Delineating the rules for structural adaptation of membrane-associated proteins to evolutionary changes in membrane lipidome
Preprint posted on 9 September 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
Categories: biochemistry, cell biology, evolutionary biology
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.
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
- Sharpe, H. J., Stevens, T. J. & Munro, S. A comprehensive comparison of transmembrane domains reveals organelle-specific properties. Cell 142, 158–69 (2010).
- 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).
- Baum, D. A. A comparison of autogenous theories for the origin of eukaryotic cells. Am. J. Bot. 102, 1954–65 (2015).
- Koga, Y. Early Evolution of Membrane Lipids: How did the Lipid Divide Occur? J. Mol. Evol. 72, 274–282 (2011).
- Gu, Y. & Oliferenko, S. Cellular geometry scaling ensures robust division site positioning. Nat. Commun. 10, 268 (2019).
- Gu, Y., Yam, C. & Oliferenko, S. Rewiring of cellular division site selection in evolution of fission yeasts. Curr. Biol. 25, 1187–94 (2015).
- 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).
- Gu, Y., Yam, C. & Oliferenko, S. Divergence of mitotic strategies in fission yeasts. Nucleus-Austin 3, 220–225 (2012).
Posted on: 17 September 2019 , updated on: 18 September 2019
doi: https://doi.org/10.1242/prelights.13890
Read preprint
(No Ratings Yet)Sign up to customise the site to your preferences and to receive alerts
Register hereAlso in the biochemistry category:
Vesicles driven by dynein and kinesin exhibit directional reversals without external regulators
Genetically encoded multimeric tags for intracellular protein localisation in cryo-EM
Curvature Sensing and Membrane Remodeling of the VPS37A N-terminal Domain during Autophagy
Also in the cell biology category:
Vesicles driven by dynein and kinesin exhibit directional reversals without external regulators
Genetically encoded multimeric tags for intracellular protein localisation in cryo-EM
An improved Erk biosensor reveals oscillatory Erk dynamics driven by mitotic erasure during early development
Also in the evolutionary biology category:
The developmental basis for scaling of mammalian tooth size
Epistasis between promoter activity and coding mutations shapes gene evolvability
The ELT-3 GATA factor specifies endoderm in Caenorhabditis angaria in an ancestral gene network
preLists in the biochemistry category:
CellBio 2022 – An ASCB/EMBO Meeting
This preLists features preprints that were discussed and presented during the CellBio 2022 meeting in Washington, DC in December 2022.
| List by | Nadja Hümpfer et al. |
20th “Genetics Workshops in Hungary”, Szeged (25th, September)
In this annual conference, Hungarian geneticists, biochemists and biotechnologists presented their works. Link: http://group.szbk.u-szeged.hu/minikonf/archive/prg2021.pdf
| List by | Nándor Lipták |
Fibroblasts
The advances in fibroblast biology preList explores the recent discoveries and preprints of the fibroblast world. Get ready to immerse yourself with this list created for fibroblasts aficionados and lovers, and beyond. Here, my goal is to include preprints of fibroblast biology, heterogeneity, fate, extracellular matrix, behavior, topography, single-cell atlases, spatial transcriptomics, and their matrix!
| List by | Osvaldo Contreras |
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 et al. |
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 | Dey Lab |
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 |
MitoList
This list of preprints is focused on work expanding our knowledge on mitochondria in any organism, tissue or cell type, from the normal biology to the pathology.
| List by | Sandra Franco Iborra |
Also in the cell biology category:
CellBio 2022 – An ASCB/EMBO Meeting
This preLists features preprints that were discussed and presented during the CellBio 2022 meeting in Washington, DC in December 2022.
| List by | Nadja Hümpfer et al. |
Fibroblasts
The advances in fibroblast biology preList explores the recent discoveries and preprints of the fibroblast world. Get ready to immerse yourself with this list created for fibroblasts aficionados and lovers, and beyond. Here, my goal is to include preprints of fibroblast biology, heterogeneity, fate, extracellular matrix, behavior, topography, single-cell atlases, spatial transcriptomics, and their matrix!
| List by | Osvaldo Contreras |
EMBL Synthetic Morphogenesis: From Gene Circuits to Tissue Architecture (2021)
A list of preprints mentioned at the #EESmorphoG virtual meeting in 2021.
| List by | Alex Eve |
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 | Dey Lab, 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 et al. |
3D Gastruloids
A curated list of preprints related to Gastruloids (in vitro models of early development obtained by 3D aggregation of embryonic cells). Updated until July 2021.
| 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 et al. |
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 | Dey Lab |
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 | Dey Lab |
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 | Dey Lab, Amanda Haage |
Also in the evolutionary biology category:
EMBL Synthetic Morphogenesis: From Gene Circuits to Tissue Architecture (2021)
A list of preprints mentioned at the #EESmorphoG virtual meeting in 2021.
| List by | Alex Eve |
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 |
TAGC 2020
Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20
| List by | Maiko Kitaoka et al. |
ECFG15 – Fungal biology
Preprints presented at 15th European Conference on Fungal Genetics 17-20 February 2020 Rome
| List by | Hiral Shah |
COVID-19 / SARS-CoV-2 preprints
List of important preprints dealing with the ongoing coronavirus outbreak. See http://covidpreprints.com for additional resources and timeline, and https://connect.biorxiv.org/relate/content/181 for full list of bioRxiv and medRxiv preprints on this topic
| List by | Dey Lab, Zhang-He Goh |
1
SDB 78th Annual Meeting 2019
A curation of the preprints presented at the SDB meeting in Boston, July 26-30 2019. The preList will be updated throughout the duration of the meeting.
| List by | Alex Eve |
Pattern formation during development
The aim of this preList is to integrate results about the mechanisms that govern patterning during development, from genes implicated in the processes to theoritical models of pattern formation in nature.
| List by | Alexa Sadier |