Interactions of phosphate solubilising microorganisms with natural rare-earth phosphate minerals: a study utilizing Western Australian monazite

Abstract

Many microbial species are capable of solubilising insoluble forms of phosphate and are used in agriculture to improve plant growth. In this study, we apply the use of known phosphate solubilising microbes (PSM) to the release of rare-earth elements (REE) from the rare-earth phosphate mineral, monazite. Two sources of monazite were used, a weathered monazite and mineral sand monazite, both from Western Australia. When incubated with PSM, the REE were preferentially released into the leachate. Penicillum sp. released a total concentration of 12.32 mg L−1 rare-earth elements (Ce, La, Nd, and Pr) from the weathered monazite after 192 h with little release of thorium and iron into solution. However, cultivation on the mineral sands monazite resulted in the preferential release of Fe and Th. Analysis of the leachate detected the production of numerous low-molecular weight organic acids. Gluconic acid was produced by all microorganisms; however, other organic acids produced differed between microbes and the monazite source provided. Abiotic leaching with equivalent combinations of organic acids resulted in the lower release of REE implying that other microbial processes are playing a role in solubilisation of the monazite ore. This study demonstrates that microbial solubilisation of monazite is promising; however, the extent of the reaction is highly dependent on the monazite matrix structure and elemental composition.

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References

  1. 1.

    Long KR, Van Gosen BS, Foley NK, Cordier D (2012) The principle rare earth elements deposits of the United States: a summary of domestic deposits and a global perspective. In: Larsen RS, Wellmer F-W (eds) Non-renewable resource issues: geoscientific and societal challenges, Springer, New York

    Google Scholar 

  2. 2.

    EPA US (2012) Rare earth elements: a review of production, processing, recycling and associated environmental issues. National Risk Management Research Laboratory

  3. 3.

    Chu S (2011) Critical materials strategy. In: Energy UDo (ed) United States of America, p 189

  4. 4.

    Gupta CK, Krishnamurthy N (2004) Extractive Metallurgy of Rare Earths, CRC Press

  5. 5.

    Neelameggham NR, Alam S, Oosterhof H, Jha AA, Wang S (2014) Rare metal technology 2014. Wiley, Hoboken

    Google Scholar 

  6. 6.

    Falconer A (2003) Gravity separation: old technique/new methods. Phys Sep Sci Eng 12:31–48

    CAS  Article  Google Scholar 

  7. 7.

    Zhang J, Zhao B, Schreiner B (2016) Separation hydrometallurgy of rare earth elements. Springer, Berlin

    Google Scholar 

  8. 8.

    Fuerstenau D (2013) Design and development of novel flotation reagents for the beneficiation of mountain pass rare-earth ore. Miner Metall Process 30:1–9

    Google Scholar 

  9. 9.

    Jha MK, Kumari A, Panda R, Rajesh Kumar J, Yoo K, Lee JY (2016) Review on hydrometallurgical recovery of rare earth metals. Hydrometallurgy 161:77

    CAS  Article  Google Scholar 

  10. 10.

    Ragheb M (2011) Thorium resources in rare earth elements.

  11. 11.

    Brady PV, House WA (1996) Surface-controlled dissolution and growth of minerals. Brady PV (ed) Physics and chemistry of mineral surfaces. CRC Press, Boca Raton

    Google Scholar 

  12. 12.

    Emsbo P, McLaughlin PI, Breit GN, Du Bray EA, Koenig AE (2015) Rare earth elements in sedimentary phosphate deposits: solution to the global REE crisis? Gondwana Res 27:776–785

    CAS  Article  Google Scholar 

  13. 13.

    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

    Article  Google Scholar 

  14. 14.

    Son HJ, Park GT, Cha MS, Heo MS (2006) Solubilization of insoluble inorganic phosphates by a novel salt-and pH-tolerant Pantoea agglomerans R-42 isolated from soybean rhizosphere. Bioresour Technol 97:204–210

    CAS  Article  Google Scholar 

  15. 15.

    Igual JM, Valverde A, Cervantes E, Velázquez E (2001) Phosphate-solubilizing bacteria as inoculants for agriculture: use of updated molecular techniques in their study. Agronomie 21:561–568

    Article  Google Scholar 

  16. 16.

    Taunton AE, Welch SA, Banfield JF (2000) Geomicrobiological controls on light rare earth element, Y and Ba distributions during granite weathering and soil formation. J Alloys Compd 303:30–36

    Article  Google Scholar 

  17. 17.

    Feng MH, Ngwenya BT, Wang L, Li WC, Olive V, Ellam RM (2011) Bacterial dissolution of fluorapatite as a possible source of elevated dissolved phosphate in the environment. Geochim Et Cosmochim Acta 75:5785–5796

    CAS  Article  Google Scholar 

  18. 18.

    Watling HR (2015) Review of biohydrometallurgical metals extraction from polymetallic mineral resources. Minerals 5:1–60

    Article  Google Scholar 

  19. 19.

    Qu Y, Lian B (2013) Bioleaching of rare earth and radioactive elements from red mud using Penicillium tricolor RM-10. Bioresour Technol 136:16–23

    CAS  Article  Google Scholar 

  20. 20.

    Brisson VL, Zhuang W-Q, Alvarez-Cohen L (2016) Bioleaching of rare earth elements from monazite sand. Biotechnol Bioeng 113:339–348

    CAS  Article  Google Scholar 

  21. 21.

    Shin D, Kim J, Kim B, Jeong J, Lee J (2015) Use of phosphate solubilizing bacteria to leach rare earth elements from monazite bearing ore. Minerals 5:189–202

    Article  Google Scholar 

  22. 22.

    Domic EM (2007) A review of the development and current status of copper bioleaching operations in Chile: 25 years of successful commercial implementation. In: Rawlings DE, Johnson DB (eds) Biomining. Springer, Berlin

    Google Scholar 

  23. 23.

    Bosecker K (1997) Bioleaching: metal solubilization by microorganisms. FEMS Microbiol Rev 20:591–604

    CAS  Article  Google Scholar 

  24. 24.

    Lane DJ (1991) 16s/23s rRNA sequencing. Nucleic acid techniques in bacterial systematics, Wiley, New York

    Google Scholar 

  25. 25.

    Al-Samarrai TH, Schmid J (2000) A simple method for extraction of fungal genomic DNA. Lett Appl Microbiol 30:53–56

    CAS  Article  Google Scholar 

  26. 26.

    White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. Academic Press, San Diego

    Google Scholar 

  27. 27.

    Nautiyal CS (1999) An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett 170:265–270

    CAS  Article  Google Scholar 

  28. 28.

    Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36

    CAS  Article  Google Scholar 

  29. 29.

    Lide DR, Frederikse HPR (1995) Dissociation constants of organic acids and bases. CRC handbook of chemistry and physics

  30. 30.

    Uroz S, Calvaruso C, Turpault MP, Frey-Klett P (2009) Mineral weathering by bacteria: ecology, actors and mechanisms. Trends Microbiol 17:378–387

    CAS  Article  Google Scholar 

  31. 31.

    Binnemans K, Jones PT, Blanpain B, Van Gerven T, Yang Y, Walton A, Buchert M (2013) Recycling of rare earths: a critical review. J Cleaner Prod 51:1–22

    CAS  Article  Google Scholar 

  32. 32.

    Dave SR, Kaur H, Menon SK (2010) Selective solid-phase extraction of rare earth elements by the chemically modified amberlite XAD-4 resin with azacrown ether. React Funct Polym 70:692–698

    CAS  Article  Google Scholar 

  33. 33.

    Van den Bogaert B, Havaux D, Binnemans K, Van Gerven T (2015) Photochemical recycling of europium from Eu/Y mixtures in red lamp phosphor waste streams. Green Chem 17:2180–2187

    Article  Google Scholar 

  34. 34.

    Marsden JO, House CI (1960) The chemistry of gold extraction, 2nd edn. Society for Mining, Metallurgy and Exploration, Inc., United States of America

    Google Scholar 

  35. 35.

    Johnson SE, Loeppert RH (2006) Role of organic acids in phosphate mobilization from iron oxide. Soil Sci Soc Am J 70:222–234

    CAS  Article  Google Scholar 

  36. 36.

    Jorjani E, Shahbazi M (2012) The production of rare earth elements group via tributyl phosphate extraction and precipitation stripping using oxalic acid. Arab J Chem

  37. 37.

    Woyski MM, Harris RE (1963) Treatise on analytical chemistry. Interscience Publishers, New York

    Google Scholar 

  38. 38.

    Xie F, Zhang TA, Dreisinger D, Doyle F (2014) A critical review on solvent extraction of rare earths from aqueous solutions. Miner Eng 56:10–28

    CAS  Article  Google Scholar 

  39. 39.

    Vander Hoogerstraete T, Wellens S, Verachtert K, Binnemans K (2013) Removal of transition metals from rare earths by solvent extraction with an undiluted phosphonium ionic liquid: separations relevant to rare-earth magnet recycling. Green Chem 15:919–927

    CAS  Article  Google Scholar 

  40. 40.

    Illmer P, Schinner F (1995) Solubilization of inorganic calcium phosphates—solubilization mechanisms. Soil Biol Biochem 27:257–263

    CAS  Article  Google Scholar 

  41. 41.

    Scofield V, Jacques SMSs, Guimarães JRD, Farjalla VF (2015) Potential changes in bacterial metabolism associated with increased water temperature and nutrient inputs in tropical humic lagoons. Front Microbiol 6:310

    Article  Google Scholar 

  42. 42.

    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

    CAS  Article  Google Scholar 

  43. 43.

    Chi R, Xu Z (1999) A solution chemistry approach to the study of rare earth element precipitation by oxalic acid. Metall Mater Trans B 30:189–195

    Article  Google Scholar 

  44. 44.

    Alam S, Kim H, Neelameggham NR, Ouchi T, Oosterhof H (2016) Rare metal technology 2016. Wiley, Hoboken

    Google Scholar 

  45. 45.

    Lopes CFF, Iha K, Neves EA, Suárez-Iha MEV (1996) A comparison of carboxylate complexes of lanthanum (iii): formate, acetate and propionate. J Coord Chem 40:27–34

    CAS  Article  Google Scholar 

  46. 46.

    Sawyer DT, Ambrose RT (1962) Cerium (IV) gluconate complexes. Inorg Chem 1:296–303

    CAS  Article  Google Scholar 

  47. 47.

    Jones DL (1998) Organic acids in the rhizosphere—a critical review. Plant Soil 205:25–44

    CAS  Article  Google Scholar 

  48. 48.

    Sinha SP (1966) Complexes of the rare earths. Pergamon Press Ltd, London

    Google Scholar 

  49. 49.

    Goyne KW, Brantley SL, Chorover J (2010) Rare earth element release from phosphate minerals in the presence of organic acids. Chem Geol 278:1–14

    CAS  Article  Google Scholar 

  50. 50.

    Van Hees PAW, Jones DL, Godbold DL (2003) Biodegradation of low molecular weight organic acids in a limed forest soil. Water Air Soil Pollut Focus 3:121–144

    Article  Google Scholar 

  51. 51.

    Max B, Salgado JM, Rodríguez N, Cortés S, Converti A, Domínguez JM (2010) Biotechnological production of citric acid. Braz J Microbiol 41:862–875

    CAS  Article  Google Scholar 

  52. 52.

    Clark DS, Ito K, Horitsu H (1966) Effect of manganese and other heavy metals on submerged citric acid fermentation of molasses. Biotechnol Bioeng 8:465–471

    CAS  Article  Google Scholar 

  53. 53.

    Acharya C, Kar RN, Sukla LB (2003) Studies on reaction mechanism of bioleaching of manganese ore. Miner Eng 16:1027–1030

    CAS  Article  Google Scholar 

  54. 54.

    Donati ER, Sand W (2007) Microbial processing of metal sulfides. Springer, Netherlands

    Google Scholar 

  55. 55.

    Adrio JL, Demain AL (2005) Microbial enzymes and biotransformations. Humana Press Inc, Totowa

    Google Scholar 

  56. 56.

    Clark DS, Blanch HW (1997) Biochemical engineering, 2nd edn. Taylor & Francis, London

    Google Scholar 

  57. 57.

    Bonnarme P, Gillet B, Sepulchre AM, Role C, Beloeil JC, Ducrocq C (1995) Itaconate biosynthesis in Aspergillus terreus. J Bacteriol 177:3573–3578

    CAS  Article  Google Scholar 

  58. 58.

    Fox TR, Comerford NB (1992) Influence of oxalate loading on phosphorus and aluminum solubility in spodosols. Soil Sci Soc Am J 56:290–294

    CAS  Article  Google Scholar 

  59. 59.

    Walpola BC, Arunakumara KKIU, Yoon MH (2014) Isolation and characterisation of phosphate solubilizing bacteria (Klebiella oxytoca) with enhanced tolerant to environmental stress. Afr J Micrbiol Res 8:2970–2978

    CAS  Article  Google Scholar 

  60. 60.

    Chung H, Park M, Madhaiyan M, Seshadri S, Song J, Cho H, Sa T (2005) Isolation and characterization of phosphate solubilizing bacteria from the rhizosphere of crop plants of Korea. Soil Biol Biochem 37:1970–1974

    CAS  Article  Google Scholar 

  61. 61.

    Brynhildsen L, Rosswall T (1989) Effects of cadmium, copper, magnesium, and zinc on the decomposition of citrate by a Klebsiella sp. Appl Environ Microbiol 55:1375–1379

    CAS  Google Scholar 

  62. 62.

    Illmer P, Schinner F (1997) Influence of aluminum on motility and swarming of Pseudomonas sp. and. Arthrobacter sp. FEMS Microbiol Lett 155:121–124

    CAS  Article  Google Scholar 

  63. 63.

    Sulbarán M, Pérez E, Ball MM, Bahsas A, Yarzábal LA (2009) Characterization of the mineral phosphate-solubilizing activity of Pantoea agglomerans MMB051 isolated from an iron-rich soil in Southeastern Venezuela (Bolívar state). Curr Microbiol 58:378–383

    Article  Google Scholar 

  64. 64.

    Jauregui MA, Reisenauer HM (1982) Dissolution of oxides of manganese and iron by root exudate components. Soil Sci Soc Am J 46:314–317

    CAS  Article  Google Scholar 

  65. 65.

    Martin JE, Waters LS, Storz G, Imlay JA (2015) The Escherichia coli small protein MntS and exporter MntP optimize the intracellular concentration of manganese. PLos Genet 11:e1004977

    Article  Google Scholar 

  66. 66.

    Rodriguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339

    CAS  Article  Google Scholar 

  67. 67.

    Kim Y-H, Bae B, Choung Y-K (2005) Optimization of biological phosphorus removal from contaminated sediments with phosphate-solubilizing microorganisms. J Biosci Bioeng 99:23–29

    CAS  Article  Google Scholar 

  68. 68.

    Malboobi MA, Owlia P, Behbahani M, Sarokhani E, Moradi S, Yakhchali B, Deljou A, Morabbi Heravi K (2009) Solubilization of organic and inorganic phosphates by three highly efficient soil bacterial isolates. World J Microbiol Biotechnol 25:1471–1477

    CAS  Article  Google Scholar 

  69. 69.

    Rodriguez H, Gonzalez T, Goire I, Bashan Y (2004) Gluconic acid production and phosphate solubilization by the plant growth-promoting bacterium Azospirillum spp. Naturwissenschaften 91:552–555

    CAS  Article  Google Scholar 

  70. 70.

    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 App Microbiol 108:366–374

    CAS  Article  Google Scholar 

  71. 71.

    Ben Farhat M, Farhat A, Bejar W, Kammoun R, Bouchaala K, Fourati A, Antoun H, Bejar S, Chouayekh H (2009) Characterization of the mineral phosphate solubilizing activity of Serratia marcescens CTM 50650 isolated from the phosphate mine of Gafsa. Arch Microbiol 191:815–824

    CAS  Article  Google Scholar 

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Acknowledgements

This research was funded by the Minerals Research Institute of Western Australia (M434), supported by Curtin Health Innovation Research Institute and Minerals Engineering, Curtin University. We acknowledge the use of Curtin University’s Microscopy and Microanalysis Facility, whose instrumentation has been partially funded by the University, State and Commonwealth Governments. We are grateful to the Lynas Corporation for funding and donation of a weathered monazite ore.

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Correspondence to Elizabeth L. J. Watkin.

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Corbett, M.K., Eksteen, J.J., Niu, X. et al. Interactions of phosphate solubilising microorganisms with natural rare-earth phosphate minerals: a study utilizing Western Australian monazite. Bioprocess Biosyst Eng 40, 929–942 (2017). https://doi.org/10.1007/s00449-017-1757-3

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Keywords

  • Monazite
  • Rare-earth elements
  • Phosphate solubilising microorganisms
  • Bioleaching
  • Recovery rates