Black Queen Evolution and Trophic Interactions Determine Plasmid Survival after the Disruption of the Conjugation Network.
Johannes Cairns, Katariina Koskinen, Reetta Penttinen, Tommi Patinen, Anna Hartikainen, Roosa Jokela, Liisa Ruusulehto, Sirja Viitamäki, Sari Mattila, Teppo Hiltunen, Matti Jalasvuori
Author Information
Johannes Cairns: Department of Microbiology, University of Helsinki, Helsinki, Finland. ORCID
Katariina Koskinen: Department of Biological and Environmental Science, Centre of Excellence in Biological Interactions, Nanoscience Center, University of Jyväskylä, Jyväskylä, Finland.
Reetta Penttinen: Department of Biological and Environmental Science, Centre of Excellence in Biological Interactions, Nanoscience Center, University of Jyväskylä, Jyväskylä, Finland. ORCID
Tommi Patinen: Department of Biological and Environmental Science, Centre of Excellence in Biological Interactions, Nanoscience Center, University of Jyväskylä, Jyväskylä, Finland.
Anna Hartikainen: Department of Microbiology, University of Helsinki, Helsinki, Finland.
Roosa Jokela: Department of Microbiology, University of Helsinki, Helsinki, Finland. ORCID
Liisa Ruusulehto: Department of Microbiology, University of Helsinki, Helsinki, Finland.
Sirja Viitamäki: Department of Microbiology, University of Helsinki, Helsinki, Finland.
Sari Mattila: Department of Biological and Environmental Science, Centre of Excellence in Biological Interactions, Nanoscience Center, University of Jyväskylä, Jyväskylä, Finland.
Teppo Hiltunen: Department of Microbiology, University of Helsinki, Helsinki, Finland. ORCID
Matti Jalasvuori: Department of Biological and Environmental Science, Centre of Excellence in Biological Interactions, Nanoscience Center, University of Jyväskylä, Jyväskylä, Finland. ORCID
Mobile genetic elements such as conjugative plasmids are responsible for antibiotic resistance phenotypes in many bacterial pathogens. The ability to conjugate, the presence of antibiotics, and ecological interactions all have a notable role in the persistence of plasmids in bacterial populations. Here, we set out to investigate the contribution of these factors when the conjugation network was disturbed by a plasmid-dependent bacteriophage. Phage alone effectively caused the population to lose plasmids, thus rendering them susceptible to antibiotics. Leakiness of the antibiotic resistance mechanism allowing Black Queen evolution (i.e. a "race to the bottom") was a more significant factor than the antibiotic concentration (lethal vs sublethal) in determining plasmid prevalence. Interestingly, plasmid loss was also prevented by protozoan predation. These results show that outcomes of attempts to resensitize bacterial communities by disrupting the conjugation network are highly dependent on ecological factors and resistance mechanisms. Bacterial antibiotic resistance is often a part of mobile genetic elements that move from one bacterium to another. By interfering with the horizontal movement and the maintenance of these elements, it is possible to remove the resistance from the population. Here, we show that a so-called plasmid-dependent bacteriophage causes the initially resistant bacterial population to become susceptible to antibiotics. However, this effect is efficiently countered when the system also contains a predator that feeds on bacteria. Moreover, when the environment contains antibiotics, the survival of resistance is dependent on the resistance mechanism. When bacteria can help their contemporaries to degrade antibiotics, resistance is maintained by only a fraction of the community. On the other hand, when bacteria cannot help others, then all bacteria remain resistant. The concentration of the antibiotic played a less notable role than the antibiotic used. This report shows that the survival of antibiotic resistance in bacterial communities represents a complex process where many factors present in real-life systems define whether or not resistance is actually lost.
