Skip to main content
SpringerLink
Log in

Oxidative stress management in the filamentous, heterocystous, diazotrophic cyanobacterium, Anabaena PCC7120

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

Abstract

Reactive oxygen species (ROS) are inevitably generated as by-products of respiratory/photosynthetic electron transport in oxygenic photoautotrophs. Unless effectively scavenged, these ROS can damage all cellular components. The filamentous, heterocystous, nitrogen-fixing strains of the cyanobacterium, Anabaena, serve as naturally abundant contributors of nitrogen biofertilizers in tropical rice paddy fields. Anabaena strains are known to tolerate several abiotic stresses, such as heat, UV, gamma radiation, desiccation, etc., that are known to generate ROS. ROS are detoxified by specific antioxidant enzymes like superoxide dismutases (SOD), catalases and peroxiredoxins. The genome of Anabaena PCC7120 encodes two SODs, two catalases and seven peroxiredoxins, indicating the presence of an elaborate antioxidant enzymatic machinery to defend its cellular components from ROS. This article summarizes recent findings and depicts important perspectives in oxidative stress management in Anabaena PCC7120.

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

Similar content being viewed by others

References

  • Alquéres SM, Oliveira JH, Nogueira EM, Guedes HV, Oliveira PL, Câmara F, Baldani JI, Martins OB (2010) Antioxidant pathways are up-regulated during biological nitrogen fixation to prevent ROS-induced nitrogenase inhibition in Gluconacetobacter diazotrophicus. Arch Microbiol 192:835–841

    Article  PubMed  Google Scholar 

  • Andrews SC (2010) The ferritin-like superfamily: evolution of the biological iron storeman from a rubreythrin-like ancestor. Biochim Biophys Acta 1800:691–705

    Article  PubMed  CAS  Google Scholar 

  • Apte SK (2001) Coping with salinity/water stress: cyanobacteria show the way. Proc Indian Natl Sci Acad B 67:285–310

    Google Scholar 

  • Asada K (1994) Production and action of active oxygen species in photosynthesis tissues. In: Foyer CH, Mullineaux PM (eds) Causes of photooxidative stress and amelioration of defence systems in plants. CRC Press Inc., Boca Raton, pp 77–104

    Google Scholar 

  • Atzenhofer W, Regelsberger G, Jacob U, Peschek G, Furtmüller P, Huber R, Obinger C (2002) The 2.0A resolution structure of the catalytic portion of a cyanobacterial membrane-bound manganese superoxide dismutase. J Mol Biol 3213:479–489

    Article  Google Scholar 

  • Banerjee M, Ballal A, Apte SK (2012a) A novel glutaredoxin domain-containing peroxiredoxin ‘All1541’ protects the N2-fixing cyanobacterium Anabaena PCC7120 from oxidative stress. Biochem J 442:671–680

    Article  PubMed  CAS  Google Scholar 

  • Banerjee M, Ballal A, Apte SK (2012b) Mn-catalase (Alr0998) protects the photosynthetic, nitrogenfixing cyanobacterium Anabaena PCC7120 from oxidative stress. Environ Microbiol 14:2891–2900

    Article  PubMed  CAS  Google Scholar 

  • Benov L, Fridovich I (1999) Why superoxide imposes an aromatic amino acid auxotrophy in Escherichia coli. J Biol Chem 274:4202–4206

    Article  PubMed  CAS  Google Scholar 

  • Bernroitner M, Zamocky M, Furtmüller PG, Peschek GA, Obinger C (2009) Occurrence, phylogeny, structure, and function of catalases and peroxidases in cyanobacteria. J Exp Bot 60:423–440

    Article  PubMed  CAS  Google Scholar 

  • Bhargava P, Atri N, Srivastava AK, Rai LC (2007) Cadmium mitigates ultraviolet-B stress in Anabaena doliolum: enzymatic and non-enzymatic antioxidants. Biol Plant 51:546–555

    Article  CAS  Google Scholar 

  • Boileau C, Eme L, Brochier-Armanet C, Janicki A, Zhang CC, Latifi A (2011) A eukaryotic-like sulfiredoxin involved in oxidative stress responses and in the reduction of the sulfinic form of 2-Cys peroxiredoxin in the cyanobacterium Anabaena PCC7120. New Phytol 191:1108–1118

    Article  PubMed  CAS  Google Scholar 

  • Brock TD (1973) Evolutionary and ecological aspects of cyanophytes. In: Carr NG, Whitton BA (eds) The biology of blue-green algae. Blackwell, Oxford, pp 487–500

    Google Scholar 

  • Caiola MG, Canini A, Galiazzo F, Rotilio G (1991) Superoxide dismutase in vegetative cells, heterocysts and akinetes of Anabaena cylindrica Lemm. FEMS Microbiol Lett 80:161–165

    Article  Google Scholar 

  • Campbell WS, Laudenbach DE (1995) Characterization of four superoxide dismutase genes from a filamentous cyanobacterium. J Bacteriol 177:964–972

    PubMed  CAS  Google Scholar 

  • Cha M, Hong SK, Kim IH (2007) Four thiol peroxidases contain a conserved GCT catalytic motif and act as a versatile array of lipid peroxidases in Anabaena sp. PCC7120. Free Radic Biol Med 42:1736–1748

    Article  PubMed  CAS  Google Scholar 

  • Choudhury S, Panda P, Sahoo L, Panda SK. (2013) Reactive oxygen species signaling in plants under abiotic stress. Plant Signal Behav 8(4). pii: e23681

  • Cui H, Wang Y, Wang Y, Qin S (2012) Genome-wide analysis of putative peroxiredoxin in unicellular and filamentous cyanobacteria. BMC Evol Biol 12:220. doi:10.1186/1471-2148-12-220

    Article  PubMed  CAS  Google Scholar 

  • Dadheech N (2010) Desiccation tolerance in cyanobacteria. Afr J Microbiol Res 4:1584–1593

    CAS  Google Scholar 

  • Fay P (1992) Oxygen relations of nitrogen fixation in cyanobacteria. Microbiol Rev 56:340–373

    PubMed  CAS  Google Scholar 

  • Fridovich I (1997) Superoxide anion radical (O2−•), superoxide dismutases, and related matters. J Biol Chem 272:18515–18517

    Article  PubMed  CAS  Google Scholar 

  • Friedmann EI, Galun M (1974) Desert algae, lichens and fungi. In: Brown GW Jr (ed) Desert biology, vol 2. Academic Press, London, pp 165–212

    Google Scholar 

  • González A, Bes MT, Peleato ML, Fillat MF (2011) Unravelling the regulatory function of FurA in Anabaena sp. PCC7120 through 2-D DIGE proteomic analysis. J Proteomics 74:660–671

    Article  PubMed  Google Scholar 

  • Halliwell B, Gutteridge JMC (1986) Oxygen free radicals and iron in relation to biology and medicine: some problems and concepts. Arch Biochem Biophys 246:501–514

    Article  PubMed  CAS  Google Scholar 

  • Haselkorn R (1978) Heterocysts. Ann Rev Plant Physiol 29:319–344

    Article  CAS  Google Scholar 

  • Henry LE, Gogotov IN, Hall DO (1978) Superoxide dismutase and catalase in the protection of the proton-donating systems of nitrogen fixation in the blue-green alga Anabaena cylindrica. Biochem J 174:373–377

    PubMed  CAS  Google Scholar 

  • Herbert SK, Samson G, Fork DC, Laudenbach DE (1992) Characterization of damage to photosystems I and II in a cyanobacterium lacking detectable iron superoxide dismutase activity. Proc Natl Acad Sci USA 89:8716–8720

    Article  PubMed  CAS  Google Scholar 

  • Hernández JA, Pellicer S, Huang L, Peleato ML, Fillat MF (2007) FurA modulates gene expression of alr3808, a DpsA homologue in Nostoc (Anabaena) sp. PCC7120. FEBS Lett 581:1351–1356

    Article  PubMed  Google Scholar 

  • Hosoya-Matsuda N, Motohashi K, Yoshimura H, Nozaki A, Inoue K, Ohmori M, Hisabori T (2005) Anti-oxidative stress system in cyanobacteria. Significance of type II peroxiredoxin and the role of 1-Cys peroxiredoxin in Synechocystis sp. strain PCC 6803. J Biol Chem 280:840–846

    PubMed  CAS  Google Scholar 

  • Imlay JA (2003) Pathways of oxidative damage. Annu Rev Microbiol 57:395–418

    Article  PubMed  CAS  Google Scholar 

  • Jakopitsch C, Rüker F, Regelsberger G, Dockal M, Peschek GA, Obinger C (1999) Catalase-peroxidase from the cyanobacterium Synechocystis PCC 6803: cloning, overexpression in Escherichia coli, and kinetic characterization. Biol Chem 380:1087–1096

    Article  PubMed  CAS  Google Scholar 

  • Kagawa M, Murakoshi N, Nishikawa Y, Matsumoto G, Kurata Y, Mizobata T, Kawata Y, Nagai J (1999) Purification and cloning of a thermostable manganese catalase from a thermophilic bacterium. Arch Biochem Biophys 362:346–355

    Article  PubMed  CAS  Google Scholar 

  • Katoh H (2012) Desiccation-inducible genes are related to N(2)-fixing system under desiccation in a terrestrial cyanobacterium. Biochim Biophys Acta 1817:1263–1269

    Article  PubMed  CAS  Google Scholar 

  • Katoh H, Asthana RK, Ohmori M (2004) Gene expression in the cyanobacterium Anabaena sp. PCC7120 under desiccation. Microb Ecol 47:164–174

    Article  PubMed  CAS  Google Scholar 

  • Kim JH, Suh KH (2005) Light-dependent expression of superoxide dismutase from cyanobacteriumSynechocystis sp. strain PCC 6803. Arch Microbiol 183:218–223

    Article  PubMed  CAS  Google Scholar 

  • Kim SJ, Woo JR, Hwang YS, Jeong DG, Shin DH, Kim K, Ryu SE (2003) The tetrameric structure of Haemophilus influenza hybrid Prx5 reveals interactions between electron donor and acceptor proteins. J Biol Chem 278:10790–10798

    Article  PubMed  CAS  Google Scholar 

  • Kumsta C, Jakob U (2009) Redox-regulated chaperones. Biochemistry. 48:4666–4676 (Review)

    Article  PubMed  CAS  Google Scholar 

  • Latifi A, Ruiz M, Jeanjean R, Zhang CC (2007) PrxQ-A, a member of the peroxiredoxin Q family, plays a major role in defense against oxidative stress in the cyanobacterium Anabaena sp. strain PCC7120. Free Radic Biol Med 2:424–431

    Article  Google Scholar 

  • Li T, Huang X, Zhou R, Liu Y, Li B, Nomura C, Zhao J (2002) Differential expression and localization of Mn and Fe superoxide dismutases in the heterocystous cyanobacterium Anabaena sp. strain PCC7120. J Bacteriol 184:5096–5103

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Zhou R, Zhao J (2000) Molecular cloning and sequencing of the sodB gene from a heterocystous cyanobacterium Anabaena sp. PCC7120. Biochim Biophys Acta 1491:248–252

    Article  PubMed  CAS  Google Scholar 

  • Mallick N, Lai LC (1999) Response of the antioxidant systems of the nitrogen fixing cyanobacterium Anabaena doliolum to copper. J Plant Physiol 155:146–149

    Article  CAS  Google Scholar 

  • Mella-Flores D, Six C, Ratin M, Partensky F, Boutte C, Le Corguillé G, Marie D, Blot N, Gourvil P, Kolowrat C, Garczarek K (2012) Prochlorococcus and Synechococcus have evolved different adaptive mechanisms to cope with light and UV stress. Front Microbiol 3:285

    Article  PubMed  CAS  Google Scholar 

  • Mishra Y, Chaurasia N, Rai LC (2009) AhpC (alkyl hydroperoxide reductase) from Anabaena sp. PCC7120 protects Escherichia coli from multiple abiotic stresses. Biochem Biophys Res Commun 381:606–611

    Article  PubMed  CAS  Google Scholar 

  • Mittler R, Tel-Or E (1991) Oxidative stress responses in the unicellular cyanobacterium Synechococcus PCC 7942. Free Radic Res Commun 12–13(Pt 2):845–850

    Article  PubMed  Google Scholar 

  • Miyake C, Michihata F, Asada Kozi (1990) Scavenging of hydrogen peroxide in prokaryotic and eukaryotic algae: acquisition of ascorbate peroxidase during the evolution of cyanobacteria. Plant Cell Physiol 32:33–43

    Google Scholar 

  • Murata N, Wada H (1995) Acyl-lipid desaturases and their importance in the tolerance and acclimatization of cold cyanobacteria. Biochem J 308:1–8

    PubMed  CAS  Google Scholar 

  • Mutsuda M, Ishikawa T, Takeda T, Shigeoka S (1996) The catalase-peroxidase of Synechococcus PCC7942: purification, nucleotide sequence analysis and expression in Escherichia coli. Biochem J 316:251–257

    PubMed  CAS  Google Scholar 

  • Narayan OP, Kumari N, Rai LC (2010) Heterologous expression of Anabaena PCC7120 all3940 (a Dps family gene) protects Escherichia coli from nutrient limitation and abiotic stresses. Biochem Biophys Res Commun 394:163–169

    Article  PubMed  CAS  Google Scholar 

  • Narayan OP, Kumari N, Rai LC (2011) Iron starvation-induced proteomic changes in Anabaena (Nostoc) sp. PCC7120: exploring survival strategy. J Microbiol Biotechnol 21:136–146

    Article  PubMed  CAS  Google Scholar 

  • Nishiyama Y, Allakhverdiev SI, Murata N (2011) Protein synthesis is the primary target of reactive oxygen species in the photoinhibition of photosystem II. Physiol Plant 142:35–46

    Article  PubMed  CAS  Google Scholar 

  • Obinger C, Regelsberger G, Strasser G, Burner U, Peschek GA (1997) Purification and characterization of a homodimeric catalase-peroxidase from the cyanobacterium Anacystis nidulans. Biochem Biophys Res Commun 235:545–552

    Article  PubMed  CAS  Google Scholar 

  • Ogola HJ, Kamiike T, Hashimoto N, Ashida H, Ishikawa T, Shibata H, Sawa Y (2009) Molecular characterization of a novel peroxidase from the cyanobacterium Anabaena sp. strain PCC7120. Appl Environ Microbiol 75:7509–7518

    Article  PubMed  CAS  Google Scholar 

  • Pascual MB, Mata-Cabana A, Florencio FJ, Lindahl M, Cejudo FJ (2010) Overoxidation of 2-Cys peroxiredoxin in prokaryotes: cyanobacterial 2-Cys peroxiredoxins sensitive to oxidative stress. J Biol Chem 285:34485–34492

    Article  PubMed  CAS  Google Scholar 

  • Perelman A, Uzan A, Hacohen D, Schwarz R (2003) Oxidative stress in Synechococcus sp. strain PCC 7942: various mechanisms for H2O2 detoxification with different physiological roles. J Bacteriol 185:3654–3660

    Article  PubMed  CAS  Google Scholar 

  • Pérez-Pérez ME, Mata-Cabana A, Sánchez-Riego AM, Lindahl M, Florencio FJ (2009) A comprehensive analysis of the peroxiredoxin reduction system in the Cyanobacterium Synechocystis sp. strain PCC 6803 reveals that all five peroxiredoxins are thioredoxin dependent. J Bacteriol 191:7477–7489

    Article  PubMed  Google Scholar 

  • Priya B, Premanandh J, Dhanalakshmi RT, Seethalakshmi T, Uma L, Prabaharan D, Subramanian G (2007) Comparative analysis of cyanobacterial superoxide dismutases to discriminate canonical forms. BMC Genomics 8:435

    Article  PubMed  Google Scholar 

  • Raghavan PS, Rajaram H, Apte SK (2011) Nitrogen status dependent oxidative stress tolerance conferred by overexpression of MnSOD and FeSOD proteins in Anabaena sp. strain PCC7120. Plant Mol Biol 77:407–417

    Google Scholar 

  • Raghavan PS, Rajaram H and Apte SK (2013) N-terminal processing of membrane-targeted MnSOD and formation of multiple active SOD dimers in the nitrogen-fixing cyanobacterium, Anabaena sp strain PCC7120. FEBS J 280:4827–38

    Google Scholar 

  • Regelsberger G, Atzenhofer W, Ruker F, Peschek GA, Jakopitsch C, Paumann M, Furtmüller PG, Obinger C (2002) Biochemical characterization of a membrane-bound manganese-containing superoxide dismutase from the cyanobacterium Anabaena PCC7120. J Biol Chem 277:43615–43622

    Article  PubMed  CAS  Google Scholar 

  • Regelsberger G, Laaha U, Dietmann D, Rüker F, Canini A, Grilli-Caiola M, Furtmüller PG, Jakopitsch C, Peschek GA, Obinger C (2004) The iron superoxide dismutase from the filamentous cyanobacterium Nostoc PCC7120. Localization, overexpression, and biochemical characterization. J Biol Chem 279:44384–44393

    Article  PubMed  CAS  Google Scholar 

  • Robson RL, Postgate JR (1980) Oxygen and hydrogen in biological nitrogen fixation. Ann Rev Microbiol 34:183–207

    Article  CAS  Google Scholar 

  • Rochat T, Gratadoux JJ, Gruss A, Corthier G, Maguin E, Langella P, van de Guchte M (2006) Production of a heterologous nonheme catalase by Lactobacillus casei: an efficient tool for removal of H2O2 and protection of Lactobacillus bulgaricus from oxidative stress in milk. Appl Environ Microbiol 72:5143–5149

    Article  PubMed  CAS  Google Scholar 

  • Rouhier N, Gama F, Wingsle G, Gelhaye E, Gans P, Jacquot JP (2006) Engineering functional artificial hybrid proteins between poplar peroxiredoxin II and glutaredoxin or thioredoxin. Biochem Biophys Res Commun 341:1300–1308

    Article  PubMed  CAS  Google Scholar 

  • Sato N, Moriyama T, Toyoshima M, Mizusawa M, Tajima N (2012) The all0458/lti46.2 gene encodes a low temperature-induced Dps protein homologue in the cyanobacteria Anabaena sp. PCC7120 and Anabaena variabilis M3. Microbiol 158:2527–2536

    Article  CAS  Google Scholar 

  • Schopf JW (1975) Precambrian paleobiology: problems and perspectives. Ann Rev Earth Planet Sci 3:213–249

    Article  Google Scholar 

  • Shcolnick S, Summerfield TC, Reytman L, Sherman LA, Keren N (2009) The mechanism of iron homeostasis in the unicellular cyanobacterium Synechocystis sp. PCC6803 and its relationship to oxidative stress. Plant Physiol 150:2045–2056

    Article  PubMed  CAS  Google Scholar 

  • Shirkey B, Kovarcik DP, Wright DJ, Wilmoth G, Prickett TF, Helm RF, Gregory EM, Potts M (2000) Active Fe-containing superoxide dismutase and abundant sodF mRNA in Nostoc commune (cyanobacteria) after years of desiccation. J Bacteriol 182:189–197

    Article  PubMed  CAS  Google Scholar 

  • Shrivastava AK, Pandey S, Singh PK, Rai S, Rai LC (2012) alr0882 encoding a hypothetical protein of Anabaena PCC7120 protects Escherichia coli from nutrient starvation and abiotic stresses. Gene 511:248–255

    Article  PubMed  CAS  Google Scholar 

  • Singh H, Fernandes T, Apte SK (2010) Unusual radioresistance of nitrogen-fixing cultures of Anabaena strains. J Biosci 35:427–434

    Article  PubMed  Google Scholar 

  • Srivastava AK, Bhargava P, Thapar R, Rai LC (2009) Differential response of antioxidative defense system of Anabaena doliolum under arsenite and arsenate stress. J Basic Microbiol 49(Suppl 1):S63–S72

    Article  PubMed  Google Scholar 

  • Tel-Or E, Huflejt ME, Packer L (1986) Hydroperoxide metabolism in cyanobacteria. Arch Biochem Biophys 246:396–402

    Article  PubMed  CAS  Google Scholar 

  • Thomas DJ, Avenson TJ, Thomas JB, Herbert SK (1998) A cyanobacterium lacking iron superoxide dismutase is sensitized to oxidative stress induced with methyl viologen but is not sensitized to oxidative stress induced with norflurazon. Plant Physiol 116:1593–1602

    Article  PubMed  CAS  Google Scholar 

  • Thomas DJ, Thomas JB, Prier SD, Nasso NE, Herbert SK (1999) Iron superoxide dismutase protects against chilling damage in the cyanobacterium Synechococcus species PCC7942. Plant Physiol 120:275–282

    Article  PubMed  CAS  Google Scholar 

  • Tichy M, Vermaas W (1999) In vivo role of catalase-peroxidase in Synechocystis sp. strain PCC 6803. J Bacteriol 181:1875–1882

    PubMed  CAS  Google Scholar 

  • Ushimaru T, Nishiyama Y, Hayashi H, Murata N (2002) No coordinated transcriptional regulation of the sod-kat antioxidative system in Synechocystis sp. PCC 6803. J Plant Physiol 159:805–807

    Article  CAS  Google Scholar 

  • Vallyathan V, Shi X (1997) The role of oxygen free radicals in occupational and environmental lung diseases. Environ Health Perspect. 105(Suppl 1):165–177 (Review)

    Article  PubMed  CAS  Google Scholar 

  • Wei X, Mingjia H, Xiufeng L, Yang G, Qingyu W (2007) Identification and biochemical properties of Dps (starvation-induced DNA binding protein) from cyanobacterium Anabaena sp. PCC7120. IUBMB Life 59:675–681

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto H, Miyake C, Dietz KJ, Tomizawa K, Murata N, Yokota A (1999) Thioredoxin peroxidase in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett 447:269–273

    Article  PubMed  CAS  Google Scholar 

  • Zamocky M, Furtmüller PG, Obinger C (2008) Evolution of catalases from bacteria to humans. Antioxid Redox Signal 10:1527–1548

    Article  PubMed  CAS  Google Scholar 

  • Zhao W, Ye Z, Zhao JA (2007a) Membrane-associated Mn-superoxide dismutase protects the photosynthetic apparatus and nitrogenase from oxidative damage in the cyanobacterium Anabaena sp. PCC7120. Plant Cell Physiol 48:563–572

    Article  PubMed  CAS  Google Scholar 

  • Zhao W, Ye Z, Zhao J (2007b) RbrA, A cyanobacterial rubrerythrin, functions as a FNR-dependent peroxidase in heterocysts in protection of nitrogenase from damage by hydrogen peroxide in Anabaena sp. PCC7120. Mol Microbiol 665:1219–1230

    Article  Google Scholar 

  • Zheng Y, Boeglin WE, Schneider C, Brash AR (2008) A 49-kDa mini-lipoxygenase from Anabaena sp. PCC7120 retains catalytically complete functionality. J Biol Chem 283:5138–5147

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Molecular Biology Division, Bhabha Atomic Research Centre, Mumbai, 400 085, India

    Manisha Banerjee, Prashanth S. Raghavan, Anand Ballal, Hema Rajaram & S. K. Apte

Authors
  1. Manisha Banerjee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Prashanth S. Raghavan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anand Ballal
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hema Rajaram
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. K. Apte
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to S. K. Apte.

Additional information

Manisha Banerjee, Prashanth S. Raghavan have contributed equally to this manuscript.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Banerjee, M., Raghavan, P.S., Ballal, A. et al. Oxidative stress management in the filamentous, heterocystous, diazotrophic cyanobacterium, Anabaena PCC7120. Photosynth Res 118, 59–70 (2013). https://doi.org/10.1007/s11120-013-9929-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-013-9929-8

Keywords

Search

Navigation