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The Chemolithoautotroph Acidithiobacillus ferrooxidans Can Survive under Phosphate-Limiting Conditions by Expressing a C-P Lyase Operon That Allows It To Grow on Phosphonates ^,

Mario Vera, Fernando Pagliai, Nicolas Guiliani, and Carlos A. Jerez^*

Laboratory of Molecular Microbiology and Biotechnology, Department of Biology, and Millennium Institute for Cell Dynamics and Biotechnology, Faculty of Sciences, University of Chile, Santiago, Chile

Received 13 September 2007/ Accepted 5 January 2008

The chemolithoautotrophic bacterium Acidithiobacillus ferrooxidans is of great importance in biomining operations. During the bioleaching of ores, microorganisms are subjected to a variety of environmental stresses and to the limitations of some nutrients, such as inorganic phosphate (P_i), which is an essential component for all living cells. Although the primary source of phosphorus for microorganisms is P_i, some bacteria are also able to metabolize P_i esters (with a C-O-P bond) and phosphonates (with a very inert C-P bond). By using bioinformatic analysis of genomic sequences of the type strain of A. ferrooxidans (ATCC 23270), we found that as part of a Pho regulon, this bacterium has a complete gene cluster encoding C-P lyase, which is the main bacterial enzyme involved in phosphonate (Pn) degradation in other microorganisms. A. ferrooxidans was able to grow in the presence of methyl-Pn or ethyl-Pn as an alternative phosphorus source. Under these growth conditions, a great reduction in inorganic polyphosphate (polyP) levels was seen compared with the level for cells grown in the presence of P_i. By means of reverse transcription-PCR (RT-PCR), DNA macroarrays, and real-time RT-PCR experiments, it was found that A. ferrooxidans phn genes were cotranscribed and their expression was induced when the microorganism was grown in methyl-Pn as the only phosphorus source. This is the first report of phosphonate utilization in a chemolithoautotrophic microorganism. The existence of a functional C-P lyase system is a clear advantage for the survival under P_i limitation, a condition that may greatly affect the bioleaching of ores.

Published ahead of print on 18 January 2008.

Dedicated to the memory of Arthur Kornberg, a great scientist and friend who introduced us to the "polyP world."

Present address: Aquatic Biotechnology, Biofilm Centre, University Duisburg-Essen, Geibelstr. 41, D-47057 Duisburg, Germany.