Spatial inter-centromeric interactions facilitated the emergence of evolutionary new centromeres

  1. Krishnendu Guin
  2. Yao Chen
  3. Radha Mishra
  4. Siti Rawaidah B M Muzaki
  5. Bhagya C Thimmappa
  6. Caoimhe E O'Brien
  7. Geraldine Butler
  8. Amartya Sanyal  Is a corresponding author
  9. Kaustuv Sanyal  Is a corresponding author
  1. Jawaharlal Nehru Centre for Advanced Scientific Research, India
  2. Nanyang Technological University, Singapore
  3. University College Dublin, Ireland
  4. Conway Institute, University College Dublin, Ireland

Abstract

Centromeres of Candida albicans form on unique and different DNA sequences but a closely related species, Candida tropicalis, possesses homogenized inverted repeat (HIR)-associated centromeres. To investigate the mechanism of centromere type transition, we improved the fragmented genome assembly and constructed a chromosome-level genome assembly of C. tropicalis by employing PacBio sequencing, chromosome conformation capture sequencing (3C-seq), chromoblot, and genetic analysis of engineered aneuploid strains. Further, we analyzed the 3D genome organization using 3C-seq data, which revealed spatial proximity among the centromeres as well as telomeres of seven chromosomes in C. tropicalis. Intriguingly, we observed evidence of inter-centromeric translocations in the common ancestor of C. albicans and C. tropicalis. Identification of putative centromeres in closely related Candida sojae, Candida viswanathii and Candida parapsilosis indicates loss of ancestral HIR-associated centromeres and establishment of evolutionary new centromeres (ENCs) in C. albicans. We propose that spatial proximity of the homologous centromere DNA sequences facilitated karyotype rearrangements and centromere type transitions in human pathogenic yeasts of the CUG-Ser1 clade.

Data availability

All sequencing data reported in the study and the genome assembly of C. tropicalis and C. sojae have been submitted to NCBI under the BioProject accession numbers PRJNA596050 and PRJNA604451

The following data sets were generated

Article and author information

Author details

  1. Krishnendu Guin

    Jawaharlal Nehru Centre for Advanced Scientific Research, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6957-465X
  2. Yao Chen

    Nanyang Technological University, Singapore, Singapore
    Competing interests
    The authors declare that no competing interests exist.
  3. Radha Mishra

    Jawaharlal Nehru Centre for Advanced Scientific Research, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
  4. Siti Rawaidah B M Muzaki

    Nanyang Technological University, Singapore, Singapore
    Competing interests
    The authors declare that no competing interests exist.
  5. Bhagya C Thimmappa

    Jawaharlal Nehru Centre for Advanced Scientific Research, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
  6. Caoimhe E O'Brien

    University College Dublin, Dublin, Ireland
    Competing interests
    The authors declare that no competing interests exist.
  7. Geraldine Butler

    Conway Institute, University College Dublin, Dublin, Ireland
    Competing interests
    The authors declare that no competing interests exist.
  8. Amartya Sanyal

    Nanyang Technological University, Singapore, Singapore
    For correspondence
    asanyal@ntu.edu.sg
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2109-4478
  9. Kaustuv Sanyal

    Jawaharlal Nehru Centre for Advanced Scientific Research, Bangalore, India
    For correspondence
    sanyal@jncasr.ac.in
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6611-4073

Funding

Council of Scientific and Industrial Research (Shyama Prasad Mukherjee Fellowship 07/733(0181)/2013-EMR-I)

  • Krishnendu Guin

Department of Biotechnology , Ministry of Science and Technology (BT/PR27490/Med/29/1323/2018)

  • Kaustuv Sanyal

Ministry of Education - Singapore (RG39/18)

  • Amartya Sanyal

Department of Biotechnology , Ministry of Science and Technology

  • Kaustuv Sanyal

Nanyang Technological University (Nanyang Assistant Professorship grant)

  • Amartya Sanyal

Department of Biotechnology , Ministry of Science and Technology

  • Kaustuv Sanyal

Department of Biotechnology , Ministry of Science and Technology

  • Kaustuv Sanyal

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

Reviewing Editor

  1. Job Dekker, University of Massachusetts Medical School, United States

Publication history

  1. Received: May 4, 2020
  2. Accepted: May 22, 2020
  3. Accepted Manuscript published: May 29, 2020 (version 1)
  4. Version of Record published: June 12, 2020 (version 2)
  5. Version of Record updated: June 30, 2020 (version 3)

Copyright

© 2020, Guin 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. Krishnendu Guin
  2. Yao Chen
  3. Radha Mishra
  4. Siti Rawaidah B M Muzaki
  5. Bhagya C Thimmappa
  6. Caoimhe E O'Brien
  7. Geraldine Butler
  8. Amartya Sanyal
  9. Kaustuv Sanyal
(2020)
Spatial inter-centromeric interactions facilitated the emergence of evolutionary new centromeres
eLife 9:e58556.
https://doi.org/10.7554/eLife.58556

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