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Plausible Emergence and Self Assembly of a Primitive Phospholipid from Reduced Phosphorus on the Primordial Earth

Abstract

How life arose on the primitive Earth is one of the biggest questions in science. Biomolecular emergence scenarios have proliferated in the literature but accounting for the ubiquity of oxidized (+ 5) phosphate (PO43−) in extant biochemistries has been challenging due to the dearth of phosphate and molecular oxygen on the primordial Earth. A compelling body of work suggests that exogenous schreibersite ((Fe,Ni)3P) was delivered to Earth via meteorite impacts during the Heavy Bombardment (ca. 4.1–3.8 Gya) and there converted to reduced P oxyanions (e.g., phosphite (HPO32−) and hypophosphite (H2PO2)) and phosphonates. Inspired by this idea, we review the relevant literature to deduce a plausible reduced phospholipid analog of modern phosphatidylcholines that could have emerged in a primordial hydrothermal setting. A shallow alkaline lacustrine basin underlain by active hydrothermal fissures and meteoritic schreibersite-, clay-, and metal-enriched sediments is envisioned. The water column is laden with known and putative primordial hydrothermal reagents. Small system dimensions and thermal- and UV-driven evaporation further concentrate chemical precursors. We hypothesize that a reduced phospholipid arises from Fischer–Tropsch-type (FTT) production of a C8 alkanoic acid, which condenses with an organophosphinate (derived from schreibersite corrosion to hypophosphite with subsequent methylation/oxidation), to yield a reduced protophospholipid. This then condenses with an α-amino nitrile (derived from Strecker-type reactions) to form the polar head. Preliminary modeling results indicate that reduced phospholipids do not aggregate rapidly; however, single layer micelles are stable up to aggregates with approximately 100 molecules.

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Acknowledgements

This work grew out of the first research-based undergraduate Biochemistry and Astrobiology courses taught at Dakota State University (DSU). MOG thanks the DSU leadership for the freedom to redesign these courses to be research-intensive. MOG was supported by the National Science Foundation (NSF)/EPSCoR RII Track-1: Building on the 2020 Vision: Expanding Research, Education and Innovation in South Dakota (Award OIA-1849206) and by the South Dakota Board of Regents. MOG and PV were supported by the DSU Faculty Research Initiative (FRI) Grant Program and the DSU College of Arts and Sciences. MOG and PV were further supported by the South Dakota Space Grant Consortium and Southern Oregon University, respectively. The computations supporting this project were performed on High Performance Computing systems at the University of South Dakota funded by the NSF MRI award OAC-1626516. PM, BV, and SKAA were supported by the NSF RII Track-2 FEC: Data Driven Material Discovery Center for Bioengineering Innovation award IIA-1920954. PM, BV, and SKAA acknowledge that the land this research was performed on is the original homelands of the Dakota, Lakota, and Nakota tribal nations. PM, BV, and SKAA acknowledge the painful history of genocide and forced removals from this territory, and we honor and respect the many diverse Indigenous peoples still connected to this land on which we gather. PM, BV, and SKAA give thanks for our opportunity to gather on this land to make contributions to science. LMB was supported by the Jet Propulsion Laboratory, California Institute of Technology, under a contract with the National Aeronautics and Space Administration (NASA). VAS was supported by the Barry M. Goldwater Scholarship and Excellence in Education Foundation. LJL was supported by the DSU Student Research Initiative (SRI) Program. NWF, KLC, and KR were supported by the DSU College of Arts and Sciences. LRD was supported by the DSU SRI Program. LRD and SMD were supported by the NSF/EPSCoR RII Track-1: Building on the 2020 Vision: Expanding Research, Education and Innovation in South Dakota (Award OIA-1849206) and by the South Dakota Board of Regents. SG and VK were supported by the Instituto de Astrobiología de Colombia and DSU’s Office of the Provost. We thank Don Dixon of Cosmographica (https://www.cosmographica.com) for enthusiastic permission to reproduce his artwork in support of this research. We thank Dr. Dale Droge (DSU) for many insightful conversations about the manuscript and Nancy Presuhn and Pamela Lewis (DSU) for exceptional administrative support. We are especially grateful to anonymous reviewers for sharing their considerable expertise which has significantly improved the quality and scope of this contribution. We contribute this work in memory of Julian Freitag – a much beloved DSU science student and son of our colleague and friend Dr. Dale Droge – who tragically lost his life during this work.

Funding

MOG was supported by the National Science Foundation/EPSCoR RII Track-1: Building on the 2020 Vision: Expanding Research, Education and Innovation in South Dakota (Award OIA-1849206) and the South Dakota Board of Regents, the DSU Faculty Research Initiative (FRI) Grant Program, the DSU College of Arts and Sciences, and the South Dakota Space Grant Consortium. PV was funded by the DSU Faculty Research Initiative (FRI) Grant Program, the DSU College of Arts and Sciences, and with startup funds from Southern Oregon University. PM and BV were supported by the National Science Foundation RII Track-2 FEC: Data Driven Material Discovery Center for Bioengineering Innovation award IIA-1920954, and the Department of Chemistry of the University of South Dakota (USD) for start-up funds. SKAA was supported by the National Science Foundation RII Track-2 FEC: Data Driven Material Discovery Center for Bioengineering Innovation award IIA-1920954. LMB was supported by the Jet Propulsion Laboratory, California Institute of Technology, under a contract with the National Aeronautics and Space Administration (NASA). VAS was supported by the Barry M. Goldwater Scholarship and Excellence in Education Foundation. LJL was supported by the DSU Student Research Initiative (SRI) Program. NWF and KLC were supported by the DSU College of Arts and Sciences. KR was supported by the DSU College of Arts and Sciences. LRD was supported by the DSU SRI Program. LRD and SMD were supported by the National Science Foundation/EPSCoR RII Track-1: Building on the 2020 Vision: Expanding Research, Education and Innovation in South Dakota (Award OIA-1849206) and the South Dakota Board of Regents. SG and VK were supported by the Instituto de Astrobiología de Colombia and DSU’s Office of the Provost.

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Gaylor, M.O., Miro, P., Vlaisavljevich, B. et al. Plausible Emergence and Self Assembly of a Primitive Phospholipid from Reduced Phosphorus on the Primordial Earth. Orig Life Evol Biosph 51, 185–213 (2021). https://doi.org/10.1007/s11084-021-09613-4

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Keywords

  • Prebiotic
  • Reduced phospholipid
  • Phosphorus
  • Self-assembly
  • Hydrothermal
  • Origins of life