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.2019 Dec 6;9(6):20190067.
doi: 10.1098/rsfs.2019.0067. Epub 2019 Oct 18.

Isoprenoids enhance the stability of fatty acid membranes at the emergence of life potentially leading to an early lipid divide

Affiliations

Isoprenoids enhance the stability of fatty acid membranes at the emergence of life potentially leading to an early lipid divide

Sean F Jordan et al. Interface Focus..

Abstract

Two key problems concern cell membranes during the emergence and early evolution of life: what was their initial composition, and why did the membranes of archaea and bacteria diverge? The composition of the first cell membranes could shed light on the most likely environment for the emergence of life. The opposing stereochemistry of modern lipid glycerol-phosphate headgroups in bacteria and archaea suggests that early membranes were composed of single chain amphiphiles, perhaps both fatty acids and isoprenoids. We investigated the effect of adding isoprenoids to fatty acid membranes using a combination of UV-visible spectroscopy, confocal microscopy and transmission electron microscopy. We tested the stability of these membranes across a pH range and under different concentrations of ionic species relevant to oceanic hydrothermal environments, including Na2+, Cl-, Mg2+, Ca2+,HCO3- , Fe3+, Fe2+ and S2-. We also tested the assembly of vesicles in the presence of Fe particles and FeS precipitates. We found that isoprenoids enhance the stability of membranes in the presence of salts but require 30-fold higher concentrations for membrane formation. Intriguingly, isoprenoids strongly inhibit the tendency of vesicles to aggregate together in the presence of either Fe particles or FeS precipitates. These striking physical differences in the stability and aggregation of protocells may have shaped the divergence of bacteria and archaea in early hydrothermal environments.

Keywords: fatty acids; isoprenoids; lipid divide; origin of life; protocells; vesicles.

© 2019 The Authors.

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Conflict of interest statement

We declare we have no competing interests.

Figures

Figure 1.
Figure 1.
(a) Chemical structures of single chain amphiphiles used in this study: decanoic acid (DA), decan-1-ol (DOH) and geraniol (GOH). (b) Sample dataset depicting the standard sigmoid shape observed for optical density analysis of a vesicle solution. Transition between different structural states is shown below. (Online version in colour.)
Figure 2.
Figure 2.
(a) OD data for 50 mM 1 : 1 DA/DOH solutions from pH 7 to 13. (b) OD data for 50 mM 1 : 1 DA/GOH solutions from pH 7 to 13. (c) Plot of absorbance at 480 nm versus concentration (mM) for DA/DOH. The intersection of the two trendlines indicates the CBC of 157 µM. (d) Plot of absorbance at 480 nm versus concentration (mM) for DA/GOH. The intersection of the two trendlines indicates the CBC of 4.9 mM. (e) Confocal micrograph of DA/DOH in H2O at pH 12.1. (f) Confocal micrograph of DA/GOH in H2O at pH 11.6. Arrows indicate individual vesicles in solution. (Online version in colour.)
Figure 3.
Figure 3.
Confocal and TEM micrographs of solutions prepared in 600 mM NaCl. (a) Confocal micrograph of DA/DOH at pH 11.7 showing complete aggregation of vesicles, (b) confocal micrograph of DA/GOH at pH 11.6, (c) TEM micrograph of DA/DOH at pH 11.9, (d) TEM micrograph of DA/GOH at pH 11.8. Vesicles are indicated by blue arrows. (Online version in colour.)
Figure 4.
Figure 4.
Confocal and TEM micrographs of solutions prepared in 50 mM MgCl2. (a) Confocal micrograph of DA/DOH at pH 11.2, (b) confocal micrograph of DA/GOH at pH 11.3, (c) TEM micrograph of DA/DOH at pH 11.6, (d) TEM micrograph of DA/GOH at pH 11.6. Vesicles are indicated by blue arrows. (Online version in colour.)
Figure 5.
Figure 5.
Confocal and TEM micrographs of solutions prepared in 10 mM CaCl2. (a) Confocal micrograph of DA/DOH at pH 11.6, (b) confocal micrograph of DA/GOH at pH 11.6, (c) TEM micrograph of DA/DOH at pH 11.9, (d) TEM micrograph of DA/GOH at pH 11.8. Vesicles are indicated by blue arrows. (Online version in colour.)
Figure 6.
Figure 6.
Confocal and TEM micrographs of solutions prepared in 1 mM FeCl3. (a) Confocal micrograph of DA/DOH at pH 13.0, (b) confocal micrograph of DA/GOH at pH 12.9, (c) TEM micrograph of DA/DOH at pH 12.0, (d) TEM micrograph of DA/GOH at pH 12.0. Vesicles are indicated by blue arrows. (Online version in colour.)
Figure 7.
Figure 7.
Confocal and TEM micrographs of anoxic solutions prepared in 12.5 mM FeS2. (a) Confocal micrograph of DA/DOH at pH 12.0, (b) confocal micrograph of DA/GOH at pH 12.0, (c) TEM micrograph of DA/DOH at pH 12.1, (d) TEM micrograph of DA/GOH at pH 12.2. Vesicles are indicated by blue arrows. (Online version in colour.)
Figure 8.
Figure 8.
Confocal and TEM micrographs of anoxic solutions prepared in H2O followed by addition of Fe powder (less than 212 µm mesh). (a) Confocal micrograph of DA/DOH at pH 12.1, (b) confocal micrograph of DA/GOH at pH 12.1, (c) TEM micrograph of DA/DOH at pH 12.2, (d) TEM micrograph of DA/GOH at pH 12.1. Vesicles are indicated by blue arrows. (Online version in colour.)
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