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1. Variability and bias in microbiome metagenomic sequencing: an interlaboratory study comparing experimental protocols

Author

Forry, Samuel P., Servetas, Stephanie L., Kralj, Jason G., Soh, Keng, Hadjithomas, Michalis, Cano, Raul, Carlin, Martha, Amorim, Maria G. de, Auch, Benjamin, Bakker, Matthew G., Bartelli, Thais F., Bustamante, Juan P., Cassol, Ignacio, Chalita, Mauricio, Dias-Neto, Emmanuel, Duca, Aaron Del, Gohl, Daryl M., Kazantseva, Jekaterina, Haruna, Muyideen T., Menzel, Peter, Moda, Bruno S., Neuberger-Castillo, Lorieza, Nunes, Diana N., Patel, Isha R., Peralta, Rodrigo D., Saliou, Adrien, Schwarzer, Rolf, Sevilla, Samantha, Takenaka, Isabella K. T. M., Wang, Jeremy R., Knight, Rob, Gevers, Dirk, and Jackson, Scott A.

Published
2024
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4. Insular microbiogeography

Author

Kaufman, James H., Elkins, Christopher A., Davis, Matthew, Weis, Allison M, Huang, Bihua C., Mammel, Mark K, Patel, Isha R., Beck, Kristen L., Edlund, Stefan, Chambliss, David, Bianco, Simone, Kunitomi, Mark, and Weimer, Bart C.

Subjects
Quantitative Biology - Genomics, Quantitative Biology - Populations and Evolution
Abstract

The diversity revealed by large scale genomics in microbiology is calling into question long held beliefs about genome stability, evolutionary rate, even the definition of a species. MacArthur and Wilson's theory of insular biogeography provides an explanation for the diversity of macroscopic animal and plant species as a consequence of the associated hierarchical web of species interdependence. We report a large scale study of microbial diversity that reveals that the cumulative number of genes discovered increases with the number of genomes studied as a simple power law. This result is demonstrated for three different genera comparing over 15,000 isolates. We show that this power law is formally related to the MacArthur-Wilson exponent, suggesting the emerging diversity of microbial genotypes arises because the scale independent behavior first reported by MacArthur and Wilson extends down to the scale of microbes and their genes. Assessing the depth of available whole genome sequences implies a dynamically changing core genome, suggesting that traditional taxonomic classifications should be replaced with a quasispecies model that captures the diversity and dynamic exchange of genes. We report Species population "clouds" in a defined microbiome, with scale invariance extending down to the level of single-nucleotide polymorphisms (SNPs)., Comment: 23 pages, 7 figures, including Appendices

Published
2017

7. CronobacterSpecies

Author

Tall, Ben D., primary, Gopinath, Gopal, additional, Gangiredla, Jayanthi, additional, Patel, Isha R., additional, Fanning, Séamus, additional, and Lehner, Angelika, additional

Published
2019
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9. Insular Microbiogeography: Three Pathogens as Exemplars

Author

Kaufman, James H., primary, Elkins, Christopher A., additional, Davis, Matthew, additional, Weis, Allison M., additional, Huang, Bihua C., additional, Mammel, Mark K., additional, Patel, Isha R., additional, Beck, Kristen L., additional, Edlund, Stefan, additional, Chambliss, David, additional, Douglas, Judith, additional, Bianco, Simone, additional, Kunitomi, Mark, additional, and Weimer, Bart C., additional

Published
2019
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12. Characterization of Cronobacter sakazakii Strains Originating from Plant-Origin Foods Using Comparative Genomic Analyses and Zebrafish Infectivity Studies

Author

Jang, Hyein, Eshwar, Athmanya, Lehner, Angelika, Gangiredla, Jayanthi, Patel, Isha R, Beaubrun, Junia Jean-Gilles, Chase, Hannah R, Negrete, Flavia, Finkelstein, Samantha, Weinstein, Leah M, Ko, Katie, Addy, Nicole, Ewing, Laura, Woo, Jungha, Lee, Youyoung, Seo, Kunho, Jaradat, Ziad, Srikumar, Shabarinath, Fanning, Séamus, Stephan, Roger, Tall, Ben D, Gopinath, Gopal R, University of Zurich, Tall, Ben D, and Gopinath, Gopal R

Subjects
Microbiology (medical), Virology, 2404 Microbiology, 2406 Virology, 570 Life sciences, biology, 610 Medicine & health, Cronobacter sakazakii, whole genome sequencing (WGS), draft genomes, dried foods, plant-origin foods, Microbiology, 10082 Institute of Food Safety and Hygiene, 2726 Microbiology (medical)
Abstract

Cronobacter sakazakii continues to be isolated from ready-to-eat fresh and frozen produce, flours, dairy powders, cereals, nuts, and spices, in addition to the conventional sources of powdered infant formulae (PIF) and PIF production environments. To understand the sequence diversity, phylogenetic relationship, and virulence of C. sakazakii originating from plant-origin foods, comparative molecular and genomic analyses, and zebrafish infection (ZI) studies were applied to 88 strains. Whole genome sequences of the strains were generated for detailed bioinformatic analysis. PCR analysis showed that all strains possessed a pESA3-like virulence plasmid similar to reference C. sakazakii clinical strain BAA-894. Core genome analysis confirmed a shared genomic backbone with other C. sakazakii strains from food, clinical and environmental strains. Emerging nucleotide diversity in these plant-origin strains was highlighted using single nucleotide polymorphic alleles in 2000 core genes. DNA hybridization analyses using a pan-genomic microarray showed that these strains clustered according to sequence types (STs) identified by multi-locus sequence typing (MLST). PHASTER analysis identified 185 intact prophage gene clusters encompassing 22 different prophages, including three intact Cronobacter prophages: ENT47670, ENT39118, and phiES15. AMRFinderPlus analysis identified the CSA family class C β-lactamase gene in all strains and a plasmid-borne mcr-9.1 gene was identified in three strains. ZI studies showed that some plant-origin C. sakazakii display virulence comparable to clinical strains. Finding virulent plant-origin C. sakazakii possessing significant genomic features of clinically relevant STs suggests that these foods can serve as potential transmission vehicles and supports widening the scope of continued surveillance for this important foodborne pathogen.

Published
2022
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13. Phylogenomic Analysis of Salmonella enterica subsp. enterica Serovar Bovismorbificans from Clinical and Food Samples Using Whole Genome Wide Core Genes and kmer Binning Methods to Identify Two Distinct Polyphyletic Genome Pathotypes

Author

Gopinath, Gopal R., primary, Jang, Hyein, additional, Beaubrun, Junia Jean-Gilles, additional, Gangiredla, Jayanthi, additional, Mammel, Mark K., additional, Müller, Andrea, additional, Tamber, Sandeep, additional, Patel, Isha R., additional, Ewing, Laura, additional, Weinstein, Leah M., additional, Wang, Caroline Z., additional, Finkelstein, Samantha, additional, Negrete, Flavia, additional, Muruvanda, Tim, additional, Allard, Marc, additional, Sockett, Donald C., additional, Pagotto, Franco, additional, Tall, Ben D., additional, and Stephan, Roger, additional

Published
2022
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14. Phylogenomic Analysis of Salmonella enterica subsp. enterica Serovar Bovismorbificans from Clinical and Food Samples Using Whole Genome Wide Core Genes and kmer Binning Methods to Identify Two Distinct Polyphyletic Genome Pathotypes

Author

Gopinath, Gopal R; https://orcid.org/0000-0003-2577-7548, Jang, Hyein, Beaubrun, Junia Jean-Gilles, Gangiredla, Jayanthi, Mammel, Mark K, Müller, Andrea, Tamber, Sandeep, Patel, Isha R, Ewing, Laura, Weinstein, Leah M, Wang, Caroline Z, Finkelstein, Samantha, Negrete, Flavia, Muruvanda, Tim, Allard, Marc, Sockett, Donald C, Pagotto, Franco, Tall, Ben D, Stephan, Roger; https://orcid.org/0000-0003-1002-4762, Gopinath, Gopal R; https://orcid.org/0000-0003-2577-7548, Jang, Hyein, Beaubrun, Junia Jean-Gilles, Gangiredla, Jayanthi, Mammel, Mark K, Müller, Andrea, Tamber, Sandeep, Patel, Isha R, Ewing, Laura, Weinstein, Leah M, Wang, Caroline Z, Finkelstein, Samantha, Negrete, Flavia, Muruvanda, Tim, Allard, Marc, Sockett, Donald C, Pagotto, Franco, Tall, Ben D, and Stephan, Roger; https://orcid.org/0000-0003-1002-4762

Abstract

Salmonella enterica subsp. enterica serovar Bovismorbificans has caused multiple outbreaks involving the consumption of produce, hummus, and processed meat products worldwide. To elucidate the intra-serovar genomic structure of S. Bovismorbificans, a core-genome analysis with 2690 loci (based on 150 complete genomes representing Salmonella enterica serovars developed as part of this study) and a k-mer-binning based strategy were carried out on 95 whole genome sequencing (WGS) assemblies from Swiss, Canadian, and USA collections of S. Bovismorbificans strains from foodborne infections. Data mining of a digital DNA tiling array of legacy SARA and SARB strains was conducted to identify near-neighbors of S. Bovismorbificans. The core genome analysis and the k-mer-binning methods identified two polyphyletic clusters, each with emerging evolutionary properties. Four STs (2640, 142, 1499, and 377), which constituted the majority of the publicly available WGS datasets from >260 strains analyzed by k-mer-binning based strategy, contained a conserved core genome backbone with a different evolutionary lineage as compared to strains comprising the other cluster (ST150). In addition, the assortment of genotypic features contributing to pathogenesis and persistence, such as antimicrobial resistance, prophage, plasmid, and virulence factor genes, were assessed to understand the emerging characteristics of this serovar that are relevant clinically and for food safety concerns. The phylogenomic profiling of polyphyletic S. Bovismorbificans in this study corresponds to intra-serovar variations observed in S. Napoli and S. Newport serovars using similar high-resolution genomic profiling approaches and contributes to the understanding of the evolution and sequence divergence of foodborne Salmonellae. These intra-serovar differences may have to be thoroughly understood for the accurate classification of foodborne Salmonella strains needed for the uniform development of future food safet

Published
2022

16. An FDA bioinformatics tool for microbial genomics research on molecular characterization of bacterial foodborne pathogens using microarrays

Author

Turner Steve, Ye Yanbin, Su Zhenqiang, Chen James, Foley Steven, Nayak Rajesh, Zou Wen, Frye Jonathan G, Patel Isha R, Jackson Scott A, Ding Don, Xu Joshua, Fang Hong, Harris Steve, Zhou Guangxu, Cerniglia Carl, and Tong Weida

Subjects
Computer applications to medicine. Medical informatics, R858-859.7, Biology (General), QH301-705.5
Abstract

Abstract Background Advances in microbial genomics and bioinformatics are offering greater insights into the emergence and spread of foodborne pathogens in outbreak scenarios. The Food and Drug Administration (FDA) has developed a genomics tool, ArrayTrackTM, which provides extensive functionalities to manage, analyze, and interpret genomic data for mammalian species. ArrayTrackTM has been widely adopted by the research community and used for pharmacogenomics data review in the FDA’s Voluntary Genomics Data Submission program. Results ArrayTrackTM has been extended to manage and analyze genomics data from bacterial pathogens of human, animal, and food origin. It was populated with bioinformatics data from public databases such as NCBI, Swiss-Prot, KEGG Pathway, and Gene Ontology to facilitate pathogen detection and characterization. ArrayTrackTM’s data processing and visualization tools were enhanced with analysis capabilities designed specifically for microbial genomics including flag-based hierarchical clustering analysis (HCA), flag concordance heat maps, and mixed scatter plots. These specific functionalities were evaluated on data generated from a custom Affymetrix array (FDA-ECSG) previously developed within the FDA. The FDA-ECSG array represents 32 complete genomes of Escherichia coli and Shigella. The new functions were also used to analyze microarray data focusing on antimicrobial resistance genes from Salmonella isolates in a poultry production environment using a universal antimicrobial resistance microarray developed by the United States Department of Agriculture (USDA). Conclusion The application of ArrayTrackTM to different microarray platforms demonstrates its utility in microbial genomics research, and thus will improve the capabilities of the FDA to rapidly identify foodborne bacteria and their genetic traits (e.g., antimicrobial resistance, virulence, etc.) during outbreak investigations. ArrayTrackTM is free to use and available to public, private, and academic researchers at http://www.fda.gov/ArrayTrack.

Published
2010
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17. Analysis of the Molecular Diversity Among Cronobacter Species Isolated From Filth Flies Using Targeted PCR, Pan Genomic DNA Microarray, and Whole Genome Sequencing Analyses

Author

Jang, Hyein, primary, Chase, Hannah R., additional, Gangiredla, Jayanthi, additional, Grim, Christopher J., additional, Patel, Isha R., additional, Kothary, Mahendra H., additional, Jackson, Scott A., additional, Mammel, Mark K., additional, Carter, Laurenda, additional, Negrete, Flavia, additional, Finkelstein, Samantha, additional, Weinstein, Leah, additional, Yan, QiongQiong, additional, Iversen, Carol, additional, Pagotto, Franco, additional, Stephan, Roger, additional, Lehner, Angelika, additional, Eshwar, Athmanya K., additional, Fanning, Seamus, additional, Farber, Jeffery, additional, Gopinath, Gopal R., additional, Tall, Ben D., additional, and Pava-Ripoll, Monica, additional

Published
2020
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18. The Secretion of Toxins and Other Exoproteins of Cronobacter: Role in Virulence, Adaption, and Persistence

Author

Jang, Hyein, primary, Gopinath, Gopal R., additional, Eshwar, Athmanya, additional, Srikumar, Shabarinath, additional, Nguyen, Scott, additional, Gangiredla, Jayanthi, additional, Patel, Isha R., additional, Finkelstein, Samantha B., additional, Negrete, Flavia, additional, Woo, JungHa, additional, Lee, YouYoung, additional, Fanning, Séamus, additional, Stephan, Roger, additional, Tall, Ben D., additional, and Lehner, Angelika, additional

Published
2020
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19. Cronobacter Species

Author

Tall, Ben D, Gopinath, Gopal, Gangiredla, Jayanthi, Patel, Isha R, Fanning, Séamus, Lehner, Angelika, University of Zurich, Doyle, MP, Diez-Gonzales, R, Hill, C, and Tall, Ben D

Subjects
2404 Microbiology, 2406 Virology, 570 Life sciences, biology, 610 Medicine & health, 10082 Institute of Food Safety and Hygiene, 2726 Microbiology (medical)
Published
2019
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20. The secretion of toxins and other exoproteins of cronobacter: role in virulence, adaption, and persistence

Author

Jang, Hyein, Gopinath, Gopal R, Eshwar, Athmanya, Srikumar, Shabarinath, Nguyen, Scott, Gangiredla, Jayanthi, Patel, Isha R, Finkelstein, Samantha B, Negrete, Flavia, Woo, JungHa, Lee, YouYoung, Fanning, Séamus; https://orcid.org/0000-0002-1922-8836, Stephan, Roger; https://orcid.org/0000-0003-1002-4762, Tall, Ben D; https://orcid.org/0000-0003-0399-3629, Lehner, Angelika; https://orcid.org/0000-0003-1863-5090, Jang, Hyein, Gopinath, Gopal R, Eshwar, Athmanya, Srikumar, Shabarinath, Nguyen, Scott, Gangiredla, Jayanthi, Patel, Isha R, Finkelstein, Samantha B, Negrete, Flavia, Woo, JungHa, Lee, YouYoung, Fanning, Séamus; https://orcid.org/0000-0002-1922-8836, Stephan, Roger; https://orcid.org/0000-0003-1002-4762, Tall, Ben D; https://orcid.org/0000-0003-0399-3629, and Lehner, Angelika; https://orcid.org/0000-0003-1863-5090

Abstract

Cronobacter species are considered an opportunistic group of foodborne pathogenic bacteria capable of causing both intestinal and systemic human disease. This review describes common virulence themes shared among the seven Cronobacter species and describes multiple exoproteins secreted by Cronobacter, many of which are bacterial toxins that may play a role in human disease. The review will particularly concentrate on the virulence factors secreted by C. sakazakii, C. malonaticus, and C. turicensis, which are the primary human pathogens of interest. It has been discovered that various species-specific virulence factors adversely affect a wide range of eukaryotic cell processes including protein synthesis, cell division, and ion secretion. Many of these factors are toxins which have been shown to also modulate the host immune response. These factors are encoded on a variety of mobile genetic elements such as plasmids and transposons; this genomic plasticity implies ongoing re-assortment of virulence factor genes which has complicated our efforts to categorize Cronobacter into sharply defined genomic pathotypes.

Published
2020

21. Analysis of the molecular diversity among cronobacter species isolated from filth flies using targeted PCR, pan genomic DNA microarray, and whole Genome sequencing analyses

Author

Jang, Hyein, Chase, Hannah R, Gangiredla, Jayanthi, Grim, Christopher J, Patel, Isha R, Kothary, Mahendra H, Jackson, Scott A, Mammel, Mark K, Carter, Laurenda, Negrete, Flavia, Finkelstein, Samantha, Weinstein, Leah, Yan, QiongQiong, Iversen, Carol, Pagotto, Franco, Stephan, Roger; https://orcid.org/0000-0003-1002-4762, Lehner, Angelika; https://orcid.org/0000-0003-1863-5090, Eshwar, Athmanya K, Fanning, Séamus; https://orcid.org/0000-0002-1922-8836, Farber, Jeffery, Gopinath, Gopal R, Tall, Ben D, Pava-Ripoll, Monica, Jang, Hyein, Chase, Hannah R, Gangiredla, Jayanthi, Grim, Christopher J, Patel, Isha R, Kothary, Mahendra H, Jackson, Scott A, Mammel, Mark K, Carter, Laurenda, Negrete, Flavia, Finkelstein, Samantha, Weinstein, Leah, Yan, QiongQiong, Iversen, Carol, Pagotto, Franco, Stephan, Roger; https://orcid.org/0000-0003-1002-4762, Lehner, Angelika; https://orcid.org/0000-0003-1863-5090, Eshwar, Athmanya K, Fanning, Séamus; https://orcid.org/0000-0002-1922-8836, Farber, Jeffery, Gopinath, Gopal R, Tall, Ben D, and Pava-Ripoll, Monica

Abstract

Cronobacter species are opportunistic pathogens capable of causing life-threatening infections in humans, with serious complications arising in neonates, infants, immuno-compromised individuals, and elderly adults. The genus is comprised of seven species: Cronobacter sakazakii, Cronobacter malonaticus, Cronobacter turicensis, Cronobacter muytjensii, Cronobacter dublinensis, Cronobacter universalis, and Cronobacter condimenti. Despite a multiplicity of genomic data for the genus, little is known about likely transmission vectors. Using DNA microarray analysis, in parallel with whole genome sequencing, and targeted PCR analyses, the total gene content of two C. malonaticus, three C. turicensis, and 14 C. sakazaki isolated from various filth flies was assessed. Phylogenetic relatedness among these and other strains obtained during surveillance and outbreak investigations were comparatively assessed. Specifically, microarray analysis (MA) demonstrated its utility to cluster strains according to species-specific and sequence type (ST) phylogenetic relatedness, and that the fly strains clustered among strains obtained from clinical, food and environmental sources from United States, Europe, and Southeast Asia. This combinatorial approach was useful in data mining for virulence factor genes, and phage genes and gene clusters. In addition, results of plasmidotyping were in agreement with the species identity for each strain as determined by species-specific PCR assays, MA, and whole genome sequencing. Microarray and BLAST analyses of Cronobacter fly sequence datasets were corroborative and showed that the presence and absence of virulence factors followed species and ST evolutionary lines even though such genes were orthologous. Additionally, zebrafish infectivity studies showed that these pathotypes were as virulent to zebrafish embryos as other clinical strains. In summary, these findings support a striking phylogeny amongst fly, clinical, and surveillance strains isolate

Published
2020

23. Insular Microbiogeography: Three Pathogens as Exemplars

Author

Kaufman, James H., primary, Elkins, Christopher A., additional, Davis, Matthew, additional, Weis, Allison M., additional, Huang, Bihua C., additional, Mammel, Mark K., additional, Patel, Isha R., additional, Beck, Kristen L., additional, Edlund, Stefan, additional, Chambliss, David, additional, Douglas, Judith, additional, Bianco, Simone, additional, Kunitomi, Mark, additional, and Weimer, Bart C., additional

Published
2020
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24. Prevalence, Distribution, and Phylogeny of Type Two Toxin-Antitoxin Genes Possessed by Cronobacter Species where C. sakazakii Homologs Follow Sequence Type Lineages

Author

Finkelstein, Samantha, primary, Negrete, Flavia, additional, Jang, Hyein, additional, Gangiredla, Jayanthi, additional, Mammel, Mark, additional, Patel, Isha R., additional, Chase, Hannah R., additional, Woo, JungHa, additional, Lee, YouYoung, additional, Wang, Caroline Z., additional, Weinstein, Leah, additional, Tall, Ben D., additional, and Gopinath, Gopal R., additional

Published
2019
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25. Investigating the global genomic diversity of Escherichia coli using a multi-genome DNA microarray platform with novel gene prediction strategies

Author

LeClerc Joseph E, Barnaba Tammy, Patel Isha R, Jackson Scott A, and Cebula Thomas A

Subjects
genome, diversity, microarray, Escherichia coli, Shigella, O157:H7, gene content, pathogenic determinants, Biotechnology, TP248.13-248.65, Genetics, QH426-470
Abstract

Abstract Background The gene content of a diverse group of 183 unique Escherichia coli and Shigella isolates was determined using the Affymetrix GeneChip® E. coli Genome 2.0 Array, originally designed for transcriptome analysis, as a genotyping tool. The probe set design utilized by this array provided the opportunity to determine the gene content of each strain very accurately and reliably. This array constitutes 10,112 independent genes representing four individual E. coli genomes, therefore providing the ability to survey genes of several different pathogen types. The entire ECOR collection, 80 EHEC-like isolates, and a diverse set of isolates from our FDA strain repository were included in our analysis. Results From this study we were able to define sets of genes that correspond to, and therefore define, the EHEC pathogen type. Furthermore, our sampling of 63 unique strains of O157:H7 showed the ability of this array to discriminate between closely related strains. We found that individual strains of O157:H7 differed, on average, by 197 probe sets. Finally, we describe an analysis method that utilizes the power of the probe sets to determine accurately the presence/absence of each gene represented on this array. Conclusions These elements provide insights into understanding the microbial diversity that exists within extant E. coli populations. Moreover, these data demonstrate that this novel microarray-based analysis is a powerful tool in the field of molecular epidemiology and the newly emerging field of microbial forensics.

Published
2011
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26. Cronobacter Species

Author

Doyle, MP, Diez-Gonzales, R, Hill, C, Doyle, M ( MP ), Diez-Gonzales, R ( R ), Hill, C ( C ), Tall, Ben D, Gopinath, Gopal, Gangiredla, Jayanthi, Patel, Isha R, Fanning, Séamus, Lehner, Angelika, Doyle, MP, Diez-Gonzales, R, Hill, C, Doyle, M ( MP ), Diez-Gonzales, R ( R ), Hill, C ( C ), Tall, Ben D, Gopinath, Gopal, Gangiredla, Jayanthi, Patel, Isha R, Fanning, Séamus, and Lehner, Angelika

Published
2019

29. Interlaboratory Evaluation of the U.S. Food and Drug Administration Escherichia coli Identification Microarray for Profiling Shiga Toxin–Producing Escherichia coli

Author

Patel, Isha R., primary, Gangiredla, Jayanthi, additional, Lacher, David W., additional, Mammel, Mark K., additional, Bagi, Lori, additional, Baranzoni, Gian Marco, additional, Fratamico, Pina M., additional, Roberts, Elizabeth L., additional, DebRoy, Chitrita, additional, Lindsey, Rebecca L., additional, V. Stoneburg, Devon, additional, Martin, Haley, additional, Smith, Peyton, additional, Strockbine, Nancy A., additional, Elkins, Christopher A., additional, Scheutz, Flemming, additional, and Feng, Peter C.H., additional

Published
2018
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30. Draft Genome Sequences of Escherichia albertii, Escherichia fergusonii, and Strains Belonging to Six Cryptic Lineages of Escherichia spp

Author

Gangiredla, Jayanthi, primary, Mammel, Mark K., additional, Barnaba, Tammy J., additional, Tartera, Carmen, additional, Gebru, Solomon T., additional, Patel, Isha R., additional, Leonard, Susan R., additional, Kotewicz, Michael L., additional, Lampel, Keith A., additional, Elkins, Christopher A., additional, and Lacher, David W., additional

Published
2018
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36. Comparative Genomic Characterization of the Highly Persistent and Potentially Virulent Cronobacter sakazakii ST83, CC65 Strain H322 and Other ST83 Strains

Author

Chase, Hannah R., primary, Gopinath, Gopal R., additional, Eshwar, Athmanya K., additional, Stoller, Andrea, additional, Fricker-Feer, Claudia, additional, Gangiredla, Jayanthi, additional, Patel, Isha R., additional, Cinar, Hediye N., additional, Jeong, HyeJin, additional, Lee, ChaeYoon, additional, Negrete, Flavia, additional, Finkelstein, Samantha, additional, Stephan, Roger, additional, Tall, Ben D., additional, and Lehner, Angelika, additional

Published
2017
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37. Analysis and Characterization of Proteins Associated with Outer Membrane Vesicles Secreted by Cronobacter spp.

Author

Kothary, Mahendra H., primary, Gopinath, Gopal R., additional, Gangiredla, Jayanthi, additional, Rallabhandi, Prasad V., additional, Harrison, Lisa M., additional, Yan, Qiong Q., additional, Chase, Hannah R., additional, Lee, Boram, additional, Park, Eunbi, additional, Yoo, YeonJoo, additional, Chung, Taejung, additional, Finkelstein, Samantha B., additional, Negrete, Flavia J., additional, Patel, Isha R., additional, Carter, Laurenda, additional, Sathyamoorthy, Venugopal, additional, Fanning, Séamus, additional, and Tall, Ben D., additional

Published
2017
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38. DNA Microarray-Based Genomic Characterization of the Pathotypes of Escherichia coli O26, O45, O103, O111, and O145 Isolated from Feces of Feedlot Cattle.

Author

SHRIDHAR, PRAGATHI B., PATEL, ISHA R., GANGIREDLA, JAYANTHI, NOLL, LANCE W., XIAORONG SHI, JIANFA BAI, and NAGARAJA, T. G.

Abstract

Shiga toxin–producing Escherichia coli (STEC) serogroups O26, O45, O103, O111, O121, and O145, referred to as the top six non-O157 serogroups, are responsible for more than 70% of human non-O157 STEC infections in North America. Cattle harbor non-O157 strains in the hindgut and shed them in the feces. The objective of this study was to use the U.S. Food and Drug Administration (FDA) E. coli identification (ECID) DNA microarray to identify the serotype, assess the virulence potential of each, and determine the phylogenetic relationships among five of the six non-O157 E. coli serogroups isolated from feedlot cattle feces. Forty-four strains of STEC, enterohemorrhagic E. coli (EHEC), enteropathogenic E. coli (EPEC), or putative nonpathotype E. coli (NPEC) of cattle origin and five human clinical strains of EHEC were assayed with the FDA-ECID DNA microarray. The cattle strains harbored diverse flagellar genes. The bovine and human strains belonging to serogroups O26, O45, and O103 carried stx1 only, O111 carried both stx1 and stx2, and O145 carried either stx1 or stx2. The strains were also positive for various subtypes of intimin and other adhesins (IrgA homologue adhesin, long polar fimbriae, mannose-specific adhesin, and curli). Both human and cattle strains were positive for LEE-encoded type III secretory system genes and non–LEE-encoded effector genes. SplitsTree4, a program used to determine the phylogenetic relationship among the strains, revealed that the strains within each serogroup clustered according to their pathotype. In addition to genes encoding Shiga toxins, bovine non- O157 E. coli strains possessed other major virulence genes, including those for adhesins, type III secretory system proteins, and plasmid-borne virulence genes, similar to human clinical strains. Because virulence factors encoded by these genes are involved in the pathogenesis of various pathotypes of E. coli, the bovine non-O157 strains could cause human illness. The FDA-ECID DNA microarray assay rapidly provided a profile of the virulence genes for assessment of the virulence potential of each strain. [ABSTRACT FROM AUTHOR]

Published
2019
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40. Linking genomo- and pathotype: Exploiting the Zebrafish embryo model to investigate the divergent virulence potential among cronobacter spp

Author

Eshwar, Athmanya K, Tall, Ben D, Gangiredla, Jayanthi, Gopinath, Gopal R, Patel, Isha R, Neuhauss, Stephan C F; https://orcid.org/0000-0002-9615-480X, Stephan, Roger; https://orcid.org/0000-0003-1002-4762, Lehner, Angelika; https://orcid.org/0000-0003-1863-5090, Eshwar, Athmanya K, Tall, Ben D, Gangiredla, Jayanthi, Gopinath, Gopal R, Patel, Isha R, Neuhauss, Stephan C F; https://orcid.org/0000-0002-9615-480X, Stephan, Roger; https://orcid.org/0000-0003-1002-4762, and Lehner, Angelika; https://orcid.org/0000-0003-1863-5090

Abstract

Bacteria belonging to the genus Cronobacter have been recognized as causative agents of life-threatening systemic infections primarily in premature, low-birth weight and immune-compromised neonates. Apparently not all Cronobacter species are linked to infantile infections and it has been proposed that virulence varies among strains. Whole genome comparisons and in silico analysis have proven to be powerful tools in elucidating potential virulence determinants, the presence/absence of which may explain the differential virulence behaviour of strains. However, validation of these factors has in the past been hampered by the availability of a suitable neonatal animal model. In the present study we have used zebrafish embryos to model Cronobacter infections in vivo using wild type and genetically engineered strains. Our experiments confirmed the role of the RepF1B-like plasmids as "virulence plasmids" in Cronobacter and underpinned the importantce of two putative virulence factors-cpa and zpx-in in vivo pathogenesis. We propose that by using this model in vivo infection studies are now possible on a large scale level which will boost the understanding on the virulence strategies employed by these pathogens.

Published
2016

44. Genome-wide survey of efflux pump-coding genes associated with Cronobactersurvival, osmotic adaptation, and persistence

Author

Negrete, Flavia, Jang, Hyein, Gangiredla, Jayanthi, Woo, JungHa, Lee, YouYoung, Patel, Isha R, Chase, Hannah R, Finkelstein, Samantha, Wang, Caroline Z, Srikumar, Shabarinath, Nguyen, Scott, Eshwar, Athmanya, Stephan, Roger, Lehner, Angelika, Fanning, Séamus, Tall, Ben D, and Gopinath, Gopal R

Abstract

•Cronobacterspecies possess species-specific efflux pump orthologues.•For C. sakazakii,the acquisition of efflux pumps genes followed sequence type phylogeny.•Efflux pump genes were acquired through microevolution and/or horizontal gene transfer.•Efflux activity is important in osmotic adaptation, survival, and persistence of Cronobacterspecies.

Published
2019
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45. DNA Microarray-Based Genomic Characterization of the Pathotypes of Escherichia coliO26, O45, O103, O111, and O145 Isolated from Feces of Feedlot Cattle†

Author

Shridhar, Pragathi B., Patel, Isha R., Gangiredla, Jayanthi, Noll, Lance W., Shi, Xiaorong, Bai, Jianfa, and Nagaraja, T.G.

Abstract

Shiga toxin–producing Escherichia coli(STEC) serogroups O26, O45, O103, O111, O121, and O145, referred to as the top six non-O157 serogroups, are responsible for more than 70% of human non-O157 STEC infections in North America. Cattle harbor non-O157 strains in the hindgut and shed them in the feces. The objective of this study was to use the U.S. Food and Drug Administration (FDA) E. coliidentification (ECID) DNA microarray to identify the serotype, assess the virulence potential of each, and determine the phylogenetic relationships among five of the six non-O157 E. coliserogroups isolated from feedlot cattle feces. Forty-four strains of STEC, enterohemorrhagic E. coli(EHEC), enteropathogenic E. coli(EPEC), or putative nonpathotype E. coli(NPEC) of cattle origin and five human clinical strains of EHEC were assayed with the FDA-ECID DNA microarray. The cattle strains harbored diverse flagellar genes. The bovine and human strains belonging to serogroups O26, O45, and O103 carried stx1only, O111 carried both stx1and stx2, and O145 carried either stx1or stx2. The strains were also positive for various subtypes of intimin and other adhesins (IrgA homologue adhesin, long polar fimbriae, mannose-specific adhesin, and curli). Both human and cattle strains were positive for LEE-encoded type III secretory system genes and non–LEE-encoded effector genes. SplitsTree4, a program used to determine the phylogenetic relationship among the strains, revealed that the strains within each serogroup clustered according to their pathotype. In addition to genes encoding Shiga toxins, bovine non-O157 E. colistrains possessed other major virulence genes, including those for adhesins, type III secretory system proteins, and plasmid-borne virulence genes, similar to human clinical strains. Because virulence factors encoded by these genes are involved in the pathogenesis of various pathotypes of E. coli,the bovine non-O157 strains could cause human illness. The FDA-ECID DNA microarray assay rapidly provided a profile of the virulence genes for assessment of the virulence potential of each strain.

Published
2019
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46. Recent Advances in Molecular Technologies and Their Application in Pathogen Detection in Foods with Particular Reference to Yersinia

Author

Gui, Jin and Patel, Isha R.

Subjects
Article Subject
Abstract

Yersinia enterocolitica is an important zoonotic pathogen that can cause yersiniosis in humans and animals. Food has been suggested to be the main source of yersiniosis. It is critical for the researchers to be able to detect Yersinia or any other foodborne pathogen with increased sensitivity and specificity, as well as in real-time, in the case of a foodborne disease outbreak. Conventional detection methods are known to be labor intensive, time consuming, or expensive. On the other hand, more sensitive molecular-based detection methods like next generation sequencing, microarray, and many others are capable of providing faster results. DNA testing is now possible on a single molecule, and high-throughput analysis allows multiple detection reactions to be performed at once, thus allowing a range of characteristics to be rapidly and simultaneously determined. Despite better detection efficiencies, results derived using molecular biology methods can be affected by the various food matrixes. With the improvements in sample preparation, data analysis, and testing procedures, molecular detection techniques will likely continue to simplify and increase the speed of detection while simultaneously improving the sensitivity and specificity for tracking pathogens in food matrices.

Published
2011
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47. Development of a custom-designed, pan genomic DNA microarray to characterize strain-level diversity among Cronobacter spp

Author

Tall, Ben D; https://orcid.org/0000-0003-0399-3629, Gangiredla, Jayanthi, Gopinath, Gopal R, Yan, Q, Chase, Hannah R, Lee, Boram, Hwang, Seongeun, Trach, Larisa H, Park, Eunbi, Yoo, YeonJoo, Chung, Chung, Jackson, Scott A, Patel, Isha R, Sathyamoorthy, Venugopal, Pava-Ripoll, Monica, Kotewicz, M L, Carter, Laurenda, Iversen, Carol, Pagotto, Franco, Stephan, Roger; https://orcid.org/0000-0003-1002-4762, Lehner, Angelika; https://orcid.org/0000-0003-1863-5090, Grim, Christopher J, Tall, Ben D; https://orcid.org/0000-0003-0399-3629, Gangiredla, Jayanthi, Gopinath, Gopal R, Yan, Q, Chase, Hannah R, Lee, Boram, Hwang, Seongeun, Trach, Larisa H, Park, Eunbi, Yoo, YeonJoo, Chung, Chung, Jackson, Scott A, Patel, Isha R, Sathyamoorthy, Venugopal, Pava-Ripoll, Monica, Kotewicz, M L, Carter, Laurenda, Iversen, Carol, Pagotto, Franco, Stephan, Roger; https://orcid.org/0000-0003-1002-4762, Lehner, Angelika; https://orcid.org/0000-0003-1863-5090, and Grim, Christopher J

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

Published
2015

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

Author

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

Published
2015
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50. 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.

Author

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

Subjects
DNA microarrays, PHYLOGENY, CRONOBACTER
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. [ABSTRACT FROM AUTHOR]

Published
2017
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