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Discrete cyclic di-GMP-dependent control of bacterial predation versus axenic growth in Bdellovibrio bacteriovorus

Hobley, Laura; Fung, Rowena K. Y.; Lambert, Carey; Harris, Maximilian A.T.S.; Dabh, Jayesh M.; King, Simon S.; Basford, Sarah M.; Uchida, Kaoru; Till, Robert; Ahmad, Rashidah; Aizawa, Shin-Ichi; Gomelsky, Mark; Sockett, R. Elizabeth

Authors

Laura Hobley

Rowena K. Y. Fung

Carey Lambert

Maximilian A.T.S. Harris

Jayesh M. Dabh

Simon S. King

Sarah M. Basford

Kaoru Uchida

Robert Till

Rashidah Ahmad

Shin-Ichi Aizawa

Mark Gomelsky

R. Elizabeth Sockett



Abstract

Bdellovibrio bacteriovorus is a Delta-proteobacterium that oscillates between free-living growth and predation on Gram-negative bacteria including important pathogens of man, animals and plants. After entering the prey periplasm, killing the prey and replicating inside the prey bdelloplast, several motile B. bacteriovorus progeny cells emerge. The B. bacteriovorus HD100 genome encodes numerous proteins predicted to be involved in signalling via the secondary messenger cyclic di-GMP (c-di-GMP), which is known to affect bacterial lifestyle choices. We investigated the role of c-di-GMP signalling in B. bacteriovorus, focussing on the five GGDEF domain proteins that are predicted to function as diguanylyl cyclases initiating c-di-GMP signalling cascades. Inactivation of individual GGDEF domain genes resulted in remarkably distinct phenotypes. Deletion of dgcB (Bd0742) resulted in a predation impaired, obligately axenic mutant, while deletion of dgcC (Bd1434) resulted in the opposite, obligately predatory mutant. Deletion of dgcA (Bd0367) abolished gliding motility, producing bacteria capable of predatory invasion but unable to leave the exhausted prey. Complementation was achieved with wild type dgc genes, but not with GGAAF versions. Deletion of cdgA (Bd3125) substantially slowed predation; this was restored by wild type complementation. Deletion of dgcD (Bd3766) had no observable phenotype. In vitro assays showed that DgcA, DgcB, and DgcC were diguanylyl cyclases. CdgA lacks enzymatic activity but functions as a c-di-GMP receptor apparently in the DgcB pathway. Activity of DgcD was not detected. Deletion of DgcA strongly decreased the extractable c-di-GMP content of axenic Bdellovibrio cells. We show that c-di-GMP signalling pathways are essential for both the free-living and predatory lifestyles of B. bacteriovorus and that obligately predatory dgcC- can be made lacking a propensity to survive without predation of bacterial pathogens and thus possibly useful in anti-pathogen applications. In contrast to many studies in other bacteria, Bdellovibrio shows specificity and lack of overlap in c-di-GMP signalling pathways.

Journal Article Type Article
Publication Date Feb 2, 2012
Journal PloS Pathogens
Print ISSN 1553-7366
Electronic ISSN 1553-7374
Publisher Public Library of Science
Peer Reviewed Peer Reviewed
Volume 8
Issue 2
Article Number e1002493
Institution Citation Hobley, L., Fung, R. K. Y., Lambert, C., Harris, M. A., Dabh, J. M., King, S. S., …Sockett, R. E. (2012). Discrete cyclic di-GMP-dependent control of bacterial predation versus axenic growth in Bdellovibrio bacteriovorus. PLoS Pathogens, 8(2), doi:10.1371/journal.ppat.1002493
DOI https://doi.org/10.1371/journal.ppat.1002493
Publisher URL http://www.plospathogens.org/article/info%3Adoi%2F10.1371%2Fjournal.ppat.1002493
Copyright Statement Copyright information regarding this work can be found at the following address: http://creativecommons.org/licenses/by/4.0

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Copyright Statement
Copyright information regarding this work can be found at the following address: http://creativecommons.org/licenses/by/4.0



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