Consecutive low-frequency shifts in A/T content denote nucleosome positions across microeukaryotes

Summary: Nucleosomes are the basic repeating unit, each spanning ≈150bp, that structures DNA in the nucleus and their positions have major consequences on gene activity. Here, through analyzing DNA signatures across 1117 microeukaryote genomes, we discovered ≈150bp shifts in A/T content associated w...

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Main Authors: Stephen J. Mondo, Guifen He, Aditi Sharma, Doina Ciobanu, Robert Riley, William B. Andreopoulos, Anna Lipzen, Alan Kuo, Kurt LaButti, Jasmyn Pangilinan, Asaf Salamov, Hugh Salamon, Lili Shu, John Gladden, Jon Magnuson, M. Catherine Aime, Ronan O’Malley, Igor V. Grigoriev
Format: Article
Language:English
Published: Elsevier 2025-05-01
Series:iScience
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Online Access:http://www.sciencedirect.com/science/article/pii/S2589004225007333
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author Stephen J. Mondo
Guifen He
Aditi Sharma
Doina Ciobanu
Robert Riley
William B. Andreopoulos
Anna Lipzen
Alan Kuo
Kurt LaButti
Jasmyn Pangilinan
Asaf Salamov
Hugh Salamon
Lili Shu
John Gladden
Jon Magnuson
M. Catherine Aime
Ronan O’Malley
Igor V. Grigoriev
author_facet Stephen J. Mondo
Guifen He
Aditi Sharma
Doina Ciobanu
Robert Riley
William B. Andreopoulos
Anna Lipzen
Alan Kuo
Kurt LaButti
Jasmyn Pangilinan
Asaf Salamov
Hugh Salamon
Lili Shu
John Gladden
Jon Magnuson
M. Catherine Aime
Ronan O’Malley
Igor V. Grigoriev
author_sort Stephen J. Mondo
collection DOAJ
description Summary: Nucleosomes are the basic repeating unit, each spanning ≈150bp, that structures DNA in the nucleus and their positions have major consequences on gene activity. Here, through analyzing DNA signatures across 1117 microeukaryote genomes, we discovered ≈150bp shifts in A/T content associated with nucleosome organization. Often consecutively arrayed across the genome, A/T peaks were enriched surrounding transcriptional start sites in specific clades. Most nucleosomes (both in vitro and in vivo) across eukaryotes aligned with A/T peaks, even in the presence of DNA modifications. Using artificial intelligence-based approaches, we describe DNA features associated with nucleosomes and construct a deep learning (DL) model for improved nucleosome occupancy prediction. Using this model, we found that ≈70% of “random” transfer DNA inserts from an in vivo fungal RB-TDNAseq library avoided DL predicted nucleosome-bound regions. This study reveals a eukaryote-wide strategy for generating cassettes of nucleosome-favorable DNAs that has a profound impact on nucleosome organization.
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spelling doaj-art-7cfec7be14be47dcace2ca79fa67c69f2025-08-20T02:57:02ZengElsevieriScience2589-00422025-05-0128511247210.1016/j.isci.2025.112472Consecutive low-frequency shifts in A/T content denote nucleosome positions across microeukaryotesStephen J. Mondo0Guifen He1Aditi Sharma2Doina Ciobanu3Robert Riley4William B. Andreopoulos5Anna Lipzen6Alan Kuo7Kurt LaButti8Jasmyn Pangilinan9Asaf Salamov10Hugh Salamon11Lili Shu12John Gladden13Jon Magnuson14M. Catherine Aime15Ronan O’Malley16Igor V. Grigoriev17US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA; Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA; Department of Agricultural Biology, Colorado State University, Fort Collins, CO 80523, USA; Corresponding authorUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USAUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USAUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USAUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USAUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USAUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USAUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USAUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USAUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USAUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USAUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USACollege of Horticulture, Shenyang Agricultural University, Shenyang 110866, P.R. China; Engineering Research Center of Chinese Ministry of Education for Edible and Medicinal Fungi, Jilin Agricultural University, Changchun 130118, P.R. ChinaJoint BioEnergy Institute, Emeryville, CA 94608, USAPacific Northwest National Laboratory, Richland, WA 99352, USADepartment of Botany and Plant Pathology, Purdue University, West Lafayette, IN, USAUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USAUS Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA; Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA; Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, CA 94720, USASummary: Nucleosomes are the basic repeating unit, each spanning ≈150bp, that structures DNA in the nucleus and their positions have major consequences on gene activity. Here, through analyzing DNA signatures across 1117 microeukaryote genomes, we discovered ≈150bp shifts in A/T content associated with nucleosome organization. Often consecutively arrayed across the genome, A/T peaks were enriched surrounding transcriptional start sites in specific clades. Most nucleosomes (both in vitro and in vivo) across eukaryotes aligned with A/T peaks, even in the presence of DNA modifications. Using artificial intelligence-based approaches, we describe DNA features associated with nucleosomes and construct a deep learning (DL) model for improved nucleosome occupancy prediction. Using this model, we found that ≈70% of “random” transfer DNA inserts from an in vivo fungal RB-TDNAseq library avoided DL predicted nucleosome-bound regions. This study reveals a eukaryote-wide strategy for generating cassettes of nucleosome-favorable DNAs that has a profound impact on nucleosome organization.http://www.sciencedirect.com/science/article/pii/S2589004225007333GenomicsChromosome organizationMolecular interactionModel organismArtificial intelligence
spellingShingle Stephen J. Mondo
Guifen He
Aditi Sharma
Doina Ciobanu
Robert Riley
William B. Andreopoulos
Anna Lipzen
Alan Kuo
Kurt LaButti
Jasmyn Pangilinan
Asaf Salamov
Hugh Salamon
Lili Shu
John Gladden
Jon Magnuson
M. Catherine Aime
Ronan O’Malley
Igor V. Grigoriev
Consecutive low-frequency shifts in A/T content denote nucleosome positions across microeukaryotes
iScience
Genomics
Chromosome organization
Molecular interaction
Model organism
Artificial intelligence
title Consecutive low-frequency shifts in A/T content denote nucleosome positions across microeukaryotes
title_full Consecutive low-frequency shifts in A/T content denote nucleosome positions across microeukaryotes
title_fullStr Consecutive low-frequency shifts in A/T content denote nucleosome positions across microeukaryotes
title_full_unstemmed Consecutive low-frequency shifts in A/T content denote nucleosome positions across microeukaryotes
title_short Consecutive low-frequency shifts in A/T content denote nucleosome positions across microeukaryotes
title_sort consecutive low frequency shifts in a t content denote nucleosome positions across microeukaryotes
topic Genomics
Chromosome organization
Molecular interaction
Model organism
Artificial intelligence
url http://www.sciencedirect.com/science/article/pii/S2589004225007333
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