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Applied and Environmental Microbiology, January 2005, p. 371-381, Vol. 71, No. 1
0099-2240/05/$08.00+0     doi:10.1128/AEM.71.1.371-381.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Role of Oxalic Acid Overexcretion in Transformations of Toxic Metal Minerals by Beauveria caledonica

M. Fomina,1 S. Hillier,2 J. M. Charnock,3 K. Melville,1 I. J. Alexander,4 and G. M. Gadd1*

Division of Environmental and Applied Biology, Biological Sciences Institute, School of Life Sciences, University of Dundee, Dundee,1 Macaulay Land Use Research Institute, Craigiebuckler,2 Department of Plant and Soil Science, University of Aberdeen, Aberdeen, Scotland,4 Synchrotron Radiation Source Daresbury Laboratory, Daresbury, Warrington, Cheshire, United Kingdom3

Received 9 June 2004/ Accepted 29 August 2004

The fungus Beauveria caledonica was highly tolerant to toxic metals and solubilized cadmium, copper, lead, and zinc minerals, converting them into oxalates. This fungus was found to overexcrete organic acids with strong metal-chelating properties (oxalic and citric acids), suggesting that a ligand-promoted mechanism was the main mechanism of mineral dissolution. Our data also suggested that oxalic acid was the main mineral-transforming agent. Cadmium, copper, and zinc oxalates were precipitated by the fungus in the local environment and also in association with the mycelium. The presence of toxic metal minerals often led to the formation of mycelial cords, and in the presence of copper-containing minerals, these cords exhibited enhanced excretion of oxalic acid, which resulted in considerable encrustation of the cords by copper oxalate hydrate (moolooite). It was found that B. caledonica hyphae and cords were covered by a thick hydrated mucilaginous sheath which provided a microenvironment for chemical reactions, crystal deposition, and growth. Cryo-scanning electron microscopy revealed that mycogenic metal oxalates overgrew parental fungal hyphae, leaving a labyrinth of fungal tunnels within the newly formed mineral matter. X-ray absorption spectroscopy revealed that oxygen ligands played a major role in metal coordination within the fungal biomass during the accumulation of mobilized toxic metals by B. caledonica mycelium; these ligands were carboxylic groups in copper phosphate-containing medium and phosphate groups in pyromorphite-containing medium.

* Corresponding author. Mailing address: Division of Environmental and Applied Biology, Biological Sciences Institute, School of Life Sciences, University of Dundee, Dundee DD1 4HN, Scotland, United Kingdom. Phone: 44 1382 344765. Fax: 44 1382 348216. E-mail: g.m.gadd{at}dundee.ac.uk.

Applied and Environmental Microbiology, January 2005, p. 371-381, Vol. 71, No. 1
0099-2240/05/$08.00+0     doi:10.1128/AEM.71.1.371-381.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.





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