Skip to main content

Advertisement

SpringerLink
Log in

Characterization of trophic changes and a functional oxidative pentose phosphate pathway in Synechocystis sp. PCC 6803

  • Original Paper
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Cyanobacteria have a tremendous activity to adapt to environmental changes of their growth conditions. In this study, Synechocystis sp. PCC 6803 was used as a model organism to focus on the alternatives of cyanobacterial energy metabolism. Glucose oxidation in Synechocystis sp. PCC6803 was studied by inactivation of slr1843, encoding glucose-6-phosphate dehydrogenase (G6PDH), the first enzyme of the oxidative pentose phosphate pathway (OPPP). The resulting zwf strain was not capable of glucose supported heterotrophic growth. Growth under autotrophy and under mixotrophy was similar to that of the wild-type strain, even though oxygen evolution and uptake rates of the mutant were decreased in the presence of glucose. The organic acids citrate and succinate supported photoheterotrophic growth of both WT and zwf. Proteome analysis of soluble and membrane fractions allowed identification of four growth condition-dependent proteins, pentose-5-phosphate 3-epimerase (slr1622), inorganic pyrophosphatase (sll0807), hypothetical protein (slr2032) and ammonium/methylammonium permease (sll0108) revealing details of maintenance of the cellular carbon/nitrogen/phosphate balance under different modes of growth.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

α-KGDH:

α-Ketoglutarate dehydrogenase

BN-PAGE:

Blue native page

DCBQ:

2,6-Dichloro-p-benzoquinone

DCMU:

3-(3,4-Dichlorophenyl)-1,1-dimethylurea

G6PDH:

Glucose-6-phosphate dehydrogenase

IDH:

Isocitrate dehydrogenase

LAHG:

Light-activated heterotrophic growth

OPPP:

Oxidative pentose phosphate pathway

PPDF:

Photosynthetic photon flux density

PPi :

Inorganic phosphate

TCA:

Tricarboxylic acid

WT:

Wild type

zwf :

Mutant strain lacking glucose-6-phosphate dehydrogenase

References

  • Bennet A, Bogorad L (1973) Complementary chromatic adaption in filamentous blue-green alga. J Cell Biol 58:419–4435

    Article  Google Scholar 

  • Cogne G, Gros JB, Dussap CG (2003) Identification of a metabolic network structure representative of Arthrospira (Spirulina) platensis metabolism. Biotechnol Bioeng 84:667–676

    Article  CAS  PubMed  Google Scholar 

  • Cooley JV, Vermaas WFJ (2001) Succinate dehydrogenase and other respiratory pathways in thylakoid membranes of Synechocystis sp. strain PCC 6803: capacity comparisons and physiological functions. J Bacteriol 183:4251–4258

    Article  CAS  PubMed  Google Scholar 

  • DeRuyter YA, Fromme P (2008) Molecular structure of the photosynthetic apparatus. In: Herrero A, Flores E (eds) The cyanobacteria molecular biology, genomics and evolution. Caister Academic Press, Norfolk, pp 217–269

    Google Scholar 

  • Flores E, Frías JE, Rubio LM, Herrero A (2005) Photosynthetic nitrate assimilation in cyanobacteria. Photosynth Res 83:117–133

    Article  CAS  PubMed  Google Scholar 

  • Forti G, Meyer EM (1969) Effect of pyrophosphate on photosynthetic electron transport reactions. Plant Physiol 44:1511–1514

    Article  CAS  PubMed  Google Scholar 

  • Gomez-Garcia MR, Losada M, Serrano A (2003) Concurrent transcriptional activation of ppa and ppx genes by phosphate deprivation in the cyanobacterium Synechocystis sp. strain PCC 6803. Biochem Biophys Res Commun 302:601–609

    Article  CAS  PubMed  Google Scholar 

  • Grossman A, McGowan RE (1975) Regulation of glucose 6-phosphate dehydrogenases in blue-green algae. Plant Physiol 55:658–662

    Article  CAS  PubMed  Google Scholar 

  • Herranen M, Battchikova N, Zhang PP, Graf A, Sirpiö S, Paakkarinen V, Aro EM (2004) Towards functional proteomics of membrane protein complexes in Synechocystis sp. PCC 6803. Plant Physiol 134:470–481

    Article  CAS  PubMed  Google Scholar 

  • Ikeuchi M, Tabata S (2001) Synechocystis sp. PCC 6803—a useful tool in the study of the genetics of cyanobacteria. Photosynth Res 70:73–83

    Article  CAS  PubMed  Google Scholar 

  • Knowles VL, Plaxton WC (2003) From genome to enzyme: analysis of key glycolytic and oxidative pentose phosphate pathway enzymes in the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 44:758–763

    Article  CAS  PubMed  Google Scholar 

  • Kurian D, Jansén T, Mäenpää P (2006) Proteomic analysis of heterotrophy in Synechocystis sp. PCC 6803. Proteomics 6:1483–1494

    Article  CAS  PubMed  Google Scholar 

  • Montesinos ML, Muro-Pastor AL, Herrero A, Flores E (1998) Ammonium/methylammonium permeases of a cyanobacterium, identification and analysis of three nitrogen-regulated amt genes in Synechocystis sp. PCC 6803. J Biol Chem 273:31463–31470

    Article  CAS  PubMed  Google Scholar 

  • Murata N, Suzuki I (2006) Exploitation of genomic sequences in a systematic analysis to access how cyanobacteria sense environmental stress. J Exp Bot 57:235–247

    Article  CAS  PubMed  Google Scholar 

  • Pelroy RA, Bassham JA (1972) Photosynthetic and dark carbon metabolism in unicellular blue-green algae. Arch Microbiol 86:303–332

    Google Scholar 

  • Prentki P, Krisch HM (1984) In vitro insertional mutagenesis with a selectable DNA fragment. Gene 29:303–313

    Article  CAS  PubMed  Google Scholar 

  • Rippka R (1972) Photoheterotrophy and chemoheterotrophy among unicellular blue green algae. Arch Microbiol 87:93–98

    Google Scholar 

  • Rodríguez-Ezpeleta N, Brinkmann H, Burey S, Roure B, Burger G, Löffelhardt W, Bohnert H, Philippe H, Lang B (2005) Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. Curr Biol 15:1325–1330

    Article  PubMed  Google Scholar 

  • Summers ML, Meeks JC (1996) Transcriptional regulation of zwf, encoding glucose-6-phosphate dehydrogenase, from the cyanobacterium Nostoc punctiforme strain ATCC 29133. Mol Microbiol 22:473–480

    Article  CAS  PubMed  Google Scholar 

  • Summers ML, Wallis JG, Campbell EL, Meeks JC (1995) Genetic evidence of a major role for glucose-6-phosphate dehydrogenase in nitrogen fixation and dark growth of the cyanobacterium Nostoc sp. strain ATCC 29133. J Bacteriol 177:6184–6194

    CAS  PubMed  Google Scholar 

  • Vásquez-Bermúdez MF, Paz-Yepes J, Herrero A, Flores E (2002) The NtcA activated amt1 gene encodes a permease required for uptake of low concentrations of ammonium in the cyanobacterium Synechococcus sp. PCC 7942. Microbiology 148:861–869

    Google Scholar 

  • Williams JKG (1988) Construction of specific mutations in PSII photosynthetic reaction center by genetic engineering. Methods Enzymol 167:766–778

    Article  CAS  Google Scholar 

  • Yang C, Hua Q, Shimizu K (2002) Metabolic flux analysis in Synechocystis using isotope distribution from 13C-labeled glucose. Metab Eng 4:202–216

    Article  CAS  PubMed  Google Scholar 

  • Yin JC, Krebs MP, Reznikoff WS (1988) Effect of dam methylation on Tn5 transposition. J Mol Biol 199:35–45

    Article  CAS  PubMed  Google Scholar 

  • Zhang P, Battchikova N, Jansén T, Appel J, Ogawa T, Aro EM (2004) Expression and functional roles of the two distinct NDH-1 complexes and the carbon acquisition complex NdhD3/NdhF3/CupA/Sll1753 in Synechocystis sp. PCC 6803. Plant Cell 16:3326–3340

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Baba T, Mori H, Schimidzu K (2004) Effect of zwf gene knockout on the metabolism of Escherichia coli grown on glucose or acetate. Metab Eng 6:164–174

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Academy of Finland to P.M. (203352), by NSF grant and NIH grants to M.L.S (MCB0093327, GM48680, GM63787) and by the Finnish Cultural Foundation to T.J. We thank Wim Vermaas for providing us with the glucose tolerant Synechocystis sp. strain PCC 6803 and Richard J. Debus for pHP45Gm.

Author information

Authors and Affiliations

  1. Laboratory of Plant Physiology and Molecular Biology, Department of Biology, University of Turku, 20014, Turku, Finland

    Tove Jansén & Pirkko Mäenpää

  2. Department of Veterinary Technology, Faculty of Veterinary Technology, Kasetsart University, 50 Phahon Yothin Rd, Chatuchak, Bangkok, 10900, Thailand

    Wuttinun Raksajit

  3. Henry Wellcome Laboratory for Biogerontology Research, Newcastle University, Newcastle Upon Tyne, NE4 6BE, UK

    Dominic Kurian

  4. Department of Biology, California State University, Northridge, CA, 91330-8303, USA

    Steve York & Michael L. Summers

Authors
  1. Tove Jansén
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dominic Kurian
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wuttinun Raksajit
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Steve York
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Michael L. Summers
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Pirkko Mäenpää
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pirkko Mäenpää.

Additional information

Communicated by H. Gabrys.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jansén, T., Kurian, D., Raksajit, W. et al. Characterization of trophic changes and a functional oxidative pentose phosphate pathway in Synechocystis sp. PCC 6803. Acta Physiol Plant 32, 511–518 (2010). https://doi.org/10.1007/s11738-009-0428-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11738-009-0428-7

Keywords

Search

Navigation