Skip to main content
SpringerLink
Log in

A Synechococcus elongatus PCC 7942 mutant with a higher tolerance toward the herbicide bentazone also confers resistance to sodium chloride stress

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

Abstract

Following a N-methyl-N′-nitro-N-nitrosoguanidine-based mutagenesis of Synechococcus elongatus PCC 7942 wild type, we were able to select several mutants with an enhanced tolerance toward the herbicide bentazone (3-isopropyl-1H-2,1,3-benzothiadiazine-4(3H)-one 2,2-dioxide). Mutant Mu1 has in part been previously characterized. In the present paper we report on another mutant, called Mu2, which also has a higher tolerance toward bentazone. Since Mu2 showed a better growth than WT when cultivated with elevated NaCl concentrations in the growth medium and since S. elongatus WT has previously been classified to be low salt tolerant, we were especially interested in the identification of the modifications conferring this higher salt tolerance to mutant Mu2. Immunoblot analyses provided evidence that Mu2 had a constitutively higher expression of PsbO and of IsiA. In addition, in Mu2 a significantly higher concentration of IdiA was detected under salt stress as compared to WT. These three proteins most likely contribute to a better protection and/or stabilization of photosystem II. Moreover, Mu2 had a higher amount of the photosystem I reaction center proteins PsaAB under salt stress than WT. In addition, the amount of the ferredoxin:NADP+ oxidoreductase and also of the ATP synthase was constitutively higher in Mu2 than in WT. In contrast to WT the latter two proteins did not decrease under salt stress in Mu2. Therefore, it can be assumed that Mu2 could maintain a high cyclic electron transport activity around photosystem I under salt stress. It can be assumed that the combination of these modifications of the electron transport chain cause a better protection of photosystem II against oxidative damage and cause an increase of cyclic electron transport activity around photosystem I with ATP synthesis. Thus, the overall cellular energization in Mu2 relative to WT is improved. Together with putative other not yet identified modifications this seems to enable Mu2 to energize its cytoplasmic membrane-localized ion pumps more effectively than WT and, as a consequence, to keep the intracellular NaCl concentration low.

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
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

Abbreviations

Asc.:

Ascorbate

DCPIP:

2,6-Dichlorophenolindophenol

Chl a :

Chlorophyll a

CS:

Cell suspension

FNR:

Ferredoxin:NADP+ oxidoreductase

Mu2:

Bentazone-resistant Synechococcus elongatus PCC 7942 mutant

MV:

Methylviologen

NSG:

N-methyl-N′-nitro-N-nitrosoguanidine

PCV:

Packed cell volume

PS:

Photosystem

WT:

Wild type

References

  • Allakhverdiev SI, Klimov VV, Hagemann M (2005) Cellular energization protects the photosynthetic machinery against salt-induced inactivation in Synechococcus. Biochim Biophys Acta 1708:201–208

    Article  PubMed  CAS  Google Scholar 

  • Allakhverdiev SI, Nishiyama Y, Suzuki I, Tasaka Y, Murata N (1999) Genetic engineering of the unsaturation of fatty acids in membrane lipids alters the tolerance of Synechocystis to salt stress. Proc Natl Acad Sci USA 96:5862–5867

    Article  PubMed  CAS  Google Scholar 

  • Aro EM, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochem Biophys Acta 1143:113–134

    Article  PubMed  CAS  Google Scholar 

  • Bagchi SN, Pistorius EK, Michel KP (2003) A Synechococcus sp. PCC 7942 mutant with a higher tolerance towards bentazone. Photosynth Res 75:171–182

    Article  PubMed  CAS  Google Scholar 

  • Barber J, Nield J, Duncan J, Bibby TS (2006) Accessory chlorophyll proteins in cyanobacterial photosystem I. In: Goldbeck JH (ed) Photosystem I: the light-driven plastocyanin:ferredoxin oxidoreductase. Springer, Dordrecht, The Netherlands, pp 99–117

  • Bibby TS, Nield J, Barber J (2001) Iron deficiency induces the formation of an antenna ring around trimeric photosystem I in cyanobacteria. Nature 412:743–745

    Article  PubMed  CAS  Google Scholar 

  • Boekema EJ, Hifney A, Yakushevska AE, Piotrowski M, Keegstra W, Berry S, Michel KP, Pistorius EK, Kruip J (2001) A giant chlorophyll–protein complex induced by iron deficiency in cyanobacteria. Nature 412:745–748

    Article  PubMed  CAS  Google Scholar 

  • Burnap RL, Troyan T, Sherman LA (1993) The highly abundant chlorophyll–protein complex of iron-deficient Synechococcus sp. PCC 7942 (CP43′) is encoded by the isiA gene. Plant Physiol 103:893–902

    Article  PubMed  CAS  Google Scholar 

  • De Las Rivas J, Balsera M, Barber J (2004) Evolution of oxygenic photosynthesis: genome-wide analysis of the OEC extrinsic proteins. Trends Plant Sci 9:18–25

    Article  PubMed  CAS  Google Scholar 

  • Deshnium P, Los DA, Hayashi H, Mustardy L, Murata N (1995) Transformation of Synechococcus with a gene for choline oxidase enhances tolerance to salt stress. Plant Mol Biol 29:897–907

    Article  PubMed  CAS  Google Scholar 

  • Duhring U, Axmann IM, Hess WR, Wilde A (2006) An internal antisense RNA regulates expression of the photosynthesis gene isiA. Proc Natl Acad Sci USA 103:7054–7058

    Article  PubMed  CAS  Google Scholar 

  • Durham KA, Bullerjahn GS (2002) Immunocytochemical localization of the stress-induced DpsA protein in the cyanobacterium Synechococcus sp. strain PCC 7942. J Basic Microbiol 42:367–372

    Article  PubMed  CAS  Google Scholar 

  • Dwivedi K, Sen A, Bullerjahn GS (1997) Expression and mutagenesis of the dpsA gene of Synechococcus sp. PCC 7942, encoding a DNA-binding protein involved in oxidative stress protection. FEMS Microbiol Lett 155:85–91

    Article  CAS  Google Scholar 

  • Exss-Sonne P, Tölle J, Bader KP, Pistorius EK, Michel KP (2000) The IdiA protein of Synechococcus sp. PCC 7942 functions in protecting photosystem II under oxidative stress. Photosynth Res 63:145–157

    Article  PubMed  CAS  Google Scholar 

  • Ghassemian M, Straus NA (1996) Fur regulates the expression of iron-stress genes in the cyanobacterium Synechococcus sp. strain PCC 7942. Microbiology 142:1469–1476

    PubMed  CAS  Google Scholar 

  • Golden SS, Sherman LA (1984) Biochemical and biophysical characterization of herbicide-resistant mutants of the unicellular cyanobacterium, Anacystis nidulans R2. Biochim Biophys Acta 764:239–246

    Article  CAS  Google Scholar 

  • Herdman M, Castenholz RW, Iteman I, Waterbury JB, Rippka R (2000) The archae, cyanobacteria and deeply branching bacteria. In: Boone DR, Castenholz RW, Garrity GM (eds) Bergey’s manual of systematic bacteriology. Springer-Verlag, New York

    Google Scholar 

  • Jeanjean R, Matthijs HC, Onana B, Havaux M, Joset F (1993) Exposure of the cyanobacterium Synechocystis sp. PCC 6803 to salt stress induces concerted changes in respiration and photosynthesis. Plant Cell Physiol 34:1073–1079

    CAS  Google Scholar 

  • Joset F, Jeanjean R, Hagemann M (1996) Dynamics of the response of cyanobacteria to salt stress: deciphering the molecular events. Physiol Plant 96:738–744

    Article  CAS  Google Scholar 

  • Kaku N, Hibino T, Tanaka Y, Ishikawa H, Araki E, Takabe T (2000) Effects of overexpression of Escherichia coli katE and bet genes on the tolerance for salt stress in a freshwater cyanobacterium Synechococcus sp. PCC 7942. Plant Sci 159:281–288

    Article  PubMed  CAS  Google Scholar 

  • Ke B (2001) Photosynthesis: photobiochemistry and photobiophysics. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Kunert A, Vinnemeier J, Erdmann N, Hagemann M (2003) Repression by Fur is not the main mechanism controlling the iron-inducible isiAB operon in the cyanobacterium Synechocystis sp. PCC 6803. FEMS Microbiol Lett 227:255–262

    Article  PubMed  CAS  Google Scholar 

  • Laberge D, Rouillon R, Carpentier R (2000) Comparative study of thylakoid membranes sensitivity for herbicide detection after physical or chemical immobilization. Enzyme Microb Technol 26:332–336

    Article  PubMed  CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  • Lax JA, Arteni AA, Boekema EJ, Pistorius EK, Michel KP, Rogner M (2007) Structural response of photosystem 2 to iron deficiency: characterization of a new photosystem 2-IdiA complex from the cyanobacterium Thermosynechococcus elongatus BP-1. Biochim Biophys Acta (in press)

  • Mallipudi LR, Gleason FK (1989) Characterization of a mutant of Anacystis nidulans R2 resistant to the natural herbicide cyanobacterin. Plant Sci 60:149–154

    Article  CAS  Google Scholar 

  • Marin K, Zuther E, Kerstan T, Kunert A, Hagemann M (1998) The ggpS gene from Synechocystis sp. strain PCC 6803 encoding glucosyl-glycerol-phosphate synthase is involved in osmolyte synthesis. J Bacteriol 180:4843–4849

    PubMed  CAS  Google Scholar 

  • Matthijs HC, Jeanjean R, Yeremenko N, Huiwman J, Joset F, Hellingwerf KJ (2002) Hypothesis: versatile function of ferredoxin-NADP+ reductase in cyanobacteria provides regulation for transient photosystem I-driven cyclic electron transport. Funct Plant Biol 29:201–210

    Article  CAS  Google Scholar 

  • Meunier PC, Colon-Lopez MS, Sherman LA (1997) Temporal changes in state transitions and photosystem organization in the unicellular, diazotrophic cyanobacterium Cyanothece sp. ATCC 51142. Plant Physiol 115:991–1000

    PubMed  CAS  Google Scholar 

  • Michel KP, Berry S, Hifney A, Pistorius EK (2003) Adaptation to iron deficiency: a comparison between the cyanobacterium Synechococcus elongatus PCC 7942 wild-type and a DpsA-free mutant. Photosynth Res 75:71–84

    Article  PubMed  CAS  Google Scholar 

  • Michel KP, Krüger F, Pühler A, Pistorius EK (1999) Molecular characterization of idiA and adjacent genes in the cyanobacteria Synechococcus sp. strains PCC 6301 and PCC 7942. Microbiology 145:1473–1484

    PubMed  CAS  Google Scholar 

  • Michel KP, Pistorius EK (2004) Adaptation of the photosynthetic electron transport chain in cyanobacteria to iron deficiency: the function of IdiA and IsiA. Physiol Plant 119:1–15

    Google Scholar 

  • Michel KP, Pistorius EK, Golden SS (2001) Unusual regulatory elements for iron deficiency induction of the idiA gene of Synechococcus elongatus PCC 7942. J Bacteriol 183:5015–5024

    Article  PubMed  CAS  Google Scholar 

  • Michel KP, Thole HH, Pistorius EK (1996) IdiA, a 34 kDa protein in the cyanobacteria Synechococcus sp. strains PCC 6301 and PCC 7942, is required for growth under iron and manganese limitations. Microbiology 142:2635–2645

    Article  PubMed  CAS  Google Scholar 

  • Mullineaux CW, Allen F (1990) State 1–State 2 transitions in the cyanobacterium Synechococcus 6301 are controlled by the redox state of electron carriers between photosystem I and II. Photosynth Res 23:297–311

    Article  CAS  Google Scholar 

  • Nield J, Morris EP, Bibby TS, Barber J (2003) Structural analysis of the photosystem I supercomplex of cyanobacteria induced by iron deficiency. Biochemistry 42:3180–3188

    Article  PubMed  CAS  Google Scholar 

  • Nomura M, Ishitani M, Takabe T, Rai AK (1995) Synechococcus sp. PCC7942 transformed with Escherichia coli bet genes produces glycine betaine from choline and acquires resistance to salt stress. Plant Physiol 107:703–708

    PubMed  CAS  Google Scholar 

  • Oren A (2000) Salts and brines. In: Whitton BA, Potts M (eds) The ecology of cyanobacteria: their diversity in time and space. Kluwer Academic Publishers, Dordrecht, pp 281–306

    Google Scholar 

  • Reed RH, Stewart WDP (1988) The responses of cyanobacteria to salt stress. In: Rogers LJ, Gallon JR (eds) Biochemistry of algae and cyanobacteria. Europe TPSo Oxford Science Publisher, Oxford, pp 217–231

    Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual 2 edn. Cold Spring Harbor Laboratory, New York

    Google Scholar 

  • Schaegger H, von Jagow G (1987) Tricine-sodium dodecylsulphate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166:368–379

    Article  CAS  Google Scholar 

  • Stephan DP, Ruppel HG, Pistorius EK (2000) Interrelation between cyanophycin synthesis, l-arginine catabolism and photosynthesis in the cyanobacterium Synechocystis sp. strain PCC 6803. Z Naturforsch [C] 55:927–942

    CAS  Google Scholar 

  • Tölle J, Michel KP, Kruip J, Kahmann U, Preisfeld A, Pistorius EK (2002) Localization and function of the IdiA homologue Slr1295 in the cyanobacterium Synechocystis sp. strain PCC 6803. Microbiology 148:3293–3305

    PubMed  Google Scholar 

  • van Thor JJ, Jeanjean R, Havaux M, Sjollema KA, Joset F, Hellingwerf KJ, Matthijs HC (2000) Salt shock-inducible photosystem I cyclic electron transfer in Synechocystis PCC6803 relies on binding of ferredoxin:NADP(+) reductase to the thylakoid membranes via its CpcD phycobilisome-linker homologous N-terminal domain. Biochim Biophys Acta 1457:129–144

    Article  PubMed  Google Scholar 

  • Vinnemeier J, Hagemann M (1999) Identification of salt-regulated genes in the genome of the cyanobacterium Synechocystis sp. strain PCC 6803 by subtractive RNA hybridization. Arch Microbiol 172:377–386

    Article  PubMed  CAS  Google Scholar 

  • Vinnemeier J, Kunert A, Hagemann M (1998) Transcriptional analysis of the isiAB operon in salt-stressed cells of the cyanobacterium Synechocystis sp. PCC 6803. FEMS Microbiol Lett 169:323–330

    Article  PubMed  CAS  Google Scholar 

  • Waditee R, Hibino T, Nakamura T, Incharoensakdi A, Takabe T (2002) Overexpression of a Na+/H+ antiporter confers salt tolerance on a freshwater cyanobacterium, making it capable of growth in sea water. PNAS 99:4109–4114

    Article  PubMed  CAS  Google Scholar 

  • Yeremenko N, Jeanjean R, Prommeenate P, Krasikov V, Nixon PJ, Vermaas WF, Havaux M, Matthijs HC (2005) Open reading frame ssr2016 is required for antimycin A-sensitive photosystem I-driven cyclic electron flow in the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 46:1433–1436

    Article  PubMed  CAS  Google Scholar 

  • Yousef N, Pistorius EK, Michel KP (2003) Comparative analysis of idiA and isiA transcription under iron starvation and oxidative stress in Synechococcus elongatus PCC 7942 wild type and selected mutants. Arch Microbiol 180:471–483

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The fellowship of the Humboldt Foundation to Prof. Dr. S. N. Bagchi and the financial support of the DFG are gratefully acknowledged. Moreover, we thank Prof. Dr. W. Hess, Prof. Dr. G. S. Bullerjahn, and Dr. J. Kruip for the kind gift of the anti-IsiA, the anti-DpsA, and the anti-PsaAB antisera. Bentazone was a kind gift of Dr. Kirstgen of the BASF.

Author information

Author notes

  1. Suvendra N. Bagchi

    Present address: Department of Biological Sciences, Rani Durgavati University, Jabalpur, 482001, India

Authors and Affiliations

  1. BioVIII: Lehrstuhl für Molekulare Zellphysiologie, Fakultät für Biologie, Universität Bielefeld, Universitätsstr. 25, Bielefeld, 33615, Germany

    Suvendra N. Bagchi, Tatjana Bitz, Elfriede K. Pistorius & Klaus-Peter Michel

Authors
  1. Suvendra N. Bagchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tatjana Bitz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Elfriede K. Pistorius
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Klaus-Peter Michel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Klaus-Peter Michel.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bagchi, S.N., Bitz, T., Pistorius, E.K. et al. A Synechococcus elongatus PCC 7942 mutant with a higher tolerance toward the herbicide bentazone also confers resistance to sodium chloride stress. Photosynth Res 92, 87–101 (2007). https://doi.org/10.1007/s11120-007-9176-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-007-9176-y

Keywords

Search

Navigation