Did Nature Also Choose Arsenic?

International Journal of Astrobiology 8 (2) : 69–74 (2009) Printed in the United Kingdom doi:10.1017/S1473550408004394 f Cambridge University Press 2009

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Did nature also choose arsenic ?
Felisa Wolfe-Simon1*, Paul C.W. Davies2 and Ariel D. Anbar1,3
1 Metallomics Laboratory, Department of Chemistry and Biochemistry, Arizona State University, Tempe, AZ 85287, USA 2 BEYOND: Center forFundamental Concepts in Science, Arizona State University, Tempe, AZ 85287, USA 3 School of Earth and Space Exploration, Arizona State University, Tempe, AZ 85287, USA e-mail: wolfe@eps.harvard.edu

Abstract : All known life requires phosphorus (P) in the form of inorganic phosphate (PO43x or Pi) and phosphate-containing organic molecules. Pi serves as the backbone of the nucleic acids thatconstitute genetic material and as the major repository of chemical energy for metabolism in polyphosphate bonds. Arsenic (As) lies directly below P on the periodic table and so the two elements share many chemical properties, although their chemistries are sufficiently dissimilar that As cannot directly replace P in modern biochemistry. Arsenic is toxic because As and P are similar enough that organismsattempt this substitution. We hypothesize that ancient biochemical systems, analogous to but distinct from those known today, could have utilized arsenate in the equivalent biological role as phosphate. Organisms utilizing such ‘weird life ’ biochemical pathways may have supported a ‘ shadow biosphere ’ at the time of the origin and early evolution of life on Earth or on other planets. Suchorganisms may even persist on Earth today, undetected, in unusual niches.
Received 16 July 2008, accepted 26 September 2008, first published online 30 January 2009

Key words : Arsenic, phosphate, weird life, shadow biosphere, origins of life.

Phosphorus (P) ranks just behind hydrogen, oxygen, carbon and nitrogen (H, O, C and N) in a quantitative list of the most important elements in biology (Voet &Voet 1990). However, P is usually less available to life than these other elements, particularly in the oceans. H and O are available in any aqueous solution, while C and N can be found in gaseous compounds that are readily distributed through the atmosphere and that can be converted into highly soluble chemical forms. Although there is some speculation about extraterrestrial input of P to Earth,early life may have been mainly dependent on crustal elemental sources (Pasek 2008). In contrast, while P is a relatively common element in the Earth’s crust (0.1 % by weight) (Winter 2007), there is no gas phase P compound analogous to CO2, CH4, N2 or NH3, and common phosphate minerals such as apatite (Ca5(PO4)3(OH, F, Cl)) are only sparingly soluble (Stumm & Morgan 1996). The distribution ofbioavailable P at the Earth’s surface is therefore extremely heterogeneous. Although there is some speculation about extraterrestrial input of P to Earth, early life may have been mainly dependent on crustal elemental sources (Pasek 2008). In this way, P is similar to many of the so-called ‘micronutrient ’ elements that are required in biology in trace amounts (e.g. Fe, Cu, Mn and Zn). As a result,the distribution of life at the Earth’s surface is often determined by the distribution of P, which is why phosphate (PO43x) fertilizers are commonly used to compensate for low P concentrations.
* Present address: Department of Earth and Planetary Sciences, Harvard University, 20 Oxford Street, Cambridge, MA 02138, USA.

Twenty years ago, Westheimer explained why life as we know it is based onP (Westheimer 1987). A critical feature is the acid–base chemistry of P in the 5+ oxidation state (P(V)) in the form of phosphoric acid (H3PO4), which dictates that the dominant soluble forms of P at biological pH (y7–8) are the charged species H2PO4x, HPO42x and PO43x (collectively, these species and H3PO4 are referred to as ‘inorganic phosphorus’ or Pi). Charged molecules are more easily...