Cryptic Lineages of the Genus Escherichia

Abstract

Extended multilocus sequence typing (MLST) analysis of atypical Escherichia isolates was used to identify five novel phylogenetic clades (CI to CV) among isolates from environmental, human, and animal sources. Analysis of individual housekeeping loci showed that E. coli and its sister clade, CI, remain largely indistinguishable and represent nascent evolutionary lineages. Conversely, clades of similar age (CIII and CIV) were found to be phylogenetically distinct. When all Escherichia lineages (named and unnamed) were evaluated, we found evidence that Escherichia fergusonii has evolved at an accelerated rate compared to E. coli, CI, CIII, CIV, and CV, suggesting that this species is younger than estimated by the molecular clock method. Although the five novel clades were phylogenetically distinct, we were unable to identify a discriminating biochemical marker for all but one of them (CIII) with traditional phenotypic profiling. CIII had a statistically different phenotype from E. coli that resulted from the loss of sucrose and sorbitol fermentation and lysine utilization. The lack of phenotypic distinction has likely hindered the ability to differentiate these clades from typical E. coli, and so their ecological significance and importance for applied and clinical microbiology are yet to be determined. However, our sampling suggests that CIII, CIV, and CV represent environmentally adapted Escherichia lineages that may be more abundant outside the host gastrointestinal tract.

Gene expression analysis of E. coli strains provides insights into the role of gene regulation in diversification

“…The small distances and consistent grouping of the two environmentals in all culture conditions, together with differences in their ecological strategy compared with other strains, suggest that they do indeed form a separate ecotype as proposed earlier, where extra-intestinal open environments serve as their primary habitat (Walk et al, 2009;Luo et al, 2011). It should be noted that E. coli strains belonging to the same clades as the strains used in this study are commonly detected in bird feces as well (Clermont et al, 2011), but it is currently not clear if these strains cycle between birds and the environment or whether different ecotypes with distinct primary habitats do exist within those lineages.…”

“…It spans a genetic continuum from the human associated enteric E. coli to several atypical clades that are frequently detected in the environment and in birds (Clermont et al, 2011). All clades share the same core genes (that is, atypical strains exhibit all genes considered typical for enteric E. coli) and show remarkable biochemical similarities, which left them categorized as the same species (Walk et al, 2009). Subsequently, a taxonomic placement of these atypical clades as different species was proposed because (i) phylogenetic analysis cluster human enteric strains together and apart from atypical strains, (ii) several genes that are considered important for adaptation to distinct primary habitats (the human gut versus the environment) are specifically enriched in the individual groups and (iii) the exchange of genetic material has been shown to occur predominantly within strains sharing the same primary habitat (Luo et al, 2011).…”

Genome sequencing of environmental Escherichia coli expands understanding of the ecology and speciation of the model bacterial species

“…The orders-of-magnitude higher abundances of these clades in environmental samples relative to those in human feces and the clinic (9) indicate that they represent truly environmentally adapted organisms (meaning that they are not associated primarily with mammal hosts). Consistent with this interpretation, a recent study found that strains of clades C-III, -IV, and -V form biofilms more readily, outcompete typical E. coli strains at low temperatures (which characterize the environment compared with the gastrointestinal tract of warm-blooded hosts), and are nonpathogenic in a mouse model of septicemia (13).…”

“…Consistent with this interpretation, a recent study found that strains of clades C-III, -IV, and -V form biofilms more readily, outcompete typical E. coli strains at low temperatures (which characterize the environment compared with the gastrointestinal tract of warm-blooded hosts), and are nonpathogenic in a mouse model of septicemia (13). Furthermore, screening of 2,701 strains from humans, animals, and the environment identified an additional 57 environmental clade strains, and these strains were found more often in environmental and bird samples than in human samples (9). These studies consistently support the hypothesis that the environmental clades substantially expand the known ecological niche of E. coli.…”

“…We recently described five Escherichia clades (C-I to C-V) that were recovered primarily from environmental sources and are indistinguishable from typical E. coli based on traditional phenotypic tests included in either the API20E Identification System (bioMerieux, Inc.) or the BBL Crystal Identification System (Becton, Dickinson and Company) (9). To provide genomic insights into the phylogenetic diversity and metabolic potential of these clades, we sequenced the genome of nine representatives from clades C-I, -III, -IV, and -V (Table 1, Table S1, and Fig.…”