The Formation of Condensed Phosphate in Aqueous Solution

Beck, A.; Orgel, Leslie E.

doi:10.1073/pnas.54.3.664

Cited by 33 publications

(13 citation statements)

References 3 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Although these studies provide useful data on the formation and properties of RNA oligomers formed by chemical synthesis, their prebiotic relevance was questioned (1,2). The action of several organic agents (31)(32)(33) and of inorganic polyphosphates (34) on polymerization in aqueous solution was reported.…”

Section: Discussionmentioning

confidence: 99%

Generation of Long RNA Chains in Water

Costanzo

Pino

Ciciriello

et al. 2009

Journal of Biological Chemistry

119

138

View full text Add to dashboard Cite

The synthesis of RNA chains from 3,5-cAMP and 3,5-cGMP was observed. The RNA chains formed in water, at moderate temperatures (40 -90°C), in the absence of enzymes or inorganic catalysts. As determined by RNase analyses, the bonds formed were canonical 3,5-phosphodiester bonds. The polymerizations are based on two reactions not previously described: 1) oligomerization of 3, 5-cGMP to ϳ25-nucleotide-long RNA molecules, and of 3,5-cAMP to 4-to 8-nucleotide-long molecules. Oligonucleotide A molecules were further extended by reciprocal terminal ligation to yield RNA molecules up to >120 nucleotides long and 2) chain extension by terminal ligation of newly polymerized products of 3,5-cGMP on preformed oligonucleotides. The enzyme-and template-independent synthesis of long oligomers in water from prebiotically affordable precursors approaches the concept of spontaneous generation of (pre)genetic information.The origin of informational polymers is not understood. The RNA polymerization process has been studied for five decades, the results showing that from preactivated precursors polymers of several tens can be obtained, as reviewed previously (1). These pioneering studies provide the proof-of-principle that RNA precursors can self-assemble yielding linear polymers. However, the prebiotic validity of a process based on complex preactivation procedures is limited (1, 2), and the problem of defining a prebiotically plausible chemical and thermodynamic scenario for the synthesis and accumulation of informational polymers remains open. The core of the problem is the standard state Gibbs free energy change (3, 4) stating that condensation reactions are very inefficient in water. Given that extant polymerizations occur in water, this is a major difficulty, only partially solved by the fact that these processes at present occur inside the active site of enzymes where water activity may be drastically reduced. The other part of the extant solution, fruit of evolution, is the use of biologically highly preactivated triphosphate nucleotides (3). In primordia, RNA molecules had no enzymes to catalyze their chain-wise growth, and highly activated precursors can be considered as prebiotic only with difficulty.We reasoned that for a pre-enzymatic polymerization to occur the solution must have relied on a simple and robust process. Ideally, such a process should have been based on compounds that were reactive yet relatively stable, chemically not too elaborate to allow their efficient production, and not too dissimilar from the products of their polymerization to minimize the chemical cost of the process.It was observed that phosphorylation of nucleosides occurs in formamide simply in the presence of a source of organic or inorganic phosphate at temperatures at which both the reactants and the products are stable (5). Phosphorylation occurs in every possible position of the nucleoside sugar moiety resulting, both for purine and pyrimidine nucleosides, in the production of 2Ј-, 3Ј-, 5Ј-, 2Ј,3Ј-cyclic, and 3Ј,5Ј-cyclic XMPs 3 (5). Th...

show abstract

Section: Discussionmentioning

confidence: 99%

Generation of Long RNA Chains in Water

Costanzo

Pino

Ciciriello

et al. 2009

Journal of Biological Chemistry

119

138

View full text Add to dashboard Cite

show abstract

“…Techniques used for the phosphorylation of organics include adding condensing agents to mixtures of orthophosphate and organics (7), heating orthophosphate with organics (8, 9), adding condensed phosphates to organics (10), or a combination of these methods (7,11,12). Geochemical environments where these processes may take place include a dry pond with wet/dry cycles (12), hydrothermal vents (4), or mineral surfaces (2,10).…”

Section: Phosphorus In the Origin Of Lifementioning

confidence: 99%

Rethinking early Earth phosphorus geochemistry

Pasek

2008

Proc. Natl. Acad. Sci. U.S.A.

232

209

View full text Add to dashboard Cite

Phosphorus is a key biologic element, and a prebiotic pathway leading to its incorporation into biomolecules has been difficult to ascertain. Most potentially prebiotic phosphorylation reactions have relied on orthophosphate as the source of phosphorus. It is suggested here that the geochemistry of phosphorus on the early Earth was instead controlled by reduced oxidation state phosphorus compounds such as phosphite (HPO 3 2؊ ), which are more soluble and reactive than orthophosphates. This reduced oxidation state phosphorus originated from extraterrestrial material that fell during the heavy bombardment period or was produced during impacts, and persisted in the mildly reducing atmosphere. This alternate view of early Earth phosphorus geochemistry provides an unexplored route to the formation of pertinent prebiotic phosphorus compounds, suggests a facile reaction pathway to condensed phosphates, and is consistent with the biochemical usage of reduced oxidation state phosphorus compounds in life today. Possible studies are suggested that may detect reduced oxidation state phosphorus compounds in ancient Archean rocks.meteorites ͉ origins of life ͉ phosphonates ͉ prebiotic ͉ redox chemistry P hosphorus (P) is a key biologic element and is the limiting reagent in many ecosystems. Phosphorus is ubiquitous in biochemistry because phosphorylated biomolecules play major roles in replication and information (as RNA and DNA), metabolism (as ATP, NADPH, and other coenzymes), and structure (as phospholipids). Several key properties of P as phosphate make it advantageous to biologic systems, including thermodynamic instability coupled with kinetic stability, charge and coordination state, and a constant oxidation state under typical redox conditions (1). These features are especially critical to the formation of large informational polymers, and hence highly relevant to the origin and development of early life. Phosphorus Geochemistry and CosmochemistryThe major forms of P in life are summarized in Fig. 1. Inorganic P compounds used by life include orthophosphate, pyrophosphate and other condensed phosphates, phosphite, hypophosphite, and phosphine. These inorganic forms are either used by organisms as sources of P for the synthesis of organic-P biomolecules or are possible metabolic by-products of P metabolism (PH 3 ). Additionally, orthophosphate acts as a buffer in many cells, keeping pH constant at Ϸ7. Organic forms of P include compounds with C-O-P linkages and compounds with C-P linkages, and both are formed from inorganic P by using enzymes.Phosphorus is a lithophile element at the redox conditions on the surface of the Earth, and hence orthophosphate is the dominant form of inorganic P on the surface of the Earth today. The concentration of orthophosphate is water-buffered by the solubility of orthophosphate minerals like apatite, Ca 5 (PO 4 ) 3 (OH,F,Cl), on the present-day Earth, and of whitlockite, Ca 9 MgH(PO 4 ) 7 , and brushite, CaHPO 4 ⅐2H 2 O, before the rise of life-mediated apatite deposition (2). Because ...

show abstract

“…Precipitated calcium orthophosphate is needed for pyrophosphate synthesis from eyanate (Miller and Parris, 1964;Beck and Orgel, 1965;Vieyra et al, 1995). In most of our experiments calcium (and magnesium) ions inhibit the formation of condensed phosphate bonds.…”

Section: Discussionmentioning

confidence: 86%

“…If the trimetaphosphate added to compounds such as adenosine to make ATP, then the trimetaphosphate would be a reagent rather than a catalyst. Beck and Orgel (1965) found that water soluble carbodiimides gave good yields of trimetaphosphate from tripolyphosphate, and cyanate gave 1% yields but only in the presence of calcium phosphate.…”

Section: Tripolyphosphate Trimetaphosphatementioning

confidence: 99%