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, 287 (34), 28816-9

Growth of a Bacterium That Apparently Uses Arsenic Instead of Phosphorus Is a Consequence of Massive Ribosome Breakdown

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Growth of a Bacterium That Apparently Uses Arsenic Instead of Phosphorus Is a Consequence of Massive Ribosome Breakdown

Georgeta N Basturea et al. J Biol Chem.

Abstract

A recent study (Wolfe-Simon, F., Switzer Blum, J., Kulp, T. R., Gordon, G. W., Hoeft, S. E., Pett-Ridge, J., Stolz, J. F., Webb, S. M., Weber, P. K., Davies, P. C., Anbar, A. D., and Oremland, R. S. (2011) Science 332, 1163-1166) described the isolation of a special bacterial strain, GFAJ-1, that could grow in medium containing arsenate, but lacking phosphate, and that supposedly could substitute arsenic for phosphorus in its biological macromolecules. Here, we provide an alternative explanation for these observations and show that they can be reproduced in a laboratory strain of Escherichia coli. We find that arsenate induces massive ribosome degradation, which provides a source of phosphate. A small number of arsenate-tolerant cells arise during the long lag period prior to initiation of growth in +As/-P medium, and it is this population that undergoes the very slow, limited growth observed for both E. coli and GFAJ-1. These results provide a simple explanation for the reported growth of GFAJ-1 in arsenate without invoking replacement of phosphorus by arsenic in biological macromolecules.

Figures

FIGURE 1.
FIGURE 1.
Ribosome degradation during growth of E. coli in media lacking or containing arsenate. Samples from each of four cultures prelabeled with [3H]uridine were analyzed for acid-soluble material at the indicated times as described under “Experimental Procedures.”
FIGURE 2.
FIGURE 2.
Analysis of acid-soluble material released during ribosome degradation. A portion of the acid-soluble material obtained in Fig. 1 was analyzed by paper chromatography as described under “Experimental Procedures.” The migration positions of standards are shown at the top of the figure.
FIGURE 3.
FIGURE 3.
A, growth of E. coli cells in media containing arsenate. Cultures were centrifuged, washed in Tris-buffered salts, and resuspended in the same solution containing 0.2% glucose plus either no addition or additions of 1.5 mm KH2PO4 or 40 mm arsenate. Cultures were incubated with shaking at 37 °C. A600 readings were taken to monitor cell growth. B, growth of E. coli cells pre-exposed to arsenate. Cells were initially grown with shaking at 37 °C in Tris-buffered salts/glucose medium containing 0.1 mm phosphate in the presence or absence of 40 mm arsenate. After 250 h of incubation to select for arsenate-tolerant cells, two portions were diluted into fresh medium containing 0.1 mm phosphate in the presence or absence of 40 mm arsenate. Cell growth was monitored by A600 readings.

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