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A Bacterium That Can Grow by Using Arsenic Instead of Phosphorus
Felisa Wolfe-Simon,1,2* Jodi Switzer Blum,2 Thomas R. Kulp,2 Gwyneth W. Gordon,3 Shelley E. Hoeft,2 Jennifer Pett-Ridge,4 John F. Stolz,5 Samuel M. Webb,6 Peter K. Weber,4 Paul C. W. Davies,1,7 Ariel D. Anbar,1,3,8 Ronald S. Oremland2
NASA Astrobiology Institute, USA. 2U.S. Geological Survey, Menlo Park, CA, USA. 3School of Earthand Space Exploration, Arizona State University, Tempe, AZ, USA. 4Lawrence Livermore National Laboratory, Livermore, CA, USA. 5Department of Biological Sciences, Duquesne University, Pittsburgh, PA, USA. 6Stanford Synchrotron Radiation Lightsource, Menlo Park, CA, USA. 7BEYOND: Center for Fundamental Concepts in Science, Arizona State University, Tempe, AZ, USA. 8Department of Chemistry andBiochemistry, Arizona State University, Tempe, AZ, USA.
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Life is mostly composed of the elements carbon, hydrogen, nitrogen, oxygen, sulfur and phosphorus. Although these six elements make up nucleic acids, proteins and lipids and thus the bulk of living matter,it is theoretically possible that some other elements in the periodic table could serve the same functions. Here we describe a bacterium, strain GFAJ-1 of the Halomonadaceae, isolated from Mono Lake, CA, which substitutes arsenic for phosphorus to sustain its growth. Our data show evidence for arsenate in macromolecules that normally contain phosphate, most notably nucleic acids and proteins.Exchange of one of the major bio-elements may have profound evolutionary and geochemical significance. Biological dependence on the six major nutrient elements carbon, hydrogen, nitrogen, oxygen, sulfur, and phosphorus is complemented by a selected array of other elements, usually metal(loid)s present in trace quantities that serve critical cellular functions, such as enzyme co-factors (1). There aremany cases of these trace elements substituting for one another. A few examples include the substitution of tungsten for molybdenum and cadmium for zinc in some enzyme families (2, 3) and copper for iron as an oxygen-carrier in some arthropods and mollusks (4). In these examples and others, the trace elements that interchange share chemical similarities that facilitate the swap. However, thereare no prior reports of substitutions for any of the six major elements essential for life. Here we present evidence that arsenic can substitute for phosphorus in the biomolecules of a naturallyoccurring bacterium. Arsenic (As) is a chemical analog of phosphorus (P), which lies directly below P on the periodic table. Arsenic possesses a similar atomic radius, as well as near identicalelectronegativity to P (5). The most common form of P in

biology is phosphate (PO43-), which behaves similarly to arsenate (AsO43-) over the range of biologically relevant pH and redox gradients (6). The physico-chemical similarity between AsO43- and PO43- contributes to the biological toxicity of AsO43- because metabolic pathways intended for PO43- cannot distinguish between the two molecules (7) andarsenate may be incorporated into some early steps in the pathways [(6) and refs therein]. However, it is thought that downstream metabolic processes are generally not compatible with As-incorporating molecules because of differences in the reactivities of P- and As-compounds (8). These downstream biochemical pathways may require the more chemically stable P-based metabolites; the lifetimes of moreeasily hydrolyzed As-bearing analogs are thought to be too short. However, given the similarities of As and P, and by analogy with trace element substitutions, we hypothesized that AsO43could specifically substitute for PO43- in an organism possessing mechanisms to cope with the inherent instability of AsO43- compounds (6). Here, we experimentally tested this hypothesis by using AsO43-, combined...
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