Flexibility and Symmetry of Prokaryotic Genome Rearrangement Reveal Lineage-Associated Core-Gene-Defined Genome Organizational Frameworks

ABSTRACT The prokaryotic pangenome partitions genes into core and dispensable genes. The order of core genes, albeit assumed to be stable under selection in general, is frequently interrupted by horizontal gene transfer and rearrangement, but how a core-gene-defined genome maintains its stability or...

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Autores principales:	Yu Kang, Chaohao Gu, Lina Yuan, Yue Wang, Yanmin Zhu, Xinna Li, Qibin Luo, Jingfa Xiao, Daquan Jiang, Minping Qian, Aftab Ahmed Khan, Fei Chen, Zhang Zhang, Jun Yu
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2014
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/38c289b495334aff9d85e12e1a3d5f1f
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spelling	oai:doaj.org-article:38c289b495334aff9d85e12e1a3d5f1f2021-11-15T15:47:04ZFlexibility and Symmetry of Prokaryotic Genome Rearrangement Reveal Lineage-Associated Core-Gene-Defined Genome Organizational Frameworks10.1128/mBio.01867-142150-7511https://doaj.org/article/38c289b495334aff9d85e12e1a3d5f1f2014-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01867-14https://doaj.org/toc/2150-7511ABSTRACT The prokaryotic pangenome partitions genes into core and dispensable genes. The order of core genes, albeit assumed to be stable under selection in general, is frequently interrupted by horizontal gene transfer and rearrangement, but how a core-gene-defined genome maintains its stability or flexibility remains to be investigated. Based on data from 30 species, including 425 genomes from six phyla, we grouped core genes into syntenic blocks in the context of a pangenome according to their stability across multiple isolates. A subset of the core genes, often species specific and lineage associated, formed a core-gene-defined genome organizational framework (cGOF). Such cGOFs are either single segmental (one-third of the species analyzed) or multisegmental (the rest). Multisegment cGOFs were further classified into symmetric or asymmetric according to segment orientations toward the origin-terminus axis. The cGOFs in Gram-positive species are exclusively symmetric and often reversible in orientation, as opposed to those of the Gram-negative bacteria, which are all asymmetric and irreversible. Meanwhile, all species showing strong strand-biased gene distribution contain symmetric cGOFs and often specific DnaE (α subunit of DNA polymerase III) isoforms. Furthermore, functional evaluations revealed that cGOF genes are hub associated with regard to cellular activities, and the stability of cGOF provides efficient indexes for scaffold orientation as demonstrated by assembling virtual and empirical genome drafts. cGOFs show species specificity, and the symmetry of multisegmental cGOFs is conserved among taxa and constrained by DNA polymerase-centric strand-biased gene distribution. The definition of species-specific cGOFs provides powerful guidance for genome assembly and other structure-based analysis. IMPORTANCE Prokaryotic genomes are frequently interrupted by horizontal gene transfer (HGT) and rearrangement. To know whether there is a set of genes not only conserved in position among isolates but also functionally essential for a given species and to further evaluate the stability or flexibility of such genome structures across lineages are of importance. Based on a large number of multi-isolate pangenomic data, our analysis reveals that a subset of core genes is organized into a core-gene-defined genome organizational framework, or cGOF. Furthermore, the lineage-associated cGOFs among Gram-positive and Gram-negative bacteria behave differently: the former, composed of 2 to 4 segments, have their fragments symmetrically rearranged around the origin-terminus axis, whereas the latter show more complex segmentation and are partitioned asymmetrically into chromosomal structures. The definition of cGOFs provides new insights into prokaryotic genome organization and efficient guidance for genome assembly and analysis.Yu KangChaohao GuLina YuanYue WangYanmin ZhuXinna LiQibin LuoJingfa XiaoDaquan JiangMinping QianAftab Ahmed KhanFei ChenZhang ZhangJun YuAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 6 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Yu Kang Chaohao Gu Lina Yuan Yue Wang Yanmin Zhu Xinna Li Qibin Luo Jingfa Xiao Daquan Jiang Minping Qian Aftab Ahmed Khan Fei Chen Zhang Zhang Jun Yu Flexibility and Symmetry of Prokaryotic Genome Rearrangement Reveal Lineage-Associated Core-Gene-Defined Genome Organizational Frameworks
description	ABSTRACT The prokaryotic pangenome partitions genes into core and dispensable genes. The order of core genes, albeit assumed to be stable under selection in general, is frequently interrupted by horizontal gene transfer and rearrangement, but how a core-gene-defined genome maintains its stability or flexibility remains to be investigated. Based on data from 30 species, including 425 genomes from six phyla, we grouped core genes into syntenic blocks in the context of a pangenome according to their stability across multiple isolates. A subset of the core genes, often species specific and lineage associated, formed a core-gene-defined genome organizational framework (cGOF). Such cGOFs are either single segmental (one-third of the species analyzed) or multisegmental (the rest). Multisegment cGOFs were further classified into symmetric or asymmetric according to segment orientations toward the origin-terminus axis. The cGOFs in Gram-positive species are exclusively symmetric and often reversible in orientation, as opposed to those of the Gram-negative bacteria, which are all asymmetric and irreversible. Meanwhile, all species showing strong strand-biased gene distribution contain symmetric cGOFs and often specific DnaE (α subunit of DNA polymerase III) isoforms. Furthermore, functional evaluations revealed that cGOF genes are hub associated with regard to cellular activities, and the stability of cGOF provides efficient indexes for scaffold orientation as demonstrated by assembling virtual and empirical genome drafts. cGOFs show species specificity, and the symmetry of multisegmental cGOFs is conserved among taxa and constrained by DNA polymerase-centric strand-biased gene distribution. The definition of species-specific cGOFs provides powerful guidance for genome assembly and other structure-based analysis. IMPORTANCE Prokaryotic genomes are frequently interrupted by horizontal gene transfer (HGT) and rearrangement. To know whether there is a set of genes not only conserved in position among isolates but also functionally essential for a given species and to further evaluate the stability or flexibility of such genome structures across lineages are of importance. Based on a large number of multi-isolate pangenomic data, our analysis reveals that a subset of core genes is organized into a core-gene-defined genome organizational framework, or cGOF. Furthermore, the lineage-associated cGOFs among Gram-positive and Gram-negative bacteria behave differently: the former, composed of 2 to 4 segments, have their fragments symmetrically rearranged around the origin-terminus axis, whereas the latter show more complex segmentation and are partitioned asymmetrically into chromosomal structures. The definition of cGOFs provides new insights into prokaryotic genome organization and efficient guidance for genome assembly and analysis.
format	article
author	Yu Kang Chaohao Gu Lina Yuan Yue Wang Yanmin Zhu Xinna Li Qibin Luo Jingfa Xiao Daquan Jiang Minping Qian Aftab Ahmed Khan Fei Chen Zhang Zhang Jun Yu
author_facet	Yu Kang Chaohao Gu Lina Yuan Yue Wang Yanmin Zhu Xinna Li Qibin Luo Jingfa Xiao Daquan Jiang Minping Qian Aftab Ahmed Khan Fei Chen Zhang Zhang Jun Yu
author_sort	Yu Kang
title	Flexibility and Symmetry of Prokaryotic Genome Rearrangement Reveal Lineage-Associated Core-Gene-Defined Genome Organizational Frameworks
title_short	Flexibility and Symmetry of Prokaryotic Genome Rearrangement Reveal Lineage-Associated Core-Gene-Defined Genome Organizational Frameworks
title_full	Flexibility and Symmetry of Prokaryotic Genome Rearrangement Reveal Lineage-Associated Core-Gene-Defined Genome Organizational Frameworks
title_fullStr	Flexibility and Symmetry of Prokaryotic Genome Rearrangement Reveal Lineage-Associated Core-Gene-Defined Genome Organizational Frameworks
title_full_unstemmed	Flexibility and Symmetry of Prokaryotic Genome Rearrangement Reveal Lineage-Associated Core-Gene-Defined Genome Organizational Frameworks
title_sort	flexibility and symmetry of prokaryotic genome rearrangement reveal lineage-associated core-gene-defined genome organizational frameworks
publisher	American Society for Microbiology
publishDate	2014
url	https://doaj.org/article/38c289b495334aff9d85e12e1a3d5f1f
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Flexibility and Symmetry of Prokaryotic Genome Rearrangement Reveal Lineage-Associated Core-Gene-Defined Genome Organizational Frameworks

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