Bismuth(III) Volatilization and Immobilization by Filamentous Fungus Aspergillus clavatus During Aerobic Incubation

  • Katarína Boriová
  • Martin Urík
  • Marek Bujdoš
  • Peter Matúš


As with many metals, bismuth can be accumulated or transformed by microorganisms. These interactions affect microbial consortia and bismuth environmental behaviour, mobility, and toxicity. Recent research focused specifically on bismuth anaerobic transformation by bacteria and archaea has inspired the evaluation of the mutual interactions between bismuth and filamentous fungi as presented in this article. The Aspergillus clavatus fungus proved resistant to adverse effects from bismuth contamination in culture medium with up to a concentration of 195 µmol L−1 during static 15- and 30-day cultivation. The examined resistance mechanism includes biosorption to the fungal surface and biovolatilization. Pelletized fungal biomass has shown high affinity for dissolved bismuth(III). Bismuth biosorption was rapid, reaching equilibrium after 50 min with a 0.35 mmol g−1 maximum sorption capacity as calculated from the Langmuir isotherm. A. clavatus accumulated ≤70 µmol g−1 of bismuth after 30 days. Preceding isotherm study implications that most accumulated bismuth binds to cell wall suggests that biosorption is the main detoxification mechanism. Accumulated bismuth was also partly volatilized (≤1 µmol) or sequestrated in the cytosol or vacuoles. Concurrently, ≤1.6 µmol of bismuth remaining in solution was precipitated by fungal activity. These observations indicate that complex mutual interactions between bismuth and filamentous fungi are environmentally significant regarding bismuth mobility and transformation.


Bismuth Biosorption Fungal Biomass Inductively Couple Plasma Optical Emission Spectrometry Aspergillus Clavatus 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This work was supported by the Scientific Grant Agency of the Slovak Republic Ministry of Education and the Slovak Academy of Sciences under VEGA contract Nos. 1/0860/11, 1/0836/15, and 1/0203/14.


  1. Alharbi SA, Mashat BH, Al-Harbi NA, Wainwright M, Aloufi AS, Alnaimat S (2012) Bismuth-inhibitory effects on bacteria and stimulation of fungal growth in vitro. Saudi J Biol Sci 19:147–150CrossRefGoogle Scholar
  2. Alibhai KK, Dudeney AWL, Leak DJ, Agatzini S, Tzeferis P (1993) Bioleaching and bioprecipitation of nickel and iron from laterites. FEMS Microbiol Rev 11:87–95CrossRefGoogle Scholar
  3. Bialek B, Diaz-Bone RA, Pieper D, Hollmann M, Hensel R (2011) Toxicity of methylated bismuth compounds produced by intestinal microorganisms to Bacteroides thetaiotaomicron, a member of the physiological intestinal microbiota. J Toxicol 2011:608349. doi: 10.1155/2011/608349
  4. Chojnacka K (2010) Biosorption and bioaccumulation—the prospects for practical applications. Environ Int 36:299–307CrossRefGoogle Scholar
  5. Ding P, Huang KL, Li GY, Zeng WW (2007) Mechanisms and kinetics of chelating reaction between novel chitosan derivatives and Zn(II). J Hazard Mater 146:58–64CrossRefGoogle Scholar
  6. Dodge AG, Wackett LP (2005) Metabolism of bismuth subsalicylate and intracellular accumulation of bismuth by Fusarium sp. strain Bl. Appl Environ Microbiol 71:876–882CrossRefGoogle Scholar
  7. Dopp E, Hartmann LM, Florea AM, Rettenmeier AW, Hirner AV (2004) Environmental distribution, analysis, and toxicity of organometal(loid) compounds. Crit Rev Toxicol 34:301–333CrossRefGoogle Scholar
  8. Dursun AY, Uslu G, Cuci Y, Aksu Z (2003) Bioaccumulation of copper(II), lead(II) and chromium(VI) by growing Aspergillus niger. Process Biochem 38:1647–1651CrossRefGoogle Scholar
  9. El-Shahawi MS, Al-Mehrezi RS (1997) Detection and semiquantitative determination of bismuth(III) in water on immobilized and plasticized polyurethane foams with some chromogenic reagents. Talanta 44:483–489CrossRefGoogle Scholar
  10. Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11CrossRefGoogle Scholar
  11. Huber B, Dammann P, Krüger C, Kirsch P, Bialek B, Diaz-Bone RA et al (2011) Production of toxic volatile trimethylbismuth by the intestinal microbiota of mice. J Toxicol 2011:491039. doi: 10.1155/2011/491039 CrossRefGoogle Scholar
  12. Iram S, Zaman A, Iqbal Z, Shabbir R (2013) Heavy metal tolerance of fungus isolated from soil contaminated with sewage and industrial wastewater. Pol J Environ Stud 22:691–697Google Scholar
  13. Magyarosy A, Laidlaw R, Kilaas R, Echer C, Clark D, Keasling J (2002) Nickel accumulation and nickel oxalate precipitation by Aspergillus niger. Appl Microbiol Biotechnol 59:382–388CrossRefGoogle Scholar
  14. Meyer J, Schmidt A, Michalke K, Hensel R (2007) Volatilisation of metals and metalloids by the microbial population of an alluvial soil. Syst Appl Microbiol 30:229–238CrossRefGoogle Scholar
  15. Michalke K, Wickenheiser EB, Mehring M, Hirner AV, Hensel R (2000) Production of volatile derivatives of metal(loid)s by microflora involved in anaerobic digestion of sewage sludge. Appl Environ Microbiol 66:2791–2796CrossRefGoogle Scholar
  16. Michalke K, Schmidt A, Huber B, Meyer J, Sulkowski M, Hirner AV et al (2008) Role of intestinal microbiota in transformation of bismuth and other metals and metalloids into volatile methyl and hydride derivatives in humans and mice. Appl Environ Microbiol 74:3069–3075CrossRefGoogle Scholar
  17. Sartape A, Mandhare A, Salvi P, Pawar D, Raut P, Anuse M et al (2012) Removal of Bi(III) with adsorption technique using coconut shell activated carbon. Chin J Chem Eng 20:768–775CrossRefGoogle Scholar
  18. Sayer JA, Cotter-Howells JD, Watson C, Hillier S, Gadd GM (1999) Lead mineral transformation by fungi. Curr Biol 9:691–694CrossRefGoogle Scholar
  19. Sen Gupta S, Bhattacharyya KG (2011) Kinetics of adsorption of metal ions on inorganic materials: a review. Adv Colloid Interface Sci 162:39–58CrossRefGoogle Scholar
  20. Slovák Z, Dočekal B (1980) Sorption of arsenic, antimony and bismuth on glycolmethacrylate gels with bound thiol groups for direct sampling in electrothermal atomic absorption spectrometry. Anal Chim Acta 117:293–300CrossRefGoogle Scholar
  21. Srivastava PK, Vaish A, Dwivedi S, Chakrabarty D, Singh N, Tripathi RD (2011) Biological removal of arsenic pollution by soil fungi. Sci Total Environ 409:2430–2442CrossRefGoogle Scholar
  22. Thayer JS (2002) Biological methylation of less-studied elements. Appl Organomet Chem 16:677–691CrossRefGoogle Scholar
  23. Tsezos M (2009) Metal–Microbes interactions: beyond environmental protection. Adv Mater Res 71–73:527–532CrossRefGoogle Scholar
  24. Urík M, Čerňanský S, Ševc J, Šimonovičová A, Littera P (2007) Biovolatilization of arsenic by different fungal strains. Water Air Soil Pollut 186:337–342CrossRefGoogle Scholar
  25. Zafar S, Aqil F, Ahmad I (2007) Metal tolerance and biosorption potential of filamentous fungi isolated from metal contaminated agricultural soil. Bioresour Technol 98:2557–2561CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Katarína Boriová
    • 1
  • Martin Urík
    • 1
  • Marek Bujdoš
    • 1
  • Peter Matúš
    • 1
  1. 1.Faculty of Natural Sciences, Institute of Laboratory Research on GeomaterialsComenius University in BratislavaBratislavaSlovakia

Personalised recommendations