. From lipid cellular inclusions to microbial thermoplastics. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 1245–1256. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Fuller RC (1999) Microbial inclusions with special reference to PHA inclusions and intracellular boundry envelopes. Int J Biol Macromol. 25: 21–29

    Google Scholar 

  • Fuller RC and Gibbs M (1956) Aberrant patterns of some photosynthetic enzymes. Plant Physiol 31: 31–38

    Google Scholar 

  • Fuller RC and Gibbs M (1959) Intracellular and phylogenetic distribution of ribulose 1,5-diphosphate carboxylase and Dglyceraldehyde-3-phosphate dehydrogenases. Plant Physiol 34: 324–329

    Google Scholar 

  • Fuller RC and Tatum EL (1956) Inositol-phospholipid in Neurospora and its relationship to morphology. Am J Bot 43: 361–365

    Google Scholar 

  • Fuller RC, Barratt R W and Tatum EL (1955) The relationship between hexachlorocyclohexane and inositol in Neurospora. J Biol Chem 186: 823–827

    Google Scholar 

  • Fuller RC, Smillie RM, Sisler EC and Kornberg HL (1961) Carbon metabolism in Chromatium. J Biol Chem 236: 2140–2149

    Google Scholar 

  • Gaffron H (1960) Energy Storage: Photosynthesis. In: Stewart FC (ed) Plant Physiology, A Treatise, Volume 1B: Photosynthesis and Chomosynthesis, Chapter 4, pp 3–277. Academic Press, New York

    Google Scholar 

  • Gantt E and Conti S (1965) The ultrastructure of Porphyridium cruentum. J Cell Biol 26: 365–381

    Google Scholar 

  • Gantt E and Conti S (1966) Granules associated with chloroplast lammelae. J Cell Biol 29: 423–434

    Google Scholar 

  • Gest H (1992) A long trail of serendipity – directed research on photosynthetic bacteria. FEMS Microbial Lett 100: 417–422

    Google Scholar 

  • Gest H (1994) A microbiologist's odyssey: Bacterial viruses to photosynthetic bacteria. Photosynth Res 40: 129–146

    Google Scholar 

  • Gest H and Favinger JL (1983) Heliobacterium chlorum, an oxygenic brownish-green photosynthetic bacterium containing a ‘new’ form of bacteriochlorophyll. Arch Microbiol 136: 11–16

    Google Scholar 

  • Gibbs M (1996) The boys of summer. Am Soc Plant Physiol Newslett 23(1): 1–4

    Google Scholar 

  • Gilmore DF, Antoun S, Lenz RW, Goodwin S, Austin R and Fuller RC (1992) The fate of biodegradable plastics in municipal leaf compost. J Indust Microbiol 10: 199–206

    Google Scholar 

  • Govindjee (1999) On the requirement of a minimum number of four vs. eight quanta of light for the evolution of one molecule of oxygen in photosynthesis: A historical note. Photosynth Res 59: 249–254

    Google Scholar 

  • Govindjee, Knox RS and Amesz J (eds) (1996) Photosynthetic Unit Antenna and Reaction Centers, a special issue dedicated to William A. Arnold. Photosynth Res 48: 1–319

  • Gray BH, Fowler NA, Nugent N, Rigopoulos N and Fuller RC (1973) Re-evaluation of Chloropseudomonas ethylica strain 2-K. Int J Syst Bacteriol 23: 256–264

    Google Scholar 

  • Griebel R, Smith Z and Merrick J (1968) Metabolism of poly-betahydroxybutyrate granules from Bacillus megaterium. Biochemistry 7: 3676–3681

    Google Scholar 

  • Hazer B, Lenz RW and Fuller RC (1994) Biosynthesis of methylbranched poly(β-hydroxyalkanoate)s by Pseudomonas oleovorans. Macromolecutes 27: 45–49

    Google Scholar 

  • Hill R (1939) Oxygen produced by isolated chloroplasts. Proc R Soc London, Ser B 127: 192–210

    Google Scholar 

  • Holt SC and Fuller RC (1966) Isolation and characterization of photosynthetic membranes of Chloropseudomonas ethylicum. Plant Physiol 41: 28–35

    Google Scholar 

  • Holt SC, Conti SF and Fuller RC (1966) Effect of light intensity on the formation of the photochemical apparatus in the green bacterium Chloropseudomonas ethylicum. J Bacteriol 91: 349–355

    Google Scholar 

  • Horecker BL, Gibbs M, Klenow H, and Smyrniotis PZ (1954) The mechanism of pentose phosphate conversion to hexose monophosphate. J Biochem 76: 393–403

    Google Scholar 

  • Hughes DE, Conti SF and Fuller RC (1963) Inorganic polyphosphate metabolism in Chlorobium thiosulfatophilum. J Bacteriol 85: 577–584

    Google Scholar 

  • Huisman GW, Wonink E, de Koning G, Preusting H and Witholt B (1992) Synthesis of poly (3-hydroxyalkanoates) by mutant and recombinant Pseudomonas strains. Appl Microbiol Biotechnol 38: 1–5.

    Google Scholar 

  • Kidder GW and Fuller RC (1946) The growth response of Tetrahymena geleii W to folic acid and to the Streptococcus lactis R factor. Science 104: 160–161

    Google Scholar 

  • Kidwell J, Valentin HE and Dennis D (1995) Regulated expression of the Alcaligenes eutrophus pha biosynthetic genes in Escherichia coli. Appl Environ Microbiol 61: 1391–1398

    Google Scholar 

  • Kim YB, Lenz RW and Fuller RC (1991) Preparation and characterization of poly(β-hydroxyalkanoates) obtained from Pseudomonas oleovorans grown with mixtures of 5-phenylvaleric acid and n-alkanoic acids. Macromolecules 24: 5256–5360

    Google Scholar 

  • Kim YB, Lenz RW and Fuller RC (1992) Poly (β-hydroxyalkanoate) copolymers containing brominated repeating units produced by Pseudomonas oleovorans. Macromolecules 25: 1852–1856

    Google Scholar 

  • Krebs HA (1981) Otto Warburg – Cell Physiologist – Biochemist and Eccentric, pp 1–141. Oxford University Press, New York

    Google Scholar 

  • Lageveen RG, Huisman GW, Preusting H, Ketelar P, Eggink g and Witholt B (1988) Formation of polyesters by Pseudomonas oleovorans; effect of substrates on formation and composition of poly-(R)-3-hydroxyalkanoates. Appl Environ Microbiol 54: 2924–2932

    Google Scholar 

  • Lemoigne M (1925) Etudes sur l'autolyse microbie acidification par formation d'acide β-oxybutyrique. Ann Pasteur, Paris 39: 144–146

    Google Scholar 

  • Lemoigne M(1926) Produits de dehydration et de polymerisation de l'acide β-oxobutyrique. Bull Soc Chem Biol (Paris) 8: 770–782

  • Lenz RW, Kim YB and Fuller RC (1990) Production of unusual bacterial polyesters by Pseudomonas oleovorans through cometabolism. FEMS Microbiol Rev 103: 207–214

    Google Scholar 

  • Merick JM (1978) Metabolism of reserve materials. In: Clayton RK and Sistrom WR (eds) The Photosynthetic Bacteria, pp 199–219. Plenum Press, New York

    Google Scholar 

  • Merrick JM and Doudoroff M (1961) Enzymatic synthesis of polybeta-hydroxybuterate in Bacteria. Nature 189: 890–891

    Google Scholar 

  • Merrick JM and Doudoroff M (1964) Depolymerization of polybeta-hydroxybutyrate by an intracellular enzyme system. J Bacteriol 88: 60–65

    Google Scholar 

  • Ochoa S (1948) Biosynthesis of tricarboxylic acids by CO2 fixation. III. Enzymatic mechanisms. J Biol Chem 174: 133–157

    Google Scholar 

  • Oelze J and Fuller RC (1987) Growth rate and control of development of the photosynthetic apparatus in Chloroflexus aurantiacus. Arch Microbiol 148: 132–136

    Google Scholar 

  • Olson JM (1994) Reminiscence about Chloropseudomonas ethylicum and the FMO protein. Photosynth Res 41: 3–5

    Google Scholar 

  • Olson JM, Ivanovsky RN, Fuller RC (1996 ) Obituary: Elena N. Kondratieva (1925–1995). Photosynth Res 47: 203–205

    Google Scholar 

  • Peoples OP and Sinskey AJ (1989) Poly-β-hydroxybutyrate (PHB) biosynthesis in Alcaligenes eutrophus H16. Identification and characterization of the PHB polymerase gene (phbC). J Biol Chem 264: 15298–15303

    Google Scholar 

  • Pierson BK (1994) Reflections on Chloroflexus. Photosynth Res 41: 7–15

    Google Scholar 

  • Pierson BK and Castenholz (1974) A phototrophic gliding filamentous bacterium of hot springs, Chloroflexus aurantiacus, gen. and sp. nov. Arch Microbiol 100: 5–24

    Google Scholar 

  • Pierson BK and Thornber JP (1983) Isolation and spectral characterization of photochemical reaction centers from Chloroflexus Aurantiacus. Proc Natl Acad Sci USA 80: 80–84

    Google Scholar 

  • Quayle JR, Fuller RC, Benson AA and Calvin M (1954) Enzymatic carboxylation of ribulose diphosphate. J Am Chem Soc 76: 3610–3612

    Google Scholar 

  • Racker E (1972) Bioenergetics and the problem of tumor growth. Am Sci 60: 56–63

    Google Scholar 

  • Redlinger TE, Theroux SJ, Driscoll DL, Robinson SJ and Fuller RC (1990) Assembly of chlorosomes during photosynthetic development in Chloroflexus aurantiacus. In: Drews G and Dawes EA (eds) Molecular Biology of Membrane-Bound Complexes in Phototrophic Bacteria, pp 275–284. Plenum Press, New York

    Google Scholar 

  • Roberts R (1989) Serendipity—Accidental Discoveries in Science: A Micro-History of the Phenomenon. John Wiley & Sons, New York

    Google Scholar 

  • Seaborg GT and Benson AA (1988) Melvin Calvin 1911–1997. Biographical Memoirs National Academic Press, Washington DC 75: 1–21

    Google Scholar 

  • Shaposhnikov VV, Kondratieva EN and Federof VD (1960) A new species of green sulphur bacteria. Nature 187: 167–168

    Google Scholar 

  • Shively JM, Bryant DA, Fuller RC, Konopka AE, Stevens SE and Strohl WR (1988) Functional inclusions in prokaryotic cells. Intern Rev Cytol 113: 35–100

    Google Scholar 

  • Slater S, Gallaher T and Dennis D (1988) Cloning and expression in Escherichia coli of the Alcaligenes eutrophus H16 poly-β-hydroxybutarate biosynthetic pathway. J Bacteriol 170: 4431–4436

    Google Scholar 

  • Slater S, Gallaher T and Dennis D (1992) Production of poly-(3-hydroxybutyrate-co-3-hydroxyvalerate) in a recombinant Escherichia coli strain. Appl Environ Microbiol 58: 1089–1094

    Google Scholar 

  • Smillie RW and Fuller RC (1959) The intracellular distribution of ribulose diphosphate carboxylase. Plant Physiol 34: 651–657

    Google Scholar 

  • Sprague S and Fuller RC (1990) The green phototrophic bacteria and heliobacteria in structure of phototrophic prokaryoates. In: Stolz J (ed) Microbial Inclusions, pp 79–103. CRC Press, Boca Raton, FL

    Google Scholar 

  • Sprague SG, Staehelin LA, DiBartolomeis MJ and Fuller RC (1981) Isolation and development of chlorosomes in the green bacterium Chloroflexus aurantiacus. J Bacteriol 147: 1021–1031

    Google Scholar 

  • Staehelin LA, Golecki JR, Drews G and Fuller RC (1978) Visualization of the supramolecular architecture of chlorosomes (chlorobium type vesicles) in freeze-fractured cells of Chloroflexus aurantiacus. Arch Microbiol 119: 269–277

    Google Scholar 

  • Steinbuchel A and Schlegel HG (1991) Physiology and molecular genetics of poly(β-hydroxyalkanoic acid) synthesis in Alcaligenes eutrophus. Mol Microbiol 5: 523–542

    Google Scholar 

  • Stoppani AOM, Fuller RC and Calvin M (1955) Carbon dioxide fixation by Rhodopseudomonas capsulatus. J Bacteriol 69: 491–496

    Google Scholar 

  • Stuart ES, Lenz RW and Fuller RC (1995) The ordered macromolecular surface or the polyester inclusion in Pseudomonas oleovorans. Can J Microbiol 41(Suppl 1) 84–93

    Google Scholar 

  • Walker DA (1997) ‘Tell me where all the past years are.’ Photosynth Res 51: 2–26

    Google Scholar 

  • Warburg O (1963) The photolyte of photosynthesis In: La Photosynthese (President du Colloque # 119, Wurmser MR), pp 221–228. Editions du Centre National de la Recherche Scientifque (CNRS), 15 Quai Anatole-France, Paris VII

  • Wechsler T, Brunisholz R, Suter F, Fuller RC and Zuber H (1985) The complete amino acid sequence of a bacteriochloropyll a binding polypeptide isolated from the cytoplasmic membrane of the green photosynthetic bacterium Chloroflexus aurantiacus. FEBS Lett 191: 34–38

    Google Scholar 

  • Weisbach A, Smyrniotis PZ and Horecker BL (1954) Pentose phosphate and CO2 fixation with spinach extracts. J Am Chem Soc 76: 3611–3612

    Google Scholar 

  • Wilson AT and Calvin M (1955) The photosynthetic cycle: CO2 dependent transients. J Am Chem Soc 77: 5948–5957

    Google Scholar 

  • Wood HG (1946) Reductive carboxylation reactions. Physiol Rev 26: 198–202

    Google Scholar 

  • Zannoni D and Fuller RC (1988) Functional and spectral characterization of the respiratory chain of Chloroflexus aurantiacus grown in the dark under oxygen-saturated conditions. Arch Microbiol 150: 368–373

    Google Scholar 

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  1. Department of Biochemistry and Molecular Biology, University of Massachusetts, Amherst, MA, 01003, USA

    R. Clinton Fuller

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Clinton Fuller, R. Forty years of microbial photosynthesis research: Where it came from and what it led to. Photosynthesis Research 62, 1–29 (1999). https://doi.org/10.1023/A:1006373926725

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