Broad host range plasmids can invade an unexpectedly diverse fraction of a soil bacterial community

Abstract

Conjugal plasmids can provide microbes with full complements of new genes and constitute potent vehicles for horizontal gene transfer. Conjugal plasmid transfer is deemed responsible for the rapid spread of antibiotic resistance among microbes. While broad host range plasmids are known to transfer to diverse hosts in pure culture, the extent of their ability to transfer in the complex bacterial communities present in most habitats has not been comprehensively studied. Here, we isolated and characterized transconjugants with a degree of sensitivity not previously realized to investigate the transfer range of IncP-and IncPromA-type broad host range plasmids from three proteobacterial donors to a soil bacterial community. We identified transfer to many different recipients belonging to 11 different bacterial phyla. The prevalence of transconjugants belonging to diverse Gram-positive Firmicutes and Actinobacteria suggests that inter-Gram plasmid transfer of IncP-1 and IncPromAtype plasmids is a frequent phenomenon. While the plasmid receiving fractions of the community were both plasmid-and donor-dependent, we identified a core super-permissive fraction that could take up different plasmids from diverse donor strains. This fraction, comprising 80% of the identified transconjugants, thus has the potential to dominate IncP-and IncPromA-type plasmid transfer in soil. Our results demonstrate that these broad host range plasmids have a hitherto unrecognized potential to transfer readily to very diverse bacteria and can, therefore, directly connect large proportions of the soil bacterial gene pool. This finding reinforces the evolutionary and medical significances of these plasmids.

Source–sink plasmid transfer dynamics maintain gene mobility in soil bacterial communities

“…Potential plasmid recipients can stretch across diverse microbial groups (13), and although transconjugants within sink species may be transient (due to segregation or purifying selection) (28), their continual replenishment by conjugation from the source means that microbial community richness may be more robust to occasional bouts of selection for plasmid-borne genes. Coculture enhanced plasmid persistence in the sink species even under Hg(II) selection, whereas in single-species P. putida cultures, plasmid carriers tended to be outcompeted by mutants with chromosomal Hg R .…”

“…Such interspecific conjugation, analogous to transmission of infectious disease from a reservoir host (12), could maintain access to the mobile gene pool, allowing the focal species to remain evolutionarily responsive to temporally or spatially variable selection (3). Plasmids can be shared by a considerable fraction of the microbial community (13), but surprisingly there have been few experimental tests of how the presence of alternative hosts affects plasmid population dynamics, particularly over periods longer than a few days. Moreover, most studies of plasmid dynamics have been performed in well-mixed rich laboratory media, which do not adequately represent the physical structure or nutrient availability in most natural microbial communities (14,15).…”

Co-occurrence of antibiotic and metal resistance genes revealed in complete genome collection

“…Although no obvious preference for transposons, the normal constituent of most bacterial genomes (Kleckner, 1981), was observed, integrons were much more likely to transfer pairs such as bacitracin and Cu/Zn, whereas plasmids were preferable to carry bacitracin and Cu/ Zn and beta-lactam and Hg. It is of particular concern that the ARG and MRG pairs that were once carried by MGE types with high mobility potential, such as class 1 integrons or broad-host-range plasmids, can readily move across species or even phylum boundaries (Klumper et al, 2015), thereby increasing the probability of spreading the resistance gene pairs to very diverse bacteria.…”

Klebsiella pneumoniae as a key trafficker of drug resistance genes from environmental to clinically important bacteria

“…Highly diverse environmental microbial communities, especially soils, are considered hotspots for gene transfer [76], and Enterobacteriaceae have been identified as a component of the "super--permissive community" that supports the spread of plasmids across diverse soil communities [77]. The specific role of K. pneumoniae in such activities remains to be explored, however the species has been associated with hundreds of distinct plasmids spanning many plasmid replicon types [9,10,13,78], which suggests it acts as a recipient for plasmids originating from a wide array of HGT donors.…”

“…Intriguingly, it is clear that AMR genes and plasmids are not randomly distributed amongst K. pneumoniae lineages [9,10], suggesting that there may be significant variation in plasmid permissiveness between lineages. Related species and strains can vary substantially in their ability to act as plasmid donors [77,86], however variation in plasmid--donor potential between K. pneumoniae and other bacteria, or between strains of K. pneumoniae, remains to be investigated. Conclusions K. pneumoniae have the means and opportunity to capture plasmids from environmental microbial populations; to survive within and move between multiple environmental and animal--associated niches; to maintain AMR plasmids for prolonged periods; and to pass plasmids on to other clinically important Gram negative bacteria (Fig 4).…”