Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-16T23:40:49.209Z Has data issue: false hasContentIssue false
  • English
  • Français

Did nature also choose arsenic?

Published online by Cambridge University Press:  30 January 2009

Felisa Wolfe-Simon ,
Paul C.W. Davies  and
Ariel D. Anbar
Felisa Wolfe-Simon*
Affiliation:
Metallomics Laboratory, Department of Chemistry and Biochemistry, Arizona State University, Tempe, AZ 85287, USA
Paul C.W. Davies
Affiliation:
BEYOND: Center for Fundamental Concepts in Science, Arizona State University, Tempe, AZ 85287, USA
Ariel D. Anbar
Affiliation:
Metallomics Laboratory, Department of Chemistry and Biochemistry, Arizona State University, Tempe, AZ 85287, USA School of Earth and Space Exploration, Arizona State University, Tempe, AZ 85287, USA
*
e-mail: wolfe@eps.harvard.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

All known life requires phosphorus (P) in the form of inorganic phosphate (PO43− or Pi) and phosphate-containing organic molecules. Pi serves as the backbone of the nucleic acids that constitute 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 organisms attempt 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. Such organisms may even persist on Earth today, undetected, in unusual niches.

Keywords

Arsenicphosphateweird lifeshadow biosphereorigins of life
Type
Research Article
Information
International Journal of Astrobiology , Volume 8 , Issue 2 , April 2009 , pp. 69 - 74
Copyright
Copyright © 2009 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adams, S.R., Sparkes, M.J. & Dixon, H.B. (1984). The arsonomethyl analogue of adenosine 5′-phosphate. An uncoupler of adenylate kinase. Biochem. J. 221, 829–836.CrossRefGoogle ScholarPubMed
Ali, B.R. & Dixon, H.B. (1992). Pyridoxal arsenate as a prosthetic group for aspartate aminotransferase. Biochem. J. 284(2), 349–352.CrossRefGoogle Scholar
Allison, J.D., Brown, D.S. & Novo-Gradac, K.J. (1991). MINTEQA2/prodefa2, a geochemical assessment model for environmental systems: Version 3.0 users manual.Google Scholar
Avron, M. & Jagendorf, A.T. (1959). Evidence concerning the mechanism of adenosine triphosphate formation by spinach chloroplasts. J. Biol. Chem. 234, 967–972.CrossRefGoogle ScholarPubMed
Baross, J. (ed.) (2007). The Limits of Organic Life In Planetary Systems. National Academies Press, p. 100.Google Scholar
Benner, S.A. & Hutter, D. (2002). Phosphates, DNA, and the search for nonterrean life: a second generation model for genetic molecules. Bioorg. Chem. 30, 62–80.CrossRefGoogle ScholarPubMed
Berner, R.A. (1981). A new geochemical classification of sedimentary environments. J. Sed. Res. 51, 359–365.Google Scholar
Bhattacharjee, H. & Rosen, B. (2007). Molecular Microbiology of Heavy Metals, Vol. 6, Nies, D.H. & Silver, S. (eds). Springer, Berlin, pp. 371–406.CrossRefGoogle Scholar
Brandes, J.A. & Devol, A.H. (2002). A global marine-fixed nitrogen isotopic budget: implications for holocene nitrogen cycling. Global Biogeochem. Cycles 16, 1120.CrossRefGoogle Scholar
Braunstein, A.E. (1931). Ober den Einfluß von Arsenat auf Phosphatumsatz und Glykolyse im Blut. Biochem. Z. 240, 68–93.Google Scholar
Canfield, D.E. (2005). The early history of atmospheric oxygen: homage to Robert M. Garrels. Annu. Rev. Earth Planet. Sci. 33, 1–36.CrossRefGoogle Scholar
Chawla, S., Mutenda, E.K., Dixon, H.B., Freeman, S. & Smith, A.W. (1995). Synthesis of 3-arsonopyruvate and its interaction with phosphoenolpyruvate mutase. Biochem. J. 308(3), 931–935.CrossRefGoogle ScholarPubMed
Cleland, C.E. & Copley, S.D. (2006). The possibility of alternative microbial life on Earth. Int. J. Astrobiol. 4, 165–173.CrossRefGoogle Scholar
Corliss, J.B., Dymond, J., Gordon, L.I., Edmond, J.M., von Herzen, R.P., Ballard, R.D., Green, K., Williams, D., Bainbridge, A. & Crane, K. (1979). Submarine thermal springs on the Galapagos Rift. Science 203, 1073–1083.CrossRefGoogle ScholarPubMed
Crane, R.K. & Lipmann, F. (1953). The effect of arsenate on aerobic phosphorylation. J. Biol. Chem. 201, 235–243.CrossRefGoogle ScholarPubMed
Davis, B.D. (1958). On the importance of being ionized. Arch. Biochem. Biophys. 78, 497–509.CrossRefGoogle ScholarPubMed
Davies, P.C.W., Benner, S.A., Cleland, C.E., Lineweaver, C.H., McKay, C.P. & Wolfe-Simon, F. (2009). Signatures of a shadow biosphere. Astrobio. (in press).CrossRefGoogle Scholar
Deana, A. & Belasco, J.G. (2005). Lost in translation: the influence of ribosomes on bacterial mRNA decay. Genes Dev. 19, 2526–2533.CrossRefGoogle ScholarPubMed
Dowdle, P.R., Laverman, A.M. & Oremland, R.S. (1996). Bacterial dissimilatory reduction of arsenic(V) to arsenic(III) in anoxic sediments. Appl. Environ. Microbiol. 62, 1664–1669.CrossRefGoogle Scholar
Ehrlich, H.L. (2002). Environmental Chemistry of Arsenic, Frankenberger, W.T. Marcel Dekker, New York, pp. 313–328.Google Scholar
Eigner, J., Boedtker, H. & Michaels, G. (1961). The thermal degradation of nucleic acids. Biochim. Biophys Acta. 51, 165–168.CrossRefGoogle ScholarPubMed
Forrest, M.J., Ledesma-Vázquez, J., Ussler, W. III, Kulongoski, J.T., Hilton, D.R. & Greene, H.G. (2005). Gas geochemistry of a shallow submarine hydrothermal vent associated with the el requesón fault zone, bahía concepción, baja California sur, México. Chem. Geol. 224, 82–95.CrossRefGoogle Scholar
Gresser, M.J. (1981). ADP-arsenate formation by submitochondrial particles under phosphorylating conditions. J. Biol. Chem. 256, 5981–5983.CrossRefGoogle ScholarPubMed
Kawamura, K. (1999). Measurement of the rate of RNA hydrolysis in aqueous solution at elevated temperatures using a new monitoring method for hydrothermal reactions. Nucleic Acids Symp. Ser. 42, 289–290.CrossRefGoogle Scholar
Kawamura, K. (2001a). Comparison of the rates of prebiotic formation and hydrolysis of RNA under hydrothermal environments and its implications on the chemical evolution of RNA. Nucleic Acids Symp. Ser. 1, 239–240.CrossRefGoogle Scholar
Kawamura, K. (2001b). Hydrolytic stability of ribose phosphodiester bonds within several oligonucleotides at high temperatures using a real-time monitoring method for hydrothermal reactions. Chem. Lett. 30, 1120–1121.CrossRefGoogle Scholar
Kawamura, K., Nagahama, M. & Kuranoue, K. (2005). Chemical evolution of RNA under hydrothermal conditions and the role of thermal copolymers of amino acids for the prebiotic degradation and formation of RNA. Adv. Space Res. 35, 1626–1633.CrossRefGoogle ScholarPubMed
Kenney, L.J. & Kaplan, J.H. (1988). Arsenate substitutes for phosphate in the human red cell sodium pump and anion exchanger. J. Biol. Chem. 263, 7954–7960.CrossRefGoogle ScholarPubMed
Kline, P.C. & Schramm, V.L. (1993). Purine nucleoside phosphorylase. Catalytic mechanism and transition-state analysis of the arsenolysis reaction. Biochemistry 32, 13 212–13 219.CrossRefGoogle ScholarPubMed
Kulp, T.R., Hoeft, S.E., Asao, M., Madigan, M.T., Hollibaugh, J.T., Fisher, J.C., Stolz, J.F., Culbertson, C.W., Miller, L.G. & Oremland, R.S. (2008). Arsenic(III) fuels anoxygenic photosynthesis in hot spring biofilms from Mono Lake, California. Science 321, 967–970.CrossRefGoogle ScholarPubMed
Kyrtopoulos, S.A. & Satchel, D.P. (1972). Kinetic studies with phosphotransacetylase. II. The acetylation of arsenate by acetyl coenzyme a. Biochim. Biophys. Acta 268, 334–343.CrossRefGoogle ScholarPubMed
Lagunas, R., Pestana, D. & Diez-Masa, J.C. (1984). Arsenic mononucleotides. Separation by high-performance liquid chromatography and identification with myokinase and adenylate deaminase. Biochemistry 23, 955–960.CrossRefGoogle ScholarPubMed
Langner, H., Jackson, C., McDermott, T. & Inskeep, W. (2001). Rapid oxidation of arsenite in a hot spring ecosystem, Yellowstone National Park. Environ. Sci. Technol. 35, 3302–3309.CrossRefGoogle Scholar
Levy, M. & Miller, S.L. (1998). The stability of the RNA bases: implications for the origins of life. Proc. Natl Acad. Sci. U.S.A. 95, 7933–7938.CrossRefGoogle Scholar
Lindahl, T. (1993). Instability and decay of the primary structure of DNA. Nature 362, 709–715.CrossRefGoogle ScholarPubMed
Maher, K.A. & Stevenson, D.J. (1988). Impact frustration of the origin of life. Nature 331, 612–614.CrossRefGoogle ScholarPubMed
Martin, W. & Russell, M.J. (2003). On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. Phil. Trans. R. Soc. Lond. B 358, 59–85.CrossRefGoogle Scholar
Miller, S.L. & Bada, J.L. (1988). Submarine hot springs and the origin of life. Nature 334, 609–611.CrossRefGoogle ScholarPubMed
Moore, S.A., Moennich, D.M. & Gresser, M.J. (1983). Synthesis and hydrolysis of ADP-arsenate by beef heart submitochondrial particles. J. Biol. Chem. 258, 6266–6271.CrossRefGoogle ScholarPubMed
Morel, F.M.M. & Hering, J.G. (1993). Principles and Applications of Aquatic Chemistry. John Wiley & Sons, Inc., New York, p. 588.Google Scholar
Nagahama, M. & Kawamura, K. (2002). A new approach for the cooperative chemical evolution of nucleic acids and proteins under the primitive earth environment. Nucleic Acids Symp. Ser. 2, 279–280.CrossRefGoogle Scholar
Oremland, R., Stolz, J.F. & Hollibaugh, J.T. (2004). The microbial arsenic cycle in Mono Lake, California. FEMS Microbiol Ecol. 48, pp. 15–27.CrossRefGoogle ScholarPubMed
Oremland, R.S., Newman, D.K., Kail, B.W. & Stolz, J.F. (2002). Environmental Chemistry of Arsenic, Frankenberger, W.T. (ed.). Marcel Dekker, New York, p. 391.Google Scholar
Oremland, R.S. & Stolz, J.F. (2003). The ecology of arsenic. Science. 300, pp. 939–944.CrossRefGoogle ScholarPubMed
Ozawa, T., Hagihara, M., Yamanaka, N. & Yagi, K. (1970). Mitochondrial protein biosynthesis insensitive to arsenate or rutamycin. Arch. Biochem. Biophys. 137, 585–587.CrossRefGoogle Scholar
Pasek, M.A. (2008). Rethinking early Earth phosphorus geochemistry. PNAS. 105, 853–858.CrossRefGoogle ScholarPubMed
Petrillo, M., Silvestro, G., Nocera, P.P.D., Boccia, A. & Paolella, G. (2006). Stem-loop structures in prokaryotic genomes. BMC Genomics 7, 170.CrossRefGoogle ScholarPubMed
Pilcher, T., Veizer, J. & Hall, G.E.M. (1999). The chemical composition of shallow-water hydrothermal fluids in Tutum Bay, Ambitle Island, Papua New Guinea and their effect on ambient seawater. Mar. Chem. 64, 229–252.Google Scholar
Roesler, C.S., Culbertson, C.W., Etheridge, S.M., Goericke, R., Kiene, R.P., Miller, L.G. & Oremland, R.S. (2002). Distribution, production, and ecophysiology of picocystis strain ML in Mono Lake, California. Limnol. Oceanogr. 47, 440–452.CrossRefGoogle Scholar
Rosen, B.P. (2002). Biochemistry of arsenic detoxification. FEBS Lett. 529, 86–92.CrossRefGoogle ScholarPubMed
Rozovskaya, T.A., Rechinsky, V.O., Bibilashvili, R.S., Karpeisky, M., Tarusova, N.B., Khomutov, R.M. & Dixon, H.B. (1984). The mechanism of pyrophosphorolysis of RNA by RNA polymerase. Endowment of RNA polymerase with artificial exonuclease activity. Biochem. J. 224, 645–650.CrossRefGoogle ScholarPubMed
Schoonen, M.A. & Xu, Y. (2001). Nitrogen reduction under hydrothermal vent conditions: Implications for the prebiotic synthesis of chon compounds. Astrobiology 1, 133–142.CrossRefGoogle ScholarPubMed
Selinger, D.W., Saxena, R.M., Cheung, K.J., Church, G.M. & Rosenow, C. (2003). Global RNA half-life analysis in Escherichia coli reveals positional patterns of transcript degradation. Genome Res. 13, 216–223.CrossRefGoogle ScholarPubMed
Serkiz, S.M., Allison, J.D., Perdue, E.M., Allen, H.E. & Brown, D.S. (1996). Correcting errors in the thermodynamic database for the equilibrium speciation model MINTEQA2. Water Res. 30, 1930–1933.CrossRefGoogle Scholar
Sleep, N.H. & Zahnle, K. (1998). Refugia from asteroid impacts on early Mars and the early Earth. J. Geophys. Res. 103, 28 529–28 544.CrossRefGoogle Scholar
Slomovic, S., Laufer, D., Geiger, D. & Schuster, G. (2005). Polyadenylation and degredation of human mitochondrial RNA: the prokaryotic past leaves its mark. Mol. Cell. Biol. 25, 6427–6435.CrossRefGoogle Scholar
Slooten, L. & Nuyten, A. (1983). Arsenylation of nucleoside diphosphates in Rhodospirillium rubrum chromatophores. Biochim. Biophys. Acta 725, 49–59.CrossRefGoogle Scholar
Smedley, P.L. & Kinniburgh, D.G. (2002). A review of the source, behaviour and distribution of arsenic in natural waters. Appl. Geochem. 17, 517–568.CrossRefGoogle Scholar
Stolz, J.F. & Oremland, R.S. (1999). Bacterial respiration of arsenic and selenium. FEMS Microbiol. Rev. 23, 615–627.CrossRefGoogle ScholarPubMed
Stumm, W. & Morgan, J.J. (1996). Aquatic Chemistry. Wiley, New York.Google Scholar
Voet, D. & Voet, J.G. (1990). Biochemistry. John Wiley & Sons, Inc., New York.Google Scholar
Von Damm, K.L. (1990). Seafloor hydrothermal activity: black smoker chemistry and chimneys. Annu. Rev. Earth Planet. Sci. 18, 173–204.CrossRefGoogle Scholar
Westall, J.C., Zachary, J.L. & Morel, F.M.M. (1976). MINEQL: a Computer Program for the Calculation of Chemical Equilibrium Composition of Aqueous Systems. Water Quality Laboratory, Ralph M. Parsons Laboratory for Water Resources and Environmental Engineering sic, Department of Civil Engineering, Massachusetts Institute of Technology.Google Scholar
Westheimer, F.H. (1987). Why nature chose phosphates. Science 235, 1173–1178.CrossRefGoogle ScholarPubMed
Wilkie, J.A. & Hering, J.G. (1998). Rapid oxidation of geothermal arsenic(III) in streamwaters of the Eastern Sierra Nevada. Environ. Sci. Technol. 32, 657–662.CrossRefGoogle Scholar
Winter, M. (2007). Webelements: the first periodic table on the WWW. http://www.webelements.com/.Google Scholar