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Organophosphorus Compound Formation Through the Oxidation of Reduced Oxidation State Phosphorus Compounds on the Hadean Earth

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Abstract

Reduced oxidation state phosphorus compounds may have been brought to the early Earth via meteorites or could have formed through geologic processes. These compounds could have played a role in the origin of biological phosphorus (P, hereafter) compounds. Reduced oxidation state P compounds are generally more soluble in water and are more reactive than orthophosphate and its associated minerals. However, to date no facile routes to generate C–O–P type compounds using reduced oxidation state P compounds have been reported under prebiotic conditions. In this study, we investigate the reactions between reduced oxidation state P compounds—and their oxidized products generated via Fenton reactions—with the nucleosides uridine and adenosine. The inorganic P compounds generated via Fenton chemistry readily react with nucleosides to produce organophosphites and organophosphates, including phosphate diesters via one-pot syntheses. The reactions were facilitated by NH4+ ions and urea as a condensation agent. We also present the results of the plausible stability of the organic compounds such as adenosine in an environment containing an abundance of H2O2. Such results have direct implications on finding organic compounds in Martian environments and other rocky planets (including early Earth) that were richer in H2O2 than O2. Finally, we also suggest a route for the sink of these inorganic P compounds, as a part of a plausible natural P cycle and show the possible formation of secondary phosphate minerals such as struvite and brushite on the early Earth.

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Abbreviations

P:

Phosphorus

MS:

Mass spectrometry

LCMS:

Liquid chromatography-mass spectrometry

PAA:

Phosphonoacetic acid

U-P-U and Ad-P-Ad:

Phosphate diester of uridine and adenosine

5′-UMP:

Uridine-5-monophosphate

2′-UMP:

Uridine-2-monophosphate

3′-UMP:

Uridine-3-monophosphate

5′-AMP:

Adenosine-5-monophosphate

2′-AMP:

Adenosine-2-monophosphate

3′-AMP:

Adenosine-3-monophosphate

References

  • Arrhenius G, Sales B, Mojzsis S, Lee T (1997) Entropy and charge in molecular evolution—the case of phosphate. J Theor Biol 187:503–522

    Article  CAS  Google Scholar 

  • Benner SA, Devine KG, Matveeva LN, Powell DH (2000) The missing organic molecules on Mars. Proc Natl Acad Sci U S A 97:2425–2430

    Article  CAS  Google Scholar 

  • Blankenship RE, Hartman H (1998) The origin and evolution of oxygenic photosynthesis. Trends Biochem Sci 23:94–97

    Article  CAS  Google Scholar 

  • Burcar B, Pasek M, Gull M, Cafferty BJ, Velasco F, Hud NV, Menor-Salván C (2016) Darwin’s warm little pond: a one-pot reaction for prebiotic phosphorylation and the mobilization of phosphate from minerals in a urea-based solvent. Angew Chem Int Ed Engl 55:13249–13253

    Article  CAS  Google Scholar 

  • Burcar B, Castañeda A, Lago J, Daniel M, Pasek MA, Hud NV, Menor-Salván C (2019) A stark contrast to modern Earth: phosphate mineral transformation and nucleoside phosphorylation in an Iron-and Cyanide-Rich early Earth scenario. Angew Chem 131:17137–17143

    Article  Google Scholar 

  • Clancy RT, Sandor BJ, Moriarty-Schieven GH (2004) A measurement of the 362 GHz absorption line of Mars atmospheric H2O2. Icarus 168:116–121

    Article  CAS  Google Scholar 

  • Clark BC, Kolb VM (2020) Macrobiont: cradle for the origin of life and creation of a biosphere. Life 10:278

    Article  Google Scholar 

  • Cooper GW, Onwo WM, Cronin JR (1992) Alkyl phosphonic acids and sulfonic acids in the Murchison meteorite. Geochim Cosmochim Acta 56:4109–4115

    Article  CAS  Google Scholar 

  • Damer B, Deamer D (2020) The hot spring hypothesis for an origin of life. Astrobiology 20:429–452

    Article  Google Scholar 

  • De Graaf RM, Schwartz AW (2005) Thermal synthesis of nucleoside H-phosphonates under mild conditions. Orig Life Evol Biosph 35:1–10

    Article  Google Scholar 

  • Deamer DW (2018) Assembling life: how can life begin on earth and other habitable planets? Oxford University Press, Oxford

    Google Scholar 

  • Encrenaz T, Bézard B, Owen T, Lebonnois S, Lefèvre F, Greathouse T, Forget F (2005) Infrared imaging spectroscopy of Mars: H2O mapping and determination of CO2 isotopic ratios. Icarus 179:43–54

    Article  CAS  Google Scholar 

  • Feng T, Lang C, Pasek MA (2019) The origin of blue coloration in a fulgurite from Marquette, Michigan. Lithos 342:288–294

    Article  Google Scholar 

  • Feng T, Gull M, Omran A, Abbott-Lyon H, Pasek MA (2021) Evolution of ephemeral phosphate minerals on planetary environments. ACS Earth Space Chem 5:1647–1656

    Article  CAS  Google Scholar 

  • Früh-Green GL, Kelley DS, Bernasconi SM, Karson JA, Ludwig KA, Butterfield DA, Proskurowski G (2003) 30,000 years of hydrothermal activity at the Lost City vent field. Science 301:495–498

    Article  Google Scholar 

  • Gibard C, Gorrell IB, Jiménez EI, Kee TP, Pasek MA, Krishnamurthy R (2019) Geochemical sources and availability of amidophosphates on the early Earth. Angew Chem 131:8235–8239

    Article  Google Scholar 

  • Gilbert W (1986) Origin of life: the RNA world. Nature 319:618–618

    Article  Google Scholar 

  • Gulick A (1955) Phosphorus as a factor in the origin of life. Am Sci 43:479–489

    CAS  Google Scholar 

  • Gull M (2014) Prebiotic phosphorylation reactions on the early Earth. Challenges 5:193–212

    Article  Google Scholar 

  • Gull M, Pasek MA (2013) Is struvite a prebiotic mineral? Life 3:321–330

    Article  CAS  Google Scholar 

  • Gull M, Zhou M, Fernández FM, Pasek MA (2014) Prebiotic phosphate ester syntheses in a deep eutectic solvent. J Mol Evol 78:109–117

    Article  CAS  Google Scholar 

  • Gull M, Mojica MA, Fernández FM, Gaul DA, Orlando TM, Liotta CL, Pasek MA (2015) Nucleoside phosphorylation by the mineral schreibersite. Sci Rep 5:1–6

    Article  Google Scholar 

  • Gull M, Cafferty BJ, Hud NV, Pasek MA (2017) Silicate-promoted phosphorylation of glycerol in non-aqueous solvents: a prebiotically plausible route to organophosphates. Life 7:29

    Article  Google Scholar 

  • Gull M, Omran A, Feng T, Pasek MA (2020) Silicate-, magnesium ion-, and urea-induced prebiotic phosphorylation of uridine via pyrophosphate; revisiting the hot drying water pool scenario. Life 10:122

    Article  CAS  Google Scholar 

  • Handschuh GJ, Orgel LE (1973) Struvite and prebiotic phosphorylation. Science 179:483–484

    Article  CAS  Google Scholar 

  • Handschuh GJ, Lohrmann R, Orgel LE (1973) The effect of Mg2+ and Ca2+ on urea-catalyzed phosphorylation reactions. J Mol Evol 2:251–262

    Article  CAS  Google Scholar 

  • Hazen RM, Papineau D, Bleeker W, Downs RT, Ferry JM, McCoy TJ, Yang H (2008) Mineral evolution. Am Mineral 93:1693–1720

    Article  CAS  Google Scholar 

  • He H, Wu X, Xian H, Zhu J, Yang Y, Lv Y, Konhauser KO (2021) An abiotic source of Archean hydrogen peroxide and oxygen that pre-dates oxygenic photosynthesis. Nat Commun 12:1–9

    Article  Google Scholar 

  • Herschy B, Chang SJ, Blake R, Lepland A, Abbott-Lyon H, Sampson J, Pasek MA (2018) Archean phosphorus liberation induced by iron redox geochemistry. Nat Commun 9:1–7

    Article  CAS  Google Scholar 

  • Holm G (2012) The significance of Mg in prebiotic geochemistry. Geobiology 10:269–279

    Article  CAS  Google Scholar 

  • Hud NV, Cafferty BJ, Krishnamurthy R, Williams LD (2013) The origin of RNA and “my grandfather’s axe.” Chem Biol 20:466–474

    Article  CAS  Google Scholar 

  • Ito Y, Hashimoto GL, Takahashi YO, Ishiwatari M, Kuramoto K (2020) H2O2-induced greenhouse warming on oxidized early Mars. Astrophys J 893:168

    Article  CAS  Google Scholar 

  • John Wiley & Sons, Inc. SpectraBase; SpectraBase Compound ID=Bd8zMd0lP9g SpectraBase Spectrum ID=8tYWDqwGwxD, https://spectrabase.com/spectrum/8tYWDqwGwxD (Accessed 31/8/2022).

  • Keefe AD, Miller SL (1995) Are polyphosphates or phosphate esters prebiotic reagents? J Mol Evol 41:693–702

    Article  CAS  Google Scholar 

  • Kelley DS, Karson JA, Blackman DK, Früh-Green GL, Butterfield DA, Lilley MD, Rivizzigno P (2001) An off-axis hydrothermal vent field near the Mid-Atlantic Ridge at 30 N. Nature 412:145–149

    Article  CAS  Google Scholar 

  • Kelley DS, Karson JA, Früh-Green GL, Yoerger DR, Shank TM, Butterfield DA, Sylva SP (2005) A serpentinite-hosted ecosystem: the lost city hydrothermal field. Science 307:1428–1434

    Article  CAS  Google Scholar 

  • Laetsch T, Downs R (2006) Software for identification and refinement of cell parameters from powder diffraction data of minerals using the RRUFF Project and American Mineralogist Crystal Structure Databases. In 19th General Meeting of the International Mineralogical Association, Kobe, pp 28

  • Lafuente B, Downs RT, Yang H, Stone N (2015) The power of databases: The RRUFF project. In: Armbruster T, Danisi RM (eds) Highlights in mineralogical crystallography. De Gruyter, Berlin, pp 1–30

    Google Scholar 

  • Lago JL, Burcar BT, Hud NV, Febrian R, Mehta C, Bracher PJ, Pasek MA (2020) The prebiotic provenance of semi-aqueous solvents. Orig Life Evol Biosph 50:1–14

    Article  CAS  Google Scholar 

  • Lalonde SV, Konhauser KO (2015) Benthic perspective on Earth’s oldest evidence for oxygenic photosynthesis. Proc Natl Acad Sci U S A 112:995–1000

    Article  CAS  Google Scholar 

  • Levine JS, Hays PB, Walker JC (1979) The evolution and variability of atmospheric ozone over geological time. Icarus 39:295–309

    Article  CAS  Google Scholar 

  • Liang MC, Hartman H, Kopp RE, Kirschvink JL, Yung YL (2006) Production of hydrogen peroxide in the atmosphere of a Snowball Earth and the origin of oxygenic photosynthesis. Proc Natl Acad Sci U S A 103:18896–18899

    Article  CAS  Google Scholar 

  • Lohrmann R, Orgel LE (1968) Prebiotic synthesis: phosphorylation in aqueous solution. Science 161:64–66

    Article  CAS  Google Scholar 

  • Millan M, Teinturier S, Malespin CA, Bonnet JY, Buch A, Dworkin JP, Mahaffy PR (2022) Organic molecules revealed in Mars’s Bagnold Dunes by Curiosity’s derivatization experiment. Nat Astron 6:129–140

    Article  Google Scholar 

  • Olson JM (1970) The Evolution of Photosynthesis: Hypothesis: photosynthetic bacteria and blue-green algae shared a common photoheterotrophic ancestor. Science 168:438–446

    Article  CAS  Google Scholar 

  • Padan E (1979) Facultative anoxygenic photosynthesis in cyanobacteria. Annu Rev Plant Physiol 30:27–40

    Article  CAS  Google Scholar 

  • Pasek MA (2008) Rethinking early Earth phosphorus geochemistry. Proc Natl Acad Sci U S A 105:853–858

    Article  CAS  Google Scholar 

  • Pasek MA (2019) Thermodynamics of prebiotic phosphorylation. Chem Rev 120:4690–4706

    Article  Google Scholar 

  • Pasek M, Block K (2009) Lightning-induced reduction of phosphorus oxidation state. Nat Geosci 2:553–556

    Article  CAS  Google Scholar 

  • Pasek MA, Kee TP (2011) On the origin of phosphorylated biomolecules. Origins of life: the primal self-organization. Springer, Berlin, Heidelberg, pp 57–84

    Chapter  Google Scholar 

  • Pasek MA, Lauretta DS (2005) Aqueous corrosion of phosphide minerals from iron meteorites: a highly reactive source of prebiotic phosphorus on the surface of the early Earth. Astrobiology 5:515–535

    Article  CAS  Google Scholar 

  • Pasek MA, Pasek VD (2018) The forensics of fulgurite formation. Mineral Petrol 112:185–198

    Article  CAS  Google Scholar 

  • Pasek MA, Dworkin JP, Lauretta DS (2007) A radical pathway for organic phosphorylation during schreibersite corrosion with implications for the origin of life. Geochim Cosmochim Acta 71:1721–1736

    Article  CAS  Google Scholar 

  • Pasek MA, Kee TP, Bryant DE, Pavlov AA, Lunine JI (2008) Production of potentially prebiotic condensed phosphates by phosphorus redox chemistry. Angew Chem Int Ed Engl 47:7918–7920

    Article  CAS  Google Scholar 

  • Pasek MA, Harnmeijer JP, Buick R, Gull M, Atlas Z (2013) Evidence for reactive reduced phosphorus species in the early Archean ocean. Proc Natl Acad Sci U S A 110:10089–10094

    Article  CAS  Google Scholar 

  • Pasek MA, Sampson JM, Atlas Z (2014) Redox chemistry in the phosphorus biogeochemical cycle. Proc Natl Acad Sci U S A 111:15468–15473

    Article  CAS  Google Scholar 

  • Pasek MA, Gull M, Herschy B (2017) Phosphorylation on the early eart. Chem Geol 475:149–170

    Article  CAS  Google Scholar 

  • Pech H, Henry A, Khachikian CS, Salmassi TM, Hanraha G, Foster KL (2009) Detection of geothermal phosphite using high-performance liquid chromatography. Environ Sci Technol 43:7671–7675

    Article  CAS  Google Scholar 

  • Raymond J, Blankenship RE (2008) The origin of the oxygen-evolving complex. Coord Chem Rev 252:377–383

    Article  CAS  Google Scholar 

  • Ritson DJ, Battilocchio C, Ley SV, Sutherland JD (2018) Mimicking the surface and prebiotic chemistry of early Earth using flow chemistry. Nat Commun 9:1–10

    Article  CAS  Google Scholar 

  • Ritson DJ, Mojzsis SJ, Sutherland J (2020) Supply of phosphate to early Earth by photogeochemistry after meteoritic weathering. Nat Geosci 13:344–348

    Article  CAS  Google Scholar 

  • Saladino R, Crestini C, Pino S, Costanzo G, Di Mauro E (2012) Formamide and the origin of life. Phys Life Rev 9:84–104

    Article  Google Scholar 

  • Schoffstall AM (1976) Prebiotic phosphorylation of nucleosides in formamide. Orig Life 7:399–412

    Article  CAS  Google Scholar 

  • Schwartz AW (2006) Phosphorus in prebiotic chemistry. Philos Trans R Soc Lond B Biol Sci 361:1743–1749

    Article  CAS  Google Scholar 

  • Schwartz AW, Veen MV, Bisseling T, Chittenden GJ (1975) Prebiotic nucleotide synthesis-demonstration of a geologically plausible pathway. Orig Life 6(1–2):163–168. https://doi.org/10.1007/BF01372401

    Article  CAS  Google Scholar 

  • Simonson BM, Glass BP (2004) Spherule layers–records of ancient impacts. Annu Rev Earth Planet Sci 32:329

    Article  CAS  Google Scholar 

  • Simonson BM, Davies D, Wallace M, Reeves S, Hassler SW (1998) Iridium anomaly but no shocked quartz from Late Archean microkrystite layer: Oceanic impact ejecta? Geology 26:195–198

    Article  CAS  Google Scholar 

  • Ślesak I, Ślesak H, Kruk J (2012) Oxygen and hydrogen peroxide in the early evolution of life on earth: in silico comparative analysis of biochemical pathways. Astrobiology 12:775–784

    Article  Google Scholar 

  • Steele A, Benning LG, Wirth R, Schreiber A, Araki T, McCubbin FM, Rogers K (2022) Organic synthesis associated with serpentinization and carbonation on early Mars. Science 375:172–177

    Article  CAS  Google Scholar 

  • Sutherland JD (2016) The origin of life—out of the blue. Angew Chem Int Ed Engl 55:104–121

    Article  CAS  Google Scholar 

  • Szopa C, Freissinet C, Glavin DP, Millan M, Buch A, Franz HB, Cabane M (2020) First detections of dichlorobenzene isomers and trichloromethylpropane from organic matter indigenous to Mars mudstone in Gale Crater, Mars: results from the sample analysis at Mars instrument onboard the curiosity rover. Astrobiology 20:292–306

    Article  CAS  Google Scholar 

  • Van Mooy BAS, Krupke A, Dyhrman ST, Fredricks HF, Frischkorn KR, Ossolinski JE, Sylva SP (2015) Major role of planktonic phosphate reduction in the marine phosphorus redox cycle. Science 348:783–785

    Article  Google Scholar 

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Acknowledgements

This work was supported by NASA Exobiology program (80NSSCC18K1288). This work has also been supported in part by University of South Florida Interdisciplinary NMR Facility, The Department of Chemistry and the College of Arts and Sciences, Tampa, Florida. The Chemical Purification Analysis and Screening Core Facility (CPAS) at University of South Florida have supported the mass spectrometry data analysis. This manuscript was greatly benefited from the useful discussions with Prof. Dr. Ram Krishnamurthy (Scripps Research Institute). Authors also acknowledge the help of Prof. Bill Baker, Prof. Laurent Calcul from USF Chemistry department, and Danny Lindsay with the various instrumental set-ups during the project. Maheen Gull is extremely grateful to her husband Ryan for help with the figures and graphical abstract of the paper and watching the kids so that the experiments could be finished on time. Thanks are also due to Andrew Stella-Vega for the helpful discussions about the manuscript. The authors also thank the anonymous reviewers for the helpful suggestions. Maheen Gull would also like to thank her mother in Pakistan for all the support and to her father and finally to her daughters Luna Faye and Nova Joy for the inspiration to do better.

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Authors and Affiliations

  1. School of Geosciences, University of South Florida, 4202 E Fowler Ave., NES 204, Tampa, FL, 33620, USA

    Maheen Gull, Tian Feng & Matthew A. Pasek

  2. Department of Chemistry, University of South Florida, Tampa, FL, 33620-5250, USA

    Joe Bracegirdle

  3. Department of Chemistry and Biochemistry, Kennesaw State University, 370 Paulding Ave NW, Kennesaw, GA, 30144, USA

    Heather Abbott-Lyon

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  1. Maheen Gull
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Gull, M., Feng, T., Bracegirdle, J. et al. Organophosphorus Compound Formation Through the Oxidation of Reduced Oxidation State Phosphorus Compounds on the Hadean Earth. J Mol Evol 91, 60–75 (2023). https://doi.org/10.1007/s00239-022-10086-w

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