Abstract
Fungi have received particular attention in regards to alternatives for bioremediation of heavy metal contaminated locales. Enzymes produced by filamentous fungi, such as phosphatases, can precipitate heavy metal ions in contaminated environments, forming metal phosphates (insoluble). Thus, this research aimed to analyze fungi for uranium biomineralization capacity. For this, Gongronella butleri, Penicillium piscarium, Rhodotorula sinensis and Talaromyces amestolkiae were evaluated. Phytate and glycerol 2-phosphate were used as the phosphate sources in the culture media at pH 3.5 and 5.5, with and without uranium ions. After 4 weeks of fungal growth, evaluated fungi were able to produce high concentrations of phosphates in the media. T. amestolkiae was the best phosphate producer, using phytate as an organic source. During fungal growth, there was no change in pH level of the culture medium. After 3 weeks of T. amestolkiae growth in medium supplemented with phytate, there was a reduction between 20 and 30% of uranium concentrations, with high precipitation of uranium and phosphate on the fungal biomass. The fungi analyzed in this research can use the phytic acid present in the medium and produce high concentrations of phosphate; which, in the environment, can assist in the heavy metal biomineralization processes, even in acidic environments. Such metabolic capabilities of fungi can be useful in decontaminating uranium-contaminated environments.
Similar content being viewed by others
References
Awad GEA, Helal MMI, Danial EN, Esawy MA (2014) Optimization of phytase production by Penicillium purpurogenum GE1 under solid state fermentation by using Box–Behnken design. Saudi J Biol Sci 21:81. https://doi.org/10.1016/J.SJBS.2013.06.004
Bengtsson L, Johansson B, Hackett TJ, McHale L, McHale AP (1995) Studies on the biosorption of uranium by Talaromyces emersonii CBS 814.70 biomass. Appl Microbiol Biotechnol 42:807–811. https://doi.org/10.1007/BF00171965
Cárdenas González JF, Rodríguez Pérez AS, Vargas Morales JM, Martínez Juárez VM, Rodríguez IA, Cuello CM, Fonseca GG, Escalera Chávez ME, Muñoz Morales A (2019) Bioremoval of cobalt(II) from aqueous solution by three different and resistant fungal biomasses. Bioinorg Chem Appl 2019:8757149. https://doi.org/10.1155/2019/8757149
Cavalheiro GF, Sanguine IS, da Silva Santos FR, da Costa AC, Fernandes M, da Paz MF, Fonseca GG, Leite RSR (2017) Catalytic properties of amylolytic enzymes produced by Gongronella butleri using agroindustrial residues on solid-state fermentation. BioMed Res Int 2017:1–8. https://doi.org/10.1155/2017/7507523
Coelho E, Reis TA, Cotrim M, Mullan TK, Corrêa B (2020a) Resistant fungi isolated from contaminated uranium mine in Brazil shows a high capacity to uptake uranium from water. Chemosphere. https://doi.org/10.1016/j.chemosphere.2020.126068
Coelho E, Reis TA, Cotrim M, Rizzutto M, Corrêa B (2020b) Bioremediation of water contaminated with uranium using Penicillium piscarium. Biotechnol Prog. https://doi.org/10.1002/btpr.3032
Cumberland SA, Douglas G, Grice K, Moreau JW (2016) Uranium mobility in organic matter-rich sediments: a review of geological and geochemical processes. Earth Sci Rev 159:160–185. https://doi.org/10.1016/J.EARSCIREV.2016.05.010
Das D, Chakraborty A, Santra SC (2019) Assessment of lead tolerance in gamma exposed Aspergillus niger van Tieghem & Penicillium cyclopium Westling. Int J Radiat Biol 95:771–780. https://doi.org/10.1080/09553002.2019.1569769
de Lima MAB, Nascimento AE, de Souza W, Fukushima K, de Campos-Takaki GM (2003) Effects of phosphorus on polyphosphate accumulation by Cunninghamella elegans. Braz J Microbiol 34:363–372. https://doi.org/10.1590/S1517-83822003000400016
Drangert J-O (2012) Phosphorus—a limited resource that could be made limitless. Procedia Eng 46:228–233. https://doi.org/10.1016/J.PROENG.2012.09.469
Elias F, Woyessa D, Muleta D (2016) Phosphate solubilization potential of rhizosphere fungi isolated from plants in Jimma Zone, southwest Ethiopia. Int J Microbiol 2016:1–11. https://doi.org/10.1155/2016/5472601
El-Naggar NEA, Hamouda RA, Mousa IE, Abdel-Hamid MS, Rabei NH (2018) Biosorption optimization, characterization, immobilization and application of Gelidium amansii biomass for complete Pb2+ removal from aqueous solutions. Sci Rep. https://doi.org/10.1038/s41598-018-31660-7
Fomina M, Gadd GM (2014) Biosorption: current perspectives on concept, definition and application. Bioresour Technol 160:3–14. https://doi.org/10.1016/j.biortech.2013.12.102
Gadd GM (2009) Biosorption: critical review of scientific rationale, environmental importance and significance for pollution treatment. J Chem Technol Biotechnol 84:13–28
Gadd GM, Pan X (2016) Biomineralization, bioremediation and biorecovery of toxic metals and radionuclides. Geomicrobiol J 33:175–178
Kaur R (2017) Production and characterization of a neutral phytase of Penicillium oxalicum EUFR-3 isolated from Himalayan region. Nusant Biosci. https://doi.org/10.13057/nusbiosci/n090112
Kefeni KK, Msagati TAM, Mamba BB (2017) Acid mine drainage: prevention, treatment options, and resource recovery: a review. J Clean Prod 151:475–493
Khan MS, Zaidi A, Ahemad M, Oves M, Wani PA (2010) Plant growth promotion by phosphate solubilizing fungi—current perspective. Arch Agron Soil Sci 56:73–98. https://doi.org/10.1080/03650340902806469
Khan S, Zaid MA, Ahmad E, Musarrat J (2014) Phosphate solubilizing microorganism: principles and applications of microphos technology. Springer, Berlin
Khijniak TV, Slobodkin AI, Coker V, Renshaw JC, Livens FR, Bonch-Osmolovskaya EA, Birkeland N-K, Medvedeva-Lyalikova NN, Lloyd JR (2005) Reduction of uranium(VI) phosphate during growth of the thermophilic bacterium Thermoterrabacterium ferrireducens. Appl Environ Microbiol 71:6423–6426. https://doi.org/10.1128/AEM.71.10.6423-6426.2005
Liang X, Hillier S, Pendlowski H, Gray N, Ceci A, Gadd GM (2015) Uranium phosphate biomineralization by fungi. Environ Microbiol 17:2064–2075. https://doi.org/10.1111/1462-2920.12771
Mohammed NH, Atta M, Wan Yaacub WZ (2017) Remediation of heavy metals by using industrial waste by products in acid mine drainage. Am J Eng Appl Sci 10:1001–1012. https://doi.org/10.3844/ajeassp.2017.1001.1012
Newsome L, Morris K, Lloyd JR (2014) The biogeochemistry and bioremediation of uranium and other priority radionuclides. Chem Geol 363:164–184. https://doi.org/10.1016/J.CHEMGEO.2013.10.034
Ocampo M, Patiño LF, Marín M, Salazar M, Gutiérrez PA (2012) Isolation and characterization of potential phytase-producing fungi from environmental samples of Antioquia (Colombia)/aislamiento y caracterizacin de hongos productores de fitasa a partir de muestras ambientales de Antioquia (Colombia). Rev Fac Nal Agr Medellín 65(1):6291–6303
Olstorpe M, Schnürer J, Passoth V (2009) Screening of yeast strains for phytase activity. FEMS Yeast Res 9:478–488. https://doi.org/10.1111/j.1567-1364.2009.00493.x
Paterson-Beedle M, Readman JE, Hriljac JA, Macaskie LE (2010) Biorecovery of uranium from aqueous solutions at the expense of phytic acid. Hydrometallurgy 104:524–528. https://doi.org/10.1016/J.HYDROMET.2010.01.019
Qian X, Fang C, Huang M, Achal V (2017) Characterization of fungal-mediated carbonate precipitation in the biomineralization of chromate and lead from an aqueous solution and soil. J Clean Prod 164:198–208. https://doi.org/10.1016/J.JCLEPRO.2017.06.195
Qvirist L, Carlsson N-G, Andlid T (2015) Assessing phytase activity—methods, definitions and pitfalls. J Biol Methods 2:16. https://doi.org/10.14440/jbm.2015.58
Shelobolina ES, Konishi H, Xu H, Roden EE (2009) U(VI) sequestration in hydroxyapatite produced by microbial glycerol 3-phosphate metabolism. Appl Environ Microbiol 75:5773–5778. https://doi.org/10.1128/AEM.00628-09
Sheridan C, Akcil A, Kappelmeyer U, Moodley I (2018) A review on the use of constructed wetlands for the treatment of acid mine drainage. In: Constructed wetlands for industrial wastewater treatment. Wiley, Chichester, pp 249–262
Someus E, Pugliese M (2018) Concentrated phosphorus recovery from food grade animal bones. Sustainability 10:1–17. https://doi.org/10.3390/su10072349
Vassilev N, de Oliveira Mendes G (2017) Solid-state fermentation and plant-beneficial microorganisms. Curr Dev Biotechnol Bioeng. https://doi.org/10.1016/b978-0-444-63990-5.00019-0
Vera DF, Perez H, Valencia H (2011) Aislamiento de hongos solubilizadores de fosfatos de la rizosfera de araza (Eugenia stipitata, Myrtaceae). Acta Biol Colomb 7:33–40. https://doi.org/10.1016/j.riam.2009.03.005
Wang N, Qiu Y, Xiao T, Wang J, Chen Y, Xu X, Kang Z, Fan L, Yu H (2019) Comparative studies on Pb(II) biosorption with three spongy microbe-based biosorbents: high performance, selectivity and application. J Hazard Mater 373:39–49. https://doi.org/10.1016/j.jhazmat.2019.03.056
Zheng XY, Shen YH, Wang XY, Wang TS (2018) Effect of pH on uranium(VI) biosorption and biomineralization by Saccharomyces cerevisiae. Chemosphere 203:109–116. https://doi.org/10.1016/J.CHEMOSPHERE.2018.03.165
Acknowledgements
The author thanks Fundação de Amparo à Pesquisa do Estado de São Paulo and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior for funding and research support (FAPESP: 2015/06757-1).
Author information
Authors and Affiliations
Contributions
EC, JR, MR, and BC devised the research. EC, TAR, and MC conducted the experiments. EC, TM, JR, and BC conducted the modeling. EC, TAR, and BC wrote the manuscript. All authors discussed the data, results and commented on the manuscript. BC and JR supervised the project.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that there are no competing financial interests and non-financial interests.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Coelho, E., Reis, T.A., Cotrim, M. et al. Talaromyces amestolkiae uses organic phosphate sources for the treatment of uranium-contaminated water. Biometals 35, 335–348 (2022). https://doi.org/10.1007/s10534-022-00374-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10534-022-00374-9