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A Review of the Taxonomy, Genetics and Biology of the Genus Escherichia and the Type Species Escherichia Coli

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A Review of the Taxonomy, Genetics and Biology of the Genus Escherichia and the Type Species Escherichia Coli Canadian Journal of Microbiology A Review of the Taxonomy, Genetics and Biology of the Genus Escherichia and the Type Species Escherichia coli Journal: Canadian Journal of Microbiology Manuscript ID cjm-2020-0508.R1 Manuscript Type: Review Date Submitted by the 13-Feb-2021 Author: Complete List of Authors: Yu, Daniel ; University of Alberta School of Public Health, Room 357 South Academic Bldg, University of Alberta Banting, Graham; University of Alberta School of Public Health, Room 357 South Academic Bldg, University of Alberta Neumann, DraftNorman; University of Alberta School of Public Health, Room 357 South Academic Bldg, University of Alberta; Keyword: Escherichia coli, taxonomy, host specificity, ecotype, genetics Is the invited manuscript for consideration in a Special Not applicable (regular submission) Issue? : © The Author(s) or their Institution(s) Page 1 of 67 Canadian Journal of Microbiology A Review of the Taxonomy, Genetics and Biology of the Genus Escherichia and the Type Species Escherichia coli Daniel Yu1, Graham Banting1, and Norman F. Neumann1* 1School of Public Health, University of Alberta, Edmonton, Alberta, Canada, T6G IC9 Draft * Corresponding Author: Dr. Norman F. Neumann Professor and Vice Dean School of Public Health Room 3-381 Edmonton Clinic Health Academy University of Alberta Edmonton, Alberta, Canada. T6G 1C9 Email: [email protected] 1 © The Author(s) or their Institution(s) Canadian Journal of Microbiology Page 2 of 67 ABSTRACT Historically, bacteriologists have relied heavily on biochemical and structural phenotypes for bacterial taxonomic classification. However, advances in comparative genomics has led to greater insights into the remarkable genetic diversity within the microbial world, and even within well-accepted species such as Escherichia coli. The extraordinary genetic diversity in E. coli recapitulates the evolutionary radiation of this species in exploiting a wide range of niches (i.e., ecotypes), including the gastrointestinal system of diverse vertebrate hosts as well as non-host natural environments (soil, natural waters, wastewater), which drives the adaptation, natural selection and evolution of intragenotypic conspecific specialism as a strategy for survival. Over the last several years, a growing body of evidence suggests that many E. coli strains appear to be very host (or niche)-specific. While biochemicalDraft and phylogenetic evidence support the classification of E. coli as a distinct species, the vast genomic (diverse pan-genome and intragenotypic variability), phenotypic (e.g., metabolic pathways), and ecotypic (host-/niche- specificity) diversity, comparable to the diversity observed in known species complexes, suggests that E. coli is better represented as a complex. Herein we review the taxonomic classification of the genus Escherichia and discuss how phenotype, genotype and ecotype recapitulate our understanding of the biology of this remarkable bacterium. Key Words: Escherichia coli, host-specificity, ecotype, taxonomy 2 © The Author(s) or their Institution(s) Page 3 of 67 Canadian Journal of Microbiology A. Introduction First isolated in 1885 from the fecal material of neonates and early infants, Dr. Theodor Escherich identified a common commensal of the gastrointestinal tract which he termed Bacterium coli commune (Escherich 1988 [English translation of his original work]). Originally designated as Bacillus coli in 1895, this bacterium was renamed as Escherichia coli after its founder in 1919, after which the revised nomenclature was officially recognized in 1958 thereby establishing Escherichia as a genus with E. coli as the first species (Henry 2015). Since its discovery, E. coli stands as one of the most-studied and best-characterized microorganisms, serving as one of the fundamental model systems in microbiology. While E. coli has been subject to extensive genotypic and phenotypic (biochemical)Draft examination, and as such remains the best- characterized and the representative type species within the genus, the other Escherichia species have been characterized only relatively recently. As such, the taxonomic status of the rest of the genus has experienced considerable flux as conventional molecular diagnostic tools underlying classification schemes progressed from predominantly biochemical methods to genotypic- and genomic-based techniques. In this review, we explore the changes to the taxonomic structure of the genus Escherichia in response to the development of new diagnostic methods providing pertinent information for the characterization of novel Escherichia lineages and the re- assignment of early-discovered Escherichia ‘species’. We then explore the great genetic and biological diversity of the type species E. coli that is reflected in its extensive host- and niche- specificity. Provided the incredible genotypic diversity exhibited by this bacterium, and taking into consideration the importance of phenotypic and ecotypic information in understanding bacterial taxonomy, this suggests that E. coli may be more appropriately described as a complex. 3 © The Author(s) or their Institution(s) Canadian Journal of Microbiology Page 4 of 67 B. An Overview of the Genus Escherichia I. Overview of the Genus Escherichia Biochemical analyses were the sole means by which early identification of novel Escherichia species were evaluated. Leclerc (1962) observed characteristic biochemical properties of a particular group of Escherichia strains based on an indole, methyl-red, Voges- Proskauer and citrate reaction (IMViC test) profile that prompted their classification as a new species known as E. adecarboxylata. Later, the biochemical characterization of a unique group of bacterial strains isolated from the hindgutDraft of the Oriental cockroach (Blatta orientalis) led to their designation of a new species known as E. blattae (Burgess et al. 1973). Further analyses of the biochemical boundaries defining the E. coli species revealed several additional atypical groups that appeared to be distinct species in the family Enterobactericeae. One atypical group, Enteric Group 1, was commonly associated with human wound infections while another atypical group, Enteric Group 11, was commonly isolated from clinical specimens. Both atypical groups were found to consist of yellow-pigmented enteric strains capable of growing on cyanide (KCN) media and metabolizing cellobiose, distinguishing them as distinct species from E. coli. These two atypical groups themselves were differentiated according to varying decarboxylase reaction profiles, and the positive melibiose and malonate reactions, and negative indole reaction, of Enteric Group 1. As such, Enteric Group 1 and Enteric Group 11 were proposed to be separate species in the family Enterobacteriaceae, renamed as E. vulneris and E. hermannii, respectively (Brenner et al. 1982a; Brenner et al. 1982b). Similarly, the characterization of the distinct biochemical profile of atypical Enteric Group 10, also associated with human clinical samples, 4 © The Author(s) or their Institution(s) Page 5 of 67 Canadian Journal of Microbiology prompted the reclassification of this group as another distinct Escherichia species, E. fergusonii (Farmer et al. 1985). While the early identification of novel Escherichia species relied on the differentiation of closely-related groups of Enterobacteriaceae through biochemical means, the development of genotypic and genomic diagnostic tools provided additional means for the further discrimination of Escherichia species. For instance, after identifying a biochemical profile characteristic of the Escherichia genus (Abbott et al. 2003; Janda et al. 1999), DNA-DNA hybridization and 16S rDNA sequencing analyses, alongside virulence gene identification (e.g., the enteropathogenic E. coli-specific eaeA gene and the Shigella-specific phoE gene), prompted the reclassification of a group of strains, initially named Hafnia alvei, as a separate Escherichia species, E. albertii (Huys et al. 2003). Subsequent whole-genomeDraft sequencing and average nucleotide identity (ANI) analyses have since supported the reclassification of E. albertii as a distinct taxon within Escherichia (Ooka et al. 2015). More recently, alongside biochemical analyses, phylogenetic approaches utilizing 16S rRNA gene and core genome sequences classified a group of enterobacterial strains isolated from fecal samples of the Himalayan marmot (Marmota himalayana) as a novel Escherichia species, E. marmotae (Liu et al. 2015; Liu et al. 2019). Beyond the identification of novel host-associated Escherichia species, the growth of genetic sequence-based diagnostic methods also proved essential for the characterization of a distinct set of strains commonly associated with non-host environments that, while phenotypically indistinguishable from E. coli, appear to represent genetically divergent, ‘cryptic’ Escherichia lineages. Traditional biochemical tests fail to distinguish these cryptic lineages from E. coli (Walk et al. 2009), but MLST-based phylogenetic analyses have identified 5 monophyletic groups of cryptic strains distinct from E. coli, termed the Escherichia clades I–V 5 © The Author(s) or their Institution(s) Canadian Journal of Microbiology Page 6 of 67 (Walk et al. 2009; Clermont et al. 2011a). A growing body of evidence suggests that these cryptic clades, especially clades III and V, consist of strains that are native residents of natural environments. Reflecting this, comparative genomic and physiological studies have demonstrated cryptic
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