Loss of centromere function drives karyotype evolution in closely related Malassezia species

Abstract
Data availability
Article and author information
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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.

The following data sets were generated

1. Sankaranarayanan SR
2. Ianiri G
3. Coelho MA
4. Reza MH
5. Thimmappa BC
6. Ganguly P
7. Vadnala RN
8. Sun S
9. Siddharthan R
10. Tellgren-Roth C
11. Dawson Jr TL
12. Heitman J
13. Sanyal K
(2019) Genome assembly of Malassezia slooffiae
GenBank, SAMN10720088.

https://www.ncbi.nlm.nih.gov/biosample/10720088
1. Sankaranarayanan SR
2. Ianiri G
3. Coelho MA
4. Reza MH
5. Thimmappa BC
6. Ganguly P
7. Vadnala RN
8. Sun S
9. Siddharthan R
10. Tellgren-Roth C
11. Dawson Jr TL
12. Heitman J
13. Sanyal K
(2019) Genome assembly of Malassezia globosa
GenBank, SAMN10720087.

https://www.ncbi.nlm.nih.gov/biosample/10720087
1. Sankaranarayanan SR
2. Ianiri G
3. Coelho MA
4. Reza MH
5. Thimmappa BC
6. Ganguly P
7. Vadnala RN
8. Sun S
9. Siddharthan R
10. Tellgren-Roth C
11. Dawson Jr TL
12. Heitman J
13. Sanyal K
(2019) Genome assembly of Malassezia furfur
GenBank, SAMN13341476.

https://www.ncbi.nlm.nih.gov/biosample/13341476
1. Sankaranarayanan SR
2. Ianiri G
3. Coelho MA
4. Reza MH
5. Thimmappa BC
6. Ganguly P
7. Vadnala RN
8. Sun S
9. Siddharthan R
10. Tellgren-Roth C
11. Dawson Jr TL
12. Heitman J
13. Sanyal K
(2019) Identification of centromeres in Malassezia sympodialis
BioProject, PRJNA509412.

https://www.ncbi.nlm.nih.gov/nuccore/?term=PRJNA509412

The following previously published data sets were used

1. L'Oreal
2. Stanislas Morand
(2018) Malassezia restricta CBS 7877 genome, complete sequence
NCBI BioSample, SAMN09377640.

https://www.ncbi.nlm.nih.gov/genome/702?genome_assembly_id=413940
1. Zhu Y
2. Engström PG
3. Tellgren-Roth C
4. Baudo CD
5. Kennell JC
6. Sun S
7. Billmyre RB
8. Schröder MS
9. Andersson A
10. Holm T
11. Sigurgeirsson B
12. Wu G9
13. Sankaranarayanan SR
14. Siddharthan R
15. Sanyal K
16. Lundeberg J
17. Nystedt B
18. Boekhout T
19. Dawson TL Jr
20. Heitman J
21. Scheynius A
22. Lehtiö J
(2017) Genome sequencing and integrative gene annotation of Malassezia sympodialis
NCBI BioProjects ,PRJEB13283.

https://www.ncbi.nlm.nih.gov/bioproject/PRJEB13283
1. RIKEN Center for Life Science Technologies
2. Division of Genomic Technologies
(2016) Genome sequencing of Malassezia nana JCM 12085
NCBI BioProject, PRJDB3735.

https://www.ncbi.nlm.nih.gov/bioproject/313886
1. RIKEN Center for Life Science Technologies
2. Division of Genomic Technologies
(2016) Genome sequencing of Malassezia dermatis JCM 11348
NCBI BioProject, PRJDB3732.

https://www.ncbi.nlm.nih.gov/bioproject/PRJDB3732
1. RIKEN Center for Life Science Technologies
2. Division of Genomic Technologies
(2016) Genome sequencing of Malassezia japonica JCM 11963
NCBI BioProject, PRJDB3733.

https://www.ncbi.nlm.nih.gov/bioproject/PRJDB3733
1. JM Lorch
2. JM Palmer
3. KJ Vanderwolf
4. KZ Schmidt
5. ML Verant
6. TJ Weller
7. DS Blehert
(2017) Malassezia vespertilionis strain:NWHC:44797-103 Genome sequencing and assembly
NCBI BioProject, PRJNA393681.

https://www.ncbi.nlm.nih.gov/bioproject/PRJNA393681

Article and author information

Author details

Sundar Ram Sankaranarayanan

Molecular Biology and Genetics Unit, Jawaharlal Nehru Centre for Advanced Scientific Research, Bangalore, India

Competing interests
The authors declare that no competing interests exist.
Giuseppe Ianiri

Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-3278-8678
Marco A Coelho

Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, United States

Competing interests
The authors declare that no competing interests exist.
Md Hashim Reza

Molecular Biology and Genetics Unit, Jawaharlal Nehru Centre for Advanced Scientific Research, Bangalore, India

Competing interests
The authors declare that no competing interests exist.
Bhagya C Thimmappa

Molecular Biology and Genetics Unit, Jawaharlal Nehru Centre for Advanced Scientific Research, Bangalore, India

Competing interests
The authors declare that no competing interests exist.
Promit Ganguly

Molecular Biology and Genetics Unit, Jawaharlal Nehru Centre for Advanced Scientific Research, Bangalore, India

Competing interests
The authors declare that no competing interests exist.
Rakesh Netha Vadnala

The Institute of Mathematical Sciences (HBNI), Chennai, India

Competing interests
The authors declare that no competing interests exist.
Sheng Sun

Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, United States

Competing interests
The authors declare that no competing interests exist.
Rahul Siddharthan

The Institute of Mathematical Sciences (HBNI), Chennai, India

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-2233-0954
Christian Tellgren-Roth

Department of Immunology, Genetics and Pathology, Uppsala University, Uppsala, Sweden

Competing interests
The authors declare that no competing interests exist.
Thomas L Dawson

Skin Research Institute Singapore, Agency for Science, Technology and Research, Singapore, Singapore

Competing interests
The authors declare that no competing interests exist.
Joseph Heitman

Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, United States

For correspondence
heitm001@duke.edu

Competing interests
The authors declare that no competing interests exist.
Kaustuv Sanyal

Molecular Biology and Genetics Unit, 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.

"This ORCID iD identifies the author of this article:" 0000-0002-6611-4073

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.

Copyright

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.