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Periplasmic Acid Stress Increases Cell Division Asymmetry (Polar Aging) of Escherichia coli.

ABSTRACT: Under certain kinds of cytoplasmic stress, Escherichia coli selectively reproduce by distributing the newer cytoplasmic components to new-pole cells while sequestering older, damaged components in cells inheriting the old pole. This phenomenon is termed polar aging or cell division asymmetry. It is unknown whether cell division asymmetry can arise from a periplasmic stress, such as the stress of extracellular acid, which is mediated by the periplasm. We tested the effect of periplasmic acid stress on growth and division of adherent single cells. We tracked individual cell lineages over five or more generations, using fluorescence microscopy with ratiometric pHluorin to measure cytoplasmic pH. Adherent colonies were perfused continually with LBK medium buffered at pH 6.00 or at pH 7.50; the external pH determines periplasmic pH. In each experiment, cell lineages were mapped to correlate division time, pole age and cell generation number. In colonies perfused at pH 6.0, the cells inheriting the oldest pole divided significantly more slowly than the cells inheriting the newest pole. In colonies perfused at pH 7.50 (near or above cytoplasmic pH), no significant cell division asymmetry was observed. Under both conditions (periplasmic pH 6.0 or pH 7.5) the cells maintained cytoplasmic pH values at 7.2-7.3. No evidence of cytoplasmic protein aggregation was seen. Thus, periplasmic acid stress leads to cell division asymmetry with minimal cytoplasmic stress.

SUBMITTER: Clark MW

PROVIDER: S-EPMC4694651 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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Periplasmic Acid Stress Increases Cell Division Asymmetry (Polar Aging) of Escherichia coli.

Clark Michelle W MW Yie Anna M AM Eder Elizabeth K EK Dennis Richard G RG Basting Preston J PJ Martinez Keith A KA Jones Brian D BD Slonczewski Joan L JL

PloS one 20151229 12

Under certain kinds of cytoplasmic stress, Escherichia coli selectively reproduce by distributing the newer cytoplasmic components to new-pole cells while sequestering older, damaged components in cells inheriting the old pole. This phenomenon is termed polar aging or cell division asymmetry. It is unknown whether cell division asymmetry can arise from a periplasmic stress, such as the stress of extracellular acid, which is mediated by the periplasm. We tested the effect of periplasmic acid stre ...[more]

PMID: 26713733

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Project description:Clarifying the molecular mechanisms by which bacteria acquire virulence traits is important for understanding the bacterial virulence system. In the present study, we utilized a bacterial evolution method in a silkworm infection model and revealed that deletion of the opgGH operon, encoding synthases for osmoregulated periplasmic glucan (OPG), increased the virulence of a nonpathogenic laboratory strain of Escherichia coli against silkworms. The opgGH knockout mutant exhibited resistance to host antimicrobial peptides and antibiotics. Compared with the parent strain, the opgGH knockout mutant produced greater amounts of colanic acid, which is involved in E. coli resistance to antibiotics. RNA sequence analysis revealed that the opgGH knockout altered the expression of various genes, including the evgS/evgA two-component system that functions in antibiotic resistance. In both a colanic acid-negative background and an evgS-null background, the opgGH knockout increased E. coli resistance to antibiotics and increased the silkworm-killing activity of E. coli. In the null background of the envZ/ompR two-component system, which genetically interacts with opgGH, the opgGH knockout increased antibiotic resistance and virulence in silkworms. These findings suggest that the absence of OPG confers antimicrobial resistance and virulence in E. coli in a colanic acid-, evgS/evgA-, and envZ/ompR-independent manner. IMPORTANCE The gene mutation types that increase the bacterial virulence of Escherichia coli remain unclear, in part due to the limited number of methods available for isolating bacterial mutants with increased virulence. We utilized a bacterial evolution method in the silkworm infection model, in which silkworms were infected with mutagenized bacteria and highly virulent bacterial mutants were isolated from dead silkworms. We revealed that knockout of OPG synthases increased E. coli virulence against silkworms. The OPG knockout mutants were resistant to host antimicrobial peptides as well as antibiotics. Our findings not only suggest a novel mechanism for virulence acquisition in E. coli but also support the usefulness of the bacterial experimental evolution method in the silkworm infection model.

Dataset Information

Periplasmic Acid Stress Increases Cell Division Asymmetry (Polar Aging) of Escherichia coli.

Publications

Periplasmic Acid Stress Increases Cell Division Asymmetry (Polar Aging) of Escherichia coli.

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