Menu

Close

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 Gautam Dey

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

Read preprint (No Ratings Yet)




  • Have your say

    Your email address will not be published. Required fields are marked *

    This site uses Akismet to reduce spam. Learn how your comment data is processed.

    Sign up to customise the site to your preferences and to receive alerts

    Register here

    Also in the cell biology category:

    FENS 2020

    A collection of preprints presented during the virtual meeting of the Federation of European Neuroscience Societies (FENS) in 2020

     



    List by Ana Dorrego-Rivas

    Planar Cell Polarity – PCP

    This preList contains preprints about the latest findings on Planar Cell Polarity (PCP) in various model organisms at the molecular, cellular and tissue levels.

     



    List by Ana Dorrego-Rivas

    BioMalPar XVI: Biology and Pathology of the Malaria Parasite

    [under construction] Preprints presented at the (fully virtual) EMBL BioMalPar XVI, 17-18 May 2020 #emblmalaria

     



    List by Gautam Dey, Samantha Seah

    1

    Cell Polarity

    Recent research from the field of cell polarity is summarized in this list of preprints. It comprises of studies focusing on various forms of cell polarity ranging from epithelial polarity, planar cell polarity to front-to-rear polarity.

     



    List by Yamini Ravichandran

    TAGC 2020

    Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20

     



    List by Maiko Kitaoka, Madhuja Samaddar, Miguel V. Almeida, Sejal Davla, Jennifer Ann Black, Gautam Dey

    3D Gastruloids

    A curated list of preprints related to Gastruloids (in vitro models of early development obtained by 3D aggregation of embryonic cells)

     



    List by Paul Gerald L. Sanchez and Stefano Vianello

    ECFG15 – Fungal biology

    Preprints presented at 15th European Conference on Fungal Genetics 17-20 February 2020 Rome

     



    List by Hiral Shah

    ASCB EMBO Annual Meeting 2019

    A collection of preprints presented at the 2019 ASCB EMBO Meeting in Washington, DC (December 7-11)

     



    List by Madhuja Samaddar, Ramona Jühlen, Amanda Haage, Laura McCormick, Maiko Kitaoka

    EMBL Seeing is Believing – Imaging the Molecular Processes of Life

    Preprints discussed at the 2019 edition of Seeing is Believing, at EMBL Heidelberg from the 9th-12th October 2019

     



    List by Gautam Dey

    Autophagy

    Preprints on autophagy and lysosomal degradation and its role in neurodegeneration and disease. Includes molecular mechanisms, upstream signalling and regulation as well as studies on pharmaceutical interventions to upregulate the process.

     



    List by Sandra Malmgren Hill

    Lung Disease and Regeneration

    This preprint list compiles highlights from the field of lung biology.

     



    List by Rob Hynds

    Cellular metabolism

    A curated list of preprints related to cellular metabolism at Biorxiv by Pablo Ranea Robles from the Prelights community. Special interest on lipid metabolism, peroxisomes and mitochondria.

     



    List by Pablo Ranea Robles

    BSCB/BSDB Annual Meeting 2019

    Preprints presented at the BSCB/BSDB Annual Meeting 2019

     



    List by Gautam Dey

    Biophysical Society Annual Meeting 2019

    Few of the preprints that were discussed in the recent BPS annual meeting at Baltimore, USA

     



    List by Joseph Jose Thottacherry

    ASCB/EMBO Annual Meeting 2018

    This list relates to preprints that were discussed at the recent ASCB conference.

     



    List by Gautam Dey, Amanda Haage
    Close