Abstract
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.
Similar content being viewed by others
References
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 19:147–150
Alibhai KK, Dudeney AWL, Leak DJ, Agatzini S, Tzeferis P (1993) Bioleaching and bioprecipitation of nickel and iron from laterites. FEMS Microbiol Rev 11:87–95
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
Chojnacka K (2010) Biosorption and bioaccumulation—the prospects for practical applications. Environ Int 36:299–307
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 146:58–64
Dodge AG, Wackett LP (2005) Metabolism of bismuth subsalicylate and intracellular accumulation of bismuth by Fusarium sp. strain Bl. Appl Environ Microbiol 71:876–882
Dopp E, Hartmann LM, Florea AM, Rettenmeier AW, Hirner AV (2004) Environmental distribution, analysis, and toxicity of organometal(loid) compounds. Crit Rev Toxicol 34:301–333
Dursun AY, Uslu G, Cuci Y, Aksu Z (2003) Bioaccumulation of copper(II), lead(II) and chromium(VI) by growing Aspergillus niger. Process Biochem 38:1647–1651
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 44:483–489
Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11
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
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 22:691–697
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 59:382–388
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 30:229–238
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 66:2791–2796
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 74:3069–3075
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 20:768–775
Sayer JA, Cotter-Howells JD, Watson C, Hillier S, Gadd GM (1999) Lead mineral transformation by fungi. Curr Biol 9:691–694
Sen Gupta S, Bhattacharyya KG (2011) Kinetics of adsorption of metal ions on inorganic materials: a review. Adv Colloid Interface Sci 162:39–58
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 117:293–300
Srivastava PK, Vaish A, Dwivedi S, Chakrabarty D, Singh N, Tripathi RD (2011) Biological removal of arsenic pollution by soil fungi. Sci Total Environ 409:2430–2442
Thayer JS (2002) Biological methylation of less-studied elements. Appl Organomet Chem 16:677–691
Tsezos M (2009) Metal–Microbes interactions: beyond environmental protection. Adv Mater Res 71–73:527–532
Urík M, Čerňanský S, Ševc J, Šimonovičová A, Littera P (2007) Biovolatilization of arsenic by different fungal strains. Water Air Soil Pollut 186:337–342
Zafar S, Aqil F, Ahmad I (2007) Metal tolerance and biosorption potential of filamentous fungi isolated from metal contaminated agricultural soil. Bioresour Technol 98:2557–2561
Acknowledgments
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.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Boriová, K., Urík, M., Bujdoš, M. et al. Bismuth(III) Volatilization and Immobilization by Filamentous Fungus Aspergillus clavatus During Aerobic Incubation. Arch Environ Contam Toxicol 68, 405–411 (2015). https://doi.org/10.1007/s00244-014-0096-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00244-014-0096-5