Skip to main content
SpringerLink
Log in

Large reallocations of carbon, nitrogen, and photosynthetic reductant among phycobilisomes, photosystems, and Rubisco during light acclimation in Synechococcus elongatus strain PCC7942 are constrained in cells under low environmental inorganic carbon

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Synechococcus elongatus strain PCC7942 cells were grown in high or low environmental concentrations of inorganic C (high-Ci, low-Ci) and subjected to a light shift from 50 µmol m−2 s−1 to 500 µmol m−2 s−1. We quantified photosynthetic reductant (O2 evolution) and molar cellular contents of phycobilisomes, PSII, PSI, and ribulose-1,5-bisphosphate carboxylase oxygenase (Rubisco) through the light shift. Upon the increase in light, small initial relative decreases in phycobilisomes per cell resulted from near cessation of phycobilisome synthesis and their dilution into daughter cells. Thus, allocation of reductant to phycobilisome synthesis dropped fivefold from pre- to post-light shift. The decrease in phycobilisome synthesis liberated enough material and reductant to allow a doubling of Rubisco and up to a sixfold increase in PSII complexes per cell. Low-Ci cells had smaller initial phycobilisome pools and upon increased light; their reallocation of reductant from phycobilisome synthesis may have limited the rate and extent of light acclimation, compared to high-Ci cells. Acclimation to increased light involved large reallocations of C, N, and reductant among different components of the photosynthetic apparatus, but total allocation to the apparatus was fairly stable at ca. 50% of cellular N, and drew 25–50% of reductant from photosynthesis.

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
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Allen MM, Smith AJ (1969) Nitrogen chlorosis in blue-green algae. Arch Microbiol 69:114–120

    CAS  Google Scholar 

  • Badger MR, Price GD (2003) CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J Exp Bot 54:609–622

    Google Scholar 

  • Barber J, Nield J, Morris EP, Zheleva D, Hankamer B (1997) The structure, function and dynamics of photosystem two. Physiol Plant 100:817–827

    Google Scholar 

  • Behrenfeld M-J, Prasil O, Kolber ZS, Babin M, Falkowski PG (1998) Compensatory changes in Photosystem II electron turnover rates protect photosynthesis from photoinhibition. Photosynth Res 58:259–268

    CAS  Google Scholar 

  • Bertilsson S, Berglund O, Karl DM, Chisholm SW (2003) Elemental composition of marine Prochlorococcus and Synechococcus: Implications for the ecological stoichiometry of the sea. Limnol Oceanogr 48:1721–1731

    Google Scholar 

  • Burns RA, MacDonald CA, McGinn PJ, Campbell DA (2005) High inorganic carbon disrupts photosynthetic acclimation to low temperature in the cyanobacterium Synechococcus PCC7942. J Phycol JPY-04-101-ART.R1

  • Campbell DA, Cockshutt AM, Porankiewicz-Asplund J (2003) Analysing photosynthetic complexes in uncharacterized species or mixed microalgal communities using global antibodies. Physiol Plant 119:322–327

    Google Scholar 

  • Choi A, Kim SG, Yoon BD, Oh HM (2003) Growth and amino acid contents of Spirulina platensis with different nitrogen sources. Biotechnol Bioproc Eng 8:368–372

    Google Scholar 

  • Clarke AK, Soitamo A, Gustafsson P, Öquist G (1992) Rapid interchange between two distinct forms of cyanobacterial photosystem II reaction-center protein D1 in response to photoinhibition. Proc Natl Acad Sci USA 90:9973–9977

    Google Scholar 

  • Clarke AK, Campbell D, Gustafsson P, Öquist G (1995) Dynamic responses of photosystem II and phycobilisomes to changing light in the cyanobacterium Synechococcus sp. PCC-7942. Planta 197:553–562

    Article  CAS  Google Scholar 

  • Cole JJ, Caraco NF, Kling GW, Kratz TK (1994) Carbon dioxide supersaturation in the surface waters of lakes. Science 265:1568–1570

    Google Scholar 

  • Collier JR, Grossman AR (1992) Chlorosis induced by nutrient deprivation in Synechococcus sp. strain PCC 7942: not all bleaching is the same. J Bacteriol 174:4718–4726

    CAS  PubMed  Google Scholar 

  • Cramer WA, Zhang HM, Yan JS, Kurisu G, Smith JL (2004) Evolution of photosynthesis: time-independent structure of the cytochrome b(6)f complex. Biochemistry 43:5921–5929

    Google Scholar 

  • Eley JH (1980) Effect of carbon dioxide concentration on pigmentation in the blue-green alga Anacystis nidulans. Plant Cell Physiol 12:311–316

    Google Scholar 

  • Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838

    Google Scholar 

  • Fromme P, Jordan P, Krauss N (2001) Structure of photosystem I. Biochim Biophys Acta 1507:5–31

    Google Scholar 

  • Fujita Y (1997) A study on the dynamic features of photosystem stoichiometry: Accomplishments and problems for future studies. Photosynth Res 53:83–93

    Google Scholar 

  • Giordano M (2001) Interactions between C and N metabolism in Dunaliella salina cells cultured at elevated CO2 and high N concentrations. J Plant Phys 158:577–581

    Google Scholar 

  • Glazer AN (1994) Adaptive variations in phycobilisome structure. In: Bittar EE and Barber J (eds) Advances in molecular and cell biology, vol 10: molecular processes of photosynthesis. JAI, Hampton Hill, Middlesex, UK

    Google Scholar 

  • Golden SS, Cho DS, Nalty MS (1989) Two functional psbD genes in the cyanobacterium Synechococcus sp. strain PCC 7942. J Bacteriol 171:4707–4713

    Google Scholar 

  • Görl M, Sauer J, Baier T, Forchhammer K (1998) Nitrogen-starvation-induced chlorosis in Synechococcus PCC 7942: adaptation to long-term survival. Microbiology 144:2449–2458

    Google Scholar 

  • Heldal M, Scanlan DJ, Norland S, Thingstad F, Mann NH (2003) Elemental composition of single cells of various strains of marine Prochlorococcus and Synechococcus using X-ray microanalysis. Limnol Oceanogr 48:1732–1743

    Google Scholar 

  • Herranen M, Aro E-M, Tyystjaärvi T (2001) Two distinct mechanisms regulate the transcription of photosystem II genes in Synechocystis sp. PCC 6803. Plant Physiol 112:531–539

    Google Scholar 

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

    Google Scholar 

  • Hihara Y, Sonoike K, Ikeuchi M (1998) A novel gene, pmgA, specifically regulates photosystem stoichiometry in the cyanobacterium Synechocystis species PCC 6803 in response to high light. Plant Physiol 117:1205–1216

    Google Scholar 

  • Huner NPA, Öquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends Plant Sci 3:224–230

    Article  Google Scholar 

  • Kaneko T, Sato S, Kotani H, Tanaka A,Asamizu E, Nakamura Y, Miyajima N, Hirosawa M, Sugiura M, Sasamoto S, Kimura T, Hosouchi T, Matsuno A, Muraki A, Nakazaki N, Naruo K, Okumura S, Shimpo S, Takeuchi C, Wada T, Watanabe A, Yamada M, Yasuda M, Tabata S (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3:109–136

    CAS  PubMed  Google Scholar 

  • Koike H, Ikeuchi M, Hiyama T, Inoue Y (1989) Identification of photosystem I components from the cyanobacterium, Synechococcus volcanus by N-terminal sequencing. FEBS Lett 253:257–263

    Google Scholar 

  • Kurisu G, Zhang H, Smith JL, Cramer WA (2003) Structure of the cytochrome b6f complex of oxygenic photosynthesis: Tuning the cavity. Science 302:1009–1014

    Google Scholar 

  • Li L-A, Tabita F (1994) Transcription control of ribulose bisphosphate carboxylase/oxygenase activase and adjacent genes in Anabaena species. J Bacteriol 176:6697–6706

    Google Scholar 

  • Liotenberg S, Campbell D, Rippka R, Houmard J, deMarsac NT (1996) Effect of the nitrogen source on phycobiliprotein synthesis and cell reserves in a chromatically adapting filamentous cyanobacterium. Microbiol UK 142:611–622

    Google Scholar 

  • MacKenzie TDB, Burns RA, Campbell, DA (2004) Carbon status constrains light acclimation in the cyanobacterium Synechococcus elongatus. Plant Physiol 136:3301–3312

    Google Scholar 

  • Manodori A, Melis A (1984) Photochemical apparatus organisation in Anacystis nidulans (Cyanophyceae). Plant Physiol 74:67–71

    Google Scholar 

  • Manodori A, Melis A (1986) Cyanobacterial acclimation to photosystem-I or photosystem-II light. Plant Physiol 82:185–189

    Google Scholar 

  • Mathews CK, van Holde KE (1996) Biochemistry, 2nd edn. Benjamin/Cummings, Menlo Park

  • McGinn PJ, Price GD, Badger MR (2004) High light enhances the expression of low-CO2-inducible transcripts involved in the CO2-concentrating mechanism in Synechocystis sp. PCC6803. Plant Cell Environ 27:615–626

    Google Scholar 

  • Müller C, Reuter W, Wehrmeyer W, Dau H, Senger H (1993) Adaptation of the photosynthetic apparatus of Anacystis nidulans to irradiance and CO2-concentration. Bot Acta 106:480–487

    Google Scholar 

  • Murakami A, Fujita Y (1991) Regulation of photosystem stoichiometry in the photosynthetic system of the cyanophyte Synechocystis PCC 6714 in response to light intensity. Plant Cell Physiol 32:223–230

    Google Scholar 

  • Murakami A, Kim S-J, Fujita Y (1997) Changes in photosystem stoichiometry in response to environmental conditions for cell growth observed with the cyanophyte Synechocystis PCC 6714. Plant Cell Physiol 38:392–397

    Google Scholar 

  • Muramatsu M, Hihara Y (2003) Transcriptional regulation of genes encoding subunits of photosystem I during acclimation to high-light conditions in Synechocystis sp. PCC 6803. Planta 216:446–453

    Google Scholar 

  • Myers J, Graham JR, Wang RT (1980) Light harvesting in Anacystis nidulans studied in pigment mutants. Plant Physiol 66:1144–1149

    CAS  Google Scholar 

  • Ogawa T, Kaplan A (2003) Inorganic carbon acquisition systems in cyanobacteria. Photosynth Res 77:105–115

    Google Scholar 

  • Perin S, Lean DRS, Pick FR, Mazumder A (2002) Photosynthetic carbon allocation: effects of planktivorous fish and nutrient enrichment. Aquat Sci 64:217–238

    Google Scholar 

  • Poorter H, Nagel O (2000) The role of biomass allocation in the growth response of plants to different levels of light, CO2, nutrients and water: a quantitative review. Aust J Plant Physiol:595–607

    Google Scholar 

  • Richaud C, Zabulon G, Joder A, Thomas J-C (2001) Nitrogen or sulfur starvation differentially affects phycobilisome degradation and expression of the nblA gene in Synechocystis strain PCC 6803. J Bacteriol 183:2989–2994

    Google Scholar 

  • Rippka R, Herdman M (1992) Pasteur culture collection of cyanobacterial strains in axenic culture, catalogue and taxonomic handbook. Institut Pasteur, Paris

    Google Scholar 

  • Rippka R, Deruelles J, Waterbury JB,Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyano-bacteria. J Gen Microbiol 11:1–61

    Google Scholar 

  • Rodríguez-Buey ML, Orús MI (2001) The response of Synechococcus PCC7942 (Cyanophyta) to changes in CO2 supply in relation to the acclimation of the CO2-concentrating mechanism. I. Physiological study. J Plant Physiol 158:325–334

    Google Scholar 

  • Sauer J, Schreiber U, Schmid R, Volker U, Forchhammer K (2001) Nitrogen starvation-induced chlorosis in Synechococcus PCC 7942. Low-level photosynthesis as a mechanism of long-term survival. Plant Physiol 126:233–243

    Article  CAS  PubMed  Google Scholar 

  • Shibata M, Ohkawa H, Katoh H, Shimoyama M, Ogawa T (2002) Two CO2 uptake systems in cyanobacteria: four systems for inorganic carbon acquisition in Synechocystis sp. strain PCC6803. Funct Plant Biol 29:123–129

    Google Scholar 

  • Stock D, Leslie AGW, Walker JE (1999) Molecular architecture of the Rotary Motor in ATP synthase. Science 286:1700–1705

    Google Scholar 

  • Vasilikiotis C, Melis A (1994) Photosystem II reaction center damage and repair cycle: Chloroplast acclimation strategy to irradiance stress. Proc Nat Acad Sci USA 91:7222–7226

    Google Scholar 

  • Vierling E, Alberte R (1980) Functional organization and plasticity of the photosynthetic unit of the cyanobacterium Anacystis nidulans. Plant Physiol 50:93–98

    Google Scholar 

  • van Waasbergen LG, Dolganov N, Grossman AR (2002) nblS, a gene involved in controlling photosynthesis-related gene expression during high light and nutrient stress in Synechococcus elongatus PCC 7942. J Bacteriol 184:2481–2490

    Google Scholar 

  • Webb M, Melis A (1995) Chloroplast response in Dunaliella salina to irradiance stress effect on thylakoid membrane protein assembly and function. Plant Physiol 107:885–893

    Google Scholar 

  • Xu W, Tang H, Wang Y, Chitnis PR (2001) Proteins of the cyanobacterial photosystem I. Biochim Biophys Acta 1507:32–40

    Google Scholar 

  • Yunus M, Pathre U, Mohanty P (2000) Probing photosynthesis: mechanisms, regulation and adaptation. Taylor & Francis, London

    Google Scholar 

Download references

Acknowledgements

This study was funded through Natural Sciences and Engineering Research Council (NSERC) of Canada Discovery and Equipment grants to D.A.C., an NSERC Post-Graduate Scholarship-B to T.D.B.M, and New Brunswick Innovation Foundation research personnel funding (R.A.B. and A.M.C.). The authors thank Mr. Chris Brown and Agrisera (http://www.agrisera.se) for their continuing research and development to prepare the antibodies and protein standards used in the protein immunodetections, and Mrs. Liliya Nikolcheva for assistance with the mathematical formulae included in the “Materials and methods” section.

Author information

Authors and Affiliations

  1. Department of Biology, University of New Brunswick, Fredericton, NB, E3B 6E1, Canada

    Tyler D.B. MacKenzie & Robert A. Burns

  2. Department of Biology and Coastal Wetlands Institute, Mount Allison University, NB, E4L 1G7, Canada

    Jeanette M. Johnson & Douglas A. Campbell

  3. Environmental Proteomics, Sackville, NB, E4L 1G7, Canada

    Amanda M. Cockshutt

Authors
  1. Tyler D.B. MacKenzie
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jeanette M. Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Amanda M. Cockshutt
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Robert A. Burns
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Douglas A. Campbell
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Douglas A. Campbell.

Rights and permissions

Reprints and permissions

About this article

Cite this article

MacKenzie, T.D., Johnson, J.M., Cockshutt, A.M. et al. Large reallocations of carbon, nitrogen, and photosynthetic reductant among phycobilisomes, photosystems, and Rubisco during light acclimation in Synechococcus elongatus strain PCC7942 are constrained in cells under low environmental inorganic carbon. Arch Microbiol 183, 190–202 (2005). https://doi.org/10.1007/s00203-005-0761-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-005-0761-1

Keywords

Search

Navigation