Loss of centromere function drives karyotype evolution in closely related Malassezia species
- Jawaharlal Nehru Centre for Advanced Scientific Research, India
- Duke University Medical Center, United States
- The Institute of Mathematical Sciences (HBNI), India
- Uppsala University, Sweden
- Agency for Science, Technology and Research, Singapore
Abstract
Genomic rearrangements associated with speciation often result in chromosome number variation among closely related species. Malassezia species show variable karyotypes ranging between 6 and 9 chromosomes. Here, we experimentally identified all 8 centromeres in M. sympodialis as 3 to 5 kb long kinetochore-bound regions spanning an AT-rich core and depleted of the canonical histone H3. Centromeres of similar sequence features were identified as CENP-A-rich regions in Malassezia furfur with 7 chromosomes, and histone H3 depleted regions in Malassezia slooffiae and Malassezia globosa with 9 chromosomes each. Analysis of synteny conservation across centromeres with newly generated chromosome-level genome assemblies suggests two distinct mechanisms of chromosome number reduction from an inferred 9-chromosome ancestral state: (a) chromosome breakage followed by loss of centromere DNA and (b) centromere inactivation accompanied by changes in DNA sequence following chromosome-chromosome fusion. We propose AT-rich centromeres drive karyotype diversity in the Malassezia species complex through breakage and inactivation.
Data availability
The Mtw1 ChIP sequencing reads reported in this paper have been deposited under NCBI BioProject (Accession number PRJNA509412). The genome sequence assemblies of M. globosa, M. slooffiae, and M. furfur have been deposited in GenBank with accession numbers SAMN10720087, SAMN10720088, and SAMN13341476 respectively.
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Genome assembly of Malassezia slooffiaeGenBank, SAMN10720088.
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Genome assembly of Malassezia globosaGenBank, SAMN10720087.
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Genome assembly of Malassezia furfurGenBank, SAMN13341476.
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Malassezia restricta CBS 7877 genome, complete sequenceNCBI BioSample, SAMN09377640.
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Genome sequencing of Malassezia nana JCM 12085NCBI BioProject, PRJDB3735.
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Genome sequencing of Malassezia dermatis JCM 11348NCBI BioProject, PRJDB3732.
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Genome sequencing of Malassezia japonica JCM 11963NCBI BioProject, PRJDB3733.
Article and author information
Author details
Funding
Tata Innovation Fellowship (BT/HRT/35/01/03/2017)
- Kaustuv Sanyal
Department of Biotechnology , Ministry of Science and Technology (BT/INF/22/SP27679/2018)
- Kaustuv Sanyal
National Institutes of Health (R37 award-AI39115-21; R01 award-AI50113-15)
- Joseph Heitman
Agency for Science, Technology and Research (H18/01a0/016)
- Thomas L Dawson
Jawaharlal Nehru Centre for Advanced Scientific Research (Graduate student fellowship)
- Sundar Ram Sankaranarayanan
Science and Engineering Research Board (PDF/2016/002858)
- Md Hashim Reza
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Wolf-Dietrich Heyer, University of California, Davis, United States
Publication history
- Received: November 26, 2019
- Accepted: January 20, 2020
- Accepted Manuscript published: January 20, 2020 (version 1)
- Version of Record published: February 17, 2020 (version 2)
Copyright
© 2020, Sankaranarayanan 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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Loss of centromere function drives karyotype evolution in closely related Malassezia species
eLife 9:e53944.
https://doi.org/10.7554/eLife.53944
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Funding This work is supported by the National Research Foundation Singapore (NRF-NRFF2017-02), PRECISION Health Research, Singapore (PRECISE) and the Agency for Science, Technology and Research (A*STAR). WP Koh was supported by National Medical Research Council, Singapore (NMRC/CSA/0055/2013). CC Khor was supported by National Research Foundation Singapore (NRF-NRFI2018-01). Rajkumar Dorajoo received a grant from the Agency for Science, Technology and Research Career Development Award (A*STAR CDA - 202D8090), and from Ministry of Health Healthy Longevity Catalyst Award (HLCA20Jan-0022). The Singapore Chinese Health Study was supported by grants from the National Medical Research Council, Singapore (NMRC/CIRG/1456/2016) and the U.S. National Institutes of Health [NIH] (R01 CA144034 and UM1 CA182876).
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