Oxygen-dependent regulation of c-di-GMP synthesis by SadC controls alginate production in Pseudomonas aeruginosa

Annika Schmidt, Anna Silke Hammerbacher, Mike Bastian, Karen Jule Nieken, Jens Klockgether, Massimo Merighi, Karine Lapouge, Claudia Poschgan, Julia Kölle, K. Ravi Acharya, Martina Ulrich, Burkhard Tümmler, Gottfried Unden, Volkhard Kaever, Stephen Lory, Dieter Haas, Sandra Schwarz, Gerd Döring

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10 Citations (Scopus)

Abstract

Pseudomonas aeruginosa produces increased levels of alginate in response to oxygen-deprived conditions. The regulatory pathway(s) that links oxygen limitation to increased synthesis of alginate has remained elusive. In the present study, using immunofluorescence microscopy, we show that anaerobiosis-induced alginate production by planktonic PAO1 requires the diguanylate cyclase (DGC) SadC, previously identified as a regulator of surface-associated lifestyles. Furthermore, we found that the gene products of PA4330 and PA4331, located in a predicted operon with sadC, have a major impact on alginate production: deletion of PA4330 (odaA, for oxygen-dependent alginate synthesis activator) caused an alginate production defect under anaerobic conditions, whereas a PA4331 (odaI, for oxygen-dependent alginate synthesis inhibitor) deletion mutant produced alginate also in the presence of oxygen, which would normally inhibit alginate synthesis. Based on their sequence, OdaA and OdaI have predicted hydratase and dioxygenase reductase activities, respectively. Enzymatic assays using purified protein showed that unlike OdaA, which did not significantly affect DGC activity of SadC, OdaI inhibited c-di-GMP production by SadC. Our data indicate that SadC, OdaA and OdaI are components of a novel response pathway of P.aeruginosa that regulates alginate synthesis in an oxygen-dependent manner.

Original languageEnglish
Pages (from-to)3390–3402
JournalEnvironmental Microbiology
Volume18
Issue number10
Early online date4 Feb 2016
DOIs
Publication statusPublished - Oct 2016

ASJC Scopus subject areas

  • Microbiology
  • Ecology, Evolution, Behavior and Systematics

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    Schmidt, A., Hammerbacher, A. S., Bastian, M., Nieken, K. J., Klockgether, J., Merighi, M., Lapouge, K., Poschgan, C., Kölle, J., Acharya, K. R., Ulrich, M., Tümmler, B., Unden, G., Kaever, V., Lory, S., Haas, D., Schwarz, S., & Döring, G. (2016). Oxygen-dependent regulation of c-di-GMP synthesis by SadC controls alginate production in Pseudomonas aeruginosa. Environmental Microbiology, 18(10), 3390–3402 . https://doi.org/10.1111/1462-2920.13208