Abstract
Phosphate-solubilizing fungi (PSF) can secrete large amounts of organic acids. In this study, the application of the fungus Penicillium oxalicum and geological fluorapatite (FAp) to lead immobilization was investigated. The formation and morphology of the lead-related minerals were analyzed by ATR-IR, XRD, Raman, and SEM. The quantity of organic acids secreted by P. oxalicum reached the maximum on the fourth day, which elevated soluble P concentrations from 0.4 to 108 mg/L in water. The secreted oxalic acid dominates the acidity in solution. P. oxalicum can survive in the solution with Pb concentration of ~ 1700 mg/L. In addition, it was shown that ~ 98% lead cations were removed while the fungus was cultured with Pb (~ 1700 mg/L) and FAp. The mechanism is that the released P from FAp (enhanced by organic acids) can react with Pb2+ to form the stable pyromorphite mineral [Pb5(PO4)3F]. The precipitation of lead oxalate also contributes to Pb immobilization. However, lead oxalate is more soluble due to its relatively high solubility. P. oxalicum has a higher rate of organic acid secretion compared with other typical PSF, e.g., Aspergillus niger. This study sheds light on bright future of applying P. oxalicum in Pb remediation.
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References
Adcock CT, Hausrath EM, Forster PM (2013) Readily available phosphate from minerals in early aqueous environments on Mars. Nat Geosci 6:824–827
Arwidsson Z, Johansson E, von Kronhelm T, Allard B, van Hees P (2010) Remediation of metal contaminated soil by organic metabolites from fungi i-production of organic acids. Water Air Soil Pollut 205:215–226
Behnoudnia F, Dehghani H (2012) Synthesis and characterization of novel three-dimensional-cauliflower-like nanostructure of lead(II) oxalate and its thermal decomposition for preparation of PbO. Inorg Chem Commun 24:32–39
Bolan NS, Naidu R, Mahimairaja S, Baskaran S (1994) Influence of low-molecular-weight organic-acids on the solubilization of phosphates. Biol Fertil Soils 18:311–319
Cao XD, Wahbi A, Ma LN, Li B, Yang YL (2009) Immobilization of Zn, Cu, and Pb in contaminated soils using phosphate rock and phosphoric acid. J Hazard Mater 164:555–564
Cazalbou S, Bertrand G, Drouet C (2015) Tetracycline-loaded biomimetic apatite: an adsorption study. J Phys Chem B 119:3014–3024
Chen XB, Wright JV, Conca JL, Peurrung LM (1997) Evaluation of heavy metal remediation using mineral apatite. Water Air Soil Pollut 98:57–78
Chen YP, Rekha PD, Arun AB, Shen FT, Lai WA, Young CC (2006) Phosphate solubilizing bacteria from subtropical soil and their tricalcium phosphate solubilizing abilities. Appl Soil Ecol 34:33–41
Chen W, Wang Q, Meng S, Yang P, Jiang L, Zou X, Li Z, Hu S (2017) Temperature-related changes of Ca and P release in synthesized hydroxylapatite, geological fluorapatite, and bone bioapatite. Chem Geol 451:183–188
CotterHowells J, Caporn S (1996) Remediation of contaminated land by formation of heavy metal phosphates. Appl Geochem 11:335–342
Coutinho FP, Felix WP, Yano-Melo AM (2012) Solubilization of phosphates in vitro by Aspergillus spp. and Penicillium spp. Ecol Eng 42:85–89
Debela F, Arocena JM, Thring RW, Whitcombe T (2010) Organic acid-induced release of lead from pyromorphite and its relevance to reclamation of Pb-contaminated soils. Chemosphere 80:450–456
Drouet C (2013) Apatite formation: why it may not work as planned, and how to conclusively identify apatite compounds. Biomed Res Int 2013:490–496
Du YJ, Wei ML, Reddy KR, Jin F, Wu HL, Liu ZB (2014) New phosphate-based binder for stabilization of soils contaminated with heavy metals: leaching, strength and microstructure characterization. J Environ Manag 146:179–188
Elliott JC (2002) Calcium phosphate biominerals. Rev Mineral Geochem 48:427–453
Giammar DE, Xie LY, Pasteris JD (2008) Immobilization of lead with nanocrystalline carbonated apatite present in fish bone. Environ Eng Sci 25:25–735
Hou DY, Qi SQ, Zhao B, Rigby M, O'Connor D (2017) Incorporating life cycle assessment with health risk assessment to select the ‘greenest’ cleanup level for Pb contaminated soil. J Clean Prod 162:1157–1168
Jiang GJ, Liu YH, Huang L, Fu QL, Deng YJ, Hu HQ (2012) Mechanism of lead immobilization by oxalic acid-activated phosphate rocks. J Environ Sci (China) 24:919–925
Kamiishi E, Utsunomiya S (2013) Nano-scale reaction processes at the interface between apatite and aqueous lead. Chem Geol 340:121–130
Keenan SW, Engel AS (2017) Early diagenesis and recrystallization of bone. Geochim Cosmochim Acta 196:209–223
Li Z, Bai T, Dai L, Wang F, Tao J, Meng S, Hu Y, Wang S, Hu S (2016a) A study of organic acid production in contrasts between two phosphate solubilizing fungi: Penicillium oxalicum and Aspergillus niger. Sci Rep-uk 6:25313
Li Z, Wang F, Bai T, Tao J, Guo J, Yang M, Wang S, Hu S (2016b) Lead immobilization by geological fluorapatite and fungus Aspergillus niger. J Hazard Mater 320:386–392
Ma LQ, Rao GN (1999) Aqueous Pb reduction in Pb-contaminated soils by Florida phosphate rocks. Water Air Soil Pollut 110:1–16
Ma QY, Traina SJ, Logan TJ, Ryan JA (1993) In-situ lead immobilization by apatite. Environ Sci Technol 27:1803–1810
Ma QY, Logan TJ, Traina SJ (1995) Lead immobilization from aqueous-solutions and contaminated soils using phosphate rocks. Environ Sci Technol 29:1118–1126
Mathew M, Takagi S (2001) Structures of biological minerals in dental research. J Res Natl Inst Stand Technol 106:1035–1044
Mendes GO, Dias CS, Silva IR, Ribeiro JI, Pereira OL, Costa MD (2013) Fungal rock phosphate solubilization using sugarcane bagasse. World J Microbiol Biotechnol 29:43–50
Mendes GD, da Silva NMRM, Anastacio TC, Vassilev NB, Ribeiro JI, da Silva IR, Costa MD (2015) Optimization of Aspergillus niger rock phosphate solubilization in solid-state fermentation and use of the resulting product as a P fertilizer. Microb Biotechnol 8:930–939
Moreno EC, Kresak M, Zahradnik RT (1974) Fluoridated hydroxyapatite solubility and caries formation. Nature 247:64–65
Narasaraju TSB, Phebe DE (1996) Some physico-chemical aspects of hydroxylapatite. J Mater Sci 31:1–21
Oliveira SCD, Mendes GDO, Silva UCD, Silva IRD, Júnior JIR, Costa MD (2015) Decreased mineral availability enhances rock phosphate solubilization efficiency in Aspergillus niger. Ann Microbiol 65:745–751
Osorio NW, Habte M (2013) Phosphate desorption from the surface of soil mineral particles by a phosphate-solubilizing fungus. Biol Fertil Soils 49:481–486
Park JH, Bolan N, Megharaj M, Naidu R (2011) Concomitant rock phosphate dissolution and lead immobilization by phosphate solubilizing bacteria (Enterobacter sp.). J Environ Manag 92:1115–1120
Radoicic TK, Raicevic S (2008) In situ lead stabilization using natural and synthetic apatite. Chem Ind Chem Eng Q 14:269–271
Rehman I, Bonfield W (1997) Characterization of hydroxyapatite and carbonated apatite by photo acoustic FTIR spectroscopy. J Mater Sci Mater Med 8:1–4
Relwani L, Krishna P, Reddy MS (2008) Effect of carbon and nitrogen sources on phosphate solubilization by a wild-type strain and uv-induced mutants of Aspergillus tubingensis. Curr Microbiol 57:401–406
Richardson AE, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability. Plant Physiol 156:989–996
Ruby MV, Davis A, Nicholson A (1994) In-situ formation of lead phosphates in soils as a method to immobilize lead. Environ Sci Technol 28:646–654
Shen YH, Li SK, Xie AJ, Xu WH, Qiu LG, Yao H, Yu XR, Chen ZX (2007) Controlled growth of calcium oxalate crystal in bicontinuous microemulsions containing amino acids. Colloid Surface B 58:298–304
Shen ZT, Tian D, Zhang XY, Tang LY, Su M, Zhang L, Li Z, Hu SJ, Hou DY (2018) Mechanisms of biochar assisted immobilization of Pb(2+) by bioapatite in aqueous solution. Chemosphere 190:260–266
Sturm EV, Frank-Kamenetskaya O, Vlasov D, Zelenskaya M, Sazanova K, Rusakov A, Kniep R (2015) Crystallization of calcium oxalate hydrates by interaction of calcite marble with fungus Aspergillus niger. Am Miner 100:2559–2565
Traina SJ, Laperche V (1999) Contaminant bioavailability in soils, sediments, and aquatic environments. Proc Natl Acad Sci USA 96:3365–3371
Vyas P, Gulati A (2009) Organic acid production in vitro and plant growth promotion in maize under controlled environment by phosphate-solubilizing fluorescent Pseudomonas. BMC Microbiol 9:174
Wahid OAA, Mehana TA (2000) Impact of phosphate-solubilizing fungi on the yield and phosphorus-uptake by wheat and faba bean plants. Microbiol Res 155:221–227
Wang YM, Chen TC, Yeh KJ, Shue MF (2001) Stabilization of an elevated heavy metal contaminated site. J Hazard Mater 88:63–74
Whitelaw MA (1999) Growth promotion of plants inoculated with phosphate-solubilizing fungi. Adv Agron 69:99–151
Zhu Y, Zhang X, Chen Y, Xie Q, Lan J, Qian M, He N (2009) A comparative study on the dissolution and solubility of hydroxylapatite and fluorapatite at 25°C and 45°C. Chem Geol 268:89–96
Acknowledgements
We thank Mr. Letian Dai and Mr. Fuwei Wang for assistance in fungus isolation and culture.
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This work was partially supported by Natural Science Foundation of Jiangsu Province of China (No. BK20150683), China Postdoctoral Science Foundation (No. 2017M610330), the Fundamental Research Funds for the Central Universities (No. KYTZ201404 and KYZ201712), and the Top-notch Academic Programs Project of Jiangsu Higher Education Institutions (PPZY2015A061).
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Tian, D., Wang, W., Su, M. et al. Remediation of lead-contaminated water by geological fluorapatite and fungus Penicillium oxalicum. Environ Sci Pollut Res 25, 21118–21126 (2018). https://doi.org/10.1007/s11356-018-2243-4
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DOI: https://doi.org/10.1007/s11356-018-2243-4