Role of Oxalic Acid Overexcretion in Transformations of Toxic Metal Minerals

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http://aem.asm.org/cgi/content/abstract/71/1/371?

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.

.

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. ,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.

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* 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@....

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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.

.