Why the Lipid Divide? Membrane Proteins as Drivers of the Split between the Lipids of the Three Domains of Life

Abstract

Recent results from engineered and natural samples show that the starkly different lipids of archaea and bacteria can form stable hybrid membranes. But if the two types can mix, why don't they? That is, why do most bacteria and all eukaryotes have only typically bacterial lipids, and archaea archaeal lipids? It is suggested here that the reason may lie on the other main component of cellular membranes: membrane proteins, and their close adaptation to the lipids. Archaeal lipids in modern bacteria could suggest that the last universal common ancestor (LUCA) had both lipid types. However, this would imply a rather elaborate evolutionary scenario, while negating simpler alternatives. In light of widespread horizontal gene transfer across the prokaryotic domains, hybrid membranes reveal that the lipid divide did not just occur once at the divergence of archaea and bacteria from LUCA. Instead, it continues to occur actively to this day. Also see the video abstract here https://youtu.be/TdKjxoDAtsg.

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

“…If there is no obvious penalty for mixing lipids, then why did the lipid divide occur? One possibility is that membrane proteins rather than lipids drove the divergence [61]. While appealing, this idea is undermined by the propensity of membrane proteins to evolve rapidly [62], which could compensate for subtle differences in lipid chemistry.…”

Is it possible that cells have had more than one origin?

“…Fibrobacteres/Chlorobi/Bacteroidetes), a membrane typical of archaea (Villanueva et al 2018). However, phylogenetic analyses tend to suggest that the acquisition of specific pathways from one domain to another are better explained by lateral transference and natural selection once the archaeal membrane is known to be more stable in high temperatures (Coleman et al 2019, Sojo 2019.…”

“…Since then, the search for characteristics of LUCA and explanations about how it originated have been guiding important works in the origin of life research program (Forterre et al 2005, Mat et al 2008, Gogarten and Deamer 2016, Martin et al 2016. Today, however, we know that the domain Eukarya evolved from a specific group of archaebacteria from the phylum Lokiarchaeota (subphylum Asgard) that was involved in symbiotic relationships with bacterial clades (Spang et al 2015, Spang et al 2019. Eukaryotes are therefore a derivate clade and were not involved in the constitution of LUCA.…”

The archaeal-bacterial lipid divide, could a distinct lateral proton route hold the answer?

“…Though archaeal and bacterial membranes are functional homologues, the chemical structure of their lipidic components reveals a split that is difficult to reconcile with a common origin, to the point that it has been proposed that the divide started from LUCA [1][2][3] and has been maintained until today. Archaea have sn-glycerol-1phosphate (G1P) phospholipids with ether-bond isoprenoid chains, while bacteria have sn-glycerol-3phosphate (G3P) esterified to fatty-acids.…”

“…Although there are pathways for synthesis of isoprenoids and fatty-acids in both domains [4], there are marked differences in their utilization of these biomolecules in membrane lipid synthesis. Recent research (see [3]) suggests that a transition could have taken place, during which the two sets of enzymatic machineries coexisted. Supporting this view, it is known that bacteria living in some extreme environments contain lipids with ether bonds in addition to the "normal" ester ones ( [5] and references therein).…”