Phylogenetic Analyses of Shigella and Enteroinvasive Escherichia coli for the Identification of Molecular Epidemiological Markers: Whole-Genome Comparative Analysis Does Not Support Distinct Genera Designation
Abstract
As a leading cause of bacterial dysentery, Shigella represents a significant threat to public health and food safety. Related, but often overlooked, enteroinvasive Escherichia coli (EIEC) can also cause dysentery. Current typing methods have limited ability to identify and differentiate between these pathogens despite the need for rapid and accurate identification of pathogens for clinical treatment and outbreak response. We present a comprehensive phylogeny of Shigella and EIEC using whole genome sequencing of 169 samples, constituting unparalleled strain diversity, and observe a lack of monophyly between Shigella and EIEC and among Shigella taxonomic groups. The evolutionary relationships in the phylogeny are supported by analyses of population structure and hierarchical clustering patterns of translated gene homolog abundance. Lastly, we identified a panel of 404 single nucleotide polymorphism (SNP) markers specific to each phylogenetic cluster for more accurate identification of Shigella and EIEC. Our findings show that Shigella and EIEC are not distinct evolutionary groups within the E. coli genus and, thus, EIEC as a group is not the ancestor to Shigella. The multiple analyses presented provide evidence for reconsidering the taxonomic placement of Shigella. The SNP markers offer more discriminatory power to molecular epidemiological typing methods involving these bacterial pathogens.
- Authors:
-
- U.S. Food and Drug Administration, College Park, MD (United States)
- Publication Date:
- Research Org.:
- U.S. Food and Drug Administration, Center for Food Safety and Applied Nutrition, College Park, MD (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1378565
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Frontiers in Microbiology
- Additional Journal Information:
- Journal Volume: 6; Journal ID: ISSN 1664-302X
- Publisher:
- Frontiers Research Foundation
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Shigella; enteroinvasive E. coli (EIEC); phylogeny; whole genome sequencing; classification; epidemiological markers
Citation Formats
Pettengill, Emily A., Pettengill, James B., and Binet, Rachel. Phylogenetic Analyses of Shigella and Enteroinvasive Escherichia coli for the Identification of Molecular Epidemiological Markers: Whole-Genome Comparative Analysis Does Not Support Distinct Genera Designation. United States: N. p., 2016.
Web. doi:10.3389/fmicb.2015.01573.
Pettengill, Emily A., Pettengill, James B., & Binet, Rachel. Phylogenetic Analyses of Shigella and Enteroinvasive Escherichia coli for the Identification of Molecular Epidemiological Markers: Whole-Genome Comparative Analysis Does Not Support Distinct Genera Designation. United States. https://doi.org/10.3389/fmicb.2015.01573
Pettengill, Emily A., Pettengill, James B., and Binet, Rachel. Tue .
"Phylogenetic Analyses of Shigella and Enteroinvasive Escherichia coli for the Identification of Molecular Epidemiological Markers: Whole-Genome Comparative Analysis Does Not Support Distinct Genera Designation". United States. https://doi.org/10.3389/fmicb.2015.01573. https://www.osti.gov/servlets/purl/1378565.
@article{osti_1378565,
title = {Phylogenetic Analyses of Shigella and Enteroinvasive Escherichia coli for the Identification of Molecular Epidemiological Markers: Whole-Genome Comparative Analysis Does Not Support Distinct Genera Designation},
author = {Pettengill, Emily A. and Pettengill, James B. and Binet, Rachel},
abstractNote = {As a leading cause of bacterial dysentery, Shigella represents a significant threat to public health and food safety. Related, but often overlooked, enteroinvasive Escherichia coli (EIEC) can also cause dysentery. Current typing methods have limited ability to identify and differentiate between these pathogens despite the need for rapid and accurate identification of pathogens for clinical treatment and outbreak response. We present a comprehensive phylogeny of Shigella and EIEC using whole genome sequencing of 169 samples, constituting unparalleled strain diversity, and observe a lack of monophyly between Shigella and EIEC and among Shigella taxonomic groups. The evolutionary relationships in the phylogeny are supported by analyses of population structure and hierarchical clustering patterns of translated gene homolog abundance. Lastly, we identified a panel of 404 single nucleotide polymorphism (SNP) markers specific to each phylogenetic cluster for more accurate identification of Shigella and EIEC. Our findings show that Shigella and EIEC are not distinct evolutionary groups within the E. coli genus and, thus, EIEC as a group is not the ancestor to Shigella. The multiple analyses presented provide evidence for reconsidering the taxonomic placement of Shigella. The SNP markers offer more discriminatory power to molecular epidemiological typing methods involving these bacterial pathogens.},
doi = {10.3389/fmicb.2015.01573},
journal = {Frontiers in Microbiology},
number = ,
volume = 6,
place = {United States},
year = {2016},
month = {1}
}
Web of Science
Works referenced in this record:
Molecular Evolutionary Relationships of Enteroinvasive Escherichia coli and Shigella spp.
journal, August 2004
- Lan, R.; Alles, M. C.; Donohoe, K.
- Infection and Immunity, Vol. 72, Issue 9
QUAST: quality assessment tool for genome assemblies
journal, February 2013
- Gurevich, Alexey; Saveliev, Vladislav; Vyahhi, Nikolay
- Bioinformatics, Vol. 29, Issue 8
SolexaQA: At-a-glance quality assessment of Illumina second-generation sequencing data
journal, September 2010
- Cox, Murray P.; Peterson, Daniel A.; Biggs, Patrick J.
- BMC Bioinformatics, Vol. 11, Issue 1
A phylogenomic analysis of Escherichia coli / Shigella group: implications of genomic features associated with pathogenicity and ecological adaptation
journal, January 2012
- Zhang, Yan; Lin, Kui
- BMC Evolutionary Biology, Vol. 12, Issue 1
Evolutionary Genetics of a New Pathogenic Escherichia Species: Escherichia albertii and Related Shigella boydii Strains
journal, January 2005
- Hyma, K. E.; Lacher, D. W.; Nelson, A. M.
- Journal of Bacteriology, Vol. 187, Issue 2
A Specific Genetic Background Is Required for Acquisition and Expression of Virulence Factors in Escherichia coli
journal, June 2004
- Escobar-Páramo, Patricia; Clermont, Olivier; Blanc-Potard, Anne-Béatrice
- Molecular Biology and Evolution, Vol. 21, Issue 6
Pvclust: an R package for assessing the uncertainty in hierarchical clustering
journal, April 2006
- Suzuki, R.; Shimodaira, H.
- Bioinformatics, Vol. 22, Issue 12
Infection strategies of enteric pathogenic Escherichia coli
journal, March 2012
- Clements, Abigail; Young, Joanna C.; Constantinou, Nicholas
- Gut Microbes, Vol. 3, Issue 2
The Comprehensive Antibiotic Resistance Database
journal, May 2013
- McArthur, Andrew G.; Waglechner, Nicholas; Nizam, Fazmin
- Antimicrobial Agents and Chemotherapy, Vol. 57, Issue 7
Characterization of an emergent clone of enteroinvasive Escherichia coli circulating in Europe
journal, March 2016
- Michelacci, V.; Prosseda, G.; Maugliani, A.
- Clinical Microbiology and Infection, Vol. 22, Issue 3
Genomic analysis of the emergence of 20th century epidemic dysentery
journal, January 2014
- Rohmer, Laurence; Jacobs, Michael A.; Brittnacher, Mitchell J.
- BMC Genomics, Vol. 15, Issue 1
Organised Genome Dynamics in the Escherichia coli Species Results in Highly Diverse Adaptive Paths
journal, January 2009
- Touchon, Marie; Hoede, Claire; Tenaillon, Olivier
- PLoS Genetics, Vol. 5, Issue 1
GET_HOMOLOGUES, a Versatile Software Package for Scalable and Robust Microbial Pangenome Analysis
journal, October 2013
- Contreras-Moreira, Bruno; Vinuesa, Pablo
- Applied and Environmental Microbiology, Vol. 79, Issue 24
distruct: a program for the graphical display of population structure: PROGRAM NOTE
journal, December 2003
- Rosenberg, Noah A.
- Molecular Ecology Notes, Vol. 4, Issue 1
A severe foodborne outbreak of diarrhoea linked to a canteen in Italy caused by enteroinvasive Escherichia coli , an uncommon agent
journal, February 2014
- Escher, M.; Scavia, G.; Morabito, S.
- Epidemiology and Infection, Vol. 142, Issue 12
Detecting the number of clusters of individuals using the software structure: a simulation study
journal, July 2005
- Evanno, G.; Regnaut, S.; Goudet, J.
- Molecular Ecology, Vol. 14, Issue 8
When Whole-Genome Alignments Just Won't Work: kSNP v2 Software for Alignment-Free SNP Discovery and Phylogenetics of Hundreds of Microbial Genomes
journal, December 2013
- Gardner, Shea N.; Hall, Barry G.
- PLoS ONE, Vol. 8, Issue 12
Past and future species definitions for Bacteria and Archaea
journal, June 2015
- Rosselló-Móra, Ramon; Amann, Rudolf
- Systematic and Applied Microbiology, Vol. 38, Issue 4
Rapid detection of Shigella and enteroinvasive Escherichia coli in produce enrichments by a conventional multiplex PCR assay
journal, June 2014
- Binet, Rachel; Deer, Deanne M.; Uhlfelder, Samantha J.
- Food Microbiology, Vol. 40
DendroPy: a Python library for phylogenetic computing
journal, April 2010
- Sukumaran, J.; Holder, M. T.
- Bioinformatics, Vol. 26, Issue 12
Microbial species delineation using whole genome sequences
journal, July 2015
- Varghese, Neha J.; Mukherjee, Supratim; Ivanova, Natalia
- Nucleic Acids Research, Vol. 43, Issue 14
Shigella Strains Are Not Clones of Escherichia coli but Sister Species in the Genus Escherichia
journal, February 2013
- Zuo, Guanghong; Xu, Zhao; Hao, Bailin
- Genomics, Proteomics & Bioinformatics, Vol. 11, Issue 1
STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method
journal, October 2011
- Earl, Dent A.; vonHoldt, Bridgett M.
- Conservation Genetics Resources, Vol. 4, Issue 2
Advances in Rapid Detection Methods for Foodborne Pathogens
journal, March 2014
- Zhao, Xihong; Lin, Chii-Wann; Wang, Jun
- Journal of Microbiology and Biotechnology, Vol. 24, Issue 3
The evolution of the Escherichia coli phylogeny
journal, March 2012
- Chaudhuri, Roy R.; Henderson, Ian R.
- Infection, Genetics and Evolution, Vol. 12, Issue 2
Structure and genetics of Shigella O antigens
journal, July 2008
- Liu, Bin; Knirel, Yuriy A.; Feng, Lu
- FEMS Microbiology Reviews, Vol. 32, Issue 4
Development of a duplex real-time PCR for differentiation between E. coli and Shigella spp.: Shigella-E. coli differentiation PCR
journal, March 2011
- Pavlovic, M.; Luze, A.; Konrad, R.
- Journal of Applied Microbiology, Vol. 110, Issue 5
Similarity-Based Codes Sequentially Assigned to Ebolavirus Genomes Are Informative of Species Membership, Associated Outbreaks, and Transmission Chains
journal, January 2015
- Weisberg, Alexandra J.; Elmarakeby, Haitham A.; Heath, Lenwood S.
- Open Forum Infectious Diseases, Vol. 2, Issue 1
The large-scale blast score ratio (LS-BSR) pipeline: a method to rapidly compare genetic content between bacterial genomes
journal, January 2014
- Sahl, Jason W.; Caporaso, J. Gregory; Rasko, David A.
- PeerJ, Vol. 2
CanSNPer: a hierarchical genotype classifier of clonal pathogens
journal, February 2014
- Larkeryd, A.; Myrtennas, K.; Karlsson, E.
- Bioinformatics, Vol. 30, Issue 12
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing
journal, May 2012
- Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry
- Journal of Computational Biology, Vol. 19, Issue 5
Escherichia coli in disguise: molecular origins of Shigella
journal, September 2002
- Lan, Ruiting; Reeves, Peter R.
- Microbes and Infection, Vol. 4, Issue 11
Pathogenesis of Escherichia coli Diarrhea
journal, July 1971
- DuPont, Herbert L.; Formal, Samuel B.; Hornick, Richard B.
- New England Journal of Medicine, Vol. 285, Issue 1
Bacterial Phylogenetic Reconstruction from Whole Genomes Is Robust to Recombination but Demographic Inference Is Not
journal, November 2014
- Hedge, Jessica; Wilson, Daniel J.
- mBio, Vol. 5, Issue 6
The Evolutionary History of Shigella and Enteroinvasive Escherichia coli Revised
journal, August 2003
- Escobar-P�ramo, Patricia; Giudicelli, Catherine; Parsot, Claude
- Journal of Molecular Evolution, Vol. 57, Issue 2
Complete Genome Sequence of Enteroinvasive Escherichia coli O96:H19 Associated with a Severe Foodborne Outbreak
journal, August 2015
- Pettengill, Emily A.; Hoffmann, Maria; Binet, Rachel
- Genome Announcements, Vol. 3, Issue 4
Whole-genome phylogeny of Escherichia coli/Shigella group by feature frequency profiles (FFPs)
journal, May 2011
- Sims, G. E.; Kim, S. -H.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 20
Multiple independent origins of Shigella clones of Escherichia coli and convergent evolution of many of their characteristics
journal, August 2000
- Pupo, G. M.; Lan, R.; Reeves, P. R.
- Proceedings of the National Academy of Sciences, Vol. 97, Issue 19
A System to Automatically Classify and Name Any Individual Genome-Sequenced Organism Independently of Current Biological Classification and Nomenclature
journal, February 2014
- Marakeby, Haitham; Badr, Eman; Torkey, Hanaa
- PLoS ONE, Vol. 9, Issue 2
The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST)
journal, November 2013
- Overbeek, Ross; Olson, Robert; Pusch, Gordon D.
- Nucleic Acids Research, Vol. 42, Issue D1
Etiology of Diarrhea in Older Children, Adolescents and Adults: A Systematic Review
journal, August 2010
- Fischer Walker, Christa L.; Sack, David; Black, Robert E.
- PLoS Neglected Tropical Diseases, Vol. 4, Issue 8
The Inference of Gene Trees with Species Trees
journal, July 2014
- Szöllősi, Gergely J.; Tannier, Eric; Daubin, Vincent
- Systematic Biology, Vol. 64, Issue 1
Shigella sonnei genome sequencing and phylogenetic analysis indicate recent global dissemination from Europe
journal, August 2012
- Holt, Kathryn E.; Baker, Stephen; Weill, François-Xavier
- Nature Genetics, Vol. 44, Issue 9
Evolution of Pan-Genomes of Escherichia coli, Shigella spp., and Salmonella enterica
journal, April 2013
- Gordienko, E. N.; Kazanov, M. D.; Gelfand, M. S.
- Journal of Bacteriology, Vol. 195, Issue 12
Defining the Phylogenomics of Shigella Species: a Pathway to Diagnostics
journal, January 2015
- Sahl, Jason W.; Morris, Carolyn R.; Emberger, Jennifer
- Journal of Clinical Microbiology, Vol. 53, Issue 3
Microbial taxonomy in the post-genomic era: Rebuilding from scratch?
journal, December 2014
- Thompson, Cristiane C.; Amaral, Gilda R.; Campeão, Mariana
- Archives of Microbiology, Vol. 197, Issue 3
A Newly Recognized Cause of Travelers' Diarrhea: Enteroadherent Escherichia coli
journal, March 1985
- Mathewson, J. J.; Johnson, P. C.; DuPont, H. L.
- Journal of Infectious Diseases, Vol. 151, Issue 3
Clinical and microbiologic features of Shigella and enteroinvasive Escherichia coli infections detected by DNA hybridization.
journal, January 1988
- Taylor, D. N.; Echeverria, P.; Sethabutr, O.
- Journal of Clinical Microbiology, Vol. 26, Issue 7
Mutations in virus-derived small RNAs
journal, June 2020
- Nigam, Deepti; LaTourrette, Katherine; Garcia-Ruiz, Hernan
- Scientific Reports, Vol. 10, Issue 1
Works referencing / citing this record:
Shifting national surveillance of Shigella infections toward geno‐serotyping by the development of a tailored Luminex assay and NGS workflow
journal, March 2019
- Ventola, Eleonora; Bogaerts, Bert; De Keersmaecker, Sigrid C. J.
- MicrobiologyOpen
Bacterial genome sequencing in clinical microbiology: a pathogen-oriented review
journal, June 2017
- Tagini, F.; Greub, G.
- European Journal of Clinical Microbiology & Infectious Diseases, Vol. 36, Issue 11
A comparative assessment of conventional and molecular methods, including MinION nanopore sequencing, for surveying water quality
journal, October 2019
- Acharya, Kishor; Khanal, Santosh; Pantha, Kalyan
- Scientific Reports, Vol. 9, Issue 1
Standardized phylogenetic and molecular evolutionary analysis applied to species across the microbial tree of life
journal, February 2020
- Shakya, Migun; Ahmed, Sanaa A.; Davenport, Karen W.
- Scientific Reports, Vol. 10, Issue 1
Phylogenetic comparison of enteroinvasive Escherichia coli isolated from cases of diarrhoeal disease in England, 2005–2016
journal, June 2018
- Cowley, Lauren A.; Oresegun, Damilola R.; Chattaway, Marie A.
- Journal of Medical Microbiology, Vol. 67, Issue 6
Use of whole genome sequencing in surveillance for antimicrobial-resistant Shigella sonnei infections acquired from domestic and international sources
journal, May 2019
- Abelman, Rebecca L.; M'ikanatha, Nkuchia M.; Figler, Hillary M.
- Microbial Genomics, Vol. 5, Issue 5
A tale of two bacterial enteropathogens and one multivalent vaccine
journal, July 2019
- Barry, Eileen M.; Levine, Myron M.
- Cellular Microbiology, Vol. 21, Issue 11
A PCR-Based Method for Distinguishing between Two Common Beehive Bacteria, Paenibacillus larvae and Brevibacillus laterosporus
journal, September 2018
- Berg, Jordan A.; Merrill, Bryan D.; Breakwell, Donald P.
- Applied and Environmental Microbiology, Vol. 84, Issue 22
Investigating the Relatedness of Enteroinvasive Escherichia coli to Other E. coli and Shigella Isolates by Using Comparative Genomics
journal, June 2016
- Hazen, Tracy H.; Leonard, Susan R.; Lampel, Keith A.
- Infection and Immunity, Vol. 84, Issue 8
Evaluation of a Culture-Dependent Algorithm and a Molecular Algorithm for Identification of Shigella spp., Escherichia coli , and Enteroinvasive E. coli
journal, July 2018
- van den Beld, Maaike J. C.; de Boer, Richard F.; Reubsaet, Frans A. G.
- Journal of Clinical Microbiology, Vol. 56, Issue 10
Identification of Escherichia coli and Shigella Species from Whole-Genome Sequences
journal, December 2016
- Chattaway, Marie A.; Schaefer, Ulf; Tewolde, Rediat
- Journal of Clinical Microbiology, Vol. 55, Issue 2
Genome-wide association studies of Shigella spp. and Enteroinvasive Escherichia coli isolates demonstrate an absence of genetic markers for prediction of disease severity
journal, February 2020
- Hendriks, Amber C. A.; Reubsaet, Frans A. G.; Kooistra-Smid, A. M. D. ( Mirjam)
- BMC Genomics, Vol. 21, Issue 1
Incidence, clinical implications and impact on public health of infections with Shigella spp. and entero-invasive Escherichia coli (EIEC): results of a multicenter cross-sectional study in the Netherlands during 2016–2017
journal, December 2019
- van den Beld, Maaike J. C.; Warmelink, Esther; Friedrich, Alexander W.
- BMC Infectious Diseases, Vol. 19, Issue 1
Improved metagenomic analysis with Kraken 2
journal, November 2019
- Wood, Derrick E.; Lu, Jennifer; Langmead, Ben
- Genome Biology, Vol. 20, Issue 1
The Intriguing Evolutionary Journey of Enteroinvasive E. coli (EIEC) toward Pathogenicity
journal, December 2017
- Pasqua, Martina; Michelacci, Valeria; Di Martino, Maria Letizia
- Frontiers in Microbiology, Vol. 8
First Detection of Carbapenem-Resistant Escherichia fergusonii Strains Harbouring Beta-Lactamase Genes from Clinical Samples
journal, September 2019
- Adesina, Tomilola; Nwinyi, Obinna; De, Nandita
- Pathogens, Vol. 8, Issue 4