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Enzymically mediated bioprecipitation of uranium by a Citrobacter sp.: a concerted role for exocellular lipopolysaccharide and associated phosphatase in biomineral formation

School of Biosciences, The University of Birmingham, Edgbaston, Birmingham B15 2TT, UK¹
Research and Technology, BNFL, Springfields Works, Preston PR4 OXJ, UK²

Author for correspondence: Lynne E. Macaskie. Tel: +44 121 414 5889. Fax: +44 121 414 6557. e-mail: l.e.macaskie{at}bham.ac.uk

A Citrobacter sp. accumulated uranyl ion () via precipitation with phosphate ligand liberated by phosphatase activity. The onset and rate of uranyl phosphate deposition were promoted by , forming NH₄UO₂PO₄, which has a lower solubility product than NaUO₂PO₄. This acceleration decoupled the rate-limiting chemical crystallization process from the biochemical phosphate ligand generation. This provided a novel approach to monitor the cell-surface-associated changes using atomic-force microscopy in conjunction with transmission electron microscopy and electron-probe X-ray microanalysis, to visualize deposition of uranyl phosphate at the cell surface. Analysis of extracted surface materials by ³¹P NMR spectroscopy showed phosphorus resonances at chemical shifts of 0·3 and 2·0 p.p.m., consistent with monophosphate groups of the lipid A backbone of the lipopolysaccharide (LPS). Addition of to the extract gave a yellow precipitate which contained uranyl phosphate, while addition of Cd²⁺ gave a chemical shift of both resonances to a single new resonance at 3 p.p.m. Acid-phosphatase-mediated crystal growth exocellularly was suggested by the presence of acid phosphatase, localized by immunogold labelling, on the outer membrane and on material exuded from the cells. Metal deposition is proposed to occur via an initial nucleation with phosphate groups localized within the LPS, shown by other workers to be produced exocellularly in association with phosphatase. The crystals are further consolidated with additional, enzymically generated phosphate in close juxtaposition, giving high loads of LPS-bound uranyl phosphate without loss of activity and distinguishing this from simple biosorption, or periplasmic or cellular metal accumulation mechanisms. Accumulation of ‘tethered’ metal phosphate within the LPS is suggested to prevent fouling of the cell surface by the accumulated precipitate and localization of phosphatase exocellularly is consistent with its possible functions in homeostatis and metal resistance.

Keywords: Citrobacter, lipopolysaccharide, phosphatase, metal biomineral

Abbreviations: AFM, atomic-force microscopy; EPM, extracellular polymeric materials; EPXMA, electron-probe X-ray microanalysis; PIXE, proton-induced X-ray emission; TEM, transmission electron microscopy; XRD, X-ray powder diffraction analysis

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