4.5 Article

Bridging Chromosomal Architecture and Pathophysiology of Streptococcus pneumoniae

Journal

GENOME BIOLOGY AND EVOLUTION
Volume 9, Issue 2, Pages 350-+

Publisher

OXFORD UNIV PRESS
DOI: 10.1093/gbe/evw299

Keywords

interactome; topoisomerase; topological domain; virulence factor; X-state

Funding

  1. Spanish Ministry of Health
  2. Ministry of Economy and Competitiveness [BIO2014-55462-R]

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The chromosome of Streptococcus pneumoniae is organized into topological domains based on its transcriptional response to DNA relaxation: Up-regulated (UP), down-regulated (DOWN), nonregulated (NR), and AT-rich. In the present work, NR genes found to have highly conserved chromosomal locations (17% of the genome) were categorized as members of position-conserved nonregulated (pcNR) domains, while NR genes with a variable position (36% of the genome) were classified as members of position-variable nonregulated (pvNR) domains. On average, pcNR domains showed high transcription rates, optimized codon usage, and were found to contain only a small number of RUP/BOX/SPLICE repeats. They were also poor in exogenous genes but enriched in leading strand genes that code for proteins involved in primary metabolism with central roles within the interactome. In contrast, pvNR genes coding for cell wall proteins, paralogs, virulence factors and immunogenic candidates for protein-based vaccines were found to be overrepresented. DOWN domains were enriched in genes essential for infection. Many UP and DOWN domain genes were seen to be activated during different stages of competence, whereas pcNR genes tended to be repressed until the competence was switched off. Pneumococcal genes appear to be subject to a topology-driven selection pressure that defines the chromosomal location of genes involved in metabolism, virulence and competence. The pcNR domains are interleaved between UP and DOWN domains according to a pattern that suggests the existence of macrodomain entities. The term topogenomics is here proposed to describe the study of the topological rules of genomes and their relationship with physiology.

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