Chromosomal periodicity and positional networks of genes in Escherichia coli

Abstract The structure of dynamic folds in microbial chromosomes is largely unknown. Here, we find that genes with a highly biased codon composition and characterizing a functional core in Escherichia coli K12 show to be periodically distributed along the arcs, suggesting an encoded three‐dimensiona...

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Main Authors: Anthony Mathelier, Alessandra Carbone
Format: Article
Language:English
Published: Springer Nature 2010-05-01
Series:Molecular Systems Biology
Subjects:
Online Access:https://doi.org/10.1038/msb.2010.21
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author Anthony Mathelier
Alessandra Carbone
author_facet Anthony Mathelier
Alessandra Carbone
author_sort Anthony Mathelier
collection DOAJ
description Abstract The structure of dynamic folds in microbial chromosomes is largely unknown. Here, we find that genes with a highly biased codon composition and characterizing a functional core in Escherichia coli K12 show to be periodically distributed along the arcs, suggesting an encoded three‐dimensional genomic organization helping functional activities among which are translation and, possibly, transcription. This extends to functional classes of genes that are shown to systematically organize into two independent positional gene networks, one driven by metabolic genes and the other by genes involved in cellular processing and signaling. We conclude that functional reasons justify periodic gene organization. This finding generates new questions on evolutionary pressures imposed on the chromosome. Our methodological approach is based on single genome analysis. Given either core genes or genes organized in functional classes, we analyze the detailed distribution of distances between pairs of genes through a parameterized model based on signal processing and find that these groups of genes tend to be separated by a regular integral distance. The methodology can be applied to any set of genes and can be taken as a footprint for large‐scale bacterial and archaeal analysis.
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spelling doaj-art-de2ceff53feb4068b4a1711ec32d1bbd2025-08-24T12:00:36ZengSpringer NatureMolecular Systems Biology1744-42922010-05-016111210.1038/msb.2010.21Chromosomal periodicity and positional networks of genes in Escherichia coliAnthony Mathelier0Alessandra Carbone1UPMC Univ Paris 06, FRE3214, Génomique Analytique, 15 rue de l'École de MédecineUPMC Univ Paris 06, FRE3214, Génomique Analytique, 15 rue de l'École de MédecineAbstract The structure of dynamic folds in microbial chromosomes is largely unknown. Here, we find that genes with a highly biased codon composition and characterizing a functional core in Escherichia coli K12 show to be periodically distributed along the arcs, suggesting an encoded three‐dimensional genomic organization helping functional activities among which are translation and, possibly, transcription. This extends to functional classes of genes that are shown to systematically organize into two independent positional gene networks, one driven by metabolic genes and the other by genes involved in cellular processing and signaling. We conclude that functional reasons justify periodic gene organization. This finding generates new questions on evolutionary pressures imposed on the chromosome. Our methodological approach is based on single genome analysis. Given either core genes or genes organized in functional classes, we analyze the detailed distribution of distances between pairs of genes through a parameterized model based on signal processing and find that these groups of genes tend to be separated by a regular integral distance. The methodology can be applied to any set of genes and can be taken as a footprint for large‐scale bacterial and archaeal analysis.https://doi.org/10.1038/msb.2010.21chromosome structureCOGs classescore genesEscherichia coli K12essential genes
spellingShingle Anthony Mathelier
Alessandra Carbone
Chromosomal periodicity and positional networks of genes in Escherichia coli
Molecular Systems Biology
chromosome structure
COGs classes
core genes
Escherichia coli K12
essential genes
title Chromosomal periodicity and positional networks of genes in Escherichia coli
title_full Chromosomal periodicity and positional networks of genes in Escherichia coli
title_fullStr Chromosomal periodicity and positional networks of genes in Escherichia coli
title_full_unstemmed Chromosomal periodicity and positional networks of genes in Escherichia coli
title_short Chromosomal periodicity and positional networks of genes in Escherichia coli
title_sort chromosomal periodicity and positional networks of genes in escherichia coli
topic chromosome structure
COGs classes
core genes
Escherichia coli K12
essential genes
url https://doi.org/10.1038/msb.2010.21
work_keys_str_mv AT anthonymathelier chromosomalperiodicityandpositionalnetworksofgenesinescherichiacoli
AT alessandracarbone chromosomalperiodicityandpositionalnetworksofgenesinescherichiacoli