Skip to main content
SpringerLink
Log in

The dissolution of fluorapatite by phosphate-solubilizing fungi: a balance between enhanced phosphorous supply and fluorine toxicity

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Fluorapatite (FAp) is the largest phosphorous (P) reservoir on Earth. However, due to its low solubility, dissolved P is severely deficient in the pedosphere. Fungi play a significant role in P dissolution via excretion of organic acids, and in this regard, it is important to understand their impact on P cycling. The object of this study was to elucidate the balance between P release and F toxicity during FAp dissolution. The bioweathering of FAp was assisted by a typical phosphate-solubilizing fungus, Aspergillus niger. The release of elements and microbial activities were monitored during 5-day incubation. We found that the release of fluorine (F) was activated after day 1 (~90 mg/L), which significantly lowered the phosphate-solubilizing process by day 2. Despite P release from FAp being enhanced over the following 3 days, decreases in both the amount of biomass (52% decline) and the respiration rate (81% decline) suggest the strong inhibitory effect of F on the fungus. We thus concluded that F toxicity outweighs P supply, which in turn inhibits fungi growth and prevents further dissolution of FAp. This mechanism might reflect an underappreciated cause for P deficiency in soils.

Graphical abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1.
Figure 2.
Figure 3.
Figure 4.
Figure 5.
Figure 6.
Figure 7.

Similar content being viewed by others

References

  • Barbier O, Arreola-Mendoza L, Del Razo LM (2010) Molecular mechanisms of fluoride toxicity. Chem Biol Interact 188:319–333

    Article  CAS  Google Scholar 

  • Bartolomeesteban H, Schenck NC (1994) Spore germination and hyphal growth of arbuscular mycorrhizal fungi in relation to soil aluminum saturation. Mycologia 86:217–226

    Article  CAS  Google Scholar 

  • Brahim K, Soussi-Baatout A, Khattech I, Jemal M (2017) Dissolution kinetics of fluorapatite in the hydrochloric acid solution. J Therm Anal Calorim 129:701–708

    Article  CAS  Google Scholar 

  • Brindha K, Jagadeshan G, Kalpana L, Elango L (2016) Fluoride in weathered rock aquifers of southern India: managed aquifer recharge for mitigation. Environ Sci Pollut Res 23(9):8302–8316

    Article  CAS  Google Scholar 

  • Butler OM, Elser JJ, Lewis T, Mackey B, Chen CR (2018) The phosphorus-rich signature of fire in the soil-plant system: a global meta-analysis. Ecol Lett 21:335–344

    Article  Google Scholar 

  • Chen XB, Wright JV, Conca JL, Peurrung LM (1997) Evaluation of heavy metal remediation using mineral apatite. Water Air Soil Pollut 98:57–78

    Article  CAS  Google Scholar 

  • Edwards HGM, Russell NC, Weinstein R, Wynnwilliams DD (1995) Fourier transform Raman spectroscopic study of fungi. J Raman Spectrosc 26:911–916

    Article  CAS  Google Scholar 

  • Fuge R (2019) Fluorine in the environment, a review of its sources and geochemistry. Appl Geochem 100:393–406

    Article  CAS  Google Scholar 

  • Gadd GM (2005) Microorganisms in toxic metal-polluted soils. Soil Bio 3:325–356

    Article  CAS  Google Scholar 

  • Ghosh A, Mukherjee K, Ghosh SK, Saha B (2013) Sources and toxicity of fluoride in the environment. Res Chem Intermed 39:2881–2915

    Article  CAS  Google Scholar 

  • Ji C, Stockbridge RB, Miller C (2014) Bacterial fluoride resistance, Fluc channels, and the weak acid accumulation effect. J Gen Physiol 144:257–261

    Article  CAS  Google Scholar 

  • Jones DL, Oburger E (2011) Solubilization of phosphorus by soil microorganisms. In: Bünemann EOA, Frossard E (eds) Phosphorus in Action: Biological Processes in Soil Phosphorus Cycling. Springer Berlin Heidelberg, Berlin, pp 169–198

    Chapter  Google Scholar 

  • Kauwenbergh, S.J.V. (2006) Fertilizer raw material resources of Africa.

    Google Scholar 

  • Konhauser K, Fyfe W, Schultze-Lam S, Ferris F, Beveridge T (2011) Iron phosphate precipitation by epilithic microbial biofilms in Arctic Canada. Can J Earth Sci 31:1320–1324

    Article  Google Scholar 

  • Lebioda L, Zhang E, Lewinski K, Brewer JM (1993) Fluoride inhibition of yeast enolase: crystal structure of the enolase–Mg2+–F−–Pi complex at 2.6 Å resolution. Proteins 16:219–225

    Article  CAS  Google Scholar 

  • Li L (2003) The biochemistry and physiology of metallic fluoride: action, mechanism, and implications. Crit Rev Oral Biol Med 14:100–114

    Article  Google Scholar 

  • Li Z, Liu L, Chen J, Teng HH (2016a) Cellular dissolution at hypha- and spore-mineral interfaces revealing unrecognized mechanisms and scales of fungal weathering. Geology 44:319–322

    Article  CAS  Google Scholar 

  • Li Z, Wang FW, Bai TS, Tao JJ, Guo JY, Yang MY et al (2016b) Lead immobilization by geological fluorapatite and fungus Aspergillus niger. J Hazard Mater 320:386–392

    Article  CAS  Google Scholar 

  • Li Z, Bai TS, Dai LT, Wang FW, Tao JJ, Meng ST et al (2016c) A study of organic acid production in contrasts between two phosphate solubilizing fungi: Penicillium oxalicum and Aspergillus niger. Sci Rep 6:25313

    Article  CAS  Google Scholar 

  • Mcmillen BG, Juniper S, Abbott LK (1998) Inhibition of hyphal growth of a vesicular-arbuscular mycorrhizal fungus in soil containing sodium chloride limits the spread of infection from spores. Soil Biol Biochem 30:1639–1646

    Article  CAS  Google Scholar 

  • Mendes GDO, Vassilev N, Bonduki VHA, Silva IRD, Ribeiro JI, Costa MD (2013) Inhibition of Aspergillus niger phosphate solubilization by fluoride released from rock phosphate. Appl Environ Microbiol 79:4906–4913

    Article  CAS  Google Scholar 

  • Moody SC, Bull JC, Dudley E, Loveridge EJ (2019) The impact of combinatorial stress on the growth dynamics and metabolome of Burkholderia mesoacidophila demonstrates the complexity of tolerance mechanisms. J Appl Microbiol 127:1521–1531

    Article  CAS  Google Scholar 

  • Moradi H, Ahmad A, Shepherdson D, Vuong NH, Niedbala G, Eapen L, Vanderhyden B, Nyiri B, Murugkar S (2017) Raman micro-spectroscopy applied to treatment resistant and sensitive human ovarian cancer cells. J Biophotonics 10:1327–1334

    Article  CAS  Google Scholar 

  • Natasha G (2009) The Disappearing Nutrient. Nature 461:716–718

    Article  Google Scholar 

  • Ochoa-Herrera V, Banihani Q, Leon G, Khatri C, Field JA, Sierra-Alvarez R (2009) Toxicity of fluoride to microorganisms in biological wastewater treatment systems. Water Res 43:3177–3186

    Article  CAS  Google Scholar 

  • Palma-Guerrero J, Jansson HB, Salinas J, Lopez-Llorca LV (2008) Effect of chitosan on hyphal growth and spore germination of plant pathogenic and biocontrol fungi. J Appl Microbiol 104:541–553

    CAS  Google Scholar 

  • Pan HB, Darvell BW (2007) Solubility of calcium fluoride and fluorapatite by solid titration. Arch Oral Biol 52:861–868

    Article  CAS  Google Scholar 

  • Pan YM, Fleet ME (2002) Compositions of the apatite-group minerals: substitution mechanisms and controlling factors. Rev Mineral Geochem 48:13–49

    Article  CAS  Google Scholar 

  • Pickering W (1985) The mobility of soluble fluoride in soils. Environ Pollut B 9:281–308

    Article  CAS  Google Scholar 

  • Plata LG, Ramos CG, Oliveira MLS, Oliveira LFS (2021) Release kinetics of multi-nutrients from volcanic rock mining by-products: evidences for their use as a soil remineralizer. J Clean Prod 279:123668

    Article  CAS  Google Scholar 

  • Roberts TL, Stewart JWB, Bettany JR (1985) The influence of topography on the distribution of organic and inorganic soil phosphorus across a narrow environmental gradient. Can J Soil Sci 65:651–665

    Article  CAS  Google Scholar 

  • Song JF, Ru JX, Liu XP, Cui XY (2019) Oxalic acid and succinic acid mediate the weathering process of granite in the cold-temperate forest regions of northeast China. Eurasian Soil Sci 52:903–915

    Article  CAS  Google Scholar 

  • Tew K (2018) Fetter CW, Boving T, Kreamer D (eds): Contaminant hydrogeology. Environ Earth Sci 77:745

    Article  Google Scholar 

  • Tiessen H, Stewart JWB, Cole CV (1984) Pathways of phosphorus transformations in soils of differing pedogenesis. Soil Sci Soc Am J 48:853–858

    Article  CAS  Google Scholar 

  • Wainwright M, Ali TA, Barakah F (1993) A review of the role of oligotrophic micro-organisms in biodeterioration. Int Biodeterior Biodegrad 31:1–13

    Article  Google Scholar 

  • Walan P, Davidsson S, Johansson S, Höök M (2014) Phosphate rock production and depletion: regional disaggregated modeling and global implications. Resour Conserv Recycl 93:178–187

    Article  Google Scholar 

  • Wang L, Nancollas GH (2008) Calcium orthophosphates: crystallization and dissolution. Chem Rev 108:4628–4669

    Article  CAS  Google Scholar 

  • Whitelaw MA (2000) Growth promotion of plants inoculated with phosphate-solubilizing fungi. Adv Agron 69:99–151

    Article  CAS  Google Scholar 

  • Yadav KK, Kumar S, Pham QB, Gupta N, Rezania S, Kamyab H, Yadav S, Vymazal J, Kumar V, Tri DQ, Talaiekhozani A, Prasad S, Reece LM, Singh N, Maurya PK, Cho J (2019) Fluoride contamination, health problems and remediation methods in Asian groundwater: a comprehensive review. Ecotoxicol Environ Saf 182:109362

    Article  CAS  Google Scholar 

  • Yin DX, Zeng AL (1993) Phosphorus resources, soil phosphorus status and application of phosphorus fertilizer in Guizhou Province. Guizhou Agricul Sci 013:49–53

    Google Scholar 

  • Zhang Q, Qiu Y, Cao J, Wang Y, Hu J (2014) Study on the rare earth containing phosphate rock in guizhou and the way to concentrate phosphate and rare earth metal thereof. J Powder Metallurgy & Mining 3:44–55

    Google Scholar 

  • Zhou M, Wang H, Zhu S, Liu Y, Xu J (2015) Electrokinetic remediation of fluorine-contaminated soil and its impact on soil fertility. Environ Sci Pollut Res 22(21):16907–16913

    Article  CAS  Google Scholar 

  • Zhu L, Li J, Mu C (2000) Environmental geochemistry of fluorine in the rock-soil-water system in the karst region of central Guizhou Province. Chin J Geochem 19:145–151

    Article  CAS  Google Scholar 

  • Zuo H, Chen L, Kong M, Qiu L, Lü P, Wu P, Yang Y, Chen K (2018) Toxic effects of fluoride on organisms. Life Sci 198:18–24

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We also thank Dr. Xudong Che at Nanjing University State Key Laboratory for the EMPA analyses.

Availability of data and materials

All data generated or analyzed during this study are included in this published article (and its supplementary information files).

Funding

This work was supported by National Key R&D Program of China (No. 2020YFC1808000). This work was also partially supported by the Fundamental Research Funds for the Central Universities (KYZ202123) and partially supported by Program for Student Innovation Through Research and Training (S20190010 & 201910307090P).

Author information

Authors and Affiliations

  1. College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing, 210095, Jiangsu, China

    Xiaoqing Shao, Yanan Gao, Lingyi Tang, Mu Su & Zhen Li

  2. Department of Earth & Atmospheric Sciences, University of Alberta, Edmonton, Alberta, T6G 2E3, Canada

    Weiduo Hao & Kurt O. Konhauser

  3. Jiangsu Key Laboratory for Organic Waste Utilization, Nanjing Agricultural University, Nanjing, 210095, Jiangsu, China

    Zhen Li

Authors
  1. Xiaoqing Shao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Weiduo Hao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kurt O. Konhauser
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yanan Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lingyi Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mu Su
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zhen Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

The manuscript was written by X.S., W.H., and K.K., with assistance of Y.G., M.S., and L.T; Ms. Y.G. contributed to the graphical abstract; X.S., L.T., and M.S. participated in the experiment design; X.S., W.H., and Y.G. analyzed and interpreted the data; the project was supervised by Z.L.

Corresponding author

Correspondence to Zhen Li.

Ethics declarations

Ethics approval and consent to participate

Not applicable

Consent for publication

Not applicable

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Robert Duran

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

ESM 1

(DOCX 1673 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shao, ., Hao, W., Konhauser, K.O. et al. The dissolution of fluorapatite by phosphate-solubilizing fungi: a balance between enhanced phosphorous supply and fluorine toxicity. Environ Sci Pollut Res 28, 69393–69400 (2021). https://doi.org/10.1007/s11356-021-15551-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-15551-5

Keywords

Search

Navigation