Open Access Highly Accessed Research article

Pan-genome analysis of the emerging foodborne pathogen Cronobacter spp. suggests a species-level bidirectional divergence driven by niche adaptation

Christopher J Grim12, Michael L Kotewicz1, Karen A Power3, Gopal Gopinath1, Augusto A Franco1, Karen G Jarvis1, Qiong Q Yan3, Scott A Jackson1, Venugopal Sathyamoorthy1, Lan Hu12, Franco Pagotto4, Carol Iversen5, Angelika Lehner6, Roger Stephan6, Séamus Fanning3 and Ben D Tall1*

Author Affiliations

1 CFSAN, FDA, Laurel, USA

2 Oak Ridge Institute for Science and Education, Oak Ridge, USA

3 UCD Centre for Food Safety, School of Public Health, Physiotherapy & Population Science, University College, Dublin & WHO Collaborating Centre for Cronobacter, Belfield, Dublin, Ireland

4 Food Directorate / Direction des aliments, Bureau of Microbial Hazards / Bureau des dangers microbiens, Health Canada / Santé Canada, and Sir F.G. Banting Research Centre / Centre de recherches Sir F.G. Banting, Ottawa, ON, Canada

5 Nestle Research Center, Lausanne, Switzerland

6 Institute for Food Safety and Hygiene, University of Zurich, Zurich, Switzerland

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BMC Genomics 2013, 14:366  doi:10.1186/1471-2164-14-366

Published: 31 May 2013



Members of the genus Cronobacter are causes of rare but severe illness in neonates and preterm infants following the ingestion of contaminated infant formula. Seven species have been described and two of the species genomes were subsequently published. In this study, we performed comparative genomics on eight strains of Cronobacter, including six that we sequenced (representing six of the seven species) and two previously published, closed genomes.


We identified and characterized the features associated with the core and pan genome of the genus Cronobacter in an attempt to understand the evolution of these bacteria and the genetic content of each species. We identified 84 genomic regions that are present in two or more Cronobacter genomes, along with 45 unique genomic regions. Many potentially horizontally transferred genes, such as lysogenic prophages, were also identified. Most notable among these were several type six secretion system gene clusters, transposons that carried tellurium, copper and/or silver resistance genes, and a novel integrative conjugative element.


Cronobacter have diverged into two clusters, one consisting of C. dublinensis and C. muytjensii (Cdub-Cmuy) and the other comprised of C. sakazakii, C. malonaticus, C. universalis, and C. turicensis, (Csak-Cmal-Cuni-Ctur) from the most recent common ancestral species. While several genetic determinants for plant-association and human virulence could be found in the core genome of Cronobacter, the four Cdub-Cmuy clade genomes contained several accessory genomic regions important for survival in a plant-associated environmental niche, while the Csak-Cmal-Cuni-Ctur clade genomes harbored numerous virulence-related genetic traits.