Niche and local geography shape the pangenome of wastewater- and livestock-associated Enterobacteriaceae

Escherichia coli and other Enterobacteriaceae are diverse species with “open” pangenomes, where genes move intra- and interspecies via horizontal gene transfer. However, most analyses focus on clinical isolates. The pangenome dynamics of natural populations remain understudied, despite their suggested role as reservoirs for antimicrobial resistance (AMR) genes. Here, we analyze near-complete genomes for 827 Enterobacteriaceae (553 Escherichia and 274 non-Escherichia spp.) with 2292 circularized plasmids in total, collected from 19 locations (livestock farms and wastewater treatment works in the United Kingdom) within a 30-km radius at three time points over a year. We find different dynamics for chromosomal and plasmid-borne genes. Plasmids have a higher burden of AMR genes and insertion sequences, and AMR-gene-carrying plasmids show evidence of being under stronger selective pressure. Environmental niche and local geography both play a role in shaping plasmid dynamics. Our results highlight the importance of local strategies for controlling the spread of AMR.

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Niche and local geography shape the pangenome of wastewater- and livestock-associated Enterobacteriaceae

10.1101/2020.07.23.215756 ◽

2020 ◽

Author(s):

Liam P. Shaw ◽

Kevin K. Chau ◽

James Kavanagh ◽

Manal AbuOun ◽

Emma Stubberfield ◽

...

Keyword(s):

Escherichia Coli ◽

Selective Pressure ◽

Natural Populations ◽

Insertion Sequences ◽

E Coli ◽

The United Kingdom ◽

Diverse Species ◽

Complete Genomes ◽

Show Evidence

Escherichia coli and other Enterobacteriaceae are highly diverse species with ‘open’ pangenomes1,2, where genes move intra- and inter-species via horizontal gene transfer3. These species can cause clinical infections4,5 as well as persist environmentally6,7. Environmental populations have been suggested as important reservoirs of antimicrobial resistance (AMR) genes. However, as most analyses focus on clinical isolates8,9, the pangenome dynamics of natural populations remain understudied, particularly the role of plasmids. Here, we reconstructed near-complete genomes for 828 Enterobacteriaceae, including 553 Escherichia spp. and 275 non-Escherichia species with 2,293 circularised plasmids in total, collected from nineteen locations (livestock farms and wastewater treatment works in the United Kingdom) within a 30km radius at three timepoints over the course of a year. We find different dynamics for the chromosomal and plasmid-borne components of the pangenome, showing that plasmids have a higher burden of both AMR genes and insertion sequences, and AMR plasmids show evidence of being under stronger selective pressure. Focusing on E. coli, we observe that plasmid dynamics are more strongly dominated by niche and local geography, rather than phylogeny or season. Our results highlight the diversity of the AMR reservoir in these species and niches, and the importance of local strategies for controlling the emergence and spread of AMR.

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Analysis of Insertion Sequences in Thermophilic Cyanobacteria: Exploring the Mechanisms of Establishing, Maintaining, and Withstanding High Insertion Sequence Abundance

Applied and Environmental Microbiology ◽

10.1128/aem.05090-11 ◽

2011 ◽

Vol 77 (15) ◽

pp. 5458-5466 ◽

Cited By ~ 18

Author(s):

William C. Nelson ◽

Lori Wollerman ◽

Devaki Bhaya ◽

John F. Heidelberg

Keyword(s):

Microbial Mats ◽

Hot Spring ◽

Natural Populations ◽

Metagenomic Data ◽

Insertion Sequences ◽

Content Type ◽

A Genome ◽

Thermophilic Cyanobacteria ◽

Show Evidence ◽

High Sequence Conservation

ABSTRACTInsertion sequences (ISs) are simple mobile genetic elements capable of relocating within a genome. Through this transposition activity, they are known to create mutations which are mostly deleterious to the cell, although occasionally they are beneficial. Two closely related isolates of thermophilicSynechococcusspecies from hot spring microbial mats are known to harbor a large number of diverse ISs. To explore the mechanism of IS acquisition within natural populations and survival in the face of high IS abundance, we examined IS content and location in natural populations ofSynechococcusby comparing metagenomic data to the genomes of fully sequenced cultured isolates. The observed IS distribution in the metagenome was equivalent to the distribution in the isolates, indicating that the cultured isolates are appropriate models for the environmental population. High sequence conservation between IS families shared between the two isolates suggests that ISs are able to move between individuals within populations and between species via lateral gene transfer, consistent with models for IS family accumulation. Most IS families show evidence of recent activity, and interruption of critical genes in some individuals was observed, demonstrating that transposition is an ongoing mutational force in the populations.

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Natural populations of Escherichia coli and Salmonella typhimurium harbor the same classes of insertion sequences.

Genetics ◽

10.1093/genetics/133.3.449 ◽

1993 ◽

Vol 133 (3) ◽

pp. 449-454 ◽

Cited By ~ 1

Author(s):

M Bisercić ◽

H Ochman

Keyword(s):

Escherichia Coli ◽

Salmonella Typhimurium ◽

Natural Populations ◽

Sequence Divergence ◽

Insertion Sequences ◽

Related Factors ◽

Specific Element ◽

E Coli ◽

Close Phylogenetic Relationship ◽

Polymerase Chain

Abstract Despite their close phylogenetic relationship, Escherichia coli and Salmonella typhimurium were long considered as having distinct classes of transposable elements maintained by either host-related factors or very restricted gene exchange. In this study, genetically diverse collections of E. coli and S. typhimurium (subgroup I) were surveyed for the presence of several classes of insertion sequences by Southern blot analysis and the polymerase chain reaction. A majority of salmonellae contained IS1 or IS3, elements originally recovered from E. coli, while IS200, a Salmonella-specific element, was present in about 20% of the tested strains of E. coli. Based on restriction mapping, the extent of sequence divergence between copies of IS200 from E. coli and S. typhimurium is on the order of that observed in comparisons of chromosomally encoded genes from these taxa. This suggests that copies of IS200 have not been recently transferred between E. coli and S. typhimurium and that the element was present in the common ancestor to both species. IS200 is polymorphic within E. coli but homogeneous among isolates of S. typhimurium, providing evidence that these species might differ in their rates of transfer and turnover of insertion sequences.

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Specific phenotypic, genomic, and fitness evolutionary trajectories toward streptomycin resistance induced by pesticide co-stressors in Escherichia coli

ISME Communications ◽

10.1038/s43705-021-00041-z ◽

2021 ◽

Vol 1 (1) ◽

Author(s):

Yue Xing ◽

Xiaoxi Kang ◽

Siwei Zhang ◽

Yujie Men

Keyword(s):

Escherichia Coli ◽

Antibiotic Resistance ◽

Selective Pressure ◽

Fold Increase ◽

Streptomycin Resistance ◽

Evolutionary Stage ◽

Fitness Costs ◽

Evolutionary Trajectories ◽

K 12 ◽

Late Stages

AbstractTo explore how co-occurring non-antibiotic environmental stressors affect evolutionary trajectories toward antibiotic resistance, we exposed susceptible Escherichia coli K-12 populations to environmentally relevant levels of pesticides and streptomycin for 500 generations. The coexposure substantially changed the phenotypic, genotypic, and fitness evolutionary trajectories, resulting in much stronger streptomycin resistance (>15-fold increase) of the populations. Antibiotic target modification mutations in rpsL and rsmG, which emerged and dominated at late stages of evolution, conferred the strong resistance even with less than 1% abundance, while the off-target mutations in nuoG, nuoL, glnE, and yaiW dominated at early stages only led to mild resistance (2.5–6-fold increase). Moreover, the strongly resistant mutants exhibited lower fitness costs even without the selective pressure and had lower minimal selection concentrations than the mildly resistant ones. Removal of the selective pressure did not reverse the strong resistance of coexposed populations at a later evolutionary stage. The findings suggest higher risks of the selection and propagation of strong antibiotic resistance in environments potentially impacted by antibiotics and pesticides.

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An outbreak of Shiga toxin-producing Escherichia coli O157:H7 associated with contaminated salad leaves: epidemiological, genomic and food trace back investigations

Epidemiology and Infection ◽

10.1017/s0950268817002874 ◽

2017 ◽

Vol 146 (2) ◽

pp. 187-196 ◽

Cited By ~ 25

Author(s):

A. F. W. MIKHAIL ◽

C. JENKINS ◽

T. J. DALLMAN ◽

T. INNS ◽

A. DOUGLAS ◽

...

Keyword(s):

Escherichia Coli ◽

Shiga Toxin ◽

Recent Common Ancestor ◽

Outbreak Strain ◽

The United Kingdom ◽

Run Off ◽

Trace Back ◽

Close Phylogenetic Relationship ◽

Foodborne Outbreaks

SUMMARYIn August 2015, Public Health England detected an outbreak of Shiga toxin-producing Escherichia coli (STEC) serotype O157:H7 caused by contaminated salad leaves in a mixed leaf prepacked salad product from a national retailer. The implicated leaves were cultivated at five different farms and the zoonotic source of the outbreak strain was not determined. In March 2016, additional isolates from new cases were identified that shared a recent common ancestor with the outbreak strain. A case–case study involving the cases identified in 2016 revealed that ovine exposures were associated with illness (n = 16; AOR 8·24; 95% CI 1·55–39·74). By mapping the recent movement of sheep and lambs across the United Kingdom, epidemiological links were established between the cases reporting ovine exposures. Given the close phylogenetic relationship between the outbreak strain and the isolates from cases with ovine exposures, it is plausible that ovine faeces may have contaminated the salad leaves via untreated irrigation water or run-off from fields nearby. Timely and targeted veterinary and environmental sampling should be considered during foodborne outbreaks of STEC, particularly where ready to eat vegetables and salads are implicated.

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