Staphylococcus aureus Transcriptome Architecture: From Laboratory to Infection-Mimicking Conditions

PLoS Genet. 2016 Apr 1;12(4):e1005962. doi: 10.1371/journal.pgen.1005962. eCollection 2016 Apr.

Abstract

Staphylococcus aureus is a major pathogen that colonizes about 20% of the human population. Intriguingly, this Gram-positive bacterium can survive and thrive under a wide range of different conditions, both inside and outside the human body. Here, we investigated the transcriptional adaptation of S. aureus HG001, a derivative of strain NCTC 8325, across experimental conditions ranging from optimal growth in vitro to intracellular growth in host cells. These data establish an extensive repertoire of transcription units and non-coding RNAs, a classification of 1412 promoters according to their dependence on the RNA polymerase sigma factors SigA or SigB, and allow identification of new potential targets for several known transcription factors. In particular, this study revealed a relatively low abundance of antisense RNAs in S. aureus, where they overlap only 6% of the coding genes, and only 19 antisense RNAs not co-transcribed with other genes were found. Promoter analysis and comparison with Bacillus subtilis links the small number of antisense RNAs to a less profound impact of alternative sigma factors in S. aureus. Furthermore, we revealed that Rho-dependent transcription termination suppresses pervasive antisense transcription, presumably originating from abundant spurious transcription initiation in this A+T-rich genome, which would otherwise affect expression of the overlapped genes. In summary, our study provides genome-wide information on transcriptional regulation and non-coding RNAs in S. aureus as well as new insights into the biological function of Rho and the implications of spurious transcription in bacteria.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Binding Sites
  • Blotting, Northern
  • Gene Expression
  • Genes, Bacterial
  • Promoter Regions, Genetic
  • Staphylococcus aureus / genetics*
  • Transcription Factors / metabolism
  • Transcriptome*

Substances

  • Transcription Factors

Grant support

This work was supported by CEU projects LSHG-CT-2006-037469 (BaSysBio) and LSHM-CT-2006-019064 (StaphDynamics); the Top Institute Pharma projects T4-213 and T4-502; the Institut Pasteur; CNRS; the ANR projects ANR-08-ALIA-0011 NABAB and ANR-09-MIEN-0010 GRABIRON; the BMBF via ZIK-FunGene (03Z1CN22); and the Deutsche Forschungsgemeinschaft within the framework of SFB/Transregio 34 and GRK1870. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.