Minicells as a Damage Disposal Mechanism in <named-content content-type="genus-species">Escherichia coli</named-content>

ABSTRACT Many bacteria produce small, spherical minicells that lack chromosomal DNA and therefore are unable to proliferate. Although minicells have been used extensively by researchers as a molecular tool, nothing is known about why bacteria produce them. Here, we show that minicells help Escherich...

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Autores principales:	Camilla U. Rang, Audrey Proenca, Christen Buetz, Chao Shi, Lin Chao
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	Escherichia coli aging antibiotic resistance minicells oxidative damage Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/32c9e586b00c4f4e92b3a67c1d0ed1b5
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spelling	oai:doaj.org-article:32c9e586b00c4f4e92b3a67c1d0ed1b52021-11-15T15:22:25ZMinicells as a Damage Disposal Mechanism in <named-content content-type="genus-species">Escherichia coli</named-content>10.1128/mSphere.00428-182379-5042https://doaj.org/article/32c9e586b00c4f4e92b3a67c1d0ed1b52018-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00428-18https://doaj.org/toc/2379-5042ABSTRACT Many bacteria produce small, spherical minicells that lack chromosomal DNA and therefore are unable to proliferate. Although minicells have been used extensively by researchers as a molecular tool, nothing is known about why bacteria produce them. Here, we show that minicells help Escherichia coli cells to rid themselves of damaged proteins induced by antibiotic stress. By comparing the survival and growth rates of wild-type strains with the E. coli ΔminC mutant, which produces excess minicells, we found that the mutant was more resistant to streptomycin. To determine the effects of producing minicells at the single-cell level, we also tracked the growth of ΔminC lineages by microscopy. We were able to show that the mutant increased the production of minicells in response to a higher level of the antibiotic. When we compared two sister cells, in which one produced minicells and the other did not, the daughters of the former had a shorter doubling time at this higher antibiotic level. Additionally, we found that minicells were more likely produced at the mother’s old pole, which is known to accumulate more aggregates. More importantly, by using a fluorescent IbpA chaperone to tag damage aggregates, we found that polar aggregates were contained by and ejected with the minicells produced by the mother bacterium. These results demonstrate for the first time the benefit to bacteria for producing minicells. IMPORTANCE Bacteria have the ability to produce minicells, or small spherical versions of themselves that lack chromosomal DNA and are unable to replicate. A minicell can constitute as much as 20% of the cell’s volume. Although molecular biology and biotechnology have used minicells as laboratory tools for several decades, it is still puzzling that bacteria should produce such costly but potentially nonfunctional structures. Here, we show that bacteria gain a benefit by producing minicells and using them as a mechanism to eliminate damaged or oxidated proteins. The elimination allows the bacteria to tolerate higher levels of stress, such as increasing levels of streptomycin. If this mechanism extends from streptomycin to other antibiotics, minicell production could be an overlooked pathway that bacteria are using to resist antimicrobials.Camilla U. RangAudrey ProencaChristen BuetzChao ShiLin ChaoAmerican Society for MicrobiologyarticleEscherichia coliagingantibiotic resistanceminicellsoxidative damageMicrobiologyQR1-502ENmSphere, Vol 3, Iss 5 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	Escherichia coli aging antibiotic resistance minicells oxidative damage Microbiology QR1-502
spellingShingle	Escherichia coli aging antibiotic resistance minicells oxidative damage Microbiology QR1-502 Camilla U. Rang Audrey Proenca Christen Buetz Chao Shi Lin Chao Minicells as a Damage Disposal Mechanism in <named-content content-type="genus-species">Escherichia coli</named-content>
description	ABSTRACT Many bacteria produce small, spherical minicells that lack chromosomal DNA and therefore are unable to proliferate. Although minicells have been used extensively by researchers as a molecular tool, nothing is known about why bacteria produce them. Here, we show that minicells help Escherichia coli cells to rid themselves of damaged proteins induced by antibiotic stress. By comparing the survival and growth rates of wild-type strains with the E. coli ΔminC mutant, which produces excess minicells, we found that the mutant was more resistant to streptomycin. To determine the effects of producing minicells at the single-cell level, we also tracked the growth of ΔminC lineages by microscopy. We were able to show that the mutant increased the production of minicells in response to a higher level of the antibiotic. When we compared two sister cells, in which one produced minicells and the other did not, the daughters of the former had a shorter doubling time at this higher antibiotic level. Additionally, we found that minicells were more likely produced at the mother’s old pole, which is known to accumulate more aggregates. More importantly, by using a fluorescent IbpA chaperone to tag damage aggregates, we found that polar aggregates were contained by and ejected with the minicells produced by the mother bacterium. These results demonstrate for the first time the benefit to bacteria for producing minicells. IMPORTANCE Bacteria have the ability to produce minicells, or small spherical versions of themselves that lack chromosomal DNA and are unable to replicate. A minicell can constitute as much as 20% of the cell’s volume. Although molecular biology and biotechnology have used minicells as laboratory tools for several decades, it is still puzzling that bacteria should produce such costly but potentially nonfunctional structures. Here, we show that bacteria gain a benefit by producing minicells and using them as a mechanism to eliminate damaged or oxidated proteins. The elimination allows the bacteria to tolerate higher levels of stress, such as increasing levels of streptomycin. If this mechanism extends from streptomycin to other antibiotics, minicell production could be an overlooked pathway that bacteria are using to resist antimicrobials.
format	article
author	Camilla U. Rang Audrey Proenca Christen Buetz Chao Shi Lin Chao
author_facet	Camilla U. Rang Audrey Proenca Christen Buetz Chao Shi Lin Chao
author_sort	Camilla U. Rang
title	Minicells as a Damage Disposal Mechanism in <named-content content-type="genus-species">Escherichia coli</named-content>
title_short	Minicells as a Damage Disposal Mechanism in <named-content content-type="genus-species">Escherichia coli</named-content>
title_full	Minicells as a Damage Disposal Mechanism in <named-content content-type="genus-species">Escherichia coli</named-content>
title_fullStr	Minicells as a Damage Disposal Mechanism in <named-content content-type="genus-species">Escherichia coli</named-content>
title_full_unstemmed	Minicells as a Damage Disposal Mechanism in <named-content content-type="genus-species">Escherichia coli</named-content>
title_sort	minicells as a damage disposal mechanism in <named-content content-type="genus-species">escherichia coli</named-content>
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/32c9e586b00c4f4e92b3a67c1d0ed1b5
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Minicells as a Damage Disposal Mechanism in <named-content content-type="genus-species">Escherichia coli</named-content>

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