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Sublethal detergent concentrations increase metabolization of recalcitrant polyphosphonates by the cyanobacterium Spirulina platensis

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Abstract

As a consequence of increasing industrial applications, thousand tons of polyphosphonates are introduced every year into the environment. The inherent stability of the C–P bond results in a prolonged half-life. Moreover, low uptake rates limit further their microbial metabolization. To assess whether low detergent concentrations were able to increase polyphosphonate utilization by the cyanobacterium Spirulina platensis, tolerance limits to the exposure to various detergents were determined by measuring the growth rate in the presence of graded levels below the critical micellar concentration. Then, the amount of hexamethylenediamine-N,N,N′,N′-tetrakis(methylphosphonic acid) that is metabolized in the absence or in the presence of sublethal detergent concentrations was quantified by 31P NMR analysis on either P-starved or P-fed cyanobacterial cultures. The strain tolerated the presence of detergents in the order: nonionic > anionic > cationic. When added to the culture medium at the highest concentrations showing no detrimental effects upon cell viability, detergents either improved or decreased polyphosphonate utilization, the anionic sodium dodecyl sulfate being the most beneficial. Metabolization was not lower in P-fed cells—a result that strengthens the possibility of using, in the future, this strain for bioremediation purposes.

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References

  • Alden L, Demoling F, Baath E (2001) Rapid method of determining factors limiting bacterial growth in soil. Appl Environ Microbiol 67:1830–1838

    Article  CAS  Google Scholar 

  • Chen CM, Ye QZ, Zhu ZM, Wanner BL, Walsh CT (1990) Molecular biology of carbon-phosphorus bond cleavage. Cloning and sequencing of the phn (psiD) genes involved in alkylphosphonate uptake and C–P lyase activity in Escherichia coli B. J Biol Chem 265:4461–4471

    CAS  Google Scholar 

  • Dubey SK, Dubey J, Mehra S, Tiwari P, Bishwas AJ (2011) Potential use of cyanobacterial species in bioremediation of industrial effluents. African J Biotech 10:1125–1132

    Google Scholar 

  • Dyhrman ST, Chappell PD, Haley ST, Moffett JW, Orchard ED, Waterbury JB, Webb EA (2006) Phosphonate utilization by the globally important marine diazotroph Trichodesmium. Nature 439:68–71

    Article  CAS  Google Scholar 

  • El-Bestawy EA, Abd El-Salam AZ, Mansy AE-RH (2007) Potential use of environmental cyanobacterial species in bioremediation of lindane-contaminated effluents. Int Biodet Biodegr 59:180–192

    Article  CAS  Google Scholar 

  • EU Commission Report to the European Parliament and the Council (2009) Pursuant to Article 16 of Regulation (EC) No 648/2004 of the European Parliament and of the Council of 31 March 2004 on detergents, concerning the biodegradation of main non-surfactant organic detergent ingredients. Brussels, 4.5

  • Forlani G, Klimek-Ochab M, Jaworski J, Lejczak B, Picco AM (2006) Phosphonoacetic acid utilization by fungal isolates: occurrence and properties of a phosphonoacetate hydrolase in some penicillia. Mycol Res 110:1455–1463

    Article  CAS  Google Scholar 

  • Forlani G, Pavan M, Gramek M, Kafarski P, Lipok J (2008) Biochemical bases for a widespread tolerance of cyanobacteria to the phosphonate herbicide glyphosate. Plant Cell Physiol 49:443–456

    Article  CAS  Google Scholar 

  • Forlani G, Prearo V, Wieczorek D, Kafarski P, Lipok J (2011) Polyphosphonate degradation by Spirulina strains: cyanobacterial biofilters for the removal of anticorrosive polyphosphonates from wastewater. Enzyme Microb Tech 48:299–305

    Article  CAS  Google Scholar 

  • Gledhill WE, Feijtel TCJ (1992) Environmental properties and safety assessment of organic phosphonates used for detergent and water treatment applications. In: de Oude NT (ed) Detergents, the handbook of environmental chemistry, Volume 3. Part F. Anthropogenic compounds. Springer, Berlin, pp 261–285

    Google Scholar 

  • Gomez-Garcia MR, Davison M, Blain-Hartnung M, Grossman AR, Bhaya D (2011) Alternative pathways for phosphonate metabolism in thermophilic cyanobacteria from microbial mats. ISME J 5:141–149

    Article  CAS  Google Scholar 

  • HERA (2004) Human & environmental risk assessment on ingredients of European household cleaning products. Phosphonates (CAS 6419-19-8; 2809-21-4; 15827-60-8), pp 114

  • Hsieh YJ, Wanner BL (2010) Global regulation by the seven-component Pi signaling system. Curr Opin Microbiol 13:198–203

    Article  CAS  Google Scholar 

  • Jochimsen B, Lolle S, McSorley FR, Nabi M, Stougaard J, Zechel DL, Hove-Jensen B (2011) Five phosphonate operon gene products as components of a multi-subunit complex of the carbon-phosphorus lyase pathway. Proc Natl Acad Sci USA 108:11393–11398

    Article  CAS  Google Scholar 

  • Knepper TP (2003) Synthetic chelating agents and compounds exhibiting complexing properties in the aquatic environment. Trends Anal Chem 22:708–724

    Article  CAS  Google Scholar 

  • Kononova SV, Nesmeyanova MA (2002) Phosphonates and their degradation by microorganisms. Biochemistry 67:184–195

    CAS  Google Scholar 

  • Labjara N, Lebrini M, Bentiss F, Chihib N-E, El Hajjaji S, Jama C (2010) Corrosion inhibition of carbon steel and antibacterial properties of aminotris-(methylenephosphonic) acid. Mater Chem Phys 119:330–336

    Article  Google Scholar 

  • Lahiri SD, Zhang G, Dai J, Dunaway-Mariano D, Allen KN (2004) Analysis of the substrate specificity loop of the HAD superfamily cap domain. Biochemistry 43:2812–2820

    Article  CAS  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382

    Article  CAS  Google Scholar 

  • Lipok J, Owsiak T, Młynarz P, Forlani G, Kafarski P (2007) Phosphorus NMR as a tool to study mineralization of organophosphonates—the ability of Spirulina spp. to degrade glyphosate. Enzyme Microb Tech 41:286–291

    Article  CAS  Google Scholar 

  • Quinn JP, Kulakova AN, Cooley NA, McGrath JW (2007) New ways to break an old bond: the bacterial carbon-phosphorus hydrolases and their role in biogeochemical phosphorus cycling. Environ Microbiol 9:2392–2400

    Article  CAS  Google Scholar 

  • Ternan NG, Mc Grath JW, Mc Mullan G, Quinn JP (1998) Organophosphonates: occurrence, synthesis and biodegradation by microorganisms. World J Microbiol Biotech 14:635–647

    Article  CAS  Google Scholar 

  • Zhang Q, van der Donk WA (2012) Answers to the carbon-phosphorus lyase conundrum. ChemBioChem 13:627–629

    Article  CAS  Google Scholar 

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Acknowledgments

Support from the University of Ferrara (Fondo di Ateneo per la Ricerca 2010 and 2011) and from Polish National Science Centre (grant 2011/01/B/NZ9/04722) is acknowledged. The authors thank Mr. Amedeo Mazzocco for technical assistance.

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Correspondence to Giuseppe Forlani.

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Responsible editor: Robert Duran

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Forlani, G., Bertazzini, M., Giberti, S. et al. Sublethal detergent concentrations increase metabolization of recalcitrant polyphosphonates by the cyanobacterium Spirulina platensis . Environ Sci Pollut Res 20, 3263–3270 (2013). https://doi.org/10.1007/s11356-012-1253-x

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