Cultivation at high osmotic pressure confers ubiquinone 8–independent protection of respiration onEscherichia coli

Author:

Tempelhagen Laura,Ayer Anita,Culham Doreen E.,Stocker RolandORCID,Wood Janet M.

Abstract

Ubiquinone 8 (coenzyme Q8 or Q8) mediates electron transfer within the aerobic respiratory chain, mitigates oxidative stress, and contributes to gene expression inEscherichia coli. In addition, Q8 was proposed to confer bacterial osmotolerance by accumulating during growth at high osmotic pressure and altering membrane stability. The osmolyte trehalose and membrane lipid cardiolipin accumulate inE. colicells cultivated at high osmotic pressure. Here, Q8 deficiency impairedE. coligrowth at low osmotic pressure and rendered growth osmotically sensitive. The Q8 deficiency impeded cellular O2uptake and also inhibited the activities of two proton symporters, the osmosensing transporter ProP and the lactose transporter LacY. Q8 supplementation decreased membrane fluidity in liposomes, but did not affect ProP activity in proteoliposomes, which is respiration-independent. Liposomes and proteoliposomes prepared withE. colilipids were used for these experiments. Similar oxygen uptake rates were observed for bacteria cultivated at low and high osmotic pressures. In contrast, respiration was dramatically inhibited when bacteria grown at the same low osmotic pressure were shifted to high osmotic pressure. Thus, respiration was restored during prolonged growth ofE. coliat high osmotic pressure. Of note, bacteria cultivated at low and high osmotic pressures had similar Q8 concentrations. The protection of respiration was neither diminished by cardiolipin deficiency nor conferred by trehalose overproduction during growth at low osmotic pressure, but rather might be achieved by Q8-independent respiratory chain remodeling. We conclude that osmotolerance is conferred through Q8-independent protection of respiration, not by altering physical properties of the membrane.

Funder

Government of Canada | Natural Sciences and Engineering Research Council of Canada

Department of Education and Training | Australian Research Council

Department of Health | National Health and Medical Research Council

Publisher

Elsevier BV

Subject

Cell Biology,Molecular Biology,Biochemistry

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