Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

The astrochemical evolutionary traits of phospholipid membrane homochirality

Abstract

Compartmentalization is crucial for the evolution of life. Present-day phospholipid membranes exhibit a high level of complexity and species-dependent homochirality, the so-called lipid divide. It is possible that less stable, yet more dynamic systems, promoting out-of-equilibrium environments, facilitated the evolution of life at its early stages. The composition of the preceding primitive membranes and the evolutionary route towards complexity and homochirality remain unexplained. Organics-rich carbonaceous chondrites are evidence of the ample diversity of interstellar chemistry, which may have enriched the prebiotic milieu on early Earth. This Review evaluates the detections of simple amphiphiles — likely ancestors of membrane phospholipids — in extraterrestrial samples and analogues, along with potential pathways to form primitive compartments on primeval Earth. The chiroptical properties of the chiral backbones of phospholipids provide a guide for future investigations into the origins of phospholipid membrane homochirality. We highlight a plausible common pathway towards homochirality of lipids, amino acids, and sugars starting from enantioenriched monomers. Finally, given their high recalcitrance and resistance to degradation, lipids are among the best candidate biomarkers in exobiology.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Schematic timeline of the geological longevity of major molecular biosignatures.
Fig. 2: The membrane lipid divide.
Fig. 3: Schematic structures of a selection of simple amphiphiles.
Fig. 4: Chiroptical properties of stereospecifically numbered sn-glycerol-1-phosphate lithium salt and d-glyceraldehyde-3-phoshate.
Fig. 5: Schematic illustrating a potential pathway from enantioenriched amphiphiles towards the build-up of homochiral phospholipid membranes and proto-peptides.
Fig. 6: Schematics illustrating two conceptual space missions that could enable the identification of potential extraterrestrial lipids.

Similar content being viewed by others

References

  1. Howlett, M. G. & Fletcher, S. P. From autocatalysis to survival of the fittest in self-reproducing lipid systems. Nat. Rev. Chem. 7, 673–691 (2023).

    Article  PubMed  Google Scholar 

  2. Schmitt-Kopplin, P. et al. High molecular diversity of extraterrestrial organic matter in Murchison meteorite revealed 40 years after its fall. Proc. Natl Acad. Sci. USA 107, 2763–2768 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Öberg, K. I. Photochemistry and astrochemistry: photochemical pathways to interstellar complex organic molecules. Chem. Rev. 116, 9631–9663 (2016).

    Article  PubMed  Google Scholar 

  4. van Dishoeck, E. F. Astrochemistry of dust, ice and gas: introduction and overview. Faraday Discuss. 168, 9–47 (2014).

    Article  CAS  PubMed  Google Scholar 

  5. Tielens, A. G. G. M. The molecular universe. Rev. Mod. Phys. 85, 1021–1081 (2013).

    Article  CAS  Google Scholar 

  6. Burke, D. J. & Brown, W. A. Ice in space: surface science investigations of the thermal desorption of model interstellar ices on dust grain analogue surfaces. Phys. Chem. Chem. Phys. 12, 5947–5969 (2010).

    Article  CAS  PubMed  Google Scholar 

  7. Potapov, A., Jäger, C. & Henning, T. Ice coverage of dust grains in cold astrophysical environments. Phys. Rev. Lett. 124, 221103 (2020).

    Article  CAS  PubMed  Google Scholar 

  8. Rosu-Finsen, A. et al. Peeling the astronomical onion. Phys. Chem. Chem. Phys. 18, 31930–31935 (2016).

    Article  CAS  PubMed  Google Scholar 

  9. Cohen, Z. R. et al. Plausible sources of membrane-forming fatty acids on the early Earth: a review of the literature and an estimation of amounts. ACS Earth Space Chem. 7, 11–27 (2023).

    Article  CAS  PubMed  Google Scholar 

  10. Glavin, D. P., Burton, A. S., Elsila, J. E., Aponte, J. C. & Dworkin, J. P. The search for chiral asymmetry as a potential biosignature in our Solar System. Chem. Rev. 120, 4660–4689 (2020).

    Article  CAS  PubMed  Google Scholar 

  11. Wilhelm, M. B. et al. Extraction instruments to enable detection of origin-diagnostic lipids for life detection. In 52nd Lunar and Planetary Science Conference LPI contribution no. 2548, id.2634 (LPI, 2021).

  12. Finkel, P. L., Carrizo, D., Parro, V. & Sánchez-García, L. An overview of lipid biomarkers in terrestrial extreme environments with relevance for Mars exploration. Astrobiology 23, 563–604 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  13. Peretó, J., López-García, P. & Moreira, D. Ancestral lipid biosynthesis and early membrane evolution. Trends Biochem. Sci. 29, 469–477 (2004).

    Article  PubMed  Google Scholar 

  14. Chen, L. L., Pousada, M. & Haines, T. H. The flagellar membrane of Ochromonas danica. Lipid composition. J. Biol. Chem. 251, 1835–1842 (1976).

    Article  CAS  PubMed  Google Scholar 

  15. Moss, F. R. et al. Halogenation-dependent effects of the chlorosulfolipids of Ochromonas danica on lipid bilayers. ACS Chem. Biol. 15, 2986–2995 (2020).

    Article  PubMed Central  Google Scholar 

  16. Pohorille, A. & Deamer, D. Self-assembly and function of primitive cell membranes. Res. Microbiol. 160, 449–456 (2009).

    Article  CAS  PubMed  Google Scholar 

  17. Namani, T. et al. Novel chimeric amino acid-fatty alcohol ester amphiphiles self-assemble into stable primitive membranes in diverse geological settings. Astrobiology 23, 327–343 (2023).

    Article  CAS  PubMed  Google Scholar 

  18. Suzuki, N. & Itabashi, Y. Possible roles of amphiphilic molecules in the origin of biological homochirality. Symmetry 11, 966 (2019).

    Article  CAS  Google Scholar 

  19. Azua-Bustos, A. et al. Dark microbiome and extremely low organics in Atacama fossil delta unveil Mars life detection limits. Nat. Commun. 14, 808 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Martin, H. S., Podolsky, K. A. & Devaraj, N. K. Probing the role of chirality in phospholipid membranes. ChemBioChem 22, 3148–3157 (2021).

    Article  CAS  PubMed  Google Scholar 

  21. Bilia, A. R. et al. Vesicles and micelles: two versatile vectors for the delivery of natural products. J. Drug Deliv. Sci. Technol. 32, 241–255 (2016).

    Article  CAS  Google Scholar 

  22. Liu, P., Chen, G. & Zhang, J. A review of liposomes as a drug delivery system: current status of approved products, regulatory environments, and future perspectives. Molecules 27, 1372 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Liu, W., Ye, A., Han, F. & Han, J. Advances and challenges in liposome digestion: surface interaction, biological fate, and GIT modeling. Adv. Colloid Interface Sci. 263, 52–67 (2019).

    Article  CAS  PubMed  Google Scholar 

  24. Benvegnu, T., Lemiègre, L. & Cammas-Marion, S. New generation of liposomes called archaeosomes based on natural or synthetic archaeal lipids as innovative formulations for drug delivery. Recent Pat. Drug Deliv. Formul. 3, 206–220 (2009).

    Article  CAS  PubMed  Google Scholar 

  25. Paolucci, V., Leriche, G., Koyanagi, T. & Yang, J. Evaluation of tetraether lipid-based liposomal carriers for encapsulation and retention of nucleoside-based drugs. Bioorg. Med. Chem. Lett. 27, 4319–4322 (2017).

    Article  CAS  PubMed  Google Scholar 

  26. Penkauskas, T. & Preta, G. Biological applications of tethered bilayer lipid membranes. Biochimie 157, 131–141 (2019).

    Article  CAS  PubMed  Google Scholar 

  27. Jiang, Y., Thienpont, B., Sturgis, J. N., Dittman, J. & Scheuring, S. Membrane-mediated protein interactions drive membrane protein organization. Nat. Commun. 13, 7373 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Fiore, M. & Buchet, R. Symmetry breaking of phospholipids. Symmetry 12, 1488 (2020).

    Article  CAS  Google Scholar 

  29. Gattinger, A., Schloter, M. & Munch, J. C. Phospholipid etherlipid and phospholipid fatty acid fingerprints in selected euryarchaeotal monocultures for taxonomic profiling. FEMS Microbiol. Lett. 213, 133–139 (2002).

    Article  CAS  PubMed  Google Scholar 

  30. Dibrova, D. V., Galperin, M. Y. & Mulkidjanian, A. Y. Phylogenomic reconstruction of archaeal fatty acid metabolism. Environ. Microbiol. 16, 907–918 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Damsté, J. S. et al. Structural characterization of diabolic acid-based tetraester, tetraether and mixed ether/ester, membrane-spanning lipids of bacteria from the order Thermotogales. Arch. Microbiol. 188, 629–641 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  32. Weijers, J. W. H. et al. Membrane lipids of mesophilic anaerobic bacteria thriving in peats have typical archaeal traits. Environ. Microbiol. 8, 648–657 (2006).

    Article  CAS  PubMed  Google Scholar 

  33. Villanueva, L. et al. Bridging the membrane lipid divide: bacteria of the FCB group superphylum have the potential to synthesize archaeal ether lipids. ISME J. 15, 168–182 (2021).

    Article  CAS  PubMed  Google Scholar 

  34. Wächtershäuser, G. From pre-cells to Eukarya – a tale of two lipids. Mol. Microbiol. 47, 13–22 (2003).

    Article  PubMed  Google Scholar 

  35. Koga, Y. Early evolution of membrane lipids: how did the lipid divide occur? J. Mol. Evol. 72, 274–282 (2011).

    Article  CAS  PubMed  Google Scholar 

  36. Shimada, H. & Yamagishi, A. Stability of heterochiral hybrid membrane made of bacterial sn-G3P lipids and archaeal sn-G1P lipids. Biochemistry 50, 4114–4120 (2011).

    Article  CAS  PubMed  Google Scholar 

  37. Caforio, A. et al. Converting Escherichia coli into an archaebacterium with a hybrid heterochiral membrane. Proc. Natl Acad. Sci. USA 115, 3704–3709 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Kates, M., Joo, C. N., Palameta, B. & Shier, T. Absolute stereochemical configuration of phytanyl (dihydrophytyl) groups in lipids of Halobacterium cutirubrum. Biochemistry 6, 3329–3338 (1967).

    Article  CAS  PubMed  Google Scholar 

  39. Leseigneur, G., Filippi, J. J., Baldovini, N. & Meierhenrich, U. Absolute configuration of aliphatic hydrocarbon enantiomers identified by gas chromatography: theorized application for isoprenoid alkanes and the search of molecular biosignatures on Mars. Symmetry 14, 326 (2022).

    Article  CAS  Google Scholar 

  40. Caforio, A. & Driessen, A. J. M. Archaeal phospholipids: structural properties and biosynthesis. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1862, 1325–1339 (2017).

    Article  CAS  PubMed  Google Scholar 

  41. Fiore, M. et al. Synthesis of phospholipids under plausible prebiotic conditions and analogies with phospholipid biochemistry for origin of life studies. Astrobiology 22, 598–627 (2022).

    Article  CAS  PubMed  Google Scholar 

  42. Lang, C., Lago, J. & Pasek, M. A. in Handbook of Astrobiology 1st edn (ed. Kolb, V. M.) Ch. 5.8 (Taylor & Francis Group, 2019).

  43. Hargreaves, W. R. & Deamer, D. W. Liposomes from ionic, single-chain amphiphiles. Biochemistry 17, 3759–3768 (1978).

    Article  CAS  PubMed  Google Scholar 

  44. Gebicki, J. M. & Hicks, M. Ufasomes are stable particles surrounded by unsaturated fatty acid membranes. Nature 243, 232–234 (1973).

    Article  CAS  PubMed  Google Scholar 

  45. Apel, C. L., Deamer, D. W. & Mautner, M. N. Self-assembled vesicles of monocarboxylic acids and alcohols: conditions for stability and for the encapsulation of biopolymers. Biochim. Biophys. Acta Biomembr. 1559, 1–9 (2002).

    Article  CAS  Google Scholar 

  46. Namani, T. & Deamer, D. W. Stability of model membranes in extreme environments. Orig. Life Evol. Biosph. 38, 329–341 (2008).

    Article  CAS  PubMed  Google Scholar 

  47. Mansy, S. S. & Szostak, J. W. Thermostability of model protocell membranes. Proc. Natl Acad. Sci. USA 105, 13351–13355 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Mansy, S. S. Model protocells from single-chain lipids. Int. J. Mol. Sci. 10, 835–843 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Milshteyn, D., Damer, B., Havig, J. & Deamer, D. Amphiphilic compounds assemble into membranous vesicles in hydrothermal hot spring water but not in seawater. Life 8, 11 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  50. Black, R. A. et al. Nucleobases bind to and stabilize aggregates of a prebiotic amphiphile, providing a viable mechanism for the emergence of protocells. Proc. Natl Acad. Sci. USA 110, 13272–13276 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Cornell, C. E. et al. Prebiotic amino acids bind to and stabilize prebiotic fatty acid membranes. Proc. Natl Acad. Sci. USA 116, 17239–17244 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Jordan, S. F., Nee, E. & Lane, N. Isoprenoids enhance the stability of fatty acid membranes at the emergence of life potentially leading to an early lipid divide. Interface Focus 9, 20190067 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  53. Lin, Y., Jing, H., Liu, Z., Chen, J. & Liang, D. Dynamic behavior of complex coacervates with internal lipid vesicles under nonequilibrium conditions. Langmuir 36, 1709–1717 (2020).

    Article  CAS  PubMed  Google Scholar 

  54. Pir Cakmak, F., Grigas, A. T. & Keating, C. D. Lipid vesicle-coated complex coacervates. Langmuir 35, 7830–7840 (2019).

    Article  CAS  PubMed  Google Scholar 

  55. Dora Tang, T. Y. et al. Fatty acid membrane assembly on coacervate microdroplets as a step towards a hybrid protocell model. Nat. Chem. 6, 527–533 (2014).

    Article  CAS  PubMed  Google Scholar 

  56. Ianeselli, A. et al. Non-equilibrium conditions inside rock pores drive fission, maintenance and selection of coacervate protocells. Nat. Chem. 14, 32–39 (2022).

    Article  CAS  PubMed  Google Scholar 

  57. Jia, T. Z. et al. Membraneless polyester microdroplets as primordial compartments at the origins of life. Proc. Natl Acad. Sci. USA 116, 15830–15835 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Joshi, M. P., Sawant, A. A. & Rajamani, S. Spontaneous emergence of membrane-forming protoamphiphiles from a lipid–amino acid mixture under wet–dry cycles. Chem. Sci. 12, 2970–2978 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Joshi, M. P., Uday, A. & Rajamani, S. Elucidating N-acyl amino acids as a model protoamphiphilic system. Commun. Chem. 5, 147 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Forsythe, J. G. et al. Ester-mediated amide bond formation driven by wet–dry cycles: a possible path to polypeptides on the prebiotic Earth. Angew. Chem. Int. Ed. 54, 9871–9875 (2015).

    Article  CAS  Google Scholar 

  61. Frenkel-Pinter, M. et al. Thioesters provide a plausible prebiotic path to proto-peptides. Nat. Commun. 13, 2569 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Schmitt-Kopplin, P. et al. Complex carbonaceous matter in Tissint martian meteorites give insights into the diversity of organic geochemistry on Mars. Sci. Adv. 9, eadd6439 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  63. Oró, J. Comets and the formation of biochemical compounds on the primitive Earth. Nature 190, 389–390 (1961).

    Article  Google Scholar 

  64. Miller, S. L. & Urey, H. C. Organic compound synthesis on the primitive Earth. Science 130, 245–251 (1959).

    Article  CAS  PubMed  Google Scholar 

  65. Oparin, A. I. The Origin of Life on the Earth (Academic Press, 1957).

  66. Russell, M. J., Hall, A. J., Cairns-Smith, A. G. & Braterman, P. S. Submarine hot springs and the origin of life. Nature 336, 117 (1988).

    Article  Google Scholar 

  67. Powner, M. W., Gerland, B. & Sutherland, J. D. Synthesis of activated pyrimidine ribonucleotides in prebiotically plausible conditions. Nature 459, 239–242 (2009).

    Article  CAS  PubMed  Google Scholar 

  68. Buckner, D. K. et al. Origin-diagnostic patterns in lipid distributions: strategies for life detection. In 53rd Lunar and Planetary Science Conference LPI contribution no. 2678, id.2571 (LPI, 2022).

  69. Dworkin, J. P., Deamer, D. W., Sandford, S. A. & Allamandola, L. J. Self-assembling amphiphilic molecules: synthesis in simulated interstellar/precometary ices. Proc. Natl Acad. Sci. USA 98, 815–819 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Pierazzo, E. & Chyba, C. F. Amino acid survival in large cometary impacts. Meteorit. Planet. Sci. 34, 909–918 (1999).

    Article  CAS  Google Scholar 

  71. Chyba, C. F., Thomas, P. J., Brookshaw, L. & Sagan, C. Cometary delivery of organic molecules to the early Earth. Science 249, 366–373 (1990).

    Article  CAS  PubMed  Google Scholar 

  72. Osinski, G. R., Cockell, C. S., Pontefract, A. & Sapers, H. M. The role of meteorite impacts in the origin of life. Astrobiology 20, 1121–1149 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Mehta, C., Perez, A., Thompson, G. & Pasek, M. A. Caveats to exogenous organic delivery from ablation, dilution, and thermal degradation. Life 8, 13 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  74. Blackmond, D. G. The origin of biological homochirality. Cold Spring Harb. Perspect. Biol. 11, a032540 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Garcia, A. D. et al. The astrophysical formation of asymmetric molecules and the emergence of a chiral bias. Life 9, 29 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Nam, I., Lee, J. K., Nam, H. G. & Zare, R. N. Abiotic production of sugar phosphates and uridine ribonucleoside in aqueous microdroplets. Proc. Natl Acad. Sci. USA 114, 12396–12400 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Pasek, M. A., Gull, M. & Herschy, B. Phosphorylation on the early earth. Chem. Geol. 475, 149–170 (2017).

    Article  CAS  Google Scholar 

  78. Pasek, M. A. Schreibersite on the early Earth: scenarios for prebiotic phosphorylation. Geosci. Front. 8, 329–335 (2017).

    Article  CAS  Google Scholar 

  79. Hess, B. L., Piazolo, S. & Harvey, J. Lightning strikes as a major facilitator of prebiotic phosphorus reduction on early Earth. Nat. Commun. 12, 1535 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Pasek, M. A. Thermodynamics of prebiotic phosphorylation. Chem. Rev. 120, 4690–4706 (2020).

    Article  CAS  PubMed  Google Scholar 

  81. Pasek, M. A., Harnmeijer, J. P., Buick, R., Gull, M. & Atlas, Z. Evidence for reactive reduced phosphorus species in the early Archean ocean. Proc. Natl Acad. Sci. USA 110, 10089–10094 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Gibard, C., Bhowmik, S., Karki, M., Kim, E. K. & Krishnamurthy, R. Phosphorylation, oligomerization and self-assembly in water under potential prebiotic conditions. Nat. Chem. 10, 212–217 (2018).

    Article  CAS  PubMed  Google Scholar 

  83. Agúndez, M., Cernicharo, J., Decin, L., Encrenaz, P. & Teyssier, D. Confirmation of circumstellar phosphine. Astrophys. J. Lett. 790, L27 (2014).

    Article  Google Scholar 

  84. Ridgway, S. T., Wallace, L. & Smith, G. R. The 800-1200 inverse centimeter absorption spectrum of Jupiter. Astrophys. J. 207, 1002–1006 (1976).

    Article  CAS  Google Scholar 

  85. Larson, H. P., Fink, U., Smith, H. A. & Davis, D. S. The middle-infrared spectrum of Saturn - evidence for phosphine and upper limits to other trace atmospheric constituents. Astrophys. J. 240, 327–337 (1980).

    Article  CAS  Google Scholar 

  86. Rivilla, V. M. et al. ALMA and ROSINA detections of phosphorus-bearing molecules: the interstellar thread between star-forming regions and comets. Mon. Not. R. Astron. Soc. 492, 1180–1198 (2020).

    Article  CAS  Google Scholar 

  87. Rivilla, V. M. et al. Phosphorus-bearing molecules in the Galactic Center. Mon. Not. R. Astron. Soc. Lett. 475, L30–L34 (2018).

    Article  CAS  Google Scholar 

  88. Zhu, C. et al. An interstellar synthesis of glycerol phosphates. Astrophys. J. Lett. 899, L3 (2020).

    Article  CAS  Google Scholar 

  89. Aleksandrova, M., Rahmatova, F., Russell, D. A. & Bonfio, C. Ring opening of glycerol cyclic phosphates leads to a diverse array of potentially prebiotic phospholipids. J. Am. Chem. Soc. 145, 25614–25620 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Rivilla, V. M. et al. Discovery in space of ethanolamine, the simplest phospholipid head group. Proc. Natl Acad. Sci. USA 118, e2101314118 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Glavin, D. P. et al. Extraterrestrial amino acids in the Almahata Sitta meteorite. Meteorit. Planet. Sci. 45, 1695–1709 (2010).

    Article  CAS  Google Scholar 

  92. Bernstein, M. P., Dworkin, J. P., Sandford, S. A., Cooper, G. W. & Allamandola, L. J. Racemic amino acids from the ultraviolet photolysis of interstellar ice analogues. Nature 416, 401–403 (2002).

    Article  CAS  PubMed  Google Scholar 

  93. Bocková, J., Garcia, A. D., Jones, N. C., Hoffmann, S. V. & Meinert, C. Chiroptical properties of membrane glycerophospholipids and their chiral backbones. Chirality 36, e23654 (2024).

    Article  PubMed  Google Scholar 

  94. Meinert, C. et al. Anisotropy spectra of amino acids. Angew. Chem. Int. Ed. 51, 4484–4487 (2012).

    Article  CAS  Google Scholar 

  95. De Marcellus, P. et al. Aldehydes and sugars from evolved precometary ice analogs: importance of ices in astrochemical and prebiotic evolution. Proc. Natl Acad. Sci. USA 112, 956–970 (2015).

    Article  Google Scholar 

  96. Meinert, C. et al. Ribose and related sugars from ultraviolet irradiation of interstellar ice analogs. Science 352, 208–212 (2016).

    Article  CAS  PubMed  Google Scholar 

  97. Pizzarello, S., Schrader, D. L., Monroe, A. A. & Lauretta, D. S. Large enantiomeric excesses in primitive meteorites and the diverse effects of water in cosmochemical evolution. Proc. Natl Acad. Sci. USA 109, 11949–11954 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Ishigami, T., Suga, K. & Umakoshi, H. Chiral recognition of l-amino acids on liposomes prepared with l-phospholipid. ACS Appl. Mater. Interfaces 7, 21065–21072 (2015).

    Article  CAS  PubMed  Google Scholar 

  99. Ishigami, T., Kaneko, Y., Suga, K., Okamoto, Y. & Umakoshi, H. Homochiral oligomerization of L-histidine in the presence of liposome membranes. Colloid Polym. Sci. 293, 3649–3653 (2015).

    Article  CAS  Google Scholar 

  100. Bocková, J., Jones, N. C., Meierhenrich, U. J., Hoffmann, S. V. & Meinert, C. Chiroptical activity of hydroxycarboxylic acids with implications for the origin of biological homochirality. Commun. Chem. 4, 86 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  101. Pizzarello, S., Wang, Y. & Chaban, G. M. A comparative study of the hydroxy acids from the Murchison, GRA 95229 and LAP 02342 meteorites. Geochim. Cosmochim. Acta 74, 6206–6217 (2010).

    Article  CAS  Google Scholar 

  102. Burton, A. S. & Berger, E. L. Insights into abiotically-generated amino acid enantiomeric excesses found in meteorites. Life 8, 14 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  103. Glavin, D. P., Callahan, M. P., Dworkin, J. P. & Elsila, J. E. The effects of parent body processes on amino acids in carbonaceous chondrites. Meteorit. Planet. Sci. 45, 1948–1972 (2010).

    Article  CAS  Google Scholar 

  104. Mamajanov, I. et al. Ester formation and hydrolysis during wet-dry cycles: generation of far-from-equilibrium polymers in a model prebiotic reaction. Macromolecules 47, 1334–1343 (2014).

    Article  CAS  Google Scholar 

  105. Frenkel-Pinter, M. et al. Selective incorporation of proteinaceous over nonproteinaceous cationic amino acids in model prebiotic oligomerization reactions. Proc. Natl Acad. Sci. USA 116, 16338–16346 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Blocher, M., Hitz, T. & Luisi, P. L. Stereoselectivity in the oligomerization of racemic tryptophan N-carboxyanhydride (NCA-Trp) as determined by isotope labeling and mass spectrometry. Helv. Chim. Acta 84, 842–848 (2001).

    Article  CAS  Google Scholar 

  107. Blair, N. E. & Bonner, W. A. A model for the enantiomeric enrichment of polypeptides on the primitive Earth. Orig. Life 11, 331–335 (1981).

    Article  CAS  PubMed  Google Scholar 

  108. Deng, M., Yu, J. & Blackmond, D. G. Symmetry breaking and chiral amplification in prebiotic ligation reactions. Nature 626, 1019–1024 (2024).

    Article  CAS  PubMed  Google Scholar 

  109. Canavelli, P., Islam, S. & Powner, M. W. Peptide ligation by chemoselective aminonitrile coupling in water. Nature 571, 546–549 (2019).

    Article  CAS  PubMed  Google Scholar 

  110. Schneider, H.-J. Limitations and extensions of the lock-and-key principle: differences between gas state, solution and solid state structures. Int. J. Mol. Sci. 16, 6694–6717 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Sheng, X., Kazemi, M., Planas, F. & Himo, F. Modeling enzymatic enantioselectivity using quantum chemical methodology. ACS Catal. 10, 6430–6449 (2020).

    Article  CAS  Google Scholar 

  112. Reetz, M. T. Controlling the enantioselectivity of enzymes by directed evolution: practical and theoretical ramifications. Proc. Natl Acad. Sci. USA 101, 5716–5722 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Kapon, Y. et al. Evidence for new enantiospecific interaction force in chiral biomolecules. Chem 7, 2787–2799 (2021).

    Article  CAS  Google Scholar 

  114. Weissbuch, I. & Lahav, M. Crystalline architectures as templates of relevance to the origins of homochirality. Chem. Rev. 111, 3236–3267 (2011).

    Article  CAS  PubMed  Google Scholar 

  115. Hu, J., Cochrane, W. G., Jones, A. X., Blackmond, D. G. & Paegel, B. M. Chiral lipid bilayers are enantioselectively permeable. Nat. Chem. 13, 786–791 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Han, J., Kitagawa, O., Wzorek, A., Klika, K. D. & Soloshonok, V. A. The self-disproportionation of enantiomers (SDE): a menace or an opportunity? Chem. Sci. 9, 1718–1739 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Islam, S. & Powner, M. W. Prebiotic systems chemistry: complexity overcoming clutter. Chem 2, 470–501 (2017).

    Article  CAS  Google Scholar 

  118. Sacerdote, M. G. & Szostak, J. W. Semipermeable lipid bilayers exhibit diastereoselectivity favoring ribose. Proc. Natl Acad. Sci. USA 102, 6004–6008 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Pizzarello, S. & Weber, A. L. Prebiotic amino acids as asymmetric catalysts. Science 303, 1151 (2004).

    Article  CAS  PubMed  Google Scholar 

  120. Breslow, R. & Cheng, Z. L. L-amino acids catalyze the formation of an excess of D-glyceraldehyde, and thus of other D sugars, under credible prebiotic conditions. Proc. Natl Acad. Sci. USA 107, 5723–5725 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Yu, J., Jones, A. X., Legnani, L. & Blackmond, D. G. Prebiotic access to enantioenriched glyceraldehyde mediated by peptides. Chem. Sci. 12, 6350–6354 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Wu, L. F., Su, M., Liu, Z., Bjork, S. J. & Sutherland, J. D. Interstrand aminoacyl transfer in a tRNA acceptor stem-overhang mimic. J. Am. Chem. Soc. 143, 11836–11842 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Ozturk, S. F., Sasselov, D. D. & Sutherland, J. D. The central dogma of biological homochirality: how does chiral information propagate in a prebiotic network? J. Chem. Phys. 159, 061102 (2023).

    Article  CAS  PubMed  Google Scholar 

  124. Hein, J. E., Tse, E. & Blackmond, D. G. A route to enantiopure RNA precursors from nearly racemic starting materials. Nat. Chem. 3, 704–706 (2011).

    Article  CAS  PubMed  Google Scholar 

  125. Georgiou, C. D. & Deamer, D. W. Lipids as universal biomarkers of extraterrestrial life. Astrobiology 14, 541–549 (2014).

    Article  CAS  PubMed  Google Scholar 

  126. Vago, J. L. et al. Habitability on early Mars and the search for biosignatures with the ExoMars rover. Astrobiology 17, 471–510 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  127. Summons, R. E., Albrecht, P., McDonald, G. & Moldowan, J. M. Molecular biosignatures. Space Sci. Rev. 135, 133–159 (2008).

    Article  CAS  Google Scholar 

  128. Meierhenrich, U. J., Thiemann, W. H.-P., Barbier, B., Schubert, C. J. & Brack, A. in Geochemistry and the Origin of Life (eds Nakashima, S. et al.) 269–284 (Universal Academy Press, 2001).

  129. Boeren, N. J. et al. Detecting lipids on planetary surfaces with laser desorption ionization mass spectrometry. Planet. Sci. J. 3, 241 (2022).

    Article  Google Scholar 

  130. Dannenmann, M. et al. Toward detecting biosignatures of DNA, lipids, and metabolic intermediates from bacteria in ice grains emitted by Enceladus and Europa. Astrobiology 23, 60–75 (2023).

    Article  CAS  PubMed  Google Scholar 

  131. Klenner, F. et al. Analog experiments for the identification of trace biosignatures in ice grains from extraterrestrial ocean worlds. Astrobiology 20, 179–189 (2020).

    Article  CAS  PubMed  Google Scholar 

  132. Klenner, F. et al. Discriminating abiotic and biotic fingerprints of amino acids and fatty acids in ice grains relevant to ocean worlds. Astrobiology 20, 1168–1184 (2020).

    Article  CAS  PubMed  Google Scholar 

  133. Kissin, Y. V. Hydrocarbon components in carbonaceous meteorites. Geochim. Cosmochim. Acta 67, 1723–1735 (2003).

    Article  CAS  Google Scholar 

  134. Greenberg, J. M. in Cosmic Rays, Supernovae and the Interstellar Medium NATO ASI Series, Vol. 337 (eds Shapiro, M. M. et al.) 57–68 (Springer, 1991).

  135. Arumainayagam, C. R. et al. Extraterrestrial prebiotic molecules: photochemistry vs. radiation chemistry of interstellar ices. Chem. Soc. Rev. 48, 2293–2314 (2019).

    Article  CAS  PubMed  Google Scholar 

  136. Naraoka, H. et al. Soluble organic molecules in samples of the carbonaceous asteroid (162173) Ryugu. Science 379, eabn9033 (2023).

    Article  CAS  PubMed  Google Scholar 

  137. Parker, E. T. et al. Extraterrestrial amino acids and amines identified in asteroid Ryugu samples returned by the Hayabusa2 mission. Geochim. Cosmochim. Acta 347, 42–57 (2023).

    Article  CAS  Google Scholar 

  138. Bottke, W. F. & Norman, M. D. The late heavy bombardment. Annu. Rev. Earth Planet. Sci. 45, 619–647 (2017).

    Article  CAS  Google Scholar 

  139. Bailey, J. et al. Circular polarization in star-formation regions: implications for biomolecular homochirality. Science 281, 672–674 (1998).

    Article  PubMed  Google Scholar 

  140. Kwon, J. et al. Near-infrared circular polarization images of NGC 6334-V. Astrophys. J. Lett. 765, L6 (2013).

    Article  Google Scholar 

  141. Modica, P. et al. Enantiomeric excesses induced in amino acids by ultraviolet circularly polarized light irradiation of extraterrestrial ice analogs: a possible source of asymmetry for prebiotic chemistry. Astrophys. J. 788, 79 (2014).

    Article  Google Scholar 

  142. Gledhill, T. M. & McCall, A. Circular polarization by scattering from spheroidal dust grains. Mon. Not. R. Astron. Soc. 314, 123–137 (2000).

    Article  CAS  Google Scholar 

  143. Buschermöhle, M. et al. An extended search for circularly polarized infrared radiation from the OMC‐1 region of Orion. Astrophys. J. 624, 821–826 (2005).

    Article  Google Scholar 

  144. Miller, G. E. & Scalo, J. M. On the birthplaces of stars. Publ. Astron. Soc. Pac. 90, 506–513 (1978).

    Article  Google Scholar 

  145. Hillenbrand, L. A. On the stellar population and star-forming history of the Orion Nebula Cluster. Astron. J. 113, 1733–1768 (1997).

    Article  CAS  Google Scholar 

  146. Garcia, A. D. et al. Chiroptical activity of gas phase propylene oxide predicting the handedness of interstellar circular polarization in the presolar nebulae. Sci. Adv. 8, eadd4614 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. de Marcellus, P. et al. Non-racemic amino acid production by ultraviolet irradiation of achiral interstellar ice analogs with circularly polarized light. Astrophys. J. Lett. 727, L27 (2011).

    Article  Google Scholar 

  148. Flores, J. J., Bonner, W. A. & Massey, G. A. Asymmetric photolysis of (RS)-leucine with circularly polarized ultraviolet light. J. Am. Chem. Soc. 99, 3622–3625 (1977).

    Article  CAS  PubMed  Google Scholar 

  149. Meierhenrich, U. J. et al. Photolysis of rac-leucine with circularly polarized synchrotron radiation. Chem. Biodivers. 7, 1651–1659 (2010).

    Article  CAS  PubMed  Google Scholar 

  150. Meierhenrich, U. J. et al. Asymmetric vacuum UV photolysis of the amino acid leucine in the solid state. Angew. Chem. Int. Ed. 44, 5630–5634 (2005).

    Article  CAS  Google Scholar 

  151. Meinert, C. et al. Photonenergy-controlled symmetry breaking with circularly polarized light. Angew. Chem. Int. Ed. 53, 210–214 (2014).

    Article  CAS  Google Scholar 

  152. Bocková, J., Jones, N. C., Topin, J., Hoffmann, S. V. & Meinert, C. Uncovering the chiral bias of meteoritic isovaline through asymmetric photochemistry. Nat. Commun. 14, 3381 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This project received financial support from the National Centre for Scientific Research (CNRS) through the Mission for Transversal and Interdisciplinary Initiatives (MITI), the Simone and Cino Del Duca Foundation and the European Research Council under the European Union’s Horizon 2020 research and innovation programme (grant agreement 804144). Further funding was provided by the European Union’s Horizon 2020 research and innovation programme under grant agreement numbers 101004806 (MOSBRI) and 730872 (CALIPSOplus). J.B. is supported by a postdoctoral fellowship from the National Centre for Space Studies (CNES).

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to all aspects of the manuscript.

Corresponding author

Correspondence to Cornelia Meinert.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Reviews Chemistry thanks David Deamer, Matthew Pasek, and Dimitar Sasselov for their contribution to the peer review of this work.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bocková, J., Jones, N.C., Hoffmann, S.V. et al. The astrochemical evolutionary traits of phospholipid membrane homochirality. Nat Rev Chem 8, 652–664 (2024). https://doi.org/10.1038/s41570-024-00627-w

Download citation

  • Accepted:

  • Published:

  • Issue date:

  • DOI: https://doi.org/10.1038/s41570-024-00627-w

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing