Prebiotic Protocell Membranes Retain Encapsulated Contents during Flocculation, and Phospholipids Preserve Encapsulation during Dehydration

Cohen, Zachary R.; Cornell, Caitlin E.; Catling, David C.; Black, Roy A.; Keller, Sarah L.

doi:10.1021/acs.langmuir.1c03296

Cited by 15 publications

(21 citation statements)

References 40 publications

(69 reference statements)

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“…We used the reconstitution approach with synthetic systems. − Reconstitution approach is advantageous in the sense that researchers can test physical models in a well-defined environment that can inspire them to design and synthesize biomimetic systems for therapeutic purposes. − In this study, we used bottom-up reconstitution with giant unilamellar vesicle (GUV) system, a lipid bilayer vesicle with a typical diameter of 1–100 μm. GUV has a relatively well-defined lipid composition and can be readily observed by optical microscopy.…”

Section: Introductionmentioning

confidence: 99%

Membrane Cargo Density-Dependent Interaction between Protein and Lipid Domains on the Giant Unilamellar Vesicles

2022

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Protein cargos anchored on the lipid membrane can be segregated by fluidic domain phase separation. Lipid membranes at certain compositions may separate into lipid domains to segregate cargos, and protein cargos themselves may be involved in protein condensate domain formation with multivalent binding proteins to segregate cargos. Recent studies suggest that these two driving forces of phase separation closely interact on the lipid membranes to promote codomain formation. In this report, we studied the effect of cargo density on the outcome of the cargo phase separation on giant unilamellar vesicles. Proteins and lipids are connected only by the anchored cargos, so it was originally hypothesized that higher cargo density would increase the degree of interaction between the lipid and protein domains, promoting more phase separation. However, fluorescence image analysis on different cargo densities showed that the cooperative domain formation and steric pressure are at a tug of war opposing each other. Cooperative domain formation is dominant under lower anchor density conditions, and above a threshold density, steric pressure was dominant opposing the domain formation. The result suggests that the cargo density is a key parameter affecting the outcome of cargo organization on the lipid membranes by phase separation.

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Section: Introductionmentioning

confidence: 99%

Membrane Cargo Density-Dependent Interaction between Protein and Lipid Domains on the Giant Unilamellar Vesicles

2022

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“…After all fractions were collected, the column was flushed with at least 2 volume equivalents of 0.2 M bicine (pH 9) for storage. The SEC running buffer contained 0.10 M NaHCO 3 to match ionic conditions in the vesicle sample and 20 mM fatty acid (either decanoic acid or dodecanoic acid, corresponding to the vesicles) so that the total amphiphile concentration remained above the critical vesicle concentration . The pH of the running buffer was adjusted to 8.70 (±0.05) by adding small volumes of concentrated HCl or NaOH solutions.…”

Section: Methodsmentioning

confidence: 99%

“…The SEC running buffer contained 0.10 M NaHCO 3 to match ionic conditions in the vesicle sample and 20 mM fatty acid (either decanoic acid or dodecanoic acid, corresponding to the vesicles) so that the total amphiphile concentration remained above the critical vesicle concentration. 2 The pH of the running buffer was adjusted to 8.70 (±0.05) by adding small volumes of concentrated HCl or NaOH solutions. The fractions containing vesicles were combined and further diluted in SEC running buffer for analysis.…”

Section: Size Exclusion Chromatography (Sec)mentioning

confidence: 99%

“…(1) We prepared parallel samples of vesicles in the fluid or the gel phase in a 96-well plate. (2) The 96-well plate was equilibrated to the temperature of fluid or gelphase vesicles, along with a solution of decanoic acid micelles (1.0 M decanoic acid in 1.0 M NaOH). ( 3) In 5 min intervals, 10 μL of micelle solution (∼2 equiv of decanoic acid) was added to a different vesicle sample in the 96-well plate to achieve growth times of 0−40 min (the time prior to addition of the micelle solution is referred to as the "wait time" in Figure 3).…”

Section: Size Exclusion Chromatography (Sec)mentioning

confidence: 99%

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Prebiotic Vesicles Retain Solutes and Grow by Micelle Addition after Brief Cooling below the Membrane Melting Temperature

et al. 2022

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Replication of RNA genomes within membrane vesicles may have been a critical step in the development of protocells on the early Earth. Cold temperatures near 0 °C improve the stability of RNA and allow efficient copying, while some climate models suggest a cold early Earth, so the first protocells may have arisen in cold-temperature environments. However, at cold temperatures, saturated fatty acids, which would have been available on the early Earth, form gel-phase membranes that are rigid and restrict mobility within the bilayer. Two primary roles of protocell membranes are to encapsulate solutes and to grow by incorporating additional fatty acids from the environment. We test here whether fatty acid membranes in the gel phase accomplish these roles. We find that gel-phase membranes of 10carbon amphiphiles near 0 °C encapsulate aqueous dye molecules as efficiently as fluid-phase membranes do, but the contents are released if the aqueous solution is frozen at −20 °C. Gelphase membranes do not grow measurably by micelle addition, but growth resumes when membranes are warmed above the gel−liquid transition temperature. We find that longer, 12carbon amphiphiles do not retain encapsulated contents near 0 °C. Together, our results suggest that protocells could have developed within environments that experience temporary cooling below the membrane melting temperature, and that membranes composed of relatively short-chain fatty acids would encapsulate solutes more efficiently as temperatures approached 0 °C.

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“…Alternatively, and with significantly reduced selectivity, the growing oligomer could be encapsulated or bind to the surface of a mesoscopic structure formed by amphiphiles. Membrane structures such as multilayers, micelles, or vesicles could have this capability and act as efficient selectors for specific sequences of biopolymers such as polypeptides or nucleic acids [ 18 , 19 , 20 , 21 , 22 , 23 , 24 , 25 ].…”

Section: The Potential Nature Of a “Selector”mentioning

confidence: 99%

Spontaneous Formation of Functional Structures in Messy Environments

Mayer

2022

Life

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Even though prebiotic chemistry initially deals with simple molecules, its composition rapidly gains complexity with oligomerization. Starting with, e.g., 20 monomers (such as the 20 proteinogenic amino acids), we expect 400 different dimers, 3,200,000 pentamers, or more than 1013 decamers. Hence, the starting conditions are very messy but also form a very powerful pool of potentially functional oligomers. A selecting structure (a “selector” such as membrane multilayers or vesicles) may pick and accumulate those molecules from the pool that fulfill a simple function (such as the suitability to integrate into a bilayer membrane). If this “selector” is, in turn, subject to a superimposed selection in a periodic process, the accumulated oligomers may be further trimmed to fulfill more complex functions, which improve the survival rate of the selectors. Successful oligomers will be passed from generation to generation and further improved in subsequent steps. After thousands of generations, the selector, together with its integrated oligomers, can form a functional unit of considerable order and complexity. The actual power of this process of random formation and selection has already been shown in laboratory experiments. In this concept paper, earlier results are summarized and brought into a new context.

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Prebiotic Protocell Membranes Retain Encapsulated Contents during Flocculation, and Phospholipids Preserve Encapsulation during Dehydration

Cited by 15 publications

References 40 publications

Membrane Cargo Density-Dependent Interaction between Protein and Lipid Domains on the Giant Unilamellar Vesicles

Membrane Cargo Density-Dependent Interaction between Protein and Lipid Domains on the Giant Unilamellar Vesicles

Prebiotic Vesicles Retain Solutes and Grow by Micelle Addition after Brief Cooling below the Membrane Melting Temperature

Spontaneous Formation of Functional Structures in Messy Environments

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