Resolving the plasmid paradox: costs and benefits of horizontal gene transfer in a community context

Horizontal gene transfer (HGT) is a central evolutionary process enhancing
genome diversification and rapid adaptation of species to new environmental
conditions. Mobile genetic elements (MGE) facilitate genetic exchange between
species through HGT by carrying accessory gene cargos encoding beneficial traits
such as resistance to metals and antibiotics. MGE-mediated transfer of antibiotic
resistance genes between species in natural microbial communities has
contributed to the global spread of antibiotic resistance. It is therefore essential
to understand the ecological drivers of the maintenance and transmission of
MGEs in bacterial communities. Here I use conjugative plasmids as an example
MGE to study the ecological and evolutionary dynamics of plasmids in bacterial
populations and communities across a range of environments. First, I
demonstrate that plasmids selected in a single-host environment evolved host
specialism due to fitness trade-offs, whereas plasmids evolved in a multi-host
environment could overcome this trade-off to evolve host-generalism. Secondly, I
show that the costs and benefits of plasmid carriage and the long-term dynamics
of the plasmid and the mercury resistance transposon it encodes varied
extensively between diverse species of Pseudomonas. I next show that plasmid
maintenance was facilitated by compensatory evolution to ameliorate the cost of
plasmid carriage. Compensatory loci varied between species, with parallel
mutations targeting different regulatory and biosynthetic pathways in each
species. Lastly, I examine the effect of community structure on plasmid
dynamics in simple bacterial communities. When plasmids were carried by
proficient plasmid-donor species this led to higher plasmid abundance at the
community-level, while in diverse communities, plasmid transmission could be
impeded through the dilution effect, limiting plasmid spread. This thesis
demonstrates that plasmid dynamics in bacterial communities are determined by
the combination of ecological and evolutionary processes, depending on the
selective environment, the structure of the bacterial community and variation
among species in their proficiency to host plasmids and to undergo compensatory
evolution to ameliorate their costs. These data highlight the importance of
studying plasmid dynamics in a community-context.