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Edited by David A. Weitz, Harvard University, Cambridge, MA, and approved June 24, 2019 (received for review February 8, 2019)
Significance
The prebiotic milieu was likely heterogeneous, consisting of a large number of chemicals and their associated reactions, including those not only of biological compounds, but also nonbiological compounds. Although origins of life research has focused primarily on biological molecules, the nonbiological molecules which were also present may have assisted evolving chemical systems in unforeseen ways. Thus, we synthesized and assembled membraneless polyester microdroplets from drying of pools of simple α-hydroxy acid monomers and showed that they can act as plausible prebiotic compartments. By having the capacity to undergo combinatorial rearrangement, these microdroplets could have developed versatile abilities to host early genetic and metabolic systems critical for the origins of life.
Abstract
Compartmentalization was likely essential for primitive chemical systems during the emergence of life, both for preventing leakage of important components, i.e., genetic materials, and for enhancing chemical reactions. Although life as we know it uses lipid bilayer-based compartments, the diversity of prebiotic chemistry may have enabled primitive living systems to start from other types of boundary systems. Here, we demonstrate membraneless compartmentalization based on prebiotically available organic compounds, α-hydroxy acids (αHAs), which are generally coproduced along with α-amino acids in prebiotic settings. Facile polymerization of αHAs provides a model pathway for the assembly of combinatorially diverse primitive compartments on early Earth. We characterized membraneless microdroplets generated from homo- and heteropolyesters synthesized from drying solutions of αHAs endowed with various side chains. These compartments can preferentially and differentially segregate and compartmentalize fluorescent dyes and fluorescently tagged RNA, providing readily available compartments that could have facilitated chemical evolution by protecting, exchanging, and encapsulating primitive components. Protein function within and RNA function in the presence of certain droplets is also preserved, suggesting the potential relevance of such droplets to various origins of life models. As a lipid amphiphile can also assemble around certain droplets, this further shows the droplets’ potential compatibility with and scaffolding ability for nascent biomolecular systems that could have coexisted in complex chemical systems. These model compartments could have been more accessible in a “messy” prebiotic environment, enabling the localization of a variety of protometabolic and replication processes that could be subjected to further chemical evolution before the advent of the Last Universal Common Ancestor.
Footnotes
↵1T.Z.J. and K.C. contributed equally to this work.
- ↵2To whom correspondence may be addressed. Email: tzjia{at}elsi.jp or kuhan{at}ukm.edu.my.
Author contributions: T.Z.J., K.C., Y.H., R.A., T.U., and H.J.C. designed research; T.Z.J., K.C., Y.H., R.A., T.U., K.M., and H.J.C. performed research; T.Z.J., K.C., and H.J.C. contributed new reagents/analytic tools; T.Z.J., K.C., Y.H., and H.J.C. analyzed data; and T.Z.J., K.C., and H.J.C. wrote the paper.
Conflict of interest statement: The authors may file a patent application within 12 months after publication of the manuscript.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1902336116/-/DCSupplemental.
Published under the PNAS license.
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Membraneless polyester microdroplets as primordial compartments at the origins of life
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