Distinct evolutionary trajectories in the Escherichia coli pangenome occur within sequence types

Cummins, Elizabeth A.; Hall, Richard S.; Connor, Chris; McInerney, James O.; McNally, Alan

doi:10.1099/mgen.0.000903

Cited by 18 publications

(19 citation statements)

References 80 publications

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“…The 20577 E. coli genomes used here were curated from EnteroBase [31] and were fully characterised and described in a previous study (available at 10.6084/m9.figshare.21360108 ) [1]. Briefly, they were chosen to represent the phylogenetic, genotypic and phenotypic diversity of the species.…”

Section: Methodsmentioning

confidence: 99%

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Parallel loss of type VI secretion systems in two multi-drug resistantEscherichia colilineages

Cummins

Moran

Snaith

et al. 2023

Preprint

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The repeated emergence of pandemic multi-drug resistant (MDR) Escherichia coli clones is a threat to public health globally. In recent work, drug resistant E. coli were shown to be capable of displacing commensal E. coli in the human gut. We hypothesise that there are three factors potentially responsible for the apparent competitive advantage of drug resistant E. coli clones: enhanced metabolic capabilities; production of lytic phage or bacteriocins; or the presence of a type VI secretion system (T6SS). We employed genomic and experimental approaches to investigate. First, we searched for T6SS apparatus genes across a curated dataset of over 20,000 genomes representing the full phylogenetic diversity of E. coli. This revealed large, non-phylogenetic variation in the presence of T6SS genes. No association was found between T6SS gene presence and MDR clones. However, multiple MDR clones have lost essential T6SS genes. We have shown that the pandemic MDR clone ST131-H30Rx lost the essential T6SS gene tssM when it was interrupted by insertion of ISEc12. To investigate the importance of this, a three-way competition assay was designed to assess the contact-killing capabilities of three strains - ST131-H30Rx, its drug-susceptible TssM-producing ancestor, and laboratory strain K-12 MG1655. Our results confirmed the competitive advantage of ST131-H30Rx in the absence of antibiotics, but its success was not due to the presence of phage, secreted proteins or contact-dependent killing. Our findings suggest that metabolic advantages are therefore likely a key component in the success of ST131-H30Rx.

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Section: Methodsmentioning

confidence: 99%

“…All other sequence data used in this paper has been taken from ENA with the appropriate accession numbers listed within the methods section. The E. coli genome data sets used in this work are from a previous publication, the details of which can be found in the corresponding supplementary data files 10.6084/m9.figshare.21360108 x[1].…”

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confidence: 99%

Parallel loss of type VI secretion systems in two multi-drug resistantEscherichia colilineages

Cummins

Moran

Snaith

et al. 2023

Preprint

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“…As the mutation rate is often similar within species, nucleotide diversity is determined by variations in the demography and selective processes that affect N e , which allows inference of these processes ( Hartl 2020 ). Compared to mutation rates, gene transfer rates have a much larger variation between different genes and populations, resulting in inconclusive inferences of selection from the observed pangenomes ( Bobay and Ochman 2018 ; Douglas and Shapiro 2021 ; Cummins et al 2022 ).…”

Section: Major Population Genetic Processes Affecting Pangenomes Mimi...mentioning

confidence: 99%

Tackling the Pangenome Dilemma Requires the Concerted Analysis of Multiple Population Genetic Processes

Baumdicker

Kupczok

2023

Genome Biology and Evolution

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The pangenome is the set of all genes present in a prokaryotic population. Most pangenomes contain many accessory genes of low and intermediate frequencies. Different population genetics processes contribute to the shape of these pangenomes, namely selection and fitness-independent-processes such as gene transfer, gene loss, and migration. However, their relative importance is unknown and highly debated. Here we argue that the debate around prokaryotic pangenomes arose due to the imprecise application of population genetics models. Most importantly, two different processes of horizontal gene transfer act on prokaryotic populations, which are frequently confused, despite their fundamentally different behavior. Genes acquired from distantly related organisms (termed here acquiring gene transfer, AGT) is most comparable to mutation in nucleotide sequences. In contrast, gene gain within the population (termed here spreading gene transfer, SGT) has an effect on gene frequencies that is identical to the effect of positive selection on single genes. We thus show that selection and fitness-independent population genetic processes affecting pangenomes are indistinguishable at the level of single gene dynamics. Nevertheless, population genetics processes are fundamentally different when considering the joint distribution of all accessory genes across individuals of a population. We propose that, to understand to which degree the different processes shaped pangenome diversity, the development of comprehensive models and simulation tools is mandatory. Furthermore, we need to identify summary statistics and measurable features that can distinguish between the processes, where considering the joint distribution of accessory genes across individuals of a population will be particularly relevant.

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“…Escherichia coli is a highly diverse and versatile species, being both a commensal of humans and other mammals 1 , but also implicated in several intra and extra-intestinal diseases 2 . E. coli polymorphism for gene number and mobile genetic elements contributes to its extensive phenotypic diversity as a commensal and a pathogen 3 . A healthy human can be colonized by one dominant strain or, more commonly, by several strains 4 .…”

Section: Mainmentioning

confidence: 99%

Massive lateral gene transfer under strain coexistence in the gut

Frazão,

Seixas,

Barreto

et al. 2023

Preprint

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Mammals are colonized by multiple strains ofEscherichia coli, yet how such strain coexistence affects their tempo and mode of evolution is poorly understood. Here, by following the colonization of two phylogenetic distinct strains ofE. coliin the mouse gut, we find a strain-specific mode of evolution and a remarkable level of gene transfer between strains. In the same host, despite accumulating mutations at the same rate, one strain evolves by diversifying selection and the other by directional selection, and a rich dynamics of bacteriophage and plasmid transfer is found. Our results provide support for an important role of lateral transduction in the mammalian gut.

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Distinct evolutionary trajectories in the Escherichia coli pangenome occur within sequence types

Cited by 18 publications

References 80 publications

Parallel loss of type VI secretion systems in two multi-drug resistantEscherichia colilineages

Parallel loss of type VI secretion systems in two multi-drug resistantEscherichia colilineages

Tackling the Pangenome Dilemma Requires the Concerted Analysis of Multiple Population Genetic Processes

Massive lateral gene transfer under strain coexistence in the gut

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