Ecological and genetic determinants of plasmid distribution in Escherichia coli

Abstract

SummaryBacterial plasmids are important carriers of virulence and antibiotic resistance genes. Nevertheless, little is known of the determinants of plasmid distribution in bacterial populations. Here the factors affecting the diversity and distribution of the large plasmids of Escherichia coli were explored in cattle grazing on semi-natural grassland, a set of populations with low frequencies of antibiotic resistance genes. Critically, the population genetic structure of bacterial hosts was chararacterized. This revealed structured E. coli populations with high diversity between sites and individuals but low diversity within cattle hosts. Plasmid profiles, however, varied considerably within the same E. coli genotype. Both ecological and genetic factors affected plasmid distribution: plasmid profiles were affected by site, E. coli diversity, E. coli genotype and the presence of other large plasmids. Notably 3/26 E. coli serotypes accounted for half the observed plasmid-free isolates indicating that within species variation can substantially affect carriage of the major conjugative plasmids. The observed population structure suggest that most of the opportunities for within species plasmid transfer occur between different individuals of the same genotype and support recent experimental work indicating that plasmid-host coevolution, and epistatic interactions on fitness costs are likely to be important in determining occupancy.

Plasmid transfer is biased towards close kin in bacteria from natural populations

“…Spatial structure, that promotes transfer to kin in the absence of discrimination mechanisms (Dimitriu et al, 2016), can also bias transfer across a population. Indeed the E. coli populations sampled for this study show strong population structure, indicating that opportunities for transfer to plasmid null isolates occur predominantly within genotypes (Medaney et al 2016).…”

“…E. coli field isolates (Table S1) were selected from the field collection characterized in [Medaney et al, 2016], which surveyed E. coli diversity and plasmid content in grazing cattle.…”

“…We characterized transfer rates for two plasmids belonging to the incompatibility groups most abundant in the field collection (Medaney et al, 2016). R1 plasmid (Meynell and Datta, 1966) is a narrow-host range IncFII plasmid, in which regulation of transfer is representative of the majority of IncF plasmids (Fernandez-Lopez et al 2016).…”

“…Parasite success in new hosts has been correlated to genetic distance between hosts in various organisms, for instance phages (Scanlan et al, 2017) or insect viruses (Longdon et al, 2011). Transfer restriction could contribute to global patterns in plasmid host range, where different plasmid groups are specifically associated to different host lineages (Williams et al 2013, Medaney et al 2016, Méric et al 2018, a pattern also observed for pathogenic lineages (McCarthy andLindsay 2012, Mathers et al 2015). Transfer to kin i.e.…”

“…Variation might exist only at a large phylogenetic scale or be the product of environment-specific selective forces, such that strains isolated from the same environment have much more homogeneous transfer rates or display no bias in transfer towards kin. Here, we investigate the transfer rates of two resistance plasmids, R1 and RP4 with respectively narrow and broad host ranges, among a collection of E. coli host isolates from cattle, for which population structure and native plasmid content have been characterized previously (Medaney et al, 2016). We ask if the striking diversity in transfer previously observed within laboratory strain collections is still present within populations, when host bacteria are isolated from the same or similar environments and at short phylogenetic scales; and explore genetic factors that could contribute to biased transfer towards kin.…”