1. Institut Pasteur, Unité des Interactions Bactéries-Cellules, F-75015 Paris, France
2. Inserm, U604, F-75015 Paris, France
3. INRA, USC2020, F-75015 Paris, France
4. Institut Pasteur, G5 Microorganismes et Barrières de l'hôte, F-75015 Paris, France
5. Inserm, Avenir, U604, F-75015 Paris, France
6. Department of Molecular Biology,
7. The Laboratory for Molecular Infection Medicine Sweden (MIMS), Umeå University, S-90187 Umeå, Sweden
8. Institut Pasteur, Génopole, Plate-forme 2, F-75015 Paris, France
9. Institut Pasteur, UP Génétique in silico, F-75015 Paris, France
10. CNRS, URA2171, F-75015 Paris, France
11. Université Paris Descartes, Hôpital Necker-Enfants malades, Assistance Publique-Hôpitaux de Paris, Paris, F-75015 France
12. Present address: Instituto de Agrobiotecnología, Universidad Pública de Navarra-CSIC-Gobierno de Navarra, 31006-Pamplona, Spain.

Correspondence to: Pascale Cossart^1,2,3 Correspondence and requests for materials should be addressed to P.C. (Email: pascale.cossart@pasteur.fr).

Abstract

The bacterium Listeria monocytogenes is ubiquitous in the environment and can lead to severe food-borne infections. It has recently emerged as a multifaceted model in pathogenesis. However, how this bacterium switches from a saprophyte to a pathogen is largely unknown. Here, using tiling arrays and RNAs from wild-type and mutant bacteria grown in vitro, ex vivo and in vivo, we have analysed the transcription of its entire genome. We provide the complete Listeria operon map and have uncovered far more diverse types of RNAs than expected: in addition to 50 small RNAs (<500 nucleotides), at least two of which are involved in virulence in mice, we have identified antisense RNAs covering several open-reading frames and long overlapping 5' and 3' untranslated regions. We discovered that riboswitches can act as terminators for upstream genes. When Listeria reaches the host intestinal lumen, an extensive transcriptional reshaping occurs with a SigB-mediated activation of virulence genes. In contrast, in the blood, PrfA controls transcription of virulence genes. Remarkably, several non-coding RNAs absent in the non-pathogenic species Listeria innocua exhibit the same expression patterns as the virulence genes. Together, our data unravel successive and coordinated global transcriptional changes during infection and point to previously unknown regulatory mechanisms in bacteria.

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