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Pan-Genome Analysis of the Emerging Foodborne Pathogen Cronobacter Spp

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Pan-Genome Analysis of the Emerging Foodborne Pathogen Cronobacter Spp Pan-genome analysis of the emerging foodborne pathogen Cronobacter spp. suggests a species-level bidirectional divergence driven by niche adaptation Grim, C. J., Kotewicz, M. L., Power, K. A., Gopinath, G., Franco, A. A., Jarvis, K. G., Yan, Q. Q., Jackson, S. A., Sathyamoorthy, V., Hu, L., Pagotto, F., Iversen, C., Lehner, A., Stephan, R., Fanning, S., & Tall, B. D. (2013). Pan-genome analysis of the emerging foodborne pathogen Cronobacter spp. suggests a species-level bidirectional divergence driven by niche adaptation. BMC Genomics, 14, [366]. https://doi.org/10.1186/1471- 2164-14-366 Published in: BMC Genomics Document Version: Publisher's PDF, also known as Version of record Queen's University Belfast - Research Portal: Link to publication record in Queen's University Belfast Research Portal Publisher rights © 2013 Grim et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. General rights Copyright for the publications made accessible via the Queen's University Belfast Research Portal is retained by the author(s) and / or other copyright owners and it is a condition of accessing these publications that users recognise and abide by the legal requirements associated with these rights. Take down policy The Research Portal is Queen's institutional repository that provides access to Queen's research output. Every effort has been made to ensure that content in the Research Portal does not infringe any person's rights, or applicable UK laws. If you discover content in the Research Portal that you believe breaches copyright or violates any law, please contact [email protected]. Download date:25. Sep. 2021 Grim et al. BMC Genomics 2013, 14:366 http://www.biomedcentral.com/1471-2164/14/366 RESEARCH ARTICLE Open Access Pan-genome analysis of the emerging foodborne pathogen Cronobacter spp. suggests a species- level bidirectional divergence driven by niche adaptation Christopher J Grim1,2, Michael L Kotewicz1, Karen A Power3, Gopal Gopinath1, Augusto A Franco1, Karen G Jarvis1, Qiong Q Yan3, Scott A Jackson1, Venugopal Sathyamoorthy1, Lan Hu1,2, Franco Pagotto4, Carol Iversen5, Angelika Lehner6, Roger Stephan6, Séamus Fanning3 and Ben D Tall1* Abstract Background: 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. Results: 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. Conclusions: 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. Background Although E. sakazakii was synonymous with the original Cronobacter is a newly described genus that includes op- single species epithet, Iversen et al. [1], using a poly- portunistic pathogens formerly classified as Enterobacter phasic approach based on extensive genotypic and sakazakii [1]. E. sakazakii was first described by Farmer phenotypic criteria, reclassified strains of this diverse et al. [2], using DNA-DNA hybridization studies and species within the novel genus, Cronobacter. Originally, phenotyping to reclassify a group of yellow-pigmented the genus contained six recognized species, C. sakazakii Enterobacter cloacae isolates attributed to cases of neo- (Csak, biogroups 1–4, 7, 8, 11, and 13), C. malonaticus natal meningitis [3] into 15 phenotypically distinct (Cmal, biogroups 5, 9, and 14), C. muytjensii (Cmuy, biogroups. A 16th biogroup was later described [4]. biogroup 15), C. turicensis (Ctur, biogroup 16), C. dublinensis, subsp. dublinensis, lausannensis, and lactaridi (biogroups 12, Cdubdub, 10, Cdublau and 6, * Correspondence: [email protected] 1CFSAN, FDA, Laurel, USA Cdublact, respectively) and C. genomospecies 1. Joseph Full list of author information is available at the end of the article © 2013 Grim et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Grim et al. BMC Genomics 2013, 14:366 Page 2 of 16 http://www.biomedcentral.com/1471-2164/14/366 et al. [5] have updated this taxonomy by designating with meningitis [21] was sequenced [22]. In this paper, we members assigned to the genomospecies group 1 as C. describe the genomes of the type strains of Cronobacter universalis (Cuni, biotype 16c) and identifying a new dublinensis subsp. dublinensis, Cronobacter dublinensis species, C. condimenti, based on a single known strain subsp. lactaridi, Cronobacter dublinensis subsp. lausan- using a seven gene multi-locus sequence typing (MLST) nensis, Cronobacter malonaticus, Cronobacter muytjensii, scheme. and Cronobacter universalis. Comparative genomics was Cronobacter have been primarily associated with infec- performed on these six genomes, as well as two previously tions in infants, but recent reports have highlighted the published, closed genomes of Cronobacter. We identified risk posed to immune compromised adults, particularly and characterized the features associated with the core and the elderly [6,7]. Cronobacter have been recovered from a pan genome of this bacterial genus in an attempt to under- wide variety of foods, including powdered infant formula stand the evolution of these organisms and the genetic (PIF), follow-on formulas, weaning foods, milk and sodium content of each species. caseinate powders, rice seed, dried herbs, teas, and spices, spiced meats, dried flour or meal (corn, soy, potato, wheat, Results and rice), dried infant and adult cereals, dried vegetables, General features of sequenced Cronobacter genomes grains, tofu, powdered ice tea, mixed salad vegetables, Whole genome sequencing of six species type strains of tomato harvesting bins, chocolate, candied cough drops, Cronobacter was performed (Table 1). Each genome ana- and pastas [8-12]. Nevertheless, PIF remains epidemio- lyzed in this study contained a single chromosome and a logically linked to outbreaks of neonatal and infantile large repFIB plasmid, similar to Csak BAA-894 (pESA3) meningitis, and Cronobacter are routinely isolated from and Ctur z30232 (pCTU1), except the genome of C. household PIF preparation equipment, including blenders muytjensii ATCC 51329. Previously, Franco and Hu and spoons. Although PIF is regarded as an important et al. [23] reported that only 75% of strains of C. source of this pathogen, the main reservoir for Cronobacter muytjensii harbored this plasmid, while the incidence of seems to be the environment [13]. this plasmid in other Cronobacter spp. is 99%. The G + Cronobacter are capable of surviving and persisting in C% content of each genome ranged from 55 to 57% low-water environments [8], owing to their distribution (Table 1). Each of the six draft genomes contained seven in dry food goods. Although the exact genetic determin- ribosomal RNA operons, as inferred from comparative ant remains to be identified, Breeuwer et al. reported genomics with Csak BAA-894 and Ctur z3032 (Table 1). that intracellular accumulation of trehalose, among other features, prevents protein denaturation and membrane fu- Whole genome phylogeny and Cronobacter taxonomy sion and these may contribute to the desiccation-resistant To confirm the taxonomic standing of Cronobacter properties of the bacterium [14,15]. The expression of an genus novum and species [1], genome scale analyses exopolysaccharide composed of cellulose may also be re- based on nucleotide sequence were performed. Average quired [16]. Thermoresistance of Cronobacter has also nucleotide identity (ANI) has emerged as one of the pre- been reported [14,17]. Proteins unique to thermotolerant dominant genomics alternatives to DNA-DNA hybridi- Cronobacter strains have been identified by liquid chroma- zation. The pairwise ANI values between all Cronobacter tography and mass
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