Log in

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

  • Original Article
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

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.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (France)

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

ICL:

Isocitrate lyase

ICDH:

Isocitrate dehydrogenase

PA:

Pyruvic acid

PGA:

Phosphoglyceric acid

PEP:

Phosphoenolpyruvate

TCA cycle:

Tricarboxylic acid cycle

OAA:

Oxaloacetic acid

BPG:

1,3-Bisphosphoglycerate

GAP:

Glyceraldehyde-3-phosphate

References

  • 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 321–350

    Chapter  Google Scholar 

  • 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):297–309

    Article  CAS  PubMed  Google Scholar 

  • 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 25:3389–3402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bassham JA, Benson AA, Calvin M (1950) The path of carbon in photosynthesis. J Biol Chem 185:781–787

    CAS  PubMed  Google Scholar 

  • Berg IA, Kockelkorn D, Buckel W, Fuchs G (2007) A 3-hydroxypropionate/4-hydroxybutyrate autotrophic carbon dioxide assimilation pathway in archaea. Science 318:1782–1786

    Article  CAS  PubMed  Google Scholar 

  • Bowes G, Ogren WL, Hagerman RH (1971) Phosphoglycolate production catalyzed by ribulose diphosphate carboxylase. Biochem Biophys Res Commun 45:716–722

    Article  CAS  PubMed  Google Scholar 

  • 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 212:159–164

    Article  CAS  PubMed  Google Scholar 

  • 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 186:8144–8148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):6184–6194

    Article  CAS  PubMed  Google Scholar 

  • Drevland RM, Waheed A, Graham DE (2007) Enzymology and evolution of the pyruvate pathway to 2-oxobutyrate in Methanocaldococcus jannaschii. J Bacteriol 189:4391–4400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edwards J, Walker D (1986) Photosynthesis of C3 and C4 of plants: mechanisms and regulation. Mir, Moscow

    Google Scholar 

  • Eidels L, Preiss J (1970) Citrate synthase. A regulatory enzyme from Rhodopseudomonas capsulata. J Biol Chem 245:2937–2945

    CAS  PubMed  Google Scholar 

  • Ensign SA (2011) Another microbial pathway for acetate assimilation. Science 331:294

    Article  CAS  PubMed  Google Scholar 

  • 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 192:1249–1258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):928–934

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):270–278

    Article  CAS  Google Scholar 

  • Garnak M, Reeves HC (1979a) Phosphorylation of isocitrate dehydrogenase of Escherichia coli. Science 203:1111–1112

    Article  CAS  PubMed  Google Scholar 

  • Garnak M, Reeves HC (1979b) Purification and properties of phosphorylated isocitrate dehydrogenase of Escherichia coli. J Biol Chem 254:7915–7920

    CAS  PubMed  Google Scholar 

  • Gibson JL, Tabita FR (1977) Isolation and preliminary characterization of two forms of ribulose-1,5-bisphosphate carboxylase from Rhodopseudomonas capsulata. J Bacteriol 132:818–823

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 61:940–947

    Article  CAS  PubMed  Google Scholar 

  • 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 40:4703–4713

    Article  CAS  PubMed  Google Scholar 

  • 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 105:7851–7856

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 153:399–404

    Article  CAS  Google Scholar 

  • Khomyakova M, Bükmez Ö, Thomas LK, Erb TJ, Berg IA (2011) A methylaspartate cycle in Haloarchaea. Science 331:334–337

    Article  CAS  PubMed  Google Scholar 

  • Kim M-K, Harwood CS (1991) Regulation of benzoate-CoA ligase in Rhodopseudomonas palustris. FEMS Microbiol Lett 83:199–204

    CAS  Google Scholar 

  • Kornberg HL, Salder JR (1960) Microbial oxidation of glycollate via a dicarboxylic acid cycle. Nature 185:153–155

    Article  CAS  PubMed  Google Scholar 

  • 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 193:151–154

    Article  CAS  PubMed  Google Scholar 

  • LaPorte DC, Koshland DE Jr (1982) A protein with kinase and phosphatase activities involved in regulation of tricarboxylic acid cycle. Nature 300:458–460

    Article  CAS  PubMed  Google Scholar 

  • 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):55–61

    Article  CAS  PubMed  Google Scholar 

  • 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 161:1061–1072

    Article  CAS  PubMed  Google Scholar 

  • Ljungdahl LG (1986) The autotrophic pathway of acetate synthesis in acetogenic bacteria. Annu Rev Microbiol 40:415–450

    Article  CAS  PubMed  Google Scholar 

  • Martínez-Luque M, Castillo F, Blasco R (2001) Assimilation of D-malate by Rhodobacter capsulatus E1F1. Curr Microbiol 43(3):154–157

    Article  CAS  PubMed  Google Scholar 

  • McKinlay JB, Harwood CS (2010) Carbon dioxide fixation as a central redox cofactor recycling mechanism in bacteria. Proc Natl Acad Sci USA 107:11669–11675

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 224:541–548

    Article  CAS  PubMed  Google Scholar 

  • Morgulis A, Coulouris G, Raytselis Y, Madden TL, Agarwala R, Schäffer AA (2008) Database indexing for production MegaBLAST searches. Bioinformatics 24:1757–1764

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muller FM (1933) On the metabolism of the purple sulfur bacteria in organic media. Arch Mikrobiol 4:131–166

    Article  CAS  Google Scholar 

  • Nuiry II, Cook PF (1985) The pH dependence of the reductive carboxylation of pyruvate by malic enzyme. Biochim Biophys Acta 829:295–298

    Article  CAS  PubMed  Google Scholar 

  • 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):18543–18548

    Article  PubMed  PubMed Central  Google Scholar 

  • Ornston LN, Ornston MK (1969) Regulation of glyoxylate metabolism in Escherichia coli K-12. J Bacteriol 98:1098–1108

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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, Russia

  • Petushkova EP, Tsygankov AA (2017) Acetate metabolism in purple non-sulphur bacterium Rhodobacter capsulatus. Biochemistry 82(5):786–807

    Google Scholar 

  • Rey FE, Heiniger EK, Harwood CS (2007) Redirection of metabolism for biological hydrogen production. Appl Environ Microbiol 73(5):1665–1671

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):765–794

    Article  CAS  PubMed  Google Scholar 

  • Schobert P, Bowien B (1984) Unusual C3 and C4 metabolism in the chemoautotroph Alcaligenes eutrophus. J Bacteriol 159:167–172

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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):633–643

    Article  CAS  PubMed  Google Scholar 

  • Tabita FR (1988) Molecular and cellular regulation of autotrophic carbon dioxide fixation in microorganisms. Microbiol Rev 52:155–189

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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):576–599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang KH, Tang YJ, Blankenship RE (2011) Carbon metabolic pathways in phototrophic bacteria and their broader evolutionary implications. Front Microbiol 2:165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • The UniProt Consortium (2015) UniProt: a hub for protein information. Nucleic Acids Res 43:D204–D212

    Article  CAS  Google Scholar 

  • 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 51:605–612

    Article  CAS  PubMed  Google Scholar 

  • Vanderwinkel E, De Vlieghere M (1968) Physiologie et g´en´etique de l’isocitritase et des malate synthases chez Escherichia coli. Eur J Biochem 5:81–90

    Article  CAS  PubMed  Google Scholar 

  • Willison JC (1993) Biochemical genetics revisited: the use of mutants to study carbon and nitrogen metabolism in the photosynthetic bacteria. FEMS Microbiol Rev 104:1–38

    Article  CAS  Google Scholar 

  • Witzel F, Goetze J, Ebenhoeh O (2010) Slow deactivation of ribulose 1,5-bisphosphate carboxylase/oxygenase elucidated by mathematical models. FEBS J 277:931–950

    Article  CAS  PubMed  Google Scholar 

  • Zarzycki J, Fuchs G (2011) Coassimilation of organic substrates via the autotrophic 3-hydroxypropionate bi-cycle in Chloroflexus aurantiacus. Appl Environ Microbiol 77(17):6181–6188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):21317–21322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):2423–2426

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Rodionov DA, Gelfand MS, Gladyshev VN (2009) Comparative genomic analyses of nickel, cobalt and vitamin B12 utilization. BMC Genom 10:78

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anatoly Tsygankov.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 124 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Petushkova, E., Iuzhakov, S. & Tsygankov, A. Differences in possible TCA cycle replenishing pathways in purple non-sulfur bacteria possessing glyoxylate pathway. Photosynth Res 139, 523–537 (2019). https://doi.org/10.1007/s11120-018-0581-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-018-0581-1

Keywords

Navigation