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Planetary Organic Chemistry and the Origins of Biomolecules Downloaded from http://cshperspectives.cshlp.org/ on October 3, 2021 - Published by Cold Spring Harbor Laboratory Press Planetary Organic Chemistry and the Origins of Biomolecules Steven A. Benner, Hyo-Joong Kim, Myung-Jung Kim, and Alonso Ricardo Foundation for Applied Molecular Evolution and The Westheimer Institute for Science and Technology, Gainesville, Florida 32601 Correspondence: [email protected] Organic chemistry on a planetary scale is likely to have transformed carbon dioxide and reduced carbon species delivered to an accreting Earth. According to various models for the origin of life on Earth, biological molecules that jump-started Darwinian evolution arose via this planetary chemistry. The grandest of these models assumes that ribonucleic acid (RNA) arose prebiotically, together with components for compartments that held it and a primitive metabolism that nourished it. Unfortunately, it has been challenging to iden- tify possible prebiotic chemistry that might have created RNA. Organic molecules, given energy, have a well-known propensity to form multiple products, sometimes referred to col- lectively as “tar” or “tholin.” These mixtures appear to be unsuited to support Darwinian processes, and certainly have never been observed to spontaneously yield a homochiral genetic polymer. To date, proposed solutions to this challenge either involve too much direct human intervention to satisfy many in the community, or generate molecules that are unreactive “dead ends” under standard conditions of temperature and pressure. Carbohydrates, organic species having carbon, hydrogen, and oxygen atoms in a ratio of 1:2:1 and an aldehyde or ketone group, conspicuously embody this challenge. Theyare com- ponents of RNA and their reactivity can support both interesting spontaneous chemistry as part of a “carbohydrate world,” but they also easily form mixtures, polymers and tars. We describe here the latest thoughts on how on this challenge, focusing on how it might be resolved using minerals containing borate, silicate, and molybdate, inter alia. nteresting organic chemistry occurs through- certainly contributed to the reduced carbon Iout the cosmos, including in presolar nebulae inventory on Earth before life emerged, plane- (see the article in this collection by Pascale Erh- tary processing on Earth undoubtedly also con- renfreund), asteroidal bodies (see the article in tributed to the inventory of prebiotic molecules this collection by Sandra Pizzarello) and icy that were available to life as it originated (as- bodies near the outer boundary of our solar sys- suming that Earth was the site of life’s origin). tem (Bernstein et al. 2002). Although organic Indeed, in the RNA first model for the origin molecules made in off-Earth locales almost of life on Earth (Joyce and Orgel 1999)(Benner Editors: David Deamer and Jack W. Szostak Additional Perspectives on The Origins of Life available at www.cshperspectives.org Copyright # 2010 Cold Spring Harbor Laboratory Press; all rights reserved; doi: 10.1101/cshperspect.a003467 Cite this article as Cold Spring Harb Perspect Biol 2010;2:a003467 1 Downloaded from http://cshperspectives.cshlp.org/ on October 3, 2021 - Published by Cold Spring Harbor Laboratory Press S.A. Benner et al. 2009), it is often proposed that terran-based organic transformations might have occurred on chemistry produced RNA in oligomeric form dry land or below water on a planetary surface to initiate Darwinian evolution. that was totally submerged. How are we to constrain models for planetary processing to converge on a model for what actually happened on Earth four billion years BACKGROUND ago? Today, atmospheric dioxygen (O2)readily Organic Molecules with Energy converts organic materials to carbon dioxide, Spontaneously Yield Polymers and Complex making it essentially impossible to observe such Mixtures processing on the surface of Earth. Furthermore, the ubiquity of life on modern Earth means that Any model for planetary organic chemistry must any organic processing is more likely to reflect recognize that very few organic molecules are biology than prebiology. The closest we may thermodynamically stable in water, either with come today to observe organic transformations respect to conversion to their fully hydrated state absent biology on a planetary scale might be on or decomposition upon heating to elemental car- Titan, a moon of Saturn whose atmosphere and bon (charcoal), carbon dioxide, orother thermo- surface is rich in reduced carbon. dynamic “end points.” Accordingly, any model Nevertheless, it is possible to apply a general for planetary prebiotic chemistry must address understanding of organic chemical reactivity to the metastability of organic species. This word suggest chemical reactions that might have captures the concept that organic molecules that occurred on early Earth and the products that have appeared through the interaction of precur- they might have produced. These suggestions sors with energy, water, and other organics can are constrained by models for the atmosphere then disappear upon further interaction. As and mineralogy of early Earth, although these many authors have noted (Cairns-Smith 1982; constraints might change as models improve. Shapiro 1987; Shapiro 2007), any prebiotic reac- In this article, we assume that the atmos- tion scheme that requires two or more organic phere of early Earth was less oxidizing than species must be concerned about the metastabil- today’s atmosphere, although not as rich in ity of two or more species; any scheme that does methane as the simulated atmosphere used in not produce both components in useful concen- the classic experiments of Stanley Miller (Miller trations at the same time will not meet a standard 1955). Further, we assume that the atmosphere of proof that the community need to accept a on early Earth had access to many sources solution to the problem. of energy. These include electrical discharge, Here, too, the mineral inventory of early ultraviolet and visible light (although the Sun Earthcannotbeignored.Mineralsofmanykinds was almost certainly dimmer then than now, a may have guided the reactivityof organic species Titan-like haze may have prevented high energy that emerged on early Earth, altered their meta- photons from reacting the Earth’s surface), stability, and influenced the time when specific volcanism (providing not only heat but also organic species were available to emerging life. reactive species and mixtures not at thermo- dynamic equilibrium), ionizing radiation, and Carbohydrates Embody this Natural impacts.(SeePizzarelloandShock2010foradis- Propensity to Polymerize cussion of such energy sources.) We also assume that life emerged after Toexplorethese points anddevelop the scientific the planet underwent a geological fractionation methods that enable this exploration, we will use in which heavier minerals and elemental iron carbohydrates as a focus. Carbohydrates are sank towards the core, leaving lighter rocks to organic species having carbon, hydrogen and formthecrust.Openquestionsconcerntheinven- oxygen atoms in a ratio of 1:2:1. They are there- tory of water relative to the surface of early Earth, fore at the same oxidation level of elemental car- an inventory that determined whether planetary bon. Furthermore the simplest carbohydrate, 2 Cite this article as Cold Spring Harb Perspect Biol 2010;2:a003467 Downloaded from http://cshperspectives.cshlp.org/ on October 3, 2021 - Published by Cold Spring Harbor Laboratory Press Planetary Organic Chemistry and the Origins of Biomolecules formaldehyde (HCHO, H2C¼O, or C1H2O1)is and preclude certain compound classes based easily generated by electrical discharge or ultra- on the same data, characterizes the “origins” field violet radiation impinging on moist atmos- in general (Benner 2009). To evaluate such con- pheres that are rich in carbon dioxide; nearly tradicting views, participants in this field must every contemporary model for early Earth per- understand relevant features of bonding and mitssuchatmospheres(Pintoetal.1980;Cleaves reactivity in organic molecules. This understand- 2008).Becausetheycontainketoneandaldehyde ing requires in turn that they understand the for- groups (see later), carbohydrates have interest- malisms used by organic chemists to describe ing reactivity that includes the ability to form bonding and reactivity in organic molecules. newcarbon-carbonbondsunder “standardcon- Although the features and formalisms are taught ditions,” defined as those where water is liquid in introductory organic chemistry courses, it is under contemporary terran atmospheric pres- worth summarizing them here a prelude to dis- sure. By comparison, the compounds that often cussing constraints on reactions that might be concern prebiotic chemists (carboxylic acids, expected to occur in prebiotic environments. fatty acids, and amino acids, for example) have First, a single bond joining two carbon essentially no such reactivity. Indeed, carbohy- atoms is strong, on the order of 400 kJ (100 drates are “high energy” because they can rear- kcal) per mole. This means that a pair of carbon range their constituent atoms to give carboxylic atoms joined by a typical single bond will acid derivatives and other more stable end point remain joined for many millions of years at tem- “sinks.” peratures when water is a liquid at sea level on Recognizing this, some authors, most nota- Earth near neutral pH (“standard conditions”). bly Arthur Weber (Weber 2001a; Weber 2001b; This is also true
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