Journal
JOURNAL OF THE AMERICAN CHEMICAL SOCIETY
Volume 143, Issue 40, Pages 16589-16598Publisher
AMER CHEMICAL SOC
DOI: 10.1021/jacs.1c06595
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Funding
- European Union's Horizon 2020 research and innovation program under the Marie Sklodowska-Curie (RNA-Rep, MSCA grant) [839899]
- European Research Council (NANO-CELL, ERC-STG) [851667]
- Royal Commission for the Exhibition of 1851
- Mexican National Council for Science and Technology (CONACYT) [472427]
- Cambridge Trust
- EPSRC CDT in Nanoscience and Nanotechnology (NanoDTC) [EP/L015978/1]
- Natural Sciences and Engineering Research Council of Canada (NSERC) [401667]
- Royal Society [UF160152]
- European Research Council (ERC) [851667] Funding Source: European Research Council (ERC)
- Marie Curie Actions (MSCA) [839899] Funding Source: Marie Curie Actions (MSCA)
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Self-assembling single-chain amphiphiles in the prebiotic environment played a crucial role in the development of primitive cell cycles. However, the instability of prebiotic fatty acid-based membranes suggests that primitive cells could only function in stable environmental conditions. Membrane phase transitions, driven by environmental fluctuations, allowed for the generation of daughter protocells with reshuffled content, highlighting a potential environmentally driven mechanism for the emergence of functional primitive cells.
Self-assembling single-chain amphiphiles available in the prebiotic environment likely played a fundamental role in the advent of primitive cell cycles. However, the instability of prebiotic fatty acid-based membranes to temperature and pH seems to suggest that primitive cells could only host prebiotically relevant processes in a narrow range of nonfluctuating environmental conditions. Here we propose that membrane phase transitions, driven by environmental fluctuations, enabled the generation of daughter protocells with reshuffled content. A reversible membrane-to-oil phase transition accounts for the dissolution of fatty acid-based vesicles at high temperatures and the concomitant release of protocellular content. At low temperatures, fatty acid bilayers reassemble and encapsulate reshuffled material in a new cohort of protocells. Notably, we find that our disassembly/reassembly cycle drives the emergence of functional RNA-containing primitive cells from parent nonfunctional compartments. Thus, by exploiting the intrinsic instability of prebiotic fatty acid vesicles, our results point at an environmentally driven tunable prebiotic process, which supports the release and reshuffling of oligonucleotides and membrane components, potentially leading to a new generation of protocells with superior traits. In the absence of protocellular transport machinery, the environmentally driven disassembly/assembly cycle proposed herein would have plausibly supported protocellular content reshuffling transmitted to primitive cell progeny, hinting at a potential mechanism important to initiate Darwinian evolution of early life forms.
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