Photosynthesis Research

, Volume 139, Issue 1–3, pp 523–537 | Cite as

Differences in possible TCA cycle replenishing pathways in purple non-sulfur bacteria possessing glyoxylate pathway

  • Ekaterina Petushkova
  • Sergei Iuzhakov
  • Anatoly TsygankovEmail author
Original Article


Pathways replenishing tricarboxylic acid cycle were divided into four major groups based on metabolite serving as source for oxaloacetic acid or other tricarboxylic acid cycle component synthesis. Using this metabolic map, the analysis of genetic potential for functioning of tricarboxylic acid cycle replenishment pathways was carried out for seven strains of purple non-sulfur bacterium Rhodopseudomonas palustris. The results varied from strain to strain. Published microarray data for phototrophic acetate cultures of Rps. palustris CGA009 were analyzed to validate activity of the putative pathways. All the results were compared with the results for another purple non-sulfur bacterium, Rhodobacter capsulatus SB1003 and species-specific differences were clarified.


Rhodopseudomonas palustris Purple bacteria Acetate assimilation Tricarboxylic acid cycle replenishing pathways Anaplerotic pathway Glyoxylate cycle 



Isocitrate lyase


Isocitrate dehydrogenase


Pyruvic acid


Phosphoglyceric acid



TCA cycle

Tricarboxylic acid cycle


Oxaloacetic acid







The authors are grateful to Dr. Azat V. Abdullatypov for consulting, productive discussion, and careful revision of the manuscript. This work was conducted in the frame of project “Photosynthetic organisms as light energy transformers and valuable products producers” number АААА-А17-117030110141-2.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

11120_2018_581_MOESM1_ESM.docx (124 kb)
Supplementary material 1 (DOCX 124 KB)


  1. Adessi A, Corneli E, De Philippis R (2017) Photosynthetic purple non sulfur bacteria in hydrogen producing systems: new approaches in the use of well-known and innovative substrates. In: Hallenbeck PC (ed) Modern topics in the phototrophic prokaryotes. Springer, Cham, pp 321–350Google Scholar
  2. Alber BE, Spanheimer R, Ebenau-Jehle C, Fuchs G (2006) Study of an alternate glyoxylate cycle for acetate assimilation by Rhodobacter sphaeroides. Mol Microbiol 61(2):297–309Google Scholar
  3. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402Google Scholar
  4. Bassham JA, Benson AA, Calvin M (1950) The path of carbon in photosynthesis. J Biol Chem 185:781–787Google Scholar
  5. Berg IA, Kockelkorn D, Buckel W, Fuchs G (2007) A 3-hydroxypropionate/4-hydroxybutyrate autotrophic carbon dioxide assimilation pathway in archaea. Science 318:1782–1786Google Scholar
  6. Bowes G, Ogren WL, Hagerman RH (1971) Phosphoglycolate production catalyzed by ribulose diphosphate carboxylase. Biochem Biophys Res Commun 45:716–722Google Scholar
  7. Bramer CO, Steinbuchel A (2002) The malate dehydrogenase of Ralstonia eutropha and functionality of the C3/C4 metabolism in a Tn5-induced mdh mutant. FEMS Microbiol Lett 212:159–164Google Scholar
  8. Bricker TM, Zhang S, Laborde SM, Mayer PR, Frankel LK, Moroney JV (2004) The malic enzyme is required for optimal photoautotrophic growth of Synechocystis sp. strain PCC 6803 under continuous light but not under a diurnal light regimen. J Bacteriol 186:8144–8148Google Scholar
  9. Brock M, Maerker C, Schutz A, Volker U, Buckel W (2002) Oxidation of propionate to pyruvate in Escherichia coli. Involvement of methylcitrate dehydratase and aconitase. Eur J Biochem 269(24):6184–6194Google Scholar
  10. Drevland RM, Waheed A, Graham DE (2007) Enzymology and evolution of the pyruvate pathway to 2-oxobutyrate in Methanocaldococcus jannaschii. J Bacteriol 189:4391–4400Google Scholar
  11. Edwards J, Walker D (1986) Photosynthesis of C3 and C4 of plants: mechanisms and regulation. Mir, MoscowGoogle Scholar
  12. Eidels L, Preiss J (1970) Citrate synthase. A regulatory enzyme from Rhodopseudomonas capsulata. J Biol Chem 245:2937–2945Google Scholar
  13. Ensign SA (2011) Another microbial pathway for acetate assimilation. Science 331:294Google Scholar
  14. Erb TJ, Frerichs-Revermann L, Fuchs G, Alber BE (2010) The apparent malate synthase activity of Rhodobacter sphaeroides is due to two paralogous enzymes, (3S)-Malyl-coenzyme A (CoA)/β-methylmalyl-CoA lyase and (3S)-Malyl-CoA thioesterase. J Bacteriol 192:1249–1258Google Scholar
  15. Evans MCW, Buchanan BB, Arnon DI (1966) A new ferredoxin-dependent carbon reduction cycle in a photosynthetic bacterium. Proc Natl Acad Sci USA 55(4):928–934Google Scholar
  16. Filatova LV, Berg IA, Krasil’nikova EN, Ivanovsky RN (2005) A study of the mechanism of acetate assimilation in purple nonsulfur bacteria lacking the glyoxylate shunt: enzymes of the citramalate cycle in Rhodobacter sphaeroides. Microbiology 74(3):270–278Google Scholar
  17. Garnak M, Reeves HC (1979a) Phosphorylation of isocitrate dehydrogenase of Escherichia coli. Science 203:1111–1112Google Scholar
  18. Garnak M, Reeves HC (1979b) Purification and properties of phosphorylated isocitrate dehydrogenase of Escherichia coli. J Biol Chem 254:7915–7920Google Scholar
  19. Gibson JL, Tabita FR (1977) Isolation and preliminary characterization of two forms of ribulose-1,5-bisphosphate carboxylase from Rhodopseudomonas capsulata. J Bacteriol 132:818–823Google Scholar
  20. Gould TA, Van De Langemheen H, Muñoz-Elías EJ, McKinney JD, Sacchettini JC (2006) Dual role of isocitrate lyase 1 in the glyoxylate and methylcitrate cycles in Mycobacterium tuberculosis. Mol Microbiol 61:940–947Google Scholar
  21. Horswill AR, Escalante-Semerena J (2001) In vitro conversion of propionate to pyruvate by Salmonella enterica enzymes: 2-Methylcitrate dehydratase (PrpD) and aconitase enzymes catalyze the conversion of 2-methylcitrate to 2-methylisocitrate. Biochemistry 40:4703–4713Google Scholar
  22. Huber H, Gallenberger M, Jahn U, Eylert E, Berg IA, Kockelkorn D, Eisenreich W, Fuchs G (2008) A dicarboxylate/4-hydroxybutyrate autotrophic carbon assimilation cycle in the hyperthermophilic Archaeum Ignicoccus hospitalis. Proc Natl Acad Sci USA 105:7851–7856Google Scholar
  23. Ivanovsky RN, Krasilnikova EN, Berg IA (1997) A proposed citramalate cycle for acetate assimilation in the purple non-sulfur bacterium Rhodospirillum rubrum. FEMS Microbiol Lett 153:399–404Google Scholar
  24. Khomyakova M, Bükmez Ö, Thomas LK, Erb TJ, Berg IA (2011) A methylaspartate cycle in Haloarchaea. Science 331:334–337Google Scholar
  25. Kim M-K, Harwood CS (1991) Regulation of benzoate-CoA ligase in Rhodopseudomonas palustris. FEMS Microbiol Lett 83:199–204Google Scholar
  26. Kornberg HL, Salder JR (1960) Microbial oxidation of glycollate via a dicarboxylic acid cycle. Nature 185:153–155Google Scholar
  27. Laguna R, Tabita FR, Alber BE (2011) Acetate-dependent photoheterotrophic growth and the differential requirement for the Calvin–Benson–Bassham reductive pentose phosphate cycle in Rhodobacter sphaeroides and Rhodopseudomonas palustris. Arch Microbiol 193:151–154Google Scholar
  28. LaPorte DC, Koshland DE Jr (1982) A protein with kinase and phosphatase activities involved in regulation of tricarboxylic acid cycle. Nature 300:458–460Google Scholar
  29. Larimer FW, Chain P, Hauser L, Lamerdin J, Malfatti S, Do L, Land ML, Pelletier DA, Beatty JT, Lang AS, Tabita FR, Gibson JL, Hanson TE, Bobst C, Torres JL, Peres C, Harrison FH, Gibson J, Harwood CS (2004) Complete genome sequence of the metabolically versatile photosynthetic bacterium Rhodopseudomonas palustris. Nat Biotechnol 22(1):55–61Google Scholar
  30. Leroy B, Meur De Q, Moulin C, Wegria G, Wattiez R (2015) New insight into the photoheterotrophic growth of the isocitrate lyase-lacking purple bacterium Rhodospirillum rubrum on acetate. Microbiology 161:1061–1072Google Scholar
  31. Ljungdahl LG (1986) The autotrophic pathway of acetate synthesis in acetogenic bacteria. Annu Rev Microbiol 40:415–450Google Scholar
  32. Martínez-Luque M, Castillo F, Blasco R (2001) Assimilation of D-malate by Rhodobacter capsulatus E1F1. Curr Microbiol 43(3):154–157Google Scholar
  33. McKinlay JB, Harwood CS (2010) Carbon dioxide fixation as a central redox cofactor recycling mechanism in bacteria. Proc Natl Acad Sci USA 107:11669–11675Google Scholar
  34. Molina I, Pellicer MT, Badia J, Aguilar J, Baldoma L (1994) Molecular characterization of Escherichia coli malate synthase G: differentiation with the malate synthase A isoenzyme. Eur J Biochem 224:541–548Google Scholar
  35. Morgulis A, Coulouris G, Raytselis Y, Madden TL, Agarwala R, Schäffer AA (2008) Database indexing for production MegaBLAST searches. Bioinformatics 24:1757–1764Google Scholar
  36. Muller FM (1933) On the metabolism of the purple sulfur bacteria in organic media. Arch Mikrobiol 4:131–166Google Scholar
  37. Nuiry II, Cook PF (1985) The pH dependence of the reductive carboxylation of pyruvate by malic enzyme. Biochim Biophys Acta 829:295–298Google Scholar
  38. Oda Y, Larimer FW, Chain PSG, Malfatti S, Shin MV, Vergez LM, Hauser L, Land ML, Braatsch S, Beatty JT, Pelletier D, Schaefer AL, Harwood CS (2008) Multiple genome sequences reveal adaptations of a phototrophic bacterium to sediment microenvironments. Proc Natl Acad Sci USA 105(47):18543–18548Google Scholar
  39. Ornston LN, Ornston MK (1969) Regulation of glyoxylate metabolism in Escherichia coli K-12. J Bacteriol 98:1098–1108Google Scholar
  40. Petushkova EP (2018) Acetate assimilation in purple non-sulfur bacterium Rhodobacter capsulatus B10. PhD Dissertation Institute of Biochemistry and Physiology Russian Academy of Sciences, Pushchino, Moscow region, RussiaGoogle Scholar
  41. Petushkova EP, Tsygankov AA (2017) Acetate metabolism in purple non-sulphur bacterium Rhodobacter capsulatus. Biochemistry 82(5):786–807Google Scholar
  42. Rey FE, Heiniger EK, Harwood CS (2007) Redirection of metabolism for biological hydrogen production. Appl Environ Microbiol 73(5):1665–1671Google Scholar
  43. Sauer U, Eikmanns BJ (2005) The PEP-pyruvate-oxaloacetate node as the switch point for carbon flux distribution in bacteria. FEMS Microbiol Rev 29(4):765–794Google Scholar
  44. Schobert P, Bowien B (1984) Unusual C3 and C4 metabolism in the chemoautotroph Alcaligenes eutrophus. J Bacteriol 159:167–172Google Scholar
  45. Strauss G, 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(3):633–643Google Scholar
  46. Tabita FR (1988) Molecular and cellular regulation of autotrophic carbon dioxide fixation in microorganisms. Microbiol Rev 52:155–189Google Scholar
  47. Tabita FR, Hanson TE, Li H, Satagopan S, Singh J, Chan S (2007) Function, structure, and evolution of the RubisCO-like proteins and their RubisCO homologs. Microbiol Mol Biol Rev 71(4):576–599Google Scholar
  48. Tang KH, Tang YJ, Blankenship RE (2011) Carbon metabolic pathways in phototrophic bacteria and their broader evolutionary implications. Front Microbiol 2:165Google Scholar
  49. The UniProt Consortium (2015) UniProt: a hub for protein information. Nucleic Acids Res 43:D204–D212Google Scholar
  50. Tsygankov AA, Laurinavichene TV (1996) Influence of the degree and mode of light limitation on growth characteristics of the Rhodobacter capsulatus continuous cultures. Biotechnol Bioeng 51:605–612Google Scholar
  51. Vanderwinkel E, De Vlieghere M (1968) Physiologie et g´en´etique de l’isocitritase et des malate synthases chez Escherichia coli. Eur J Biochem 5:81–90Google Scholar
  52. Willison JC (1993) Biochemical genetics revisited: the use of mutants to study carbon and nitrogen metabolism in the photosynthetic bacteria. FEMS Microbiol Rev 104:1–38Google Scholar
  53. Witzel F, Goetze J, Ebenhoeh O (2010) Slow deactivation of ribulose 1,5-bisphosphate carboxylase/oxygenase elucidated by mathematical models. FEBS J 277:931–950Google Scholar
  54. Zarzycki J, Fuchs G (2011) Coassimilation of organic substrates via the autotrophic 3-hydroxypropionate bi-cycle in Chloroflexus aurantiacus. Appl Environ Microbiol 77(17):6181–6188Google Scholar
  55. Zarzycki J, Brecht V, Müller M, Fuchs G (2009) Identifying the missing steps of the autotrophic 3-hydroxypropionate CO2 fixation cycle in Chloroflexus aurantiacus. Proc Natl Acad Sci USA 106(50):21317–21322Google Scholar
  56. Zelcbuch L, Lindner SN, Zegman Y, Slutskin VI, Antonovsky N, Gleizer S, Milo R, Bar-Even A (2016) Pyruvate formate-lyase enables efficient growth of Escherichia coli on acetate and formate. Biochemistry 55(17):2423–2426Google Scholar
  57. Zhang Y, Rodionov DA, Gelfand MS, Gladyshev VN (2009) Comparative genomic analyses of nickel, cobalt and vitamin B12 utilization. BMC Genom 10:78Google Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Institute of Basic Biological ProblemsRussian Academy of SciencesPushchinoRussia
  2. 2.Faculty of BiotechnologyLomonosov Moscow State UniversityMoscowRussia

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