Fitnesses of a conjugative plasmid and its host bacteria in soil microcosms

Abstract

Microcosms containing sterile soil were used to study the effects of naphthalene, competition from another bacterium, and exchange of the naphthalene-degradative NAH7 plasmid, on the fitness of strains of the gram- negative bacterium Pseudonomas putida. Naphthalene had a negative effect on fitness: densities of all three strains tested (naphthalene degrader, isogenic nondegrader, nonisogenic nondegrader) were lower when naphthalene was present in the soil. The NAH7 plasmid provided a selective advantage to the naphthalene degrader relative to its isogenic nondegrader counterpart when the two strains were grown in soil containing naphthalene. The plasmid was disadvantageous in the absence of naphthalene, although both strains persisted under all experimental treatments. In contrast, the relative fitness of nonisogenic strains grown together was controlled by competitive effects: densities of the naphthalene degrader were depressed, and those of the nonisogenic nondegrader elevated, when the two strains were grown together regardless of whether or not naphthalene was present. The rate of horizontal transmission of the NAH7 plasmid was a function of the product of the density of the donor and recipient cells. Vertical transmission of the plasmid as the bacterial cells divided was estimated to account for almost all transconjugants produced after the third day of the experiment. Paradoxically, the greatest development of a transconjugant population occurred in microcosms that did not contain naphthalene, and hence it was not directly due to a selective advantage of naphthalene degradation. Neither selection in the presence of naphthalene nor a long prior period of coevolution was required for stable carriage of the plasmid. The stability of the plasmid in transconjugants, and the high relative fitness of the transconjugants, suggest horizontal transfer is an important component of the evolutionary success of this plasmid. Repeated bouts of horizontal transfer followed by intense competition in soil microcosms may facilitate the selection of strains well suited for bioremediation.