Black Queen Evolution and Trophic Interactions Determine Plasmid Survival after the Disruption of the Conjugation Network

ABSTRACT 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 popul...

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Autores principales:	Johannes Cairns, Katariina Koskinen, Reetta Penttinen, Tommi Patinen, Anna Hartikainen, Roosa Jokela, Liisa Ruusulehto, Sirja Viitamäki, Sari Mattila, Teppo Hiltunen, Matti Jalasvuori
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	antibiotic resistance Black Queen evolution conjugation predation trophic levels Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/8fc58313e5f840abae468070e8351b8f
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spelling	oai:doaj.org-article:8fc58313e5f840abae468070e8351b8f2021-12-02T18:15:43ZBlack Queen Evolution and Trophic Interactions Determine Plasmid Survival after the Disruption of the Conjugation Network10.1128/mSystems.00104-182379-5077https://doaj.org/article/8fc58313e5f840abae468070e8351b8f2018-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00104-18https://doaj.org/toc/2379-5077ABSTRACT 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. IMPORTANCE 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.Johannes CairnsKatariina KoskinenReetta PenttinenTommi PatinenAnna HartikainenRoosa JokelaLiisa RuusulehtoSirja ViitamäkiSari MattilaTeppo HiltunenMatti JalasvuoriAmerican Society for Microbiologyarticleantibiotic resistanceBlack Queen evolutionconjugationpredationtrophic levelsMicrobiologyQR1-502ENmSystems, Vol 3, Iss 5 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	antibiotic resistance Black Queen evolution conjugation predation trophic levels Microbiology QR1-502
spellingShingle	antibiotic resistance Black Queen evolution conjugation predation trophic levels Microbiology QR1-502 Johannes Cairns Katariina Koskinen Reetta Penttinen Tommi Patinen Anna Hartikainen Roosa Jokela Liisa Ruusulehto Sirja Viitamäki Sari Mattila Teppo Hiltunen Matti Jalasvuori Black Queen Evolution and Trophic Interactions Determine Plasmid Survival after the Disruption of the Conjugation Network
description	ABSTRACT 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. IMPORTANCE 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.
format	article
author	Johannes Cairns Katariina Koskinen Reetta Penttinen Tommi Patinen Anna Hartikainen Roosa Jokela Liisa Ruusulehto Sirja Viitamäki Sari Mattila Teppo Hiltunen Matti Jalasvuori
author_facet	Johannes Cairns Katariina Koskinen Reetta Penttinen Tommi Patinen Anna Hartikainen Roosa Jokela Liisa Ruusulehto Sirja Viitamäki Sari Mattila Teppo Hiltunen Matti Jalasvuori
author_sort	Johannes Cairns
title	Black Queen Evolution and Trophic Interactions Determine Plasmid Survival after the Disruption of the Conjugation Network
title_short	Black Queen Evolution and Trophic Interactions Determine Plasmid Survival after the Disruption of the Conjugation Network
title_full	Black Queen Evolution and Trophic Interactions Determine Plasmid Survival after the Disruption of the Conjugation Network
title_fullStr	Black Queen Evolution and Trophic Interactions Determine Plasmid Survival after the Disruption of the Conjugation Network
title_full_unstemmed	Black Queen Evolution and Trophic Interactions Determine Plasmid Survival after the Disruption of the Conjugation Network
title_sort	black queen evolution and trophic interactions determine plasmid survival after the disruption of the conjugation network
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/8fc58313e5f840abae468070e8351b8f
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Black Queen Evolution and Trophic Interactions Determine Plasmid Survival after the Disruption of the Conjugation Network

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