Use of a Pan–Genomic DNA Microarray in Determination of the Phylogenetic Relatedness among Cronobacter spp. and Its Use as a Data Mining Tool to Understand Cronobacter Biology

Ben D. Tall; Jayanthi Gangiredla; Christopher J. Grim; Isha R. Patel; Scott A. Jackson; Mark K. Mammel; Mahendra H. Kothary; Venugopal Sathyamoorthy; Laurenda Carter; Séamus Fanning; Carol Iversen; Franco Pagotto; Roger Stephan; Angelika Lehner; Jeffery Farber; Qiong Q. Yan; Gopal R. Gopinath

doi:10.3390/microarrays6010006

Use of a Pan–Genomic DNA Microarray in Determination of the Phylogenetic Relatedness among Cronobacter spp. and Its Use as a Data Mining Tool to Understand Cronobacter Biology

Ben D. Tall^*, Jayanthi Gangiredla, Christopher J. Grim, Isha R. Patel, Scott A. Jackson, Mark K. Mammel, Mahendra H. Kothary, Venugopal Sathyamoorthy, Laurenda Carter, Séamus Fanning, Carol Iversen, Franco Pagotto, Roger Stephan, Angelika Lehner, Jeffery Farber, Qiong Q. Yan, Gopal R. Gopinath

^*Corresponding author for this work

Research output: Contribution to journal › Review article › peer-review

4 Citations (Scopus)

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Abstract

Cronobacter (previously known as Enterobacter sakazakii) is a genus of Gram-negative, facultatively anaerobic, oxidase-negative, catalase-positive, rod-shaped bacteria of the family Enterobacteriaceae. These organisms cause a variety of illnesses such as meningitis, necrotizing enterocolitis, and septicemia in neonates and infants, and urinary tract, wound, abscesses or surgical site infections, septicemia, and pneumonia in adults. The total gene content of 379 strains of Cronobacter spp. and taxonomically-related isolates was determined using a recently reported DNA microarray. The Cronobacter microarray as a genotyping tool gives the global food safety community a rapid method to identify and capture the total genomic content of outbreak isolates for food safety, environmental, and clinical surveillance purposes. It was able to differentiate the seven Cronobacter species from one another and from non-Cronobacter species. The microarray was also able to cluster strains within each species into well-defined subgroups. These results also support previous studies on the phylogenic separation of species members of the genus and clearly highlight the evolutionary sequence divergence among each species of the genus compared to phylogenetically-related species. This review extends these studies and illustrates how the microarray can also be used as an investigational tool to mine genomic data sets from strains. Three case studies describing the use of the microarray are shown and include: (1) the determination of allelic differences among Cronobacter sakazakii strains possessing the virulence plasmid pESA3; (2) mining of malonate and myo-inositol alleles among subspecies of Cronobacter dublinensis strains to determine subspecies identity; and (3) lastly using the microarray to demonstrate sequence divergence and phylogenetic relatedness trends for 13 outer-membrane protein alleles among 240 Cronobacter and phylogenetically-related strains. The goal of this review is to describe microarrays as a robust tool for genomics research of this assorted and important genus, a criterion toward the development of future preventative measures to eliminate this foodborne pathogen from the global food supply.

Original language	English
Article number	6
Journal	Microarrays
Volume	6
Issue number	1
DOIs	https://doi.org/10.3390/microarrays6010006
Publication status	Published - 04 Mar 2017
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: Boram Lee, Eunbi Park, Hyerim Choi, JiHyeon Park, Seungeun Jeong, and YeonJoo Yoo, TaeJung Chung, SoYoung Jun, and Mijeong Kim, respectively. We thank the Office of Undergraduate Research and Internship Programs, the Joint institute of Food Safety and Applied Nutrition, University of Maryland, College Park, MD, for sponsoring student interns Hannah R. Chase, Flavia Negrete, and Samantha Finkelstein. Lastly, we thank the Oak Ridge Institute for Science and Education of Oak Ridge, Tennessee, for sponsoring research fellow Hannah. R. Chase. Funds supporting this work were obtained internally through U.S. FDA appropriations.

Publisher Copyright:
© 2017 by the authors. Licensee MDPI, Basel, Switzerland.

Keywords

Cronobacter
data mining
microarray

ASJC Scopus subject areas

Biotechnology
Bioengineering
Biochemistry
Biomedical Engineering

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10.3390/microarrays6010006Licence: CC BY

Use of a Pan–Genomic DNA Microarray in Determination of the Phylogenetic Relatedness among Cronobacter spp. and Its Use as a Data Mining Tool to Understand Cronobacter Biology
Copyright 2017 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, 1.66 MBLicence: CC BY

Cite this

Tall, B. D., Gangiredla, J., Grim, C. J., Patel, I. R., Jackson, S. A., Mammel, M. K., Kothary, M. H., Sathyamoorthy, V., Carter, L., Fanning, S., Iversen, C., Pagotto, F., Stephan, R., Lehner, A., Farber, J., Yan, Q. Q., & Gopinath, G. R. (2017). Use of a Pan–Genomic DNA Microarray in Determination of the Phylogenetic Relatedness among Cronobacter spp. and Its Use as a Data Mining Tool to Understand Cronobacter Biology. Microarrays, 6(1), Article 6. https://doi.org/10.3390/microarrays6010006

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title = "Use of a Pan–Genomic DNA Microarray in Determination of the Phylogenetic Relatedness among Cronobacter spp. and Its Use as a Data Mining Tool to Understand Cronobacter Biology",

abstract = "Cronobacter (previously known as Enterobacter sakazakii) is a genus of Gram-negative, facultatively anaerobic, oxidase-negative, catalase-positive, rod-shaped bacteria of the family Enterobacteriaceae. These organisms cause a variety of illnesses such as meningitis, necrotizing enterocolitis, and septicemia in neonates and infants, and urinary tract, wound, abscesses or surgical site infections, septicemia, and pneumonia in adults. The total gene content of 379 strains of Cronobacter spp. and taxonomically-related isolates was determined using a recently reported DNA microarray. The Cronobacter microarray as a genotyping tool gives the global food safety community a rapid method to identify and capture the total genomic content of outbreak isolates for food safety, environmental, and clinical surveillance purposes. It was able to differentiate the seven Cronobacter species from one another and from non-Cronobacter species. The microarray was also able to cluster strains within each species into well-defined subgroups. These results also support previous studies on the phylogenic separation of species members of the genus and clearly highlight the evolutionary sequence divergence among each species of the genus compared to phylogenetically-related species. This review extends these studies and illustrates how the microarray can also be used as an investigational tool to mine genomic data sets from strains. Three case studies describing the use of the microarray are shown and include: (1) the determination of allelic differences among Cronobacter sakazakii strains possessing the virulence plasmid pESA3; (2) mining of malonate and myo-inositol alleles among subspecies of Cronobacter dublinensis strains to determine subspecies identity; and (3) lastly using the microarray to demonstrate sequence divergence and phylogenetic relatedness trends for 13 outer-membrane protein alleles among 240 Cronobacter and phylogenetically-related strains. The goal of this review is to describe microarrays as a robust tool for genomics research of this assorted and important genus, a criterion toward the development of future preventative measures to eliminate this foodborne pathogen from the global food supply.",

keywords = "Cronobacter, data mining, microarray",

author = "Tall, {Ben D.} and Jayanthi Gangiredla and Grim, {Christopher J.} and Patel, {Isha R.} and Jackson, {Scott A.} and Mammel, {Mark K.} and Kothary, {Mahendra H.} and Venugopal Sathyamoorthy and Laurenda Carter and S{\'e}amus Fanning and Carol Iversen and Franco Pagotto and Roger Stephan and Angelika Lehner and Jeffery Farber and Yan, {Qiong Q.} and Gopinath, {Gopal R.}",

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: Boram Lee, Eunbi Park, Hyerim Choi, JiHyeon Park, Seungeun Jeong, and YeonJoo Yoo, TaeJung Chung, SoYoung Jun, and Mijeong Kim, respectively. We thank the Office of Undergraduate Research and Internship Programs, the Joint institute of Food Safety and Applied Nutrition, University of Maryland, College Park, MD, for sponsoring student interns Hannah R. Chase, Flavia Negrete, and Samantha Finkelstein. Lastly, we thank the Oak Ridge Institute for Science and Education of Oak Ridge, Tennessee, for sponsoring research fellow Hannah. R. Chase. Funds supporting this work were obtained internally through U.S. FDA appropriations. Publisher Copyright: {\textcopyright} 2017 by the authors. Licensee MDPI, Basel, Switzerland.",

year = "2017",

month = mar,

day = "4",

doi = "10.3390/microarrays6010006",

language = "English",

volume = "6",

journal = "Microarrays",

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Tall, BD, Gangiredla, J, Grim, CJ, Patel, IR, Jackson, SA, Mammel, MK, Kothary, MH, Sathyamoorthy, V, Carter, L, Fanning, S, Iversen, C, Pagotto, F, Stephan, R, Lehner, A, Farber, J, Yan, QQ & Gopinath, GR 2017, 'Use of a Pan–Genomic DNA Microarray in Determination of the Phylogenetic Relatedness among Cronobacter spp. and Its Use as a Data Mining Tool to Understand Cronobacter Biology', Microarrays, vol. 6, no. 1, 6. https://doi.org/10.3390/microarrays6010006

TY - JOUR

T1 - Use of a Pan–Genomic DNA Microarray in Determination of the Phylogenetic Relatedness among Cronobacter spp. and Its Use as a Data Mining Tool to Understand Cronobacter Biology

AU - Tall, Ben D.

AU - Gangiredla, Jayanthi

AU - Grim, Christopher J.

AU - Patel, Isha R.

AU - Jackson, Scott A.

AU - Mammel, Mark K.

AU - Kothary, Mahendra H.

AU - Sathyamoorthy, Venugopal

AU - Carter, Laurenda

AU - Fanning, Séamus

AU - Iversen, Carol

AU - Pagotto, Franco

AU - Stephan, Roger

AU - Lehner, Angelika

AU - Farber, Jeffery

AU - Yan, Qiong Q.

AU - Gopinath, Gopal R.

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: Boram Lee, Eunbi Park, Hyerim Choi, JiHyeon Park, Seungeun Jeong, and YeonJoo Yoo, TaeJung Chung, SoYoung Jun, and Mijeong Kim, respectively. We thank the Office of Undergraduate Research and Internship Programs, the Joint institute of Food Safety and Applied Nutrition, University of Maryland, College Park, MD, for sponsoring student interns Hannah R. Chase, Flavia Negrete, and Samantha Finkelstein. Lastly, we thank the Oak Ridge Institute for Science and Education of Oak Ridge, Tennessee, for sponsoring research fellow Hannah. R. Chase. Funds supporting this work were obtained internally through U.S. FDA appropriations. Publisher Copyright: © 2017 by the authors. Licensee MDPI, Basel, Switzerland.

PY - 2017/3/4

Y1 - 2017/3/4

N2 - Cronobacter (previously known as Enterobacter sakazakii) is a genus of Gram-negative, facultatively anaerobic, oxidase-negative, catalase-positive, rod-shaped bacteria of the family Enterobacteriaceae. These organisms cause a variety of illnesses such as meningitis, necrotizing enterocolitis, and septicemia in neonates and infants, and urinary tract, wound, abscesses or surgical site infections, septicemia, and pneumonia in adults. The total gene content of 379 strains of Cronobacter spp. and taxonomically-related isolates was determined using a recently reported DNA microarray. The Cronobacter microarray as a genotyping tool gives the global food safety community a rapid method to identify and capture the total genomic content of outbreak isolates for food safety, environmental, and clinical surveillance purposes. It was able to differentiate the seven Cronobacter species from one another and from non-Cronobacter species. The microarray was also able to cluster strains within each species into well-defined subgroups. These results also support previous studies on the phylogenic separation of species members of the genus and clearly highlight the evolutionary sequence divergence among each species of the genus compared to phylogenetically-related species. This review extends these studies and illustrates how the microarray can also be used as an investigational tool to mine genomic data sets from strains. Three case studies describing the use of the microarray are shown and include: (1) the determination of allelic differences among Cronobacter sakazakii strains possessing the virulence plasmid pESA3; (2) mining of malonate and myo-inositol alleles among subspecies of Cronobacter dublinensis strains to determine subspecies identity; and (3) lastly using the microarray to demonstrate sequence divergence and phylogenetic relatedness trends for 13 outer-membrane protein alleles among 240 Cronobacter and phylogenetically-related strains. The goal of this review is to describe microarrays as a robust tool for genomics research of this assorted and important genus, a criterion toward the development of future preventative measures to eliminate this foodborne pathogen from the global food supply.

AB - Cronobacter (previously known as Enterobacter sakazakii) is a genus of Gram-negative, facultatively anaerobic, oxidase-negative, catalase-positive, rod-shaped bacteria of the family Enterobacteriaceae. These organisms cause a variety of illnesses such as meningitis, necrotizing enterocolitis, and septicemia in neonates and infants, and urinary tract, wound, abscesses or surgical site infections, septicemia, and pneumonia in adults. The total gene content of 379 strains of Cronobacter spp. and taxonomically-related isolates was determined using a recently reported DNA microarray. The Cronobacter microarray as a genotyping tool gives the global food safety community a rapid method to identify and capture the total genomic content of outbreak isolates for food safety, environmental, and clinical surveillance purposes. It was able to differentiate the seven Cronobacter species from one another and from non-Cronobacter species. The microarray was also able to cluster strains within each species into well-defined subgroups. These results also support previous studies on the phylogenic separation of species members of the genus and clearly highlight the evolutionary sequence divergence among each species of the genus compared to phylogenetically-related species. This review extends these studies and illustrates how the microarray can also be used as an investigational tool to mine genomic data sets from strains. Three case studies describing the use of the microarray are shown and include: (1) the determination of allelic differences among Cronobacter sakazakii strains possessing the virulence plasmid pESA3; (2) mining of malonate and myo-inositol alleles among subspecies of Cronobacter dublinensis strains to determine subspecies identity; and (3) lastly using the microarray to demonstrate sequence divergence and phylogenetic relatedness trends for 13 outer-membrane protein alleles among 240 Cronobacter and phylogenetically-related strains. The goal of this review is to describe microarrays as a robust tool for genomics research of this assorted and important genus, a criterion toward the development of future preventative measures to eliminate this foodborne pathogen from the global food supply.

KW - Cronobacter

KW - data mining

KW - microarray

U2 - 10.3390/microarrays6010006

DO - 10.3390/microarrays6010006

M3 - Review article

AN - SCOPUS:85025459302

SN - 2076-3905

VL - 6

JO - Microarrays

JF - Microarrays

IS - 1

M1 - 6

ER -

Use of a Pan–Genomic DNA Microarray in Determination of the Phylogenetic Relatedness among Cronobacter spp. and Its Use as a Data Mining Tool to Understand Cronobacter Biology

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

Access to Document

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Cite this