Vital dye reaction and granule localization in periplasm of Escherichia coli.

<h4>Background</h4>Tetrazolium salts are widely used in biology as indicators of metabolic activity - hence termed vital dyes - but their reduction site is still debated despite decades of intensive research. The prototype, 2,3,5- triphenyl tetrazolium chloride, which was first synthesiz...

Full description

Saved in:
Bibliographic Details
Main Authors: Liyan Ping, Despoina A I Mavridou, Eldon Emberly, Martin Westermann, Stuart J Ferguson
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2012-01-01
Series:PLoS ONE
Online Access:https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0038427&type=printable
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850224990641717248
author Liyan Ping
Despoina A I Mavridou
Eldon Emberly
Martin Westermann
Stuart J Ferguson
author_facet Liyan Ping
Despoina A I Mavridou
Eldon Emberly
Martin Westermann
Stuart J Ferguson
author_sort Liyan Ping
collection DOAJ
description <h4>Background</h4>Tetrazolium salts are widely used in biology as indicators of metabolic activity - hence termed vital dyes - but their reduction site is still debated despite decades of intensive research. The prototype, 2,3,5- triphenyl tetrazolium chloride, which was first synthesized a century ago, often generates a single formazan granule at the old pole of Escherichia coli cells after reduction. So far, no explanation for their pole localization has been proposed.<h4>Method/principal findings</h4>Here we provide evidence that the granules form in the periplasm of bacterial cells. A source of reducing power is deduced to be thiol groups destined to become disulfides, since deletion of dsbA, coding for thiol-oxidase, enhances the formation of reduced formazan. However, pervasive reduction did not result in a random distribution of formazan aggregates. In filamentous cells, large granules appear at regular intervals of about four normal cell-lengths, consistent with a diffusion-to-capture model. Computer simulations of a minimal biophysical model showed that the pole localization of granules is a spontaneous process, i.e. small granules in a normal size bacterium have lower energy at the poles. This biased their diffusion to the poles. They kept growing there and eventually became fixed.<h4>Conclusions</h4>We observed that formazan granules formed in the periplasm after reduction of tetrazolium, which calls for re-evaluation of previous studies using cell-free systems that liberate inaccessible intracellular reductant and potentially generate artifacts. The localization of formazan granules in E. coli cells can now be understood. In living bacteria, the seeds formed at or migrated to the new pole would become visible only when that new pole already became an old pole, because of the relatively slow growth rate of granules relative to cell division.
format Article
id doaj-art-06be247ffc9d4e59888b7da1ec7b4312
institution OA Journals
issn 1932-6203
language English
publishDate 2012-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS ONE
spelling doaj-art-06be247ffc9d4e59888b7da1ec7b43122025-08-20T02:05:29ZengPublic Library of Science (PLoS)PLoS ONE1932-62032012-01-0176e3842710.1371/journal.pone.0038427Vital dye reaction and granule localization in periplasm of Escherichia coli.Liyan PingDespoina A I MavridouEldon EmberlyMartin WestermannStuart J Ferguson<h4>Background</h4>Tetrazolium salts are widely used in biology as indicators of metabolic activity - hence termed vital dyes - but their reduction site is still debated despite decades of intensive research. The prototype, 2,3,5- triphenyl tetrazolium chloride, which was first synthesized a century ago, often generates a single formazan granule at the old pole of Escherichia coli cells after reduction. So far, no explanation for their pole localization has been proposed.<h4>Method/principal findings</h4>Here we provide evidence that the granules form in the periplasm of bacterial cells. A source of reducing power is deduced to be thiol groups destined to become disulfides, since deletion of dsbA, coding for thiol-oxidase, enhances the formation of reduced formazan. However, pervasive reduction did not result in a random distribution of formazan aggregates. In filamentous cells, large granules appear at regular intervals of about four normal cell-lengths, consistent with a diffusion-to-capture model. Computer simulations of a minimal biophysical model showed that the pole localization of granules is a spontaneous process, i.e. small granules in a normal size bacterium have lower energy at the poles. This biased their diffusion to the poles. They kept growing there and eventually became fixed.<h4>Conclusions</h4>We observed that formazan granules formed in the periplasm after reduction of tetrazolium, which calls for re-evaluation of previous studies using cell-free systems that liberate inaccessible intracellular reductant and potentially generate artifacts. The localization of formazan granules in E. coli cells can now be understood. In living bacteria, the seeds formed at or migrated to the new pole would become visible only when that new pole already became an old pole, because of the relatively slow growth rate of granules relative to cell division.https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0038427&type=printable
spellingShingle Liyan Ping
Despoina A I Mavridou
Eldon Emberly
Martin Westermann
Stuart J Ferguson
Vital dye reaction and granule localization in periplasm of Escherichia coli.
PLoS ONE
title Vital dye reaction and granule localization in periplasm of Escherichia coli.
title_full Vital dye reaction and granule localization in periplasm of Escherichia coli.
title_fullStr Vital dye reaction and granule localization in periplasm of Escherichia coli.
title_full_unstemmed Vital dye reaction and granule localization in periplasm of Escherichia coli.
title_short Vital dye reaction and granule localization in periplasm of Escherichia coli.
title_sort vital dye reaction and granule localization in periplasm of escherichia coli
url https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0038427&type=printable
work_keys_str_mv AT liyanping vitaldyereactionandgranulelocalizationinperiplasmofescherichiacoli
AT despoinaaimavridou vitaldyereactionandgranulelocalizationinperiplasmofescherichiacoli
AT eldonemberly vitaldyereactionandgranulelocalizationinperiplasmofescherichiacoli
AT martinwestermann vitaldyereactionandgranulelocalizationinperiplasmofescherichiacoli
AT stuartjferguson vitaldyereactionandgranulelocalizationinperiplasmofescherichiacoli