Abstract
The use of phosphate-solubilizing fungi is a promising biotechnological strategy in the management of phosphorus (P) fertilization, as it enables the utilization of rock phosphates (RP) or the recovery of P fixed in soil particles. The objective of our study was to evaluate fungal isolates for mechanisms of solubilization of P-bearing compounds, such as AlPO4, FePO4, Ca3(PO4)2, Araxá RP, and Catalão RP. Four fungal isolates obtained from Brazilian soils were characterized in liquid media: Aspergillus niger FS1, Penicillium canescens FS23, Eupenicillium ludwigii FS27, and Penicillium islandicum FS30. A. niger FS1 was the only isolate able to solubilize all of the P sources, solubilizing 71, 36, 100, and 14 % of the P from AlPO4, FePO4, Ca3(PO4)2, and RPs, respectively. Medium acidification was an effective solubilization mechanism, particularly for Ca3(PO4)2. The other P sources were mainly solubilized through organic acids produced by the fungi. Oxalic acid, produced exclusively by A. niger FS1, and citric acid were decisive factors in the solubilization of AlPO4 and FePO4. Penicillium isolates produced more gluconic acid than A. niger FS1 in all treatments. However, this higher production did not result in higher solubilization for any of the P sources, showing that gluconic acid contributes little to the solubilization of the P sources evaluated. The higher capacity of medium acidification and the production of organic acids with stronger metal-complexation activity are characteristics that confer to A. niger FS1 a wider action on insoluble P sources. Consequently, this isolate qualifies as a promising candidate for application in the management of P fertilization.
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References
Alfenas AC, Ferreira FA, Mafia RG, Gonçalves RC (2007) Isolamento de fungos fitopatogênicos. In: Alfenas AC, Mafia RG (eds) Métodos em Fitopatologia, 1st edn. Editora UFV, Viçosa, pp 53–91
Asea PEA, Kucey RMN, Stewart JWB (1988) Inorganic phosphate solubilization by two Penicillium species in solution culture and soil. Soil Biol Biochem 20(4):459–464. doi:10.1016/0038-0717(88)90058-2
Banik S, Dey B (1982) Available phosphate content of an alluvial soil as influenced by inoculation of some isolated phosphate-solubilizing micro-organisms. Plant Soil 69(3):353–364. doi:10.1007/bf02372456
Bechtold T, Burtscher E, Turcanu A (2002) Ca2+-Fe3+-D-gluconate-complexes in alkaline solution. Complex stabilities and electrochemical properties. J Chem Soc Dalton Trans 13:2683–2688
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(4):311–319. doi:10.1007/bf00570634
Braga JM, Defelipo BV (1974) Determinação espectrofotométrica de fósforo em extratos de solo e material vegetal. R Ceres 21:73–85
Cannan RK, Kibrick A (1938) Complex formation between carboxylic acids and divalent metal cations. J Am Chem Soc 60(10):2314–2320. doi:10.1021/ja01277a012
Chuang CC, Kuo YL, Chao CC, Chao WL (2007) Solubilization of inorganic phosphates and plant growth promotion by Aspergillus niger. Biol Fertil Soils 43(5):575–584. doi:10.1007/s00374-006-0140-3
Cordell D, Drangert J-O, White S (2009) The story of phosphorus: global food security and food for thought. Global Environ Change 19(2):292–305. doi:10.1016/j.gloenvcha.2008.10.009
Fontes MPF, Weed SB (1996) Phosphate adsorption by clays from Brazilian Oxisols: relationships with specific surface area and mineralogy. Geoderma 72(1–2):37–51. doi:10.1016/0016-7061(96)00010-9
Fox TR, Comerford NB, McFee WW (1990a) Kinetics of phosphorus release from spodosols: effects of oxalate and formate. Soil Sci Soc Am J 54(5):1441–1447. doi:10.2136/sssaj1990.03615995005400050038x
Fox TR, Comerford NB, McFee WW (1990b) Phosphorus and aluminum release from a spodic horizon mediated by organic acids. Soil Sci Soc Am J 54(6):1763–1767. doi:10.2136/sssaj1990.03615995005400060043x
Furia TE (1972) CRC handbook of food additives, vol. 1, 2nd edn. CRC Press, Cleveland
Gadd GM (1999) Fungal production of citric and oxalic acid: importance in metal speciation, physiology and biogeochemical processes. Adv Microb Physiol 41:47–92. doi:10.1016/s0065-2911(08)60165-4
Illmer P, Schinner F (1995) Solubilization of inorganic calcium phosphates—solubilization mechanisms. Soil Biol Biochem 27(3):257–263. doi:10.1016/0038-0717(94)00190-c
Illmer P, Barbato A, Schinner F (1995) Solubilization of hardly-soluble AlPO4 with P-solubilizing microorganisms. Soil Biol Biochem 27(3):265–270. doi:10.1016/0038-0717(94)00205-f
Jain R, Saxena J, Sharma V (2010) The evaluation of free and encapsulated Aspergillus awamori for phosphate solubilization in fermentation and soil-plant system. Appl Soil Ecol 46(1):90–94. doi:10.1016/j.apsoil.2010.06.008
Jones DL (1998) Organic acids in the rhizosphere—a critical review. Plant Soil 205(1):25–44. doi:10.1023/a:1004356007312
Kpomblekou-A K, Tabatabai MA (1994) Effect of organic acids on release of phosphorus from phosphate rocks. Soil Sci 158(6):442–453
Kubicek CP, Röhr M (1985) Aconitase and citric acid fermentation by Aspergillus niger. Appl Environ Microbiol 50(5):1336–1338
Mendes GO, Dias CS, Silva IR, Junior JI, Pereira OL, Costa MD (2013) Fungal rock phosphate solubilization using sugarcane bagasse. World J Microbiol Biotechnol 29(1):43–50. doi:10.1007/s11274-012-1156-5
Mischak H, Kubicek CP, Röhr M (1985) Formation and location of glucose oxidase in citric acid producing mycelia of Aspergillus niger. Appl Microbiol Biotechnol 21(1):27–31. doi:10.1007/bf00252357
Mittal V, Singh O, Nayyar H, Kaur J, Tewari R (2008) Stimulatory effect of phosphate-solubilizing fungal strains (Aspergillus awamori and Penicillium citrinum) on the yield of chickpea (Cicer arietinum L. cv. GPF2). Soil Biol Biochem 40(3):718–727. doi:10.1016/j.soilbio.2007.10.008
Motekaitis RJ, Martell AE (1984) Complexes of aluminum(III) with hydroxy carboxylic acids. Inorg Chem 23(1):18–23. doi:10.1021/ic00169a006
Nagarajah S, Posner AM, Quirk JP (1970) Competitive adsorption of phosphate with polygalacturonate and other organic anions on kaolinite and oxide surfaces. Nature 228(5266):83–85. doi:10.1038/228083a0
Nautiyal CS (1999) An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett 170(1):265–270. doi:10.1111/j.1574-6968.1999.tb13383.x
Novais RF, Smith TJ (1999) Fósforo em solo e planta em condições tropicais, 1st edn. Editora UFV, Viçosa
Papagianni M (2007) Advances in citric acid fermentation by Aspergillus niger: biochemical aspects, membrane transport and modeling. Biotechnol Adv 25(3):244–263. doi:10.1016/j.biotechadv.2007.01.002
Papagianni M, Mattey M, Berovic M, Kristiansen B (1999) Aspergillus niger morphology and citric acid production in submerged batch fermentation: effects of culture pH, phosphate and manganese levels. Food Technol Biotechnol 37(3):165–171
Pitt JI (1979) The genus Penicillium and its teleomorphic states Eupenicillium and Talaromyces. Academic, London
Reyes I, Bernier L, Simard RR, Antoun H (1999) Effect of nitrogen source on the solubilization of different inorganic phosphates by an isolate of Penicillium rugulosum and two UV-induced mutants. FEMS Microbiol Ecol 28(3):281–290. doi:10.1016/s0168-6496(98)00119-6
Reyes I, Baziramakenga R, Bernier L, Antoun H (2001) Solubilization of phosphate rocks and minerals by a wild-type strain and two UV-induced mutants of Penicillium rugulosum. Soil Biol Biochem 33(12–13):1741–1747. doi:10.1016/S0038-0717(01)00099-2
Schneider KD, van Straaten P, de Orduna RM, Glasauer S, Trevors J, Fallow D, Smith PS (2010) Comparing phosphorus mobilization strategies using Aspergillus niger for the mineral dissolution of three phosphate rocks. J Appl Microbiol 108(1):366–374. doi:10.1111/j.1365-2672.2009.04489.x
Scott AJ, Knott M (1974) A cluster analysis method for grouping means in the analysis of variance. Biometrics 30(3):507–512
Shaff J, Schultz B, Craft E, Clark R, Kochian L (2010) GEOCHEM-EZ: a chemical speciation program with greater power and flexibility. Plant Soil 330(1):207–214. doi:10.1007/s11104-009-0193-9
Shu P, Johnson MJ (1948) The interdependence of medium constituents in citric acid production by submerged fermentation. J Bacteriol 56(5):577–585
Silva IR, Smyth TJ, Raper CD, Carter TE, Rufty TW (2001) Differential aluminum tolerance in soybean: an evaluation of the role of organic acids. Physiol Plant 112(2):200–210. doi:10.1034/j.1399-3054.2001.1120208.x
Smith RM, Martell AE (1987) Critical stability constants, enthalpies and entropies for the formation of metal complexes of aminopolycarboxylic acids and carboxylic acids. Sci Total Environ 64(1–2):125–147. doi:10.1016/0048-9697(87)90127-6
Stumm W (1986) Coordinative interactions between soil solids and water—an aquatic chemist’s point of view. Geoderma 38(1–4):19–30. doi:10.1016/0016-7061(86)90004-2
Vaccari DA, Strigul N (2011) Extrapolating phosphorus production to estimate resource reserves. Chemosphere 84(6):792–797. doi:10.1016/j.chemosphere.2011.01.052
Vassilev N, Franco I, Vassileva M, Azcon R (1996) Improved plant growth with rock phosphate solubilized by Aspergillus niger grown on sugar-beet waste. Bioresour Technol 55(3):237–241. doi:10.1016/0960-8524(96)00008-9
Vassileva M, Vassilev N, Azcon R (1998) Rock phosphate solubilization by Aspergillus niger on olive cake-based medium and its further application in a soil-plant system. World J Microbiol Biotechnol 14(2):281–284. doi:10.1023/A:1008858802855
Vassilev N, Medina A, Azcon R, Vassileva M (2006a) Microbial solubilization of rock phosphate on media containing agro-industrial wastes and effect of the resulting products on plant growth and P uptake. Plant Soil 287(1–2):77–84. doi:10.1007/s11104-006-9054-y
Vassilev N, Vassileva M, Nikolaeva I (2006b) Simultaneous P-solubilizing and biocontrol activity of microorganisms: potentials and future trends. Appl Microbiol Biotechnol 71(2):137–144. doi:10.1007/s00253-006-0380-z
Wakelin SA, Warren RA, Harvey PR, Ryder MH (2004) Phosphate solubilization by Penicillium spp. closely associated with wheat roots. Biol Fertil Soils 40(1):36–43. doi:10.1007/s00374-004-0750-6
Watanabe T (2002) Pictorial atlas of soil and seed fungi: morphologies of cultured fungi and key to species, 2nd edn. CRC Press, Boca Raton
Welch SA, Taunton AE, Banfield JF (2002) Effect of microorganisms and microbial metabolites on apatite dissolution. Geomicrobiol J 19(3):343–367. doi:10.1080/01490450290098414
Whitelaw MA (1999) Growth promotion of plants inoculated with phosphate-solubilizing fungi. Adv Agron 69:99–151. doi:10.1016/S0065-2113(08)60948-7
Whitelaw MA, Harden TJ, Helyar KR (1999) Phosphate solubilisation in solution culture by the soil fungus Penicillium radicum. Soil Biol Biochem 31(5):655–665. doi:10.1016/S0038-0717(98)00130-8
Xiao CQ, Chi RA, Huang XH, Zhang WX, Qiu GZ, Wang DZ (2008) Optimization for rock phosphate solubilization by phosphate-solubilizing fungi isolated from phosphate mines. Ecol Eng 33(2):187–193. doi:10.1016/j.ecoleng.2008.04.001
Xu D-B, Madrid CP, Röhr M, Kubicek CP (1989) The influence of type and concentration of the carbon source on production of citric acid by Aspergillus niger. Appl Microbiol Biotechnol 30(6):553–558. doi:10.1007/bf00255358
Acknowledgments
The authors are grateful to Luis Roberto Batista and Fabiana Reinis F. Passamini for their assistance in identifying the fungal isolates. Thanks are also due to Victor S. Pylro for his suggestions on preparing the manuscript. The authors are grateful to the National Council for Scientific and Technological Development (CNPq) for financing this work and providing scholarships to the first and last authors. Financial support for this study was provided by “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Capes/Brasil Fundação de Amparo à Pesquisa do Estado de Minas Gerais, FAPEMIG (GAG-APQ-00712-12)” and the Spanish projects CTM2011-027797 and P09RNM-5196.
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de Oliveira Mendes, G., Moreira de Freitas, A.L., Liparini Pereira, O. et al. Mechanisms of phosphate solubilization by fungal isolates when exposed to different P sources. Ann Microbiol 64, 239–249 (2014). https://doi.org/10.1007/s13213-013-0656-3
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DOI: https://doi.org/10.1007/s13213-013-0656-3