Golgi compartments enable controlled biomolecular assembly using promiscuous enzymes

  1. Anjali Jaiman
  2. Mukund Thattai  Is a corresponding author
  1. National Centre for Biological Sciences, India

Abstract

The synthesis of eukaryotic glycans - branched sugar oligomers attached to cell-surface proteins and lipids - is organised like a factory assembly line. Specific enzymes within successive compartments of the Golgi apparatus determine where new monomer building blocks are linked to the growing oligomer. These enzymes act promiscuously and stochastically, causing microheterogeneity (molecule-to-molecule variability) in the final oligomer products. However, this variability is tightly controlled: a given eukaryotic protein type is typically associated with a narrow, specific glycan oligomer profile. Here we use ideas from the mathematical theory of self-assembly to enumerate the enzymatic causes of oligomer variability, and show how to eliminate each cause. We rigorously demonstrate that cells can specifically synthesize a larger repertoire of glycan oligomers by partitioning promiscuous enzymes across multiple Golgi compartments. This places limits on biomolecular assembly: glycan microheterogeneity becomes unavoidable when the number of compartments is limited, or enzymes are excessively promiscuous.

Data availability

Matlab source code has been provided for generating plots in Figure 2B.

Article and author information

Author details

  1. Anjali Jaiman

    Simons Centre for the Study of Living Machines, National Centre for Biological Sciences, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
  2. Mukund Thattai

    Simons Centre for the Study of Living Machines, National Centre for Biological Sciences, Bangalore, India
    For correspondence
    thattai@ncbs.res.in
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2558-6517

Funding

Simons Foundation (287975)

  • Mukund Thattai

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Patricia Bassereau, Institut Curie, France

Version history

  1. Received: June 21, 2019
  2. Accepted: June 28, 2020
  3. Accepted Manuscript published: June 29, 2020 (version 1)
  4. Version of Record published: July 14, 2020 (version 2)

Copyright

© 2020, Jaiman & Thattai

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Anjali Jaiman
  2. Mukund Thattai
(2020)
Golgi compartments enable controlled biomolecular assembly using promiscuous enzymes
eLife 9:e49573.
https://doi.org/10.7554/eLife.49573

Share this article

https://doi.org/10.7554/eLife.49573

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