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High-Resolution 3D Genome Map of Brucella Chromosomes in Exponential and Stationary Phases

The three-dimensional (3D) genome structure of an organism or cell is highly relevant to its biological activities, but the availability of 3D genome information for bacteria, especially intracellular pathogens, is still limited. Here, we used Hi-C (high-throughput chromosome conformation capture) t...

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Autores principales: Huang, Yong-Fang, Liu, Lin, Wang, Fei, Yuan, Xin-Wei, Chen, Huan-Chun, Liu, Zheng-Fei
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10100373/
https://www.ncbi.nlm.nih.gov/pubmed/36847551
http://dx.doi.org/10.1128/spectrum.04290-22
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author Huang, Yong-Fang
Liu, Lin
Wang, Fei
Yuan, Xin-Wei
Chen, Huan-Chun
Liu, Zheng-Fei
author_facet Huang, Yong-Fang
Liu, Lin
Wang, Fei
Yuan, Xin-Wei
Chen, Huan-Chun
Liu, Zheng-Fei
author_sort Huang, Yong-Fang
collection PubMed
description The three-dimensional (3D) genome structure of an organism or cell is highly relevant to its biological activities, but the availability of 3D genome information for bacteria, especially intracellular pathogens, is still limited. Here, we used Hi-C (high-throughput chromosome conformation capture) technology to determine the 3D chromosome structures of exponential- and stationary-phase Brucella melitensis at a 1-kb resolution. We observed that the contact heat maps of the two B. melitensis chromosomes contain a prominent diagonal and a secondary diagonal. Then, 79 chromatin interaction domains (CIDs) were detected at an optical density at 600 nm (OD(600)) of 0.4 (exponential phase), with the longest CID being 106 kb and the shortest being 12 kb. Moreover, we obtained 49,363 significant cis-interaction loci and 59,953 significant trans-interaction loci. Meanwhile, 82 CIDs of B. melitensis at an OD(600) of 1.5 (stationary phase) were detected, with the longest CID being 94 kb and the shortest being 16 kb. In addition, 25,965 significant cis-interaction loci and 35,938 significant trans-interaction loci were obtained in this phase. Furthermore, we found that as the B. melitensis cells grew from the logarithmic to the plateau phase, the frequency of short-range interactions increased, while that of long-range interactions decreased. Finally, combined analysis of 3D genome and whole-genome transcriptome (RNA-seq) data revealed that the strength of short-range interactions in Chr1 is specifically and strongly correlated with gene expression. Overall, our study provides a global view of the chromatin interactions in the B. melitensis chromosomes, which will serve as a resource for further study of the spatial regulation of gene expression in Brucella. IMPORTANCE The spatial structure of chromatin plays important roles in normal cell functions and in the regulation of gene expression. Three-dimensional genome sequencing has been performed in many mammals and plants, but the availability of such data for bacteria, especially intracellular pathogens, is still limited. Approximately 10% of sequenced bacterial genomes contain more than one replicon. However, how multiple replicons are organized within bacterial cells, how they interact, and whether these interactions help to maintain or segregate these multipartite genomes are unresolved issues. Brucella is a Gram-negative, facultative intracellular, and zoonotic bacterium. Except for Brucella suis biovar 3, Brucella species have two chromosomes. Here, we applied Hi-C technology to determine the 3D genome structures of exponential- and stationary-phase Brucella melitensis chromosomes at a 1-kb resolution. Combined analysis of the 3D genome and RNA-seq data indicated that the strength of short-range interactions in B. melitensis Chr1 is specifically and strongly correlated with gene expression. Our study provides a resource to achieve a deeper understanding of the spatial regulation of gene expression in Brucella.
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spelling pubmed-101003732023-04-14 High-Resolution 3D Genome Map of Brucella Chromosomes in Exponential and Stationary Phases Huang, Yong-Fang Liu, Lin Wang, Fei Yuan, Xin-Wei Chen, Huan-Chun Liu, Zheng-Fei Microbiol Spectr Research Article The three-dimensional (3D) genome structure of an organism or cell is highly relevant to its biological activities, but the availability of 3D genome information for bacteria, especially intracellular pathogens, is still limited. Here, we used Hi-C (high-throughput chromosome conformation capture) technology to determine the 3D chromosome structures of exponential- and stationary-phase Brucella melitensis at a 1-kb resolution. We observed that the contact heat maps of the two B. melitensis chromosomes contain a prominent diagonal and a secondary diagonal. Then, 79 chromatin interaction domains (CIDs) were detected at an optical density at 600 nm (OD(600)) of 0.4 (exponential phase), with the longest CID being 106 kb and the shortest being 12 kb. Moreover, we obtained 49,363 significant cis-interaction loci and 59,953 significant trans-interaction loci. Meanwhile, 82 CIDs of B. melitensis at an OD(600) of 1.5 (stationary phase) were detected, with the longest CID being 94 kb and the shortest being 16 kb. In addition, 25,965 significant cis-interaction loci and 35,938 significant trans-interaction loci were obtained in this phase. Furthermore, we found that as the B. melitensis cells grew from the logarithmic to the plateau phase, the frequency of short-range interactions increased, while that of long-range interactions decreased. Finally, combined analysis of 3D genome and whole-genome transcriptome (RNA-seq) data revealed that the strength of short-range interactions in Chr1 is specifically and strongly correlated with gene expression. Overall, our study provides a global view of the chromatin interactions in the B. melitensis chromosomes, which will serve as a resource for further study of the spatial regulation of gene expression in Brucella. IMPORTANCE The spatial structure of chromatin plays important roles in normal cell functions and in the regulation of gene expression. Three-dimensional genome sequencing has been performed in many mammals and plants, but the availability of such data for bacteria, especially intracellular pathogens, is still limited. Approximately 10% of sequenced bacterial genomes contain more than one replicon. However, how multiple replicons are organized within bacterial cells, how they interact, and whether these interactions help to maintain or segregate these multipartite genomes are unresolved issues. Brucella is a Gram-negative, facultative intracellular, and zoonotic bacterium. Except for Brucella suis biovar 3, Brucella species have two chromosomes. Here, we applied Hi-C technology to determine the 3D genome structures of exponential- and stationary-phase Brucella melitensis chromosomes at a 1-kb resolution. Combined analysis of the 3D genome and RNA-seq data indicated that the strength of short-range interactions in B. melitensis Chr1 is specifically and strongly correlated with gene expression. Our study provides a resource to achieve a deeper understanding of the spatial regulation of gene expression in Brucella. American Society for Microbiology 2023-02-27 /pmc/articles/PMC10100373/ /pubmed/36847551 http://dx.doi.org/10.1128/spectrum.04290-22 Text en Copyright © 2023 Huang et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Huang, Yong-Fang
Liu, Lin
Wang, Fei
Yuan, Xin-Wei
Chen, Huan-Chun
Liu, Zheng-Fei
High-Resolution 3D Genome Map of Brucella Chromosomes in Exponential and Stationary Phases
title High-Resolution 3D Genome Map of Brucella Chromosomes in Exponential and Stationary Phases
title_full High-Resolution 3D Genome Map of Brucella Chromosomes in Exponential and Stationary Phases
title_fullStr High-Resolution 3D Genome Map of Brucella Chromosomes in Exponential and Stationary Phases
title_full_unstemmed High-Resolution 3D Genome Map of Brucella Chromosomes in Exponential and Stationary Phases
title_short High-Resolution 3D Genome Map of Brucella Chromosomes in Exponential and Stationary Phases
title_sort high-resolution 3d genome map of brucella chromosomes in exponential and stationary phases
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10100373/
https://www.ncbi.nlm.nih.gov/pubmed/36847551
http://dx.doi.org/10.1128/spectrum.04290-22
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