Plasmid transfer in the animal intestine and other dynamic bacterial populations: the role of community structure and environment

Abstract

The transfer of the R1drd19 plasmid between isogenic strains of Escherichia coli BJ4 in batch cultures of laboratory media and intestinal extracts was compared. Using an estimate of plasmid transfer rate that is independent of cell density, of donor :recipient ratios and of mating time, it was found that transfer occurs at a much lower rate in intestinal extracts than in laboratory media. Furthermore, the results suggest that the majority of intestinal plasmid transfer takes place in the viscous mucus layer covering the epithelial cells. Investigation of plasmid transfer in different flow systems harbouring a dynamic, continuously growing population of constant size showed that transfer kinetics were strongly influenced by bacterial biofilm formation. When donor and recipient populations were subjected to continuous mixing, as in a chemostat, transfer continued to occur at a constant rate. When donor and recipient populations retained fixed spatial locations, as in a biofilm, transfer occurred very rapidly in the initial phase, after which no further transfer was detected. From in vivo studies of plasmid transfer in the intestine of streptomycin-treated mice, results were obtained which were similar to those obtained in the biofilm, but differed markedly from those obtained in the chemostat. In spite of peristaltic movements in the gut, and of apparently even distribution of E. coli as single cells in the intestinal mucus, the intestinal environment displays transfer kinetics different from those expected of a mixed, liquid culture, but quite similar to those of a biofilm.

Modelling the spatial dynamics of plasmid transfer and persistence

“…Pinedo & Smets (2005) observed a dependence of plasmid transfer efficiency on the donor to recipient ratio in filter matings that is not captured by mass-action models. In another study (Licht et al, 1999), the dynamics of transconjugant formation in the mouse gut were shown to be quite similar to those in a laboratory-grown biofilm and different from those observed in a chemostat and expected from a mass-action model. In addition to these empirical results, it is now mathematically well established (Durrett & Levin, 1994b;Hanski & Gilpin, 1997;Tilman & Kareiva, 1997;Dieckmann et al, 2000;Wei & Krone, 2005) that ignoring spatial structure in biological systems can lead to inaccuracies that are sometimes dramatic.…”

Gut inflammation can boost horizontal gene transfer between pathogenic and commensal Enterobacteriaceae

“…Thus, in complex bacterial ecosystems, low densities of donor and recipient bacteria may lower the frequency of direct bacterial encounters and thus decrease the chance of conjugation-mediated HGT. Several studies reported inefficient enterobacterial HGT in the normal mammalian gut (15)(16)(17), whereas others identified higher rates of HGT (18,19). This suggested that particular conditions exist that might favor plasmid exchange between Enterobacteriaceae.…”

Spatial structure and nutrients promote invasion of IncP-1 plasmids in bacterial populations

“…Conjugative plasmid transfer is no exception to this, as it requires cell contact and is therefore determined by the spatial configuration of a population or community. The failure of ordinary differential equation models to capture experimentally observed dynamics of plasmid transfer has already been demonstrated in several studies (Simonsen, 1990;Licht et al, 1999;Pinedo and Smets, 2005;Krone et al, 2007). Moreover, plasmids such as those of the IncP-1 group transfer at higher rates on solid substrates than in liquids.…”

“…Hypotheses have been raised about possible plasmid transfer inhibition mechanisms, or the lack of nutrient availability in those deeper cell layers. Nutrients have been shown to positively affect plasmid transfer efficiency in some cases, but not in others (Hausner and Wuertz, 1999;van Elsas and Bailey, 2002), and therefore it remains unclear why a plasmid does not completely invade a colony or biofilm, and if specific conditions may be conducive to plasmid invasion (Licht et al, 1999;Molin and Tolker-Nielsen, 2003).…”