Skip to main content
Log in

`Every dogma has its day'*: a personal look at carbon metabolism in photosynthetic bacteria

  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Dogmas are unscientific. What is perhaps the greatest biological dogma of all time, the `unity of biochemistry' is, in the main, still having its day. According to present knowledge, the exceptions to this dogma are mere details when seen in relation to the biosystem as a whole. Nevertheless the exceptions are scientifically interesting and the understanding of them has led to a better comprehension of photosynthesis and ecology. Until the discovery of 14C, photosynthetic CO2 fixation was like a slightly opened black box. With 14C in hand scientists mapped out the path of carbon in green plant photosynthesis in the course of a few years. The impressive reductive pentose phosphate cycle was almost immediately assumed to be universal in autotrophs, including anoxygenic phototrophs, in spite of the odd observation to the contrary. A new dogma was born and held the field for about two decades. Events began to turn when green sulfur bacteria were found to contain ferredoxin-coupled ketoacid-oxidoreductases. This led to the formulation of a novel CO2-fixing pathway, the reductive citric acid cycle, but its general acceptance required much work by many investigators. However, the ice had now been broken and after some years a third mechanism of CO2 fixation was discovered, this time in Chloroflexus, and then a fourth in the same genus. One consequence of these discoveries is that it has become apparent that oxygen is an important factor that determines the kind of CO2-fixing mechanism an organism uses. With the prospect of the characterization of hordes of novel bacteria forecast by molecular ecologists we can expect further distinctive CO2 fixation mechanisms to turn up.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alber BE and Fuchs G (2002) Propionyl-coenzyme A synthase from Chloroflexus aurantiacus, a key enzyme of the 3–hydroxypropionate cycle for autotrophic CO2 fixation. J Biol Chem 277: 12137–12143

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bondar VA, Gogotova GI and Ziakum AM (1976) Fractionation of carbon isotopes by photoautotrophic microorganisms having different pathways of carbon dioxide assimilation. Dokl Akad Nauk SSSR (Biological Sciences) 228: 720–722 [English translation, pp 223–225]

    PubMed  CAS  Google Scholar 

  • Buchanan BB and Arnon DI (1990) A reverse Krebs cycle in photosynthesis: consensus at last. Photosynth Res 24:47–53

    Article  PubMed  CAS  Google Scholar 

  • Buchanan BB and Sirevåg R (1976) Ribulose 1,5–diphosphate carboxylase and Chlorobium thiosulfatophilum. Arch Microbiol 109: 15–19

    Article  PubMed  CAS  Google Scholar 

  • Buchanan BB, Schurmann P and Shanmugam KT (1972) Role of reductive carboxylic acid cycle in a photosynthetic bacterium lacking ribulose-1,5 diphosphate carboxylase. Biochim Biophys Acta 283: 136–145

    Article  PubMed  CAS  Google Scholar 

  • Burton NP, Williams TD and Norris PR (1999) Carboxylase genes of Sulfolobus metallicus. Arch Microbiol 172: 349–353

    Article  PubMed  CAS  Google Scholar 

  • Consden R, Gordon AH and Martin AJP (1940) Qualtitative analysis of proteins: a partition chromatographic method using paper. Biochem J 38: 224–232

    Google Scholar 

  • Deacon R, Lumb M, Perry J, Chanarin I, Minty B, Halsey MJ and Nunn JF (1978) Selective inactivation of vitamin B12 in rats by nitrous oxide. Lancet 1978: 1023–1024

    Article  Google Scholar 

  • Eisen JA, Nelson KE, Paulsen IT, Heidelberg JF, Wu M, Dodson RJ, Deboy R, Gwinn ML, Nelson WC, Haft DH, Hickey EK, Peterson JD, Durkin AS, Kolonay JL, Yang F, Holt I, Umayam LA, Mason T, Brenner M, Shea TP, Parksey D, Nierman WC, Feldblyum TV, Hansen CL, Craven MB, Radune D, Vamathevan J, Khouri H, White O, Gruber TM, Ketchum KA, Venter JC, Tettelin H, Bryant DA and Fraser CM (2002) The complete genome sequence of the green sulfur bacterium Chlorobium tepidum. Proc Natl Acad Sci USA 99: 9509–9514

    Article  PubMed  CAS  Google Scholar 

  • Eisenreich W, Strauss G, Werz U, Fuchs G and Bacher A (1993) Retrobiosynthetic analysis of carbon fixation in the phototrophic eubacterium Chloroflexus aurantiacus. Eur J Biochem 215: 619–632

    Article  PubMed  CAS  Google Scholar 

  • Elsden SR (1962) Photosynthsesis and lithotrophic carbon dioxide fixation. In: Gunsalus IC and Stanier RY (eds) The Bacteria, Vol3, pp 1–40. Academic Press, New York

    Google Scholar 

  • Elsden SR and Ormerod JG (1956) The effect of monofluoroacetate on the metabolism of Rhodospirillum rubrum. Biochem J 63: 691–701

    PubMed  CAS  Google Scholar 

  • Evans MCW, Buchanan BB and Arnon DI (1966) A new ferredoxindependent carbon reduction cycle in a photosynthetic bacterium. Proc Natl Acad Sci USA 55: 928–934

    Article  PubMed  CAS  Google Scholar 

  • Fjeldheim G-O (1982) Dannelse og forbruk av acetat i Chlorobium limicola f. thiosulfatophilum. [Formation and utilization of acetate in Chlorobium limicola f. thiosulfatophilum.] MSc Thesis. University of Oslo, Norway

    Google Scholar 

  • Fox GE, Stackebrandt E, Hespell RB, Gibson J, Maniloff J, Dyer TA, Wolfe RS, Balch WE, Tanner RS, Magrum LJ, Zablen LB, Blakemore R, Gupta R, Bonen L, Stahl DA, Luehrsen KR, Chen KN and Woese CR (1980) The phylogeny of prokaryotes. Science 209: 457–463

    PubMed  CAS  Google Scholar 

  • Fuchs G, Stupperich E and Jaenchen R (1980a) Autotrophic CO2fixation in Chlorobium limicola. Evidence against the operation of the Calvin cycle in growing cells. Arch Microbiol 128: 56–63

    Article  CAS  Google Scholar 

  • Fuchs G, Stupperich E and Eden G (1980b) Autotrophic CO2 fixation in Chlorobium limicola. Evidence for the operation of a reductive tricarboxylic acid cycle in growing cells. Arch Microbiol 128: 64–71

    Article  CAS  Google Scholar 

  • Fuhrmann S, Overmann J, Pfennig N and Fischer U (1993) Influence of vitamin B12 and light on the formation of chlorosomes in green-and brown-colored Chlorobium species. Arch Microbiol 160: 193–198

    CAS  Google Scholar 

  • Gaffron H (1933) Ñber den Stoffwechsel der schweifelfreien Purpurbakterien. Biochem Z 260: 1–17

    CAS  Google Scholar 

  • Gaffron H (1935) Ñber den Stoffwechsel der Purpurbakterien. Biochem Z 275: 301–319

    CAS  Google Scholar 

  • Glover J, Kamen MD and van Genderen H (1952) Studies on the metabolism of photosynthetic bacteria. XII. Comparative light and dark metabolism of acetate and carbonate by Rhodospirillum rubrum. Arch Biochem Biophys 35: 343–408

    Article  Google Scholar 

  • Gough SP, Petersen BO and Duus JØ (2000) Anaerobic chlorophyll isocyclic ring formation requires a cobalamin factor. Proc Natl Acad Sci 97: 6908–6913

    Article  PubMed  CAS  Google Scholar 

  • Hanson TE and Tabita FR (2001) A ribulose-1,5–bisphosphate carboxylase/oxygenase (Rubisco)-like protein from Chlorobium tepidum that is involved with sulfur metabolism and the response to oxidative stress. Proc Natl Acad Sci USA 98: 4397–4402

    Article  PubMed  CAS  Google Scholar 

  • Herter S, Farfsing J, Gad'On N, Rieder C, Eisenreich W, Bacher A and Fuchs G (2001) Autotrophic CO2 fixation by Chloroflexus aurantiacus: study of glyoxylate formation and assimilation via the 3–hydroxypropionate cycle. J Bacteriol 183: 4305–16

    Article  PubMed  CAS  Google Scholar 

  • Herter S, Fuchs G, Bacher A and Eisenreich W (2002) A bicyclic CO2 fixation pathway in Chloroflexus aurantiacus. J Biol Chem 277: 20277–20283

    Article  PubMed  CAS  Google Scholar 

  • Hoare DS and Gibson J (1964) Photoassimilation of acetate and the biosynthesis of amino acids by Chlorobium thiosulfatophilum. Biochem J 91: 546–559

    PubMed  CAS  Google Scholar 

  • Holo H (1989) Chloroflexus aurantiacus secretes 3–hydroxypropionate, a possible intermediate in the assimilation of CO2 and acetate. Arch Microbiol 151: 252–256

    Article  CAS  Google Scholar 

  • Holo H and Grace D (1987) Polyglucose synthesis in Chloroflexus aurantiacus studied by 13C-NMR. Arch Microbiol 148: 292–297

    Article  CAS  Google Scholar 

  • Holo H and Sirevåg R (1986) Autotrophic growth and CO2 fixation of Chloroflexus aurantiacus. Arch Microbiol 145: 173–180

    Article  CAS  Google Scholar 

  • Hugler M, Ménendez C, Schagger H and Fuchs G (2002) Malonylcoenzyme A reductase from Chloroflexus aurantiacus, a key enzyme of the 3–hydroxypropionate cycle for autotrophic CO2 fixation. J Bacteriol 184: 2404–2410

    Article  PubMed  CAS  Google Scholar 

  • Ishii M, Miyake T, Satoh T, Sugiyama H, Oshima Y, Kodama T and Igarashi Y (1997) Autotrophic carbon dioxide fixation in Acidianus brierleyi. Arch Microbiol 166: 368–371

    Article  Google Scholar 

  • Ivanovsky RN, Krasilnikova EN and Fal YI (1993) A pathway of autotrophic CO2 fixation in Chloroflexus aurantiacus. Arch Microbiol 159: 257–264

    Article  CAS  Google Scholar 

  • Ivanovsky RN, Fal YI, Berg IA, Ugolkova NV, Krasilnikova EN, Keppen OI, Zakharchuc LM and Zyakun AM (1999) Evidence for the presence of the reductive pentose phosphate cycle in a filamentous anoxygenic photosynthetic bacterium, Oscillochloris trichoides strain DG-6. Microbiology 145: 1743–1748

    Article  PubMed  CAS  Google Scholar 

  • Kelly DP (1968) Fluoroacetate toxicity in Thiobacillus neapolitanus and its relevance to the problem of obligate chemoautotrophy. Arch Mikrobiol 61: 59–76

    Article  PubMed  CAS  Google Scholar 

  • Klenk HP, Clayton RA, Tomb JF, White O, Nelson KE, Ketchum KA, Dodson RJ, Gwinn M, Hickey EK, Peterson JD, Richardson DL, Kerlavage AR, Graham DE, Kyrpides NC, Fleischmann RD, Quackenbush J, Lee NH, Sutton GG, Gill S, Kirkness EF, Dougherty BA, McKenney K, Adams MD, Loftus B, Venter JC, et al. (1997) The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus. Nature 390: 364–70

    Article  PubMed  CAS  Google Scholar 

  • Larsen H (1951) Photosynthesis of succinic acid by Chlorobium thiosulfatophilum. J Biol Chem 193: 167–173

    PubMed  CAS  Google Scholar 

  • Larsen H (1952) On the culture and general physiology of the green sulfur bacteria. J Bacteriol 64: 187–196

    Article  PubMed  CAS  Google Scholar 

  • Løken Ø and Sirevåg R (1982) Evidence for the presence of the glyoxylate cycle in Chloroflexus. Arch Microbiol 120: 151–153

    Google Scholar 

  • Madigan MT and Ormerod JG (1995) Taxonomy, physiology and ecology of Heliobacteria. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 17–30. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Ménendez C, Bauer Z, Huber H, Gad'On N, Stetter KO and Fuchs G (1999) Presence of acetyl-coenzyme A (CoA) carboxylase and propionyl-CoA carboxylase in autotrophic Crenarchaeota and indication for the operation of a 3–hydroxypropionate cycle in autotrophic carbon fixation. J Bacteriol 181: 1088–1098

    PubMed  Google Scholar 

  • Ormerod JG (1956) The use of radioactive carbon dioxide in the measurement of carbon dioxide fixation in Rhodospirillum rubrum. Biochem J 64: 373–380

    PubMed  CAS  Google Scholar 

  • Ormerod JG (1957) Investigations of the metabolism of Rhodospirillum rubrum. PhD Thesis, University of Sheffield, UK

    Google Scholar 

  • Ormerod J (1980) Photosynthesis of acetate from carbon dioxide. In 3rd Int Symp on Microbial Growth on C1 Compounds. Sheffield, pp 99–100

  • Ormerod JG (1983) The carbon cycle in aquatic ecosystems. In: Slater JH, Whittenbury R and Wimpenny JWT (eds) Microbes in Their Natural Environments. Soc Gen Microbiol Symp, Vol 34, pp 463–482. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Ormerod JG, Nesbakken T and Beale SI (1990) Specific inhibition of bacteriochlorophyll synthesis in Chlorobium vibrioforme by anesthetic gases. J Bacteriol 172: 1352–1360

    PubMed  CAS  Google Scholar 

  • Peters R, Wakelin RW, Buffa P and Thomas LC (1953) Biochemistry of fluoroacetate poisoning. The isolation and some properties of the fluorotricarboxylic acid inhibitor of citrate metabolism. Proc R Soc London Ser B 140: 497–507

    Article  CAS  Google Scholar 

  • Pfennig N and Trüper HG (1971) Type and neotype strains of the species of phototrophic bacteria maintained in pure culture. Int J Syst Bacteriol 21: 19–24

    Article  Google Scholar 

  • Pickett MW, Williamson MP and Kelly DJ (1994) An enzyme and 13C-NMR study of carbon metabolism in heliobacteria. Photosynth Res 41: 75–88

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Quandt L, Gottschalk G, Ziegler H and Stichler W (1977) Isotope discrimination by photosynthetic bacteria. FEMS Microbiol Lett 1: 125–128

    Article  CAS  Google Scholar 

  • Quandt L, Pfennig N and Gottschalk G (1978) Evidence for the key position of pyruvate synthase in the assimilation of CO2 by Chlorobium. FEMS Microbiol Lett 3: 227–230

    Article  CAS  Google Scholar 

  • Ruben S and Kamen MD (1941) Long-lived radioactive carbon C14. Phys Rev 59: 349–354

    Article  CAS  Google Scholar 

  • Sadler WR and Stanier RY (1960) The function of acetate in photosynthesis by green bacteria. Proc Natl Acad Sci USA 46: 1328–1334

    Article  PubMed  CAS  Google Scholar 

  • Sirevåg R (1974) Further studies on carbon dioxide fixation in Chlorobium. Arch Microbiol 98: 3–18

    Article  Google Scholar 

  • Sirevåg R (1975) Photoassimilation of acetate and metabolism of carbohydrate in Chlorobium thiosulfatophilum. Arch Microbiol 104: 105–111

    Article  PubMed  Google Scholar 

  • Sirevåg R and Castenholz R (1979) Aspects of carbon metabolism in Chloroflexus. Arch Microbiol 120 151–153

    Article  Google Scholar 

  • Sirevåg R and Ormerod JG (1970a) Carbon dioxide-fixation in photosynthetic green sulfur bacteria. Science 169: 186–188

    PubMed  Google Scholar 

  • Sirevåg R and Ormerod JG (1970b) Carbon dioxide-fixation in green sulfur bacteria. Biochem J 120: 399–408

    PubMed  Google Scholar 

  • Sirevåg R, Buchanan BB, Berry JA and Troughton JH (1977) Mechanisms of CO2 fixation in bacterial photosynthesis studied by the carbon isotope fractionation technique. Arch Microbiol 112: 35–38

    Article  PubMed  Google Scholar 

  • Smillie RM, Rigopoulos N and Kelly H (1962) Enzymes of the reductive pentose phosphate cycle in the purple and in the green photosynthetic sulfur bacteria. Biochim Biophys Acta 56: 612–614

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Strauss G and Fuchs G (1993) Enzymes of a novel autotrophic CO2 fixation pathway in the phototrophic bacterium Chloroflexus aurantiacus, the 3–hydroxypropionate cycle. Eur J Biochem 215: 633–43

    Article  PubMed  CAS  Google Scholar 

  • Strauss G, Eisenreich W, Bacher A and Fuchs G (1992) 13CNMR study of autotrophic CO2 fixation pathways in the sulfurreducing Archaebacterium Thermoproteus neutrophilus and in the phototrophic Eubacterium Chloroflexus aurantiacus. Eur J Biochem 205: 853–66

    Article  PubMed  CAS  Google Scholar 

  • Tabita FR, McFadden BA and Pfennig N (1974) D-ribulose-1,5–bisphosphate carboxylase in Chlorobium thiosulfatophilum Tassajara. Biochim Biophys Acta 341: 187–194

    PubMed  CAS  Google Scholar 

  • Takabe T and Akazawa T (1977) A comparative study on the effect of O2 on photosynthetic carbon metabolism by Chlorobium thiosulfatophilum and Chromatium vinosum.Plant Cell Physiol 18: 753–765

    CAS  Google Scholar 

  • Thauer RK, Rupprecht E and Jungermann K (1970) Glyoxylate inhibition of clostridial pyruvate synthase. FEBS Lett 9: 108–111

    Article  Google Scholar 

  • Tichi M and Tabita FR (2000) Maintenance and control of redox poise in Rhodobacter capsulatus strains deficient in the Calvin-Benson-Bassham pathway. Arch Microbiol 174: 322–333

    Article  PubMed  CAS  Google Scholar 

  • Tolbert NE (1980) Photorespiration. In: Davies DD (ed) The Biochemistry of Plants, Vol 2, pp 487–523. Academic Press, New York

    Google Scholar 

  • Trudinger PA (1955) Phosphoglycerate formation from pentose phosphate by extracts of Thiobacillus denitrificans. Biochim Biophys Acta 18: 581–582

    Article  PubMed  CAS  Google Scholar 

  • Trudinger PA (1956) Fixation of carbon dioxide by extracts of the strict autotroph Thiobacillus denitrificans. Biochem J 64: 274–286

    PubMed  CAS  Google Scholar 

  • Ugol'kova NV and Ivanovsky RN (2000) On the mechanism of autotrophic fixation of CO2 by Chloroflexus aurantiacus. Microbiology 69: 139–142

    Article  Google Scholar 

  • Van Niel CB (1935) Photosynthesis of bacteria. Cold Spring Harbor Symp Quant Biol 3: 138–150

    CAS  Google Scholar 

  • Watson GMF and Tabita FR (1997) Microbial ribulose 1,5–bisphosphate carboxylase/oxygenase: a molecule for phylogenetic and enzymological investigation. FEMS Microbiol Lett 146: 13–22

    Article  PubMed  CAS  Google Scholar 

  • Wood HG, Ragsdale SW and Pezaka E (1986) The acetyl-CoA pathway of autotrophic growth FEMS Microbiol Rev 39: 345–362

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ormerod, J. `Every dogma has its day'*: a personal look at carbon metabolism in photosynthetic bacteria. Photosynthesis Research 76, 135–143 (2003). https://doi.org/10.1023/A:1024938531382

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1024938531382

Navigation