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Physiological metal uptake by Nostoc punctiforme

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Abstract

Trace metals are required for many cellular processes. The acquisition of trace elements from the environment includes a rapid adsorption of metals to the cell surface, followed by a slower internalization. We investigated the uptake of the trace elements Co2+, Cu2+, Mn2+, Ni2+, and Zn2+ and the non-essential divalent cation Cd2+ in the cyanobacterium Nostoc punctiforme. For each metal, a dose response study based on cell viability showed that the highest non-toxic concentrations were: 0.5 μM Cd2+, 2 μM Co2+, 0.5 μM Cu2+, 500 μM Mn2+, 1 μM Ni2+, and 18 μM Zn2+. Cells exposed to these non-toxic concentrations with combinations of Zn2+ and Cd2+, Zn2+ and Co2+, Zn2+ and Cu2+ or Zn2+ and Ni2+, had reduced growth in comparison to controls. Cells exposed to metal combinations with the addition of 500 μM Mn2+ showed similar growth compared to the untreated controls. Metal levels were measured after one and 72 h for whole cells and absorbed (EDTA-resistant) fractions and used to calculate differential uptake rates for each metal. The differences in binding and internalisation between different metals indicate different uptake processes exist for each metal. For each metal, competitive uptake experiments using 65Zn showed that after 72 h of exposure Zn2+ uptake was reduced by most metals particularly 0.5 μM Cd2+, while 2 μM Co2+ increased Zn2+ uptake. This study demonstrates that N. punctiforme discriminates between different metals and favourably substitutes their uptake to avoid the toxic effects of particular metals.

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References

  • Ackland ML, McArdle HJ (1996) Cation-dependant uptake of Zn2+ in human fibroblasts. Biometals 9:29–37

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Asayama M, Imamura S, Yoshihara S, Miyazaki A, Yoshida N, Sazuka T, Kaneko T, Ohara O, Tabata S, Osanai T, Tanaka K, Takahashi H, Shirai M (2004) SigC, the group 2 sigma factor of RNA polymerase, contributes to the late-stage gene expression and nitrogen promoter recognition in the cyanobacterium Synechocystis sp. strain PCC6803. Biosci Biotechnol Biochem 68:477–487

    Article  PubMed  CAS  Google Scholar 

  • Awasthi M, Rai LC (2006) Interactions between Zn2+ and Cd2+ uptake by free and immobilized cells of Scenedesums quadricauda (Turp.) Breb. Acta Hydroch Hydrob 34:20–26

    Article  CAS  Google Scholar 

  • Azeez PA, Banerjee DK (1991) Ni2+ uptake and toxicity in cyanobacteria. Toxicol Environ Chem 30:43–50

    Article  CAS  Google Scholar 

  • Backor M, Fashelt D (2008) Lichen photobionts and metal toxicity. Symbiosis 46:1–10

    CAS  Google Scholar 

  • Baptista MS, Vasconcelos TM (2006) Cyanobacteria metal interactions: requirements, toxicity, and ecological implications. Crit Rev Microbiol 32:127–137

    Article  PubMed  CAS  Google Scholar 

  • Bartsevich VV, Pakrasi HB (1996) Mn2+transport in the cyanobacterium Synechocystis sp. PCC6803. J Biol Chem 271:26057–26061

    Article  PubMed  CAS  Google Scholar 

  • Bender J, Gould JP, Vatcharapijarn Y, Young JS, Phillips P (1994) Removal of Zn2+ and Mn2+ from contaminated water with cyanobacteria mats. Water Environ Res 66:679–683

    Article  CAS  Google Scholar 

  • Blindauer CA (2008) Zn2+-handling in cyanobacteria: an update. Chem Biodivers 5:1990–2013

    Article  PubMed  CAS  Google Scholar 

  • Cavet JS, Borrelly GPM, Robinson NJ (2003) Zn, Cu and Co in cyanobacteria: selective control of metal availability. FEMS Microbiol Rev 27:165–181

    Article  PubMed  CAS  Google Scholar 

  • Chong KH, Volesky B (1996) Metal biosorption equilibria in a ternary system. Biotechnol Bioeng 49:629–638

    Article  PubMed  CAS  Google Scholar 

  • Choudhary M, Jetly UK, Khan MA, Zutshi S, Fatma T (2006) Effect of heavy metal stress on proline, malondialdehyde and super dismutase activity in the cyanobacterium Spirulina platensis S5. Ecotoxicol Environ Safe 66:204–209

    Article  Google Scholar 

  • Daday A, Mackerras H, Smith GD (1988) A role for Ni2+ in cyanobacterial nitrogen fixation and growth via cyanophycin metabolism. J Gen Micro 134:2659–2663

    CAS  Google Scholar 

  • Dohnalkova A, Marshall MJ, Kennedy DW, Gorby YA, Shi L, Beliaev A, Apkarian R, Fredrickson JK (2005) The role of bacterial exopolymers in metal sorption and reduction. Microsc Microanal 11:116–117

    Article  Google Scholar 

  • Dupont CL, Butcher A, Valas RE, Bourne PE, Caetano-Anolles G (2010) History of biological metal utilization inferred through phylogenomic analysis of protein structures. Proc Natl Acad Sci 107:10567–10572

    Article  PubMed  CAS  Google Scholar 

  • El-Enany AE, Issa AA (2000) Cyanobacteria. as a biosorbent of heavy metals in sewage water. Environ Toxicol Phar 8:95–101

    Article  CAS  Google Scholar 

  • Gardea-Torresdeya JL, Arenasb JL, Franciscob NMC, Tiemanna KJ, Webbb R (1998) Ability of immobilized cyanobacteria to remove metal ions from solution and demonstration of the presence of metallothionein genes in various strains. J Hazard Sub Res 1:2–18

    Google Scholar 

  • Hameed MSA, Ebrahim OH (2007) Biotechnological potential uses of immobilized algae. Int J Agri Biol 9:183–192

    Google Scholar 

  • Hantke K (2005) Bacterial Zn2+ uptake and regulators. Curr Opin Microbiol 8:196–202

    Article  PubMed  CAS  Google Scholar 

  • Hoiczyk E, Hansel A (2000) Cyanobacterial cell walls: news from an unusual prokaryotic envelope. J Bacteriol 182:1191–1199

    Article  PubMed  CAS  Google Scholar 

  • Hudek L, Rai LC, Freestone DF, Michalczyk A, Gibson M, Song YF, Ackland ML (2009) Bioinformatic and expression analyses of genes mediating Zn2+ homeostasis in Nostoc punctiforme. Appl Environ Microbiol 75:784–791

    Article  PubMed  CAS  Google Scholar 

  • Loaec M, Olier R, Guenzennec J (1997) Uptake of lead, Cd2+ and Zn2+ by a novel bacterial exopolysaccharide. Wat Res 31:1171–1179

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  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

    Google Scholar 

  • Mehta SK, Gaur JP (2005) Use of algae for removing heavy metal ions from wastewater: progress and prospects. Crit Rev Biotechnol 25:113–152

    Article  PubMed  CAS  Google Scholar 

  • Miccadei S, Floridi A (1993) Sites of inhibition of mitochondrial electron transport by Cd2+. Chem Biol Interact 89:159–167

    Article  PubMed  CAS  Google Scholar 

  • Mullen MD, Wolf DC, Ferris FG, Beveridge TJ, Flemming CA, Bailey GW (1989) Bacterial sorption of heavy metals. Appl Environ Microb 55:3143–3149

    CAS  Google Scholar 

  • Nies DH (2007) How cells control Zn2+ homeostasis. Science 317:1695–1696

    Article  PubMed  CAS  Google Scholar 

  • Pradhan SP, Conrada JR, Paterek JR, Srivastava VJ (1998) Potential of phytoremediation for treatment of PAHs in soil at MGP sites. Soil Sediment Contam 7:467–480

    Article  CAS  Google Scholar 

  • Qiu A, Hogstrand C (2005) Functional expression of a low-affinity Zn2+ uptake transporter (Fr ZIP2) from pufferfish (Takifugu rubripes) in MDCK cells. Biochem J 390:777–786

    Article  PubMed  CAS  Google Scholar 

  • Ran L, Huang F, Ekman M, Klint J, Bergman B (2007) Proteomic analyses of the photoauto- and diazotrophically grown cyanobacterium Nostoc sp. PCC73102. Microbiology 153:608–618

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Sharma M, Kaushik A, Kiran Bala S, Kamra A (2008) Sequestration of chromium by exopolysaccharides of Nostoc and Gleocapsa from dilute aqueous solutions. J Hazard Mater 157:315–318

    Article  PubMed  CAS  Google Scholar 

  • Singh AL, Asthana RK, Srivastava SC, Singh SP (1992) Ni2+ uptake and its localization in a cyanobacterium. FEMS Microbiol Lett 99:165–168

    Article  CAS  Google Scholar 

  • Singh S (1989) Co2+-induced inhibition of growth in the cyanobacteria Anabaena doliolum and Anacystis nidulans: interaction with sulphur containing amino acids. J Exp Biol 12:1092–1093

    Google Scholar 

  • Tanioka Y, Yabuta Y, Yamaji R, Shigeoka S, Nakano Y, Watanabe F, Inui H (2009) Occurrence of psuedovitamin B12 and its possible function as the cofactor of cobalamin-dependant methionine synthase in a cyanobacterium Synechocystis sp. PCC6803. J Nutr Sci Vitaminol 55:518–521

    Article  PubMed  CAS  Google Scholar 

  • Wu CH, Wood TK, Mulchandani A, Chen W (2006) Engineering plant–microbe symbiosis for rhizoremediation of heavy metals. Appl Environ Microbiol 72:1129–1134

    Article  PubMed  CAS  Google Scholar 

  • Ybarra GR, Webbb R (1999) Effects of divalent metal cations and resistance mechanisms of the cyanobacterium Synechocystis sp. strain PCC7942. J Hazard Sub Res 2:1–9

    Google Scholar 

  • Yee N, Benning LG, Phoenix VR, Ferris FG (2004) Characterization of metal–cyanobacteria sorption reactions: a combined macroscopic investigation. Environ Sci Technol 38:775–782

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We are grateful to Professor John C. Meeks for technical assistance and helpful discussions.

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Correspondence to M. Leigh Ackland.

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Hudek, L., Rai, S., Michalczyk, A. et al. Physiological metal uptake by Nostoc punctiforme . Biometals 25, 893–903 (2012). https://doi.org/10.1007/s10534-012-9556-4

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  • DOI: https://doi.org/10.1007/s10534-012-9556-4

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