Generation of the membrane potential and its impact on the motility, ATP production and growth in Campylobacter jejuni

Summary The generation of a membrane potential (Δψ), the major constituent of the proton motive force (pmf), is crucial for ATP synthesis, transport of nutrients and flagellar rotation. Campylobacter jejuni harbors a branched electron transport chain, enabling respiration with different electron don...

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Veröffentlicht in:Molecular microbiology 2017-08, Vol.105 (4), p.637-651
Hauptverfasser: van der Stel, Anne‐Xander, Boogerd, Fred C., Huynh, Steven, Parker, Craig T., van Dijk, Linda, van Putten, Jos P. M., Wösten, Marc M. S. M.
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Sprache:eng
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Zusammenfassung:Summary The generation of a membrane potential (Δψ), the major constituent of the proton motive force (pmf), is crucial for ATP synthesis, transport of nutrients and flagellar rotation. Campylobacter jejuni harbors a branched electron transport chain, enabling respiration with different electron donors and acceptors. Here, we demonstrate that a relatively high Δψ is only generated in the presence of either formate as electron donor or oxygen as electron acceptor, in combination with an acceptor/donor respectively. We show the necessity of the pmf for motility and growth of C. jejuni. ATP generation is not only accomplished by oxidative phosphorylation via the pmf, but also by substrate‐level phosphorylation via the enzyme AckA. In response to a low oxygen tension, C. jejuni increases the transcription and activity of the donor complexes formate dehydrogenase (FdhABC) and hydrogenase (HydABCD) as well as the transcription of the alternative respiratory acceptor complexes. Our findings suggest that in the gut of warm‐blooded animals, C. jejuni depends on at least formate or hydrogen as donor (in the anaerobic lumen) or oxygen as acceptor (near the epithelial cells) to generate a pmf that sustains efficient motility and growth for colonization and pathogenesis. We determined how the branched electron transport chain of Campylobacter jejuni contributes to the generation of a membrane potential (Δψ), which is essential for its motility, generation of ATP and growth. Only in the presence of either oxygen as electron acceptor or formate/hydrogen as electron donor a Δψ is generated. Furthermore, we show that the availability of oxygen is a key determinant in the regulation of the genes encoding the electron transport chain complexes.
ISSN:0950-382X
1365-2958
DOI:10.1111/mmi.13723