Development of a Custom-Designed, Pan Genomic DNA Microarray to Characterize Strain-Level Diversity among Cronobacter spp.

Ben Davies Tall; Jayanthi Gangiredla; Gopal R. Gopinath; Qiongqiong Yan; Hannah R. Chase; Boram Lee; Seongeun Hwang; Larisa Trach; Eunbi Park; Yeon Joo Yoo; Tae Jung Chung; Scott A. Jackson; Isha R. Patel; Venugopal Sathyamoorthy; Monica Pava-Ripoll; Michael L. Kotewicz; Laurenda Carter; Carol Iversen; Franco Pagotto; Roger Stephan; Angelika Lehner; Séamus Fanning; Christopher J. Grim

doi:10.3389/fped.2015.00036

Development of a Custom-Designed, Pan Genomic DNA Microarray to Characterize Strain-Level Diversity among Cronobacter spp.

Ben Davies Tall^*, Jayanthi Gangiredla, Gopal R. Gopinath, Qiongqiong Yan, Hannah R. Chase, Boram Lee, Seongeun Hwang, Larisa Trach, Eunbi Park, Yeon Joo Yoo, Tae Jung Chung, Scott A. Jackson, Isha R. Patel, Venugopal Sathyamoorthy, Monica Pava-Ripoll, Michael L. Kotewicz, Laurenda Carter, Carol Iversen, Franco Pagotto, Roger StephanAngelika Lehner, Séamus Fanning, Christopher J. Grim

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

16 Citations (Scopus)

5 Downloads (Pure)

Abstract

Cronobacter species cause infections in all age groups; however neonates are at highest risk and remain the most susceptible age group for life-threatening invasive disease. The genus contains seven species:Cronobacter sakazakii, Cronobacter malonaticus, Cronobacter turicensis, Cronobacter muytjensii, Cronobacter dublinensis, Cronobacter universalis, and Cronobacter condimenti. Despite an abundance of published genomes of these species, genomics-based epidemiology of the genus is not well established. The gene content of a diverse group of 126 unique Cronobacter and taxonomically related isolates was determined using a pan genomic-based DNA microarray as a genotyping tool and as a means to identify outbreak isolates for food safety, environmental, and clinical surveillance purposes. The microarray constitutes 19,287 independent genes representing 15 Cronobacter genomes and 18 plasmids and 2,371 virulence factor genes of phylogenetically related Gram-negative bacteria. The Cronobacter microarray was able to distinguish the seven Cronobacter species from one another and from non-Cronobacter species; and within each species, strains grouped into distinct clusters based on their genomic diversity. These results also support the phylogenic divergence of the genus and clearly highlight the genomic diversity among each member of the genus. The current study establishes a powerful platform for further genomics research of this diverse genus, an important prerequisite toward the development of future countermeasures against this foodborne pathogen in the food safety and clinical arenas.

Original language	English
Article number	36
Journal	Frontiers in pediatrics
Volume	3
DOIs	https://doi.org/10.3389/fped.2015.00036
Publication status	Published - 30 Apr 2015
Externally published	Yes

Bibliographical note

Funding Information:
We thank the student internship programs of the International Offices of Kyungpook National University, Daegu, and Gachon University, Gyeonggi, Republic of Korea for sponsoring student interns: B. Lee, S. Hwang, E. Park, Y. J. Yoo, T. J. Chung. We thank the office of Undergraduate Research and Internship Programs, Joint institute of Food Safety and Applied Nutrition, University of Maryland, College Park, MD, USA for sponsoring student interns: H. R. Chase and L. Trach. We thank E. Strain of the Office of Analytics and Outreach, Division of Public Health and Biostatistics, CFSAN for providing us the 454 whole genome sequence of C. malonaticus strain ENBT0334. Funds supporting this work were obtained internally through U.S. FDA appropriations. If readers would like the Excel version of Table S3 in Supplementary Material, and the full data set of CEL files, they are available upon request.

Publisher Copyright:
Copyright © 2015 Tall, Gangiredla, Gopinath, Yan, Chase, Lee, Hwang, Trach, Park, Yoo, Chung, Jackson, Patel, Sathyamoorthy, Pava-Ripoll, Kotewicz, Carter, Iversen, Pagotto, Stephan, Lehner, Fanning and Grim.

Keywords

Cronobacter
genomic diversity
microarray
pan genomic
phylogenic divergence

ASJC Scopus subject areas

Pediatrics, Perinatology, and Child Health

Access to Document

10.3389/fped.2015.00036Licence: CC BY

Development of a custom-designed, pan genomic DNA microarray to characterize strain-level diversity among Cronobacter spp.
Copyright 2015 the authors. This is an open access article published under a Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium, provided the author and source are cited.
Final published version, 3.35 MBLicence: CC BY

Cite this

Tall, B. D., Gangiredla, J., Gopinath, G. R., Yan, Q., Chase, H. R., Lee, B., Hwang, S., Trach, L., Park, E., Yoo, Y. J., Chung, T. J., Jackson, S. A., Patel, I. R., Sathyamoorthy, V., Pava-Ripoll, M., Kotewicz, M. L., Carter, L., Iversen, C., Pagotto, F., ... Grim, C. J. (2015). Development of a Custom-Designed, Pan Genomic DNA Microarray to Characterize Strain-Level Diversity among Cronobacter spp. Frontiers in pediatrics, 3, [36]. https://doi.org/10.3389/fped.2015.00036

Tall, Ben Davies ; Gangiredla, Jayanthi ; Gopinath, Gopal R. ; Yan, Qiongqiong ; Chase, Hannah R. ; Lee, Boram ; Hwang, Seongeun ; Trach, Larisa ; Park, Eunbi ; Yoo, Yeon Joo ; Chung, Tae Jung ; Jackson, Scott A. ; Patel, Isha R. ; Sathyamoorthy, Venugopal ; Pava-Ripoll, Monica ; Kotewicz, Michael L. ; Carter, Laurenda ; Iversen, Carol ; Pagotto, Franco ; Stephan, Roger ; Lehner, Angelika ; Fanning, Séamus ; Grim, Christopher J. / Development of a Custom-Designed, Pan Genomic DNA Microarray to Characterize Strain-Level Diversity among Cronobacter spp. In: Frontiers in pediatrics. 2015 ; Vol. 3.

@article{4c951e04c86346ff963eec80ba1fd340,

title = "Development of a Custom-Designed, Pan Genomic DNA Microarray to Characterize Strain-Level Diversity among Cronobacter spp.",

abstract = "Cronobacter species cause infections in all age groups; however neonates are at highest risk and remain the most susceptible age group for life-threatening invasive disease. The genus contains seven species:Cronobacter sakazakii, Cronobacter malonaticus, Cronobacter turicensis, Cronobacter muytjensii, Cronobacter dublinensis, Cronobacter universalis, and Cronobacter condimenti. Despite an abundance of published genomes of these species, genomics-based epidemiology of the genus is not well established. The gene content of a diverse group of 126 unique Cronobacter and taxonomically related isolates was determined using a pan genomic-based DNA microarray as a genotyping tool and as a means to identify outbreak isolates for food safety, environmental, and clinical surveillance purposes. The microarray constitutes 19,287 independent genes representing 15 Cronobacter genomes and 18 plasmids and 2,371 virulence factor genes of phylogenetically related Gram-negative bacteria. The Cronobacter microarray was able to distinguish the seven Cronobacter species from one another and from non-Cronobacter species; and within each species, strains grouped into distinct clusters based on their genomic diversity. These results also support the phylogenic divergence of the genus and clearly highlight the genomic diversity among each member of the genus. The current study establishes a powerful platform for further genomics research of this diverse genus, an important prerequisite toward the development of future countermeasures against this foodborne pathogen in the food safety and clinical arenas.",

keywords = "Cronobacter, genomic diversity, microarray, pan genomic, phylogenic divergence",

author = "Tall, {Ben Davies} and Jayanthi Gangiredla and Gopinath, {Gopal R.} and Qiongqiong Yan and Chase, {Hannah R.} and Boram Lee and Seongeun Hwang and Larisa Trach and Eunbi Park and Yoo, {Yeon Joo} and Chung, {Tae Jung} and Jackson, {Scott A.} and Patel, {Isha R.} and Venugopal Sathyamoorthy and Monica Pava-Ripoll and Kotewicz, {Michael L.} and Laurenda Carter and Carol Iversen and Franco Pagotto and Roger Stephan and Angelika Lehner and S{\'e}amus Fanning and Grim, {Christopher J.}",

note = "Funding Information: We thank the student internship programs of the International Offices of Kyungpook National University, Daegu, and Gachon University, Gyeonggi, Republic of Korea for sponsoring student interns: B. Lee, S. Hwang, E. Park, Y. J. Yoo, T. J. Chung. We thank the office of Undergraduate Research and Internship Programs, Joint institute of Food Safety and Applied Nutrition, University of Maryland, College Park, MD, USA for sponsoring student interns: H. R. Chase and L. Trach. We thank E. Strain of the Office of Analytics and Outreach, Division of Public Health and Biostatistics, CFSAN for providing us the 454 whole genome sequence of C. malonaticus strain ENBT0334. Funds supporting this work were obtained internally through U.S. FDA appropriations. If readers would like the Excel version of Table S3 in Supplementary Material, and the full data set of CEL files, they are available upon request. Publisher Copyright: Copyright {\textcopyright} 2015 Tall, Gangiredla, Gopinath, Yan, Chase, Lee, Hwang, Trach, Park, Yoo, Chung, Jackson, Patel, Sathyamoorthy, Pava-Ripoll, Kotewicz, Carter, Iversen, Pagotto, Stephan, Lehner, Fanning and Grim.",

year = "2015",

month = apr,

day = "30",

doi = "10.3389/fped.2015.00036",

language = "English",

volume = "3",

journal = "Frontiers in pediatrics",

issn = "2296-2360",

publisher = "Frontiers Media S.A.",

}

Tall, BD, Gangiredla, J, Gopinath, GR, Yan, Q, Chase, HR, Lee, B, Hwang, S, Trach, L, Park, E, Yoo, YJ, Chung, TJ, Jackson, SA, Patel, IR, Sathyamoorthy, V, Pava-Ripoll, M, Kotewicz, ML, Carter, L, Iversen, C, Pagotto, F, Stephan, R, Lehner, A, Fanning, S & Grim, CJ 2015, 'Development of a Custom-Designed, Pan Genomic DNA Microarray to Characterize Strain-Level Diversity among Cronobacter spp.', Frontiers in pediatrics, vol. 3, 36. https://doi.org/10.3389/fped.2015.00036

Development of a Custom-Designed, Pan Genomic DNA Microarray to Characterize Strain-Level Diversity among Cronobacter spp. / Tall, Ben Davies; Gangiredla, Jayanthi; Gopinath, Gopal R.; Yan, Qiongqiong; Chase, Hannah R.; Lee, Boram; Hwang, Seongeun; Trach, Larisa; Park, Eunbi; Yoo, Yeon Joo; Chung, Tae Jung; Jackson, Scott A.; Patel, Isha R.; Sathyamoorthy, Venugopal; Pava-Ripoll, Monica; Kotewicz, Michael L.; Carter, Laurenda; Iversen, Carol; Pagotto, Franco; Stephan, Roger; Lehner, Angelika; Fanning, Séamus; Grim, Christopher J.

In: Frontiers in pediatrics, Vol. 3, 36, 30.04.2015.

Research output: Contribution to journal › Article › peer-review

TY - JOUR

T1 - Development of a Custom-Designed, Pan Genomic DNA Microarray to Characterize Strain-Level Diversity among Cronobacter spp.

AU - Tall, Ben Davies

AU - Gangiredla, Jayanthi

AU - Gopinath, Gopal R.

AU - Yan, Qiongqiong

AU - Chase, Hannah R.

AU - Lee, Boram

AU - Hwang, Seongeun

AU - Trach, Larisa

AU - Park, Eunbi

AU - Yoo, Yeon Joo

AU - Chung, Tae Jung

AU - Jackson, Scott A.

AU - Patel, Isha R.

AU - Sathyamoorthy, Venugopal

AU - Pava-Ripoll, Monica

AU - Kotewicz, Michael L.

AU - Carter, Laurenda

AU - Iversen, Carol

AU - Pagotto, Franco

AU - Stephan, Roger

AU - Lehner, Angelika

AU - Fanning, Séamus

AU - Grim, Christopher J.

N1 - Funding Information: We thank the student internship programs of the International Offices of Kyungpook National University, Daegu, and Gachon University, Gyeonggi, Republic of Korea for sponsoring student interns: B. Lee, S. Hwang, E. Park, Y. J. Yoo, T. J. Chung. We thank the office of Undergraduate Research and Internship Programs, Joint institute of Food Safety and Applied Nutrition, University of Maryland, College Park, MD, USA for sponsoring student interns: H. R. Chase and L. Trach. We thank E. Strain of the Office of Analytics and Outreach, Division of Public Health and Biostatistics, CFSAN for providing us the 454 whole genome sequence of C. malonaticus strain ENBT0334. Funds supporting this work were obtained internally through U.S. FDA appropriations. If readers would like the Excel version of Table S3 in Supplementary Material, and the full data set of CEL files, they are available upon request. Publisher Copyright: Copyright © 2015 Tall, Gangiredla, Gopinath, Yan, Chase, Lee, Hwang, Trach, Park, Yoo, Chung, Jackson, Patel, Sathyamoorthy, Pava-Ripoll, Kotewicz, Carter, Iversen, Pagotto, Stephan, Lehner, Fanning and Grim.

PY - 2015/4/30

Y1 - 2015/4/30

N2 - Cronobacter species cause infections in all age groups; however neonates are at highest risk and remain the most susceptible age group for life-threatening invasive disease. The genus contains seven species:Cronobacter sakazakii, Cronobacter malonaticus, Cronobacter turicensis, Cronobacter muytjensii, Cronobacter dublinensis, Cronobacter universalis, and Cronobacter condimenti. Despite an abundance of published genomes of these species, genomics-based epidemiology of the genus is not well established. The gene content of a diverse group of 126 unique Cronobacter and taxonomically related isolates was determined using a pan genomic-based DNA microarray as a genotyping tool and as a means to identify outbreak isolates for food safety, environmental, and clinical surveillance purposes. The microarray constitutes 19,287 independent genes representing 15 Cronobacter genomes and 18 plasmids and 2,371 virulence factor genes of phylogenetically related Gram-negative bacteria. The Cronobacter microarray was able to distinguish the seven Cronobacter species from one another and from non-Cronobacter species; and within each species, strains grouped into distinct clusters based on their genomic diversity. These results also support the phylogenic divergence of the genus and clearly highlight the genomic diversity among each member of the genus. The current study establishes a powerful platform for further genomics research of this diverse genus, an important prerequisite toward the development of future countermeasures against this foodborne pathogen in the food safety and clinical arenas.

AB - Cronobacter species cause infections in all age groups; however neonates are at highest risk and remain the most susceptible age group for life-threatening invasive disease. The genus contains seven species:Cronobacter sakazakii, Cronobacter malonaticus, Cronobacter turicensis, Cronobacter muytjensii, Cronobacter dublinensis, Cronobacter universalis, and Cronobacter condimenti. Despite an abundance of published genomes of these species, genomics-based epidemiology of the genus is not well established. The gene content of a diverse group of 126 unique Cronobacter and taxonomically related isolates was determined using a pan genomic-based DNA microarray as a genotyping tool and as a means to identify outbreak isolates for food safety, environmental, and clinical surveillance purposes. The microarray constitutes 19,287 independent genes representing 15 Cronobacter genomes and 18 plasmids and 2,371 virulence factor genes of phylogenetically related Gram-negative bacteria. The Cronobacter microarray was able to distinguish the seven Cronobacter species from one another and from non-Cronobacter species; and within each species, strains grouped into distinct clusters based on their genomic diversity. These results also support the phylogenic divergence of the genus and clearly highlight the genomic diversity among each member of the genus. The current study establishes a powerful platform for further genomics research of this diverse genus, an important prerequisite toward the development of future countermeasures against this foodborne pathogen in the food safety and clinical arenas.

KW - Cronobacter

KW - genomic diversity

KW - microarray

KW - pan genomic

KW - phylogenic divergence

U2 - 10.3389/fped.2015.00036

DO - 10.3389/fped.2015.00036

M3 - Article

AN - SCOPUS:85014447698

VL - 3

JO - Frontiers in pediatrics

JF - Frontiers in pediatrics

SN - 2296-2360

M1 - 36

ER -

Development of a Custom-Designed, Pan Genomic DNA Microarray to Characterize Strain-Level Diversity among Cronobacter spp.

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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