Skip to main content
SpringerLink
Log in

Impairment of ntcA gene revealed its role in regulating iron homeostasis, ROS production and cellular phenotype under iron deficiency in cyanobacterium Anabaena sp. PCC 7120

  • Original Paper
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Iron deficiency ends up into several unavoidable consequences including damaging oxidative stress in cyanobacteria. NtcA is a global nitrogen regulator controls wide range of metabolisms in addition to regulation of nitrogen metabolism. In present communication, NtcA based regulation of iron homeostasis, ROS production and cellular phenotype under iron deficiency in Anabaena 7120 has been investigated. NtcA regulates the concentration dependent iron uptake by controlling the expression of furA gene. NtcA also regulated pigment synthesis and phenotypic alterations in Anabaena 7120. A significant increase in ROS production and corresponding reduction in the activities of antioxidative enzymes (SOD, CAT, APX and GR) in CSE2 mutant strain in contrast to wild type Anabaena 7120 also suggested the possible involvement of NtcA in protection against oxidative stress in iron deficiency. NtcA has no impact on the expression of furB and furC in spite of presence of consensus NtcA binding site (NBS) and −10 boxes in their promoter. NtcA also regulates the thylakoid arrangement as well as related photosynthetic and respiration rates under iron deficiency in Anabaena 7120. Overall results suggested that NtcA regulates iron acquisition and in turn protect Anabaena cells from the damaging effects of oxidative stress induced under iron deficiency.

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

Similar content being viewed by others

References

  • Adams DG (2000) Heterocyst formation in cyanobacteria. Curr Opin Microbiol 3:618–624

    Article  CAS  Google Scholar 

  • Andrews SC, Robinson AK, Rodríguez-Quiñones F (2003) Bacterial iron homeostasis. FEMS Microbiol Rev 27:215–237

    Article  CAS  Google Scholar 

  • Averil BA, Orme-Johnson WH (1978) Iron sulphur protein and their synthetic analogue. In: Siegal H (ed) Metal in biological systems. Marcel Dakker, New York, pp 1387

    Google Scholar 

  • Banerjee M, Raghvan PS, Ballall A, Rajaram H, Apte SK (2013) Oxidative stress management in the filamentous, heterocystous, diazotrophic cyanobacterium, Anabaena PCC 7120. Photosyn Res 118:59–70

    Article  CAS  Google Scholar 

  • Chance B, Maehly AC (1955) Assay of catalase and peroxidases. Met Enzymol 2:764–775

    Article  Google Scholar 

  • Cheng Y, Li JH, Shi L, Wang L, Latifi A, Zhang CC (2006) A pair of iron-responsive genes encoding protein kinases with a Ser/Thr kinase domain and a His kinase domain are regulated by NtcA in the cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 188:4822–4829

    Article  CAS  Google Scholar 

  • Chiang SM, Schellhorn HE (2012) Regulators of oxidative stress response genes in Escherichia coli and their functional conservation in bacteria. Arch Biochem Biophys 525:161–169

    Article  CAS  Google Scholar 

  • Chong W, Kong HN, Wang HZ, Wu HD, Lin Y, He SB (2010) Effects of Iron on Growth and Intracellular Chemical Contents of Microcystis aeruginosa. Biomed Environ Sci 23:48–52

    Article  Google Scholar 

  • Cornelis P, Andrews SC (2010) Iron uptake and homeostasis in microorganisms. Caister Academic Press, Norfolk.

    Google Scholar 

  • Dewan PC, Anantharaman A, Chauhan VS, Sahal D (2009) Antimicrobial action of prototypic amphipathic cationic decapeptides and their branched dimers. Biochemistry 48:6542–6557

    Article  Google Scholar 

  • Dionisio-Sese MI, Tobita S (1998) Antioxidant response of rice seedlings to salinity stress. Plant Sci 135:1–9

    Article  CAS  Google Scholar 

  • Ferriera F, Straus NA (1994) Iron deprivation in cyanobacteria. J App Phycol 6:199–210

    Article  Google Scholar 

  • Frías JE, Flores E, Herrero A (1994) Requirement of the regulatory protein NtcA for the expression of nitrogen assimilation and heterocyst development genes in the cyanobacterium Anabaena sp. PCC 7120. Mol Microbiol 14:823–832

    Article  Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutase, I. Occurrence in higher plants. Plant Physiol 59:309–314

    Article  CAS  Google Scholar 

  • Gonzalez A, Bes MT, Barja F, Peleato ML, Fillat MF (2010) Overexpression of FurA in Anabaena sp. PCC 7120 reveals new targets for this regulator involved in photosynthesis, iron uptake and cellular morphology. Plant Cell Physiol 51:1900–1914

    Article  CAS  Google Scholar 

  • Gonzalez A, Bes MT, Peleato ML, Fillat MF (2011) Unraveling the regulatory function of FurA in Anabaena sp. PCC 7120 through 2-D DIGE proteomic analysis. J Proteom 74:660–671

    Article  CAS  Google Scholar 

  • Gonzalez A, Bes MT, Valladares A, Peleato ML, Fillat MF (2012) FurA is the master regulator of iron homeostasis and modulates the expression of tetrapyrrole biosynthesis genes in Anabaena sp. PCC 7120. Environ Microbiol 14:3175–3187

    Article  CAS  Google Scholar 

  • Hackenberg C, Engelhardt A, Matthijs HCP, Wittink F, Bauwe H, Kaplan A, Hagemann M (2009) Photorespiratory 2-phosphoglycolate metabolism and photoreduction of O2 cooperate in high-light acclimation of Synechocystis sp. strain PCC 6803. Planta 230:625–637

    Article  CAS  Google Scholar 

  • He YY, Hader DP (2002) Involvement of reactive oxygen species in the UV-B damage to the cyanobacterium Anabaena sp. J Photochem Photobiol B 66:73–80

    Article  CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  CAS  Google Scholar 

  • Herrero A, Muro-Pastor AM, Flores E (2001) Nitrogen control in cyanobacteria. J Bacteriol 183:411–425

    Article  CAS  Google Scholar 

  • Herrero A, Muro-Pastor AM, Valladares A, Flores E (2004) Cellular differentiation and the NtcA transcription factor in filamentous cyanobacteria. FEMS Microbiol Rev 28:469–487

    Article  CAS  Google Scholar 

  • Hyenstrand P, Rydin E, Gunnerhed M (2000) Response of pelagic cyanobacteria to iron additions-enclosure experiments from Lake Erken. J Plankton Res 22:1113–1126

    Article  CAS  Google Scholar 

  • Kaniuga Z (2008) Chilling response of plants: importance of galactolipase, free fatty acids and free radicals. Plant Biol 10:171–184

    Article  CAS  Google Scholar 

  • Kaushik MS, Mishra AK (2015) Iron induced physiological and biochemical modification in wild type and ntcA impaired mutant of Anabaena sp. PCC 7120. Indian J Biotechnol 14:87–93

    CAS  Google Scholar 

  • Kaushik MS, Srivastava M, Verma E, Mishra AK (2015a) Role of manganese in protection against oxidative stress under iron starvation in cyanobacterium Anabaena 7120. J Basic Microbiol 54:1–12

    Google Scholar 

  • Kaushik MS, Singh P, Tiwari B, Mishra AK (2015b) Ferric uptake regulator (FUR) protein: properties and implications in cyanobacteria. Ann Microbiol 66:61–75

    Article  Google Scholar 

  • Latifi A, Jeanjean R, Lemeille S, Havaux M, Zhang CC (2005) Iron starvation leads to oxidative stress in Anabaena sp. strain PCC 7120. J Bacteriol 187:6596–6598

    Article  CAS  Google Scholar 

  • Lein S (1978) Hill reaction and phosphorylation with chloroplast preparation from Chlamydomonas reinhardtii. In: Hellebust JA, Craigie JS (eds) Handbook of phycological method: physiological and biochemical methods. Cambridge University Press, Cambridge, pp 305–315

  • Lopez-Gomollon S, Hernandez JA, Wolk CP, Peleato ML, Fillat MF (2007a) Expression of FurA is modulated by NtcA and strongly enhanced in heterocysts of Anabaena sp. PCC 7120. Microbiology 153:42–50

    Article  CAS  Google Scholar 

  • Lopez-Gomollon S, Hernandez JA, Pellicer S, Angarica VE, Peleato ML, Fillat MF (2007b) Cross-talk between iron and nitrogen regulatory networks in Anabaena (Nostoc) sp. PCC 7120: identification of overlapping genes in furA and ntcA regulons. J Mol Biol 374:267–281

    Article  CAS  Google Scholar 

  • Moore K, Roberts LJ (1998) Measurement of lipid peroxidation. Free Radic Res 28:659–671

    Article  CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Narayan OP, Kumari N, Rai LC (2011) Iron starvation-induced proteomic changes in Anabaena (Nostoc) sp. PCC 7120: exploring survival strategy. J Microbiol Biotechnol 21(2):136–146

    Article  CAS  Google Scholar 

  • Ng CF, Schafer FQ, Buettner GR, VGJ (2007) The rate of cellular hydrogen peroxide removal shows dependency on GSH: Mathematical insight into in vivo H2O2 and GPx concentration. Free Radic Res 41(11):1201–1211

    Article  CAS  Google Scholar 

  • Nicolaisen K, Moslavac S, Samborski A, Valdebenito M, Hantke K, Maldener I, Muro-Pastor AM, Flores E, Schleiff E (2008) Alr0397 is an outer membrane transporter for the siderophore schizokinen in Anabaena sp. strain PCC 7120. J Bacteriol 190:7500–7507

    Article  CAS  Google Scholar 

  • Öquist G (1971) Changes in pigment composition and photosynthesis induced by iron deficiency in the blue-green algae Anacystis nidulans. Physiol Plant 25:188–191

    Article  Google Scholar 

  • Öquist G (1974a) Iron deficiency in the blue-green algae Anacystis nidulans. Physiol Plant 30:30–37

    Article  Google Scholar 

  • Öquist G (1974b) Iron deficiency in the blue-green algae Anacystis nidulans: Fluorescence and absorption spectra recorded at 77 K. Physiol Plant 31:55–58

    Article  Google Scholar 

  • Paerl HW, Fulton RS, Moisander PH (2001) Harmful freshwater algal blooms, with an emphasis on cyanobacteria. Sci World 1:76–113

    Article  CAS  Google Scholar 

  • Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61

    Google Scholar 

  • Sagisaka S (1976) The occurrence of peroxide in perennial plant Populas gebrica. Plant Physiol 57:308–309

    Article  CAS  Google Scholar 

  • Sandström S, Ivanov AG, Park YI, Öquist G, Gustafsson P (2002) Iron stress responses in the cyanobacterium Synechococcus sp. PCC 7942. Physiol Plant 116:255–263

    Article  Google Scholar 

  • Schaedle M, Bassham JA (1977) Chloroplasts glutathione reductase. Plant Physiol 59:1011–1012

    Article  CAS  Google Scholar 

  • Schopf JW (2000) The fossil record: tracing the roots of the cyanobacterial lineage. In: Whitton BA, Potts M (eds) The ecology of Cyanobacteria. Their diversity in time and space. Kluwer, Dordrecht, pp 13–35

    Google Scholar 

  • Sein-Echaluce VC, Gonzalez A, Napolitano M, Luque I, Barja F, Peleato ML, Fillat MF (2015) Zur (FurB) is a key factor in the control of the oxidative stress response in Anabaena sp. PCC 7120. Environ Microbiol 17(6):2006–2017

    Article  CAS  Google Scholar 

  • Singh SP, Sinha RP, Klisch M, Häder DP (2008) Mycosporine-like amino acids (MAAs) profile of a rice-field cyanobacterium Anabaena doliolum as influenced by PAR and UVR. Planta 229:225–233

    Article  CAS  Google Scholar 

  • Singh P, Kaushik MS, Srivastava M, Mishra AK (2014) Phylogenetic analysis of heterocystous cyanobacteria (subsections IVand V) using highly iterated palindromes as molecular markers. Physiol Mol Biol Plants 20(3):331–342.

    Article  CAS  Google Scholar 

  • Singh A, Kaushik MS, Srivastava M, Tiwari DN, Mishra AK (2016) Siderophore mediated attenuation of cadmium toxicity by paddy field cyanobacterium Anabaena oryzae. Algal Res 16:63–68

    Article  Google Scholar 

  • Speranza A, Crinelli R, Scoccianti V, Geitmann A (2012) Reactive oxygen species are involved in pollen tube initiation in kiwifruit. Plant Biol 14:64–76

    CAS  Google Scholar 

  • Stingaciu LR, O’Neill H, Liberton M, Urban VS, Pakrasi HB, Ohl M (2016) Revealing the dynamics of thylakoid membranes in living cyanobacterial cells. Nature 6:19627

    CAS  Google Scholar 

  • Stohs SJ, Bagchi D (1995) Oxidative mechanisms in the toxicity of metal ions. Free Radic Biol Med 18:321–336

    Article  CAS  Google Scholar 

  • Straus NA (1994) Iron deprivation: physiology and gene regulation. In: Bryant DA (ed) The molecular biology of cyanobacteria. Kluwer Academic Publisher, The Netherlands, pp 731–750

    Chapter  Google Scholar 

  • Su Z, Olman V, Mao F, Xu Y (2005) Comparative genomics analysis of NtcA regulons in cyanobacteria: regulation of nitrogen assimilation and its coupling to photosynthesis. Nucleic Acids Res 33:5156–5171

    Article  CAS  Google Scholar 

  • Tripathi K, Sharma NK, Kageyama K, Takabe T, Rai AK (2013) Physiological, biochemical and molecular responses of the halophilic cyanobacterium Aphanothece halophytica to Pi-deficiency. Eur J Phycol 48(4):461–473

    Article  CAS  Google Scholar 

  • Valladares A, Muro-Pastor AM, Fillat MF, Herrero A, Flores E (1999) Constitutive and nitrogen-regulated promoters of the petH gene encoding ferredoxin:NADP+ reductase in the heterocyst forming cyanobacterium Anabaena sp. FEBS Lett 449:159–164

    Article  CAS  Google Scholar 

  • Vioque A (1992) Analysis of the gene encoding the RNA subunit of ribonuclease P from cyanobacteria. Nucleic Acids Res 20:6331–6337

    Article  CAS  Google Scholar 

  • Waibel AH, Hanazawa T, Hinton GE, Shikano K, Lang KJ (1989) Phoneme recognition using time-delay neural networks. IEEE Trans Acoust Speech Signal Process 37(3):328–339

    Article  Google Scholar 

  • Wang AG, Luo GH (2002) Quantitative relation between the reaction of hydroxylamine and superoxide anion radicals in plants. Plant Physiol Commun 26:55–57

    CAS  Google Scholar 

  • Wei TF, Ramasubramanian TS, Golden JW (1994) Anabaena sp. strain PCC 7120 ntcA gene required for growth on nitrate and heterocyst development. J Bacteriol 176:4473–4482

    Article  CAS  Google Scholar 

  • Xu W-L, Jeanjean R, Liu Y-D, Zhang CC (2003) pkn22 (alr2502) encoding a putative Ser/Thr kinase in the cyanobacterium Anabaena sp. PCC 7120 is induced by both iron starvation and oxidative stress and regulates the expression of isiA. FEBS Lett 553:179–182

    Article  CAS  Google Scholar 

  • Yingping F, Lemeille S, González A, Risoul V, Denis Y, Richaud P, Lamrabet O, Fillat MF, Zhang CC, Latifi A (2015) The Pkn22 Ser/Thr kinase in Nostoc PCC 7120: role of FurA and NtcA regulators and transcript profiling under nitrogen starvation and oxidative stress. BMC Genom 16:557

    Article  Google Scholar 

Download references

Acknowledgements

The Head, Department of Botany, Banaras Hindu University, Varanasi, India is gratefully acknowledged for providing laboratory facilities. Authors are also thankful to University Grant Commission and Council of Scientific and Industrial Research (Grant No. 38(1316)/12/EMR-II), New Delhi for providing financial assistance in the form of fellowship (JRF). Advance Instrumentation Research Facility, Jawaharlal Nehru University, New Delhi and Interdisciplinary School of Life Sciences, Banaras Hindu University, Varanasi has been greatly acknowledged for providing Scanning Electron Microscopy (SEM) and Fluorescence Microscopy facility for this work.

Author information

Authors and Affiliations

  1. Laboratory of Microbial Genetics, Department of Botany, Banaras Hindu University, Varanasi, 221005, India

    Manish Singh Kaushik, Meenakshi Srivastava, Anumeha Singh & Arun Kumar Mishra

Authors
  1. Manish Singh Kaushik
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Meenakshi Srivastava
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anumeha Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Arun Kumar Mishra
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Arun Kumar Mishra.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kaushik, M.S., Srivastava, M., Singh, A. et al. Impairment of ntcA gene revealed its role in regulating iron homeostasis, ROS production and cellular phenotype under iron deficiency in cyanobacterium Anabaena sp. PCC 7120. World J Microbiol Biotechnol 33, 158 (2017). https://doi.org/10.1007/s11274-017-2323-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11274-017-2323-5

Keywords

Search

Navigation