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Open Access Highly Accessed Research article

Comparative genomics and transcriptomics of lineages I, II, and III strains of Listeria monocytogenes

Torsten Hain1, Rohit Ghai1, André Billion1, Carsten Tobias Kuenne1, Christiane Steinweg1, Benjamin Izar1, Walid Mohamed1, Mobarak Abu Mraheil1, Eugen Domann1, Silke Schaffrath1, Uwe Kärst2, Alexander Goesmann3, Sebastian Oehm3, Alfred Pühler3, Rainer Merkl4, Sonja Vorwerk5, Philippe Glaser6, Patricia Garrido7, Christophe Rusniok7, Carmen Buchrieser7, Werner Goebel8 and Trinad Chakraborty1*

Author Affiliations

1 Institute of Medical Microbiology, Justus-Liebig-University, Schubertstrasse 81, Giessen, D-35392, Germany

2 Helmholtz-Zentrum für Infektionsforschung GmbH, Inhoffenstraße 7, Braunschweig, 38124, Germany

3 Center for Biotechnology, University of Bielefeld, Bielefeld, D-33594, Germany

4 Institut für Biophysik und physikalische Biochemie, Universität Regensburg, Universitätstrasse 31, Regensburg, D-93053, Germany

5 Febit Biomed GmbH, Im Neuenheimer Feld 519, Heidelberg, D-69120, Germany

6 Institut Pasteur, Laboratoire Evolution et Génomique Bactériennes and CNRS URA 2171, Paris, 75724, France

7 Institut Pasteur, Biologie des Bactéries Intracellulaires and CNRS URA 2171, Paris, 75724, France

8 Max von Pettenkofer-Institut for Hygiene and Medical Microbiology, Ludwig Maximilians-University München, Pettenkoferstrasse 9a, Munich, D-80336, Germany

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BMC Genomics 2012, 13:144  doi:10.1186/1471-2164-13-144

Published: 24 April 2012

Abstract

Background

Listeria monocytogenes is a food-borne pathogen that causes infections with a high-mortality rate and has served as an invaluable model for intracellular parasitism. Here, we report complete genome sequences for two L. monocytogenes strains belonging to serotype 4a (L99) and 4b (CLIP80459), and transcriptomes of representative strains from lineages I, II, and III, thereby permitting in-depth comparison of genome- and transcriptome -based data from three lineages of L. monocytogenes. Lineage III, represented by the 4a L99 genome is known to contain strains less virulent for humans.

Results

The genome analysis of the weakly pathogenic L99 serotype 4a provides extensive evidence of virulence gene decay, including loss of several important surface proteins. The 4b CLIP80459 genome, unlike the previously sequenced 4b F2365 genome harbours an intact inlB invasion gene. These lineage I strains are characterized by the lack of prophage genes, as they share only a single prophage locus with other L. monocytogenes genomes 1/2a EGD-e and 4a L99. Comparative transcriptome analysis during intracellular growth uncovered adaptive expression level differences in lineages I, II and III of Listeria, notable amongst which was a strong intracellular induction of flagellar genes in strain 4a L99 compared to the other lineages. Furthermore, extensive differences between strains are manifest at levels of metabolic flux control and phosphorylated sugar uptake. Intriguingly, prophage gene expression was found to be a hallmark of intracellular gene expression. Deletion mutants in the single shared prophage locus of lineage II strain EGD-e 1/2a, the lma operon, revealed severe attenuation of virulence in a murine infection model.

Conclusion

Comparative genomics and transcriptome analysis of L. monocytogenes strains from three lineages implicate prophage genes in intracellular adaptation and indicate that gene loss and decay may have led to the emergence of attenuated lineages.

Keywords:
Listeria monocytogenes; Lineage; Comparative genomics; Gene decay; Comparative transcriptomics; Flagella; Prophage; Monocin; Isogenic deletion mutants; Murine infection