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Delineating the rules for structural adaptation of membrane-associated proteins to evolutionary changes in membrane lipidome

Maria Makarova, Maria Peter, Gabor Balogh, Attila Glatz, James I. MacRae, Nestor Lopez Mora, Paula Booth, Eugene Makeyev, Laszlo Vigh, Snezhana Oliferenko

Preprint posted on September 09, 2019 https://www.biorxiv.org/content/10.1101/762146v1

Article now published in Current Biology at http://dx.doi.org/10.1016/j.cub.2019.11.043

Greasing the wheels of change: probing the co-evolution of lipid chemistry and membrane-associated proteins using related fission yeasts

Selected by Dey Lab

Lipid membranes are woven into the basic fabric of all cellular life, delineating the interface between cells and their external environment as well as the boundaries of internal compartments. Hundreds of proteins are embedded within, or associated with, each of these membranes, conferring identity upon compartments while also controlling the exchange of metabolites and signalling effectors between them. Perhaps unsurprisingly, the biochemical and biophysical properties of membrane-associated proteins are strongly influenced by membrane composition1 and local heterogeneity2. How do these properties of membranes and their cognate proteomes co-vary on evolutionary timescales? The answers to this question have key implications not just for our understanding of functional divergence between living species, but also of the evolution of compartmentalised cells. Eukaryotes evolved from a symbiotic merger of archaea and bacteria around 2 billion years ago3. How did the original eukaryotes exchange the ether-linked lipids of their archaeal ancestor for the ester-linked lipids of their bacterial endosymbiont?4 What imprint, if any, did this lipid exchange event leave upon the hybrid archaeal-bacterial proteome of the first eukaryotes?

The related fission yeasts Schizosaccharomyces pombe (S. pombe) and Schizosaccharomyces japonicus (S. japonicus) provide an excellent experimental test case for such questions, with the two species exhibiting striking differences in the regulation of cellular geometry5, polarity, and remodelling of the ER through the cell cycle6,7. Here, the authors profiled total cellular lipid extracts from the two yeasts by mass spectrometry, revealing surprising differences in bilayer composition.  Notably, a proportion of S. japonicus lipids have highly saturated, asymmetric tails, producing in vitro membranes with a higher degree of order and bending rigidity than those produced from their S. pombe counterparts (Figure 1). The authors speculate that this might have allowed the exploration of new ecological niches – unlike S. pombe, S. japonicus can undergo the yeast-to-hyphal transition and also survive anoxic environments.

 

Figure 1. Reproduced in full from Figure 4G of Makarova et al. 2019, under a Creative Commons CC-BY-NC-ND 4.0 international license. A diagram summarizing the authors’ hypothesis on co-evolution of transmembrane helices
and membrane lipids in S. pombe and S. japonicus.

 

The authors link the key differences in membrane chemistry to a divergence in the cytosolic fatty acid synthase (FAS) genes of the two species. Underscoring the critical impact of membrane biochemistry on cellular function, replacing the S. pombe FAS with the S. japonicus one caused a bucketload of problems for the transgenic host. This S. pombe fass.j. strain exhibited reduced growth rates across the entire physiological temperature range (especially at lower temperatures), a chronic induction of the unfolded protein response (UPR), and the downregulation of a range of membrane transporters.

Based on literature showing that the transmembrane (TM) domains of single-pass TM proteins tend to be shorter for those residing in the ER and cis-Golgi – where bilayers are thinner – than in other compartments1, the authors hypothesized that the S. pombe fass.j. defects might be linked to an inability of transmembrane proteins to insert properly into the mutant strain’s thinner membranes. In particular, if these errors occurred for ER-resident proteins, they would be more likely to affect protein folding and secretion. In line with this model, a proportion of S. japonicus single-pass TM proteins exhibit shortened TM domains relative to other fission yeasts, and replacing the TM domain of an S. pombe ER-resident protein with the S. japonicus version rescues mistargeting in the S. pombe fass.j background. Possibly due to the fact that the protein the authors chose for this experiment (Anp1) is a regulator of the mannosyltransferase complex, the altered Anp1 was also able to partially rescue the UPR defect of the S. pombe fass.j strain.

This work breaks new ground in our understanding of the extent and complexity of proteome-lipidome co-evolution, and I look forward to the authors’ future work on this topic. How does the altered membrane composition of the S. pombe fass.j strain influence ER and nuclear envelope dynamics through the cell cycle, given what is known about the differences between S. pombe and S. japonicus mitotic strategies?8 Extending the work described here, would it be possible to subject S. pombe fass.j to a directed evolution experiment?

 

References

  1. Sharpe, H. J., Stevens, T. J. & Munro, S. A comprehensive comparison of transmembrane domains reveals organelle-specific properties. Cell 142, 158–69 (2010).
  2. Sezgin, E., Levental, I., Mayor, S. & Eggeling, C. The mystery of membrane organization: composition, regulation and roles of lipid rafts. Nat. Rev. Mol. Cell Biol. 18, 361–374 (2017).
  3. Baum, D. A. A comparison of autogenous theories for the origin of eukaryotic cells. Am. J. Bot. 102, 1954–65 (2015).
  4. Koga, Y. Early Evolution of Membrane Lipids: How did the Lipid Divide Occur? J. Mol. Evol. 72, 274–282 (2011).
  5. Gu, Y. & Oliferenko, S. Cellular geometry scaling ensures robust division site positioning. Nat. Commun. 10, 268 (2019).
  6. Gu, Y., Yam, C. & Oliferenko, S. Rewiring of cellular division site selection in evolution of fission yeasts. Curr. Biol. 25, 1187–94 (2015).
  7. Makarova, M. & Oliferenko, S. Mixing and matching nuclear envelope remodeling and spindle assembly strategies in the evolution of mitosis. Curr. Opin. Cell Biol. 41, 43–50 (2016).
  8. Gu, Y., Yam, C. & Oliferenko, S. Divergence of mitotic strategies in fission yeasts. Nucleus-Austin 3, 220–225 (2012).

 

Posted on: 17th September 2019 , updated on: 18th September 2019

doi: https://doi.org/10.1242/prelights.13890

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