Altered N-glycan composition impacts flagella mediated adhesion in Chlamydomonas reinhardtii

  1. Nannan Xu
  2. Anne Oltmanns
  3. Longsheng Zhao
  4. Antoine Girot
  5. Marzieh Karimi
  6. Lara Hoepfner
  7. Simon Kelterborn
  8. Martin Scholz
  9. Julia Beißel
  10. Peter Hegemann
  11. Oliver Bäumchen
  12. Lu-Ning Liu
  13. Kaiyao Huang  Is a corresponding author
  14. Michael Hippler  Is a corresponding author
  1. Institute of Hydrobiology, Chinese Academy of Sciences, China
  2. University of Münster, Germany
  3. University of Liverpool, United Kingdom
  4. Max Planck Institute for Dynamics and Self-Organization, Germany
  5. Humboldt University of Berlin, Germany
  6. Max Planck Institute for Dynamics and Self Organization, Germany

Abstract

For the unicellular alga Chlamydomonas reinhardtii, the presence of N-glycosylated proteins on the surface of two flagella is crucial for both cell-cell interaction during mating and flagellar surface adhesion. However, it is not known whether only the presence or also the composition of N-glycans attached to respective proteins is important for these processes. To this end, we tested several C. reinhardtii insertional mutants and a CRISPR/Cas9 knockout mutant of xylosyltransferase 1A, all possessing altered N-glycan compositions. Taking advantage of atomic force microscopy and micropipette force measurements, our data revealed that reduction in N-glycan complexity impedes the adhesion force required for binding the flagella to surfaces. This results in impaired polystyrene bead binding and transport but not gliding of cells on solid surfaces. Notably, assembly, intraflagellar transport and protein import into flagella are not affected by altered N-glycosylation. Thus, we conclude that proper N-glycosylation of flagellar proteins is crucial for adhering C. reinhardtii cells onto surfaces, indicating that N-glycans mediate surface adhesion via direct surface contact.

Data availability

The mass spectrometry proteomics data (Figure 1) have been deposited to the ProteomeXchange Consortium (http://proteomecentral.proteomexchange.org) via the PRIDE partner repository with the dataset identifier PXD018353.

The following data sets were generated

Article and author information

Author details

  1. Nannan Xu

    Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Anne Oltmanns

    Institute for Plant Biology and Biotechnology, University of Münster, Münster, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Longsheng Zhao

    Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Antoine Girot

    Max Planck Institute for Dynamics and Self-Organization, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Marzieh Karimi

    Max Planck Institute for Dynamics and Self-Organization, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Lara Hoepfner

    Institute for Plant Biology and Biotechnology, University of Münster, Münster, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8222-4563
  7. Simon Kelterborn

    Institute of Biology, Humboldt University of Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Martin Scholz

    Biology, University of Münster, Münster, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Julia Beißel

    Biology, University of Münster, Münster, Germany
    Competing interests
    The authors declare that no competing interests exist.
  10. Peter Hegemann

    Institute of Biology, Experimental Biophysics, Humboldt University of Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3589-6452
  11. Oliver Bäumchen

    Max Planck Institute for Dynamics and Self Organization, Goettingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4879-0369
  12. Lu-Ning Liu

    Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8884-4819
  13. Kaiyao Huang

    Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, China
    For correspondence
    huangky@ihb.ac.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8669-1065
  14. Michael Hippler

    Institute for Plant Biology and Biotechnology, University of Münster, Münster, Germany
    For correspondence
    mhippler@uni-muenster.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9670-6101

Funding

Deutsche Forschungsgemeinschaft (Hi 737 / 12-1)

  • Michael Hippler

National Natural Science Foundation of China (Grant 31671399)

  • Kaiyao Huang

Royal Society (UF120411,URF\R\180030,RGF\EA\181061 and RGF\EA\180233)

  • Lu-Ning Liu

Biotechnology and Biological Sciences Research Council (BB/R003890/1,BB/M012441/1)

  • Lu-Ning Liu

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

Reviewing Editor

  1. Ahmet Yildiz, University of California, Berkeley, United States

Publication history

  1. Received: May 11, 2020
  2. Accepted: December 9, 2020
  3. Accepted Manuscript published: December 10, 2020 (version 1)
  4. Version of Record published: December 24, 2020 (version 2)

Copyright

© 2020, Xu et al.

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. Nannan Xu
  2. Anne Oltmanns
  3. Longsheng Zhao
  4. Antoine Girot
  5. Marzieh Karimi
  6. Lara Hoepfner
  7. Simon Kelterborn
  8. Martin Scholz
  9. Julia Beißel
  10. Peter Hegemann
  11. Oliver Bäumchen
  12. Lu-Ning Liu
  13. Kaiyao Huang
  14. Michael Hippler
(2020)
Altered N-glycan composition impacts flagella mediated adhesion in Chlamydomonas reinhardtii
eLife 9:e58805.
https://doi.org/10.7554/eLife.58805
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