Skip to main content
SpringerLink
Log in

Peroxide reduction by a metal-dependent catalase in Nostoc punctiforme (cyanobacteria)

  • Applied microbial and cell physiology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

This study investigated the role of a novel metal-dependent catalase (Npun_R4582) that reduces hydrogen peroxide in the cyanobacterium Nostoc punctiforme. Quantitative real-time PCR showed that npun_R4582 relative mRNA levels were upregulated by over 16-fold in cells treated with either 2 μM added Co, 0.5 μM added Cu, 500 μM Mn, 1 μM Ni, or 18 μM Zn. For cells treated with 60 μM H2O2, no significant alteration in Npun_R4582 relative mRNA levels was detected, while in cells treated with Co, Cu, Mn, Ni, or Zn and 60 μM peroxide, relative mRNA levels were generally above control or peroxide only treated cells. Disruption or overexpression of npun_R4582 altered sensitivity to cells exposed to 60 μM H2O2 and metals for treatments beyond the highest viable concentrations, or in a mixed metal solution for Npun_R4582− cells. Moreover, overexpression of npun_R4582 increased cellular peroxidase activity in comparison with wild-type and Npun_R4582− cells, and reduced peroxide levels by over 50%. The addition of cobalt, manganese, nickel, and zinc increased the capacity of Npun_R4582 to reduce the rate or total levels of peroxide produced by cells growing under photooxidative conditions. The work presented confirms the function of NpunR4582 as a catalase and provides insights as to how cells reduce potentially lethal peroxide levels produced by photosynthesis. The findings also show how trace elements play crucial roles as enzymatic cofactors and how the role of Npun_R4582 in hydrogen peroxide breakdown is dependent on the type of metal and the level available to cells.

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

Similar content being viewed by others

References

  • Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341

    Article  CAS  PubMed  Google Scholar 

  • Anderson DC, Campbell EL, Meeks JC (2006) A soluble 3D LC/MS/MS proteome of the filamentous cyanobacterium Nostoc punctiforme. J Proteome Res 5:3096–3104

    Article  CAS  PubMed  Google Scholar 

  • Andrio E, Marino D, Marmeys A, de Segonzac MD, Damiani I, Genre A, Huguet S, Frendo P, Puppo A, Pauly N (2013) Hydrogen peroxide-regulated genes in the Medicago truncatula–Sinorhizobium meliloti symbiosis. New Phytol 198:179–189

    Article  CAS  PubMed  Google Scholar 

  • Bedwal S, Prasad S, Nair N, Saini MR, Bedwal RS (2009) Catalase in testes and epididymidis of wistar rats fed zinc deficient diet. Indian J Pharm Sci 71:55–58

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Brash AR, Niraula NP, Boeglin WE, Mashhadi Z (2014) An ancient relative of cyclooxygenase in cyanobacteria is a linoleate 10S-dioxygenase that works in tandem with a catalase-related protein with specific 10S-hydroperoxide lyase activity. J Biol Chem 289:13101–13111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campbell EL, Summers ML, Christman H, Martin ME, Meeks JC (2007) Global gene expression patterns of Nostoc punctiforme in steady-state dinitrogen-grown heterocyst-containing cultures and at single time points during the differentiation of akinetes and hormogonia. J Bacteriol 189:5247–5256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eide DJ (2006) Zinc transporters and the cellular trafficking of zinc. Biochim Biophys Acta 1763:711–722

    Article  CAS  PubMed  Google Scholar 

  • Eiglmeier K, Fsihi H, Heym B, Cole ST (1997) On the catalase-peroxidase gene, katG, of Mycobacterium leprae and the implications for treatment of leprosy with isoniazid. FEMS Microbiol Lett 149:273–278

    Article  CAS  PubMed  Google Scholar 

  • Ekman M, Sandh G, Nenninger A, Oliveira P, Stensjo K (2014) Cellular and functional specificity among ferritin-like proteins in the multicellular cyanobacterium Nostoc punctiforme. Environ Microbiol 16:829–844

    Article  CAS  PubMed  Google Scholar 

  • Herrero M, de Lorenzo V, Timmis KN (1990) Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. J Bacteriol 172:6557–6567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Higgins DG, Sharp PM (1988) CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene 73:237–244

    Article  CAS  PubMed  Google Scholar 

  • Hou Z, Mitra B (2003) The metal specificity and selectivity of ZntA from Escherichia coli using the acylphosphate intermediate. J Biol Chem 278:28455–28461

    Article  CAS  PubMed  Google Scholar 

  • Hudek L, Rai LC, Freestone D, Michalczyk A, Gibson M, Song YF, Ackland ML (2009) Bioinformatic and expression analyses of genes mediating zinc homeostasis in Nostoc punctiforme. Appl Environ Microbiol 75:784–791

    Article  CAS  PubMed  Google Scholar 

  • Hudek L, Rai S, Michalczyk A, Rai LC, Neilan BA, Ackland ML (2012) Physiological metal uptake by Nostoc punctiforme. Biometals 25:893–903

    Article  CAS  PubMed  Google Scholar 

  • Hudek L, Pearson LA, Michalczyk A, Neilan BA, Ackland ML (2013a) Functional characterization of the twin ZIP/SLC39 metal transporters, NpunF3111 and NpunF2202 in Nostoc punctiforme. Appl Microbiol Biotechnol 97:8649–8662

    Article  CAS  PubMed  Google Scholar 

  • Hudek L, Pearson LA, Michalczyk A, Neilan BA, Ackland ML (2013b) Molecular and cellular characterisation of the zinc uptake (Znu) system of Nostoc punctiforme. FEMS Microbiol Ecol 86:149–171

    Article  CAS  PubMed  Google Scholar 

  • Huertas MJ, Lopez-Maury L, Giner-Lamia J, Sanchez-Riego AM, Florencio FJ (2014) Metals in cyanobacteria: analysis of the copper, nickel, cobalt and arsenic homeostasis mechanisms. Life (Basel) 4:865–886

    CAS  Google Scholar 

  • Jakopitsch C, Ruker 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  CAS  PubMed  Google Scholar 

  • Johnsson K, Froland WA, Schultz PG (1997) Overexpression, purification, and characterization of the catalase-peroxidase KatG from Mycobacterium tuberculosis. J Biol Chem 272:2834–2840

    Article  CAS  PubMed  Google Scholar 

  • Korshunov S, Imlay JA (2006) Detection and quantification of superoxide formed within the periplasm of Escherichia coli. J Bacteriol 188:6326–6334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Latifi A, Ruiz M, Zhang CC (2009) Oxidative stress in cyanobacteria. FEMS Microbiol Rev 33:258–278

    Article  CAS  PubMed  Google Scholar 

  • Levine A, Tenhaken R, Dixon R, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593

    Article  CAS  PubMed  Google Scholar 

  • Ma Z, Jacobsen FE, Giedroc DP (2009) Coordination chemistry of bacterial metal transport and sensing. Chem Rev 109:4644–4681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matthijs HC, Visser PM, Reeze B, Meeuse J, Slot PC, Wijn G, Talens R, Huisman J (2012) Selective suppression of harmful cyanobacteria in an entire lake with hydrogen peroxide. Water Res 46:1460–1472

    Article  CAS  PubMed  Google Scholar 

  • Meeks JC, Castenholz RW (1971) Growth and photosynthesis in an extreme thermophile, Synechococcus lividus (Cyanophyta). Arch Mikrobiol 78:25–41

    Article  CAS  PubMed  Google Scholar 

  • Meeks JC, Elhai J, Thiel T, Potts M, Larimer F, Lamerdin J, Predki P, Atlas R (2001) An overview of the genome of Nostoc punctiforme, a multicellular, symbiotic cyanobacterium. Photosynth Res 70:85–106

    Article  CAS  PubMed  Google Scholar 

  • Moirangthem LD, Bhattacharya S, Stensjo K, Lindblad P, Bhattacharya J (2014) A high constitutive catalase activity confers resistance to methyl viologen-promoted oxidative stress in a mutant of the cyanobacterium Nostoc punctiforme ATCC 29133. Appl Microbiol Biotechnol 98:3809–3818

    Article  CAS  PubMed  Google Scholar 

  • Mutsuda M, Ishikawa T, Takeda T, Shigeoka S (1996) The catalase-peroxidase of Synechococcus PCC 7942: purification, nucleotide sequence analysis and expression in Escherichia coli. Biochem J 316(Pt 1):251–257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Obinger C, Regelsberger G, Furtmuller PG, Jakopitsch C, Ruker F, Pircher A, Peschek GA (1999) Catalase-peroxidases in cyanobacteria--similarities and differences to ascorbate peroxidases. Free Radic Res 31(Suppl):S243–S249

    Article  CAS  PubMed  Google Scholar 

  • Osman D, Cavet JS (2008) Copper homeostasis in bacteria. Adv Appl Microbiol 65:217–247

    Article  CAS  PubMed  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Peleg-Grossman S, Volpin H, Levine A (2007) Root hair curling and Rhizobium infection in Medicago truncatula are mediated by phosphatidylinositide-regulated endocytosis and reactive oxygen species. J Exp Bot 58:1637–1649

    Article  CAS  PubMed  Google Scholar 

  • Peleg-Grossman S, Melamed-Book N, Levine A (2012) ROS production during symbiotic infection suppresses pathogenesis-related gene expression. Plant Signal Behav 7:409–415

    Article  CAS  PubMed  PubMed Central  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Perez-Perez ME, Mata-Cabana A, Sanchez-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  CAS  PubMed  PubMed Central  Google Scholar 

  • Pires BM, Silva DM, Visentin LC, Rodrigues BL, Carvalho NM, Faria RB (2015) Synthesis and characterization of cobalt(III), nickel(II) and copper(II) mononuclear complexes with the ligand 1,3-bis[(2-aminoethyl)amino]-2-propanol and their catalase-like activity. PLoS One 10:e0137926

    Article  PubMed  PubMed Central  Google Scholar 

  • Prasad SM, Singh JB, Rai LC, Kumar HD (1991) Metal-induced inhibition of photosynthetic electron transport chain of the cyanobacterium Nostoc muscorum. FEMS Microbiol Lett 82:95–100

    Article  CAS  Google Scholar 

  • Qiu A, Hogstrand C (2005) Functional expression of a low-affinity zinc uptake transporter (FrZIP2) from pufferfish (Takifugu rubripes) in MDCK cells. Biochem J 390:777–786

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Regelsberger G, Jakopitsch C, Plasser L, Schwaiger H, Furtmüller PG, Peschek GA, Zámocký M, Obinger C (2002) Occurrence and biochemistry of hydroperoxidases in oxygenic phototrophic prokaryotes (cyanobacteria). Plant Physiol Biochem 40:479–490

    Article  CAS  Google Scholar 

  • Rodriguez RE, Misra M, Kasprzak KS (1990) Effects of nickel on catalase activity in vitro and in vivo. Toxicology 63:45–52

    Article  CAS  PubMed  Google Scholar 

  • Salinas E, Torriero AA, Sanz MI, Battaglini F, Raba J (2005) Continuous-flow system for horseradish peroxidase enzyme assay comprising a packed-column, an amperometric detector and a rotating bioreactor. Talanta 66:92–102

    Article  CAS  PubMed  Google Scholar 

  • Sambrook J, Russell D (2001) Molecular cloning: a laboratory manual, vol 1-3. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Sanchez S, Pumera M, Cabruja E, Fabregas E (2007a) Carbon nanotube/polysulfone composite screen-printed electrochemical enzyme biosensors. Analyst 132:142–147

    Article  CAS  PubMed  Google Scholar 

  • Sanchez S, Pumera M, Fabregas E (2007b) Carbon nanotube/polysulfone screen-printed electrochemical immunosensor. Biosens Bioelectron 23:332–340

    Article  PubMed  Google Scholar 

  • Sekler I, Sensi SL, Hershfinkel M, Silverman WF (2007) Mechanism and regulation of cellular zinc transport. Mol Med 13:337–343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shcolnick S, Keren N (2006) Metal homeostasis in cyanobacteria and chloroplasts. Balancing benefits and risks to the photosynthetic apparatus. Plant Physiol 141:805–810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sinclair SA, Kramer U (2012) The zinc homeostasis network of land plants. Biochim Biophys Acta 1823:1553–1567

    Article  CAS  PubMed  Google Scholar 

  • Srivastava AK (2010) Assessment of salinity-induced antioxidative defense system of diazotrophic cyanobacterium Nostoc muscorum. J Microbiol Biotechnol 20:1506–1512

    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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tripathy BC, Mohanty P (1980) Zinc-inhibited electron transport of photosynthesis in isolated barley chloroplasts. Plant Physiol 66:1174–1178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Troxell B, Hassan HM (2013) Transcriptional regulation by Ferric Uptake Regulator (Fur) in pathogenic bacteria. Front Cell Infect Microbiol 3:59

    PubMed  PubMed Central  Google Scholar 

  • Whittaker JW (2003) The irony of manganese superoxide dismutase. Biochem Soc Trans 31:1318–1321

    Article  CAS  PubMed  Google Scholar 

  • Whittaker JW (2012) Non-heme manganese catalase—the ‘other’ catalase. Arch Biochem Biophys 525:111–120

    Article  CAS  PubMed  Google Scholar 

  • Whittaker MM, Barynin VV, Igarashi T, Whittaker JW (2003) Outer sphere mutagenesis of Lactobacillus plantarum manganese catalase disrupts the cluster core. Mechanistic implications. Eur J Biochem 270:1102–1116

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Duan X, Yang J, Beeching JR, Zhang P (2013) Enhanced reactive oxygen species scavenging by overproduction of superoxide dismutase and catalase delays postharvest physiological deterioration of cassava storage roots. Plant Physiol 161:1517–1528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors would like to acknowledge the support received from the Australian Society for Microbiology whom supported this work through the Millis-Colwell Award exchange program.

Author information

Authors and Affiliations

  1. Centre for Regional and Rural Futures, Deakin University, Burwood, VIC, 3125, Australia

    L. Hudek & Lambert Bräu

  2. Centre for Cellular and Molecular Biology, School of Life and Environmental Sciences, Deakin University, Burwood, VIC, 3125, Australia

    L. Hudek, A. A. Michalczyk, M. L. Ackland & Lambert Bräu

  3. Centre for Chemistry and Biotechnology, School of Life and Environmental Sciences, Deakin University, Burwood, VIC, 3125, Australia

    A. A. J. Torriero

  4. Australian Centre for Astrobiology and School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, NSW, 2052, Australia

    B. A. Neilan

Authors
  1. L. Hudek
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. A. J. Torriero
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. A. Michalczyk
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. B. A. Neilan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. L. Ackland
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lambert Bräu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lambert Bräu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethics approval

This article does not contain any studies with human participants performed by any of the authors.

Electronic supplementary material

ESM 1

(PDF 574 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hudek, L., Torriero, A.A.J., Michalczyk, A.A. et al. Peroxide reduction by a metal-dependent catalase in Nostoc punctiforme (cyanobacteria). Appl Microbiol Biotechnol 101, 3781–3800 (2017). https://doi.org/10.1007/s00253-017-8130-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-017-8130-y

Keywords

Search

Navigation