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A proteomic portrait of dinoflagellate chromatin reveals abundant RNA-binding proteins

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Abstract

Dinoflagellate chromatin is unique among eukaryotes, as the chromosomes are permanently condensed in a liquid crystal state instead of being packed in nucleosomes. However, how it is organized is still an unsolved mystery, in part due to the lack of a comprehensive catalog of dinoflagellate nuclear proteins. Here, we report the results of CHromatin Enrichment for Proteomics (CHEP) followed by shotgun mass spectrometry sequencing of the chromatin-associated proteins from the dinoflagellate Lingulodinum polyedra. Our analysis identified proteins involved in DNA replication and repair, transcription, and mRNA splicing, and showed a low level of contamination by proteins from other organelles. A limited number of proteins containing DNA-binding domains were found, consistent with the lack of diversity of these proteins in dinoflagellate transcriptomes. However, the number of proteins containing RNA-binding domains was unexpectedly high supporting a potential role for this type of protein in mediating gene expression and chromatin organization. We also identified a number of proteins involved in chromosome condensation and cell cycle progression as well as a single histone protein (H4). Our results provide the first detailed look at the nuclear proteins associated with the unusual chromatin structure of dinoflagellate nuclei and provide important insights into the biochemical basis of its structure and function.

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Acknowledgements

Proteomics analyses were performed by the Center for Advanced Proteomics Analyses, a Node of the Canadian Genomic Innovation Network that is supported by the Canadian Government through Genome Canada. Computer-intensive analyses were made on the supercomputer Guillimin at McGill University, managed by Calcul Québec and Compute Canada. The operation of this supercomputer is funded by the Canada Foundation for Innovation (CFI), the ministère de l’Économie, de la science et de l’innovation du Québec (MESI), and the Fonds de recherche du Québec - Nature et technologies (FRQNT). We are grateful to Dr. F. van Dolah for the anti-PCNA antibody. We thank Drs. Annie Angers, James Omichinski, and William Zerges for their extensive review of this manuscript.

Funding

This study was funded by the National Science and Engineering Research Council of Canada (NSERC) through an Alexander-Graham-Bell Canada Doctoral Scholarship awarded to M. B. and an NSERC Discovery research grant awarded to D. M. (number 171382-03).

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  1. Institut de Recherche en Biologie Végétale, Département de Sciences Biologiques, Université de Montréal, Montréal, Québec, H1X 2B2, Canada

    Mathieu Beauchemin & David Morse

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  1. Mathieu Beauchemin
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  2. David Morse
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Correspondence to David Morse.

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Electronic Supplementary materials

ESM 1

Supplementary Table 1: Number of peptides and proteins identified in nine chromatin-enriched samples (PDF 11.4 kb)

ESM 2

Supplementary Table 2: List of 1245 proteins identified in the chromatin enriched sample with BLAST description, GO terms and manually classified functional characterization (PDF 372 kb)

ESM 3

Supplementary Table 3: Gene ontology terms significantly enriched and depleted in the chromatin enriched samples (PDF 26 kb)

ESM 4

Supplementary Table 4: Proteins involved in DNA repair and processing (PDF 13 kb)

ESM 5

Supplementary Table 5: Differentially expressed proteins between LD6 and LD18 (PDF 31 kb)

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Beauchemin, M., Morse, D. A proteomic portrait of dinoflagellate chromatin reveals abundant RNA-binding proteins. Chromosoma 127, 29–43 (2018). https://doi.org/10.1007/s00412-017-0643-8

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