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

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...

Full description

Bibliographic Details
Main Authors: Laura Hobley, Rowena K Y Fung, Carey Lambert, Maximilian A T S Harris, Jayesh M Dabhi, Simon S King, Sarah M Basford, Kaoru Uchida, Robert Till, Rashidah Ahmad, Shin-Ichi Aizawa, Mark Gomelsky, R Elizabeth Sockett
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2012-02-01
Series:PLoS Pathogens
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/22319440/pdf/?tool=EBI
id doaj-eefe2ffe42af4fedb0e91273f4add5da
record_format Article
spelling doaj-eefe2ffe42af4fedb0e91273f4add5da2021-04-21T17:29:14ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742012-02-0182e100249310.1371/journal.ppat.1002493Discrete cyclic di-GMP-dependent control of bacterial predation versus axenic growth in Bdellovibrio bacteriovorus.Laura HobleyRowena K Y FungCarey LambertMaximilian A T S HarrisJayesh M DabhiSimon S KingSarah M BasfordKaoru UchidaRobert TillRashidah AhmadShin-Ichi AizawaMark GomelskyR Elizabeth SockettBdellovibrio 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.https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/22319440/pdf/?tool=EBI
collection DOAJ
language English
format Article
sources DOAJ
author Laura Hobley
Rowena K Y Fung
Carey Lambert
Maximilian A T S Harris
Jayesh M Dabhi
Simon S King
Sarah M Basford
Kaoru Uchida
Robert Till
Rashidah Ahmad
Shin-Ichi Aizawa
Mark Gomelsky
R Elizabeth Sockett
spellingShingle Laura Hobley
Rowena K Y Fung
Carey Lambert
Maximilian A T S Harris
Jayesh M Dabhi
Simon S King
Sarah M Basford
Kaoru Uchida
Robert Till
Rashidah Ahmad
Shin-Ichi Aizawa
Mark Gomelsky
R Elizabeth Sockett
Discrete cyclic di-GMP-dependent control of bacterial predation versus axenic growth in Bdellovibrio bacteriovorus.
PLoS Pathogens
author_facet Laura Hobley
Rowena K Y Fung
Carey Lambert
Maximilian A T S Harris
Jayesh M Dabhi
Simon S King
Sarah M Basford
Kaoru Uchida
Robert Till
Rashidah Ahmad
Shin-Ichi Aizawa
Mark Gomelsky
R Elizabeth Sockett
author_sort Laura Hobley
title Discrete cyclic di-GMP-dependent control of bacterial predation versus axenic growth in Bdellovibrio bacteriovorus.
title_short Discrete cyclic di-GMP-dependent control of bacterial predation versus axenic growth in Bdellovibrio bacteriovorus.
title_full Discrete cyclic di-GMP-dependent control of bacterial predation versus axenic growth in Bdellovibrio bacteriovorus.
title_fullStr Discrete cyclic di-GMP-dependent control of bacterial predation versus axenic growth in Bdellovibrio bacteriovorus.
title_full_unstemmed Discrete cyclic di-GMP-dependent control of bacterial predation versus axenic growth in Bdellovibrio bacteriovorus.
title_sort discrete cyclic di-gmp-dependent control of bacterial predation versus axenic growth in bdellovibrio bacteriovorus.
publisher Public Library of Science (PLoS)
series PLoS Pathogens
issn 1553-7366
1553-7374
publishDate 2012-02-01
description 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.
url https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/22319440/pdf/?tool=EBI
work_keys_str_mv AT laurahobley discretecyclicdigmpdependentcontrolofbacterialpredationversusaxenicgrowthinbdellovibriobacteriovorus
AT rowenakyfung discretecyclicdigmpdependentcontrolofbacterialpredationversusaxenicgrowthinbdellovibriobacteriovorus
AT careylambert discretecyclicdigmpdependentcontrolofbacterialpredationversusaxenicgrowthinbdellovibriobacteriovorus
AT maximilianatsharris discretecyclicdigmpdependentcontrolofbacterialpredationversusaxenicgrowthinbdellovibriobacteriovorus
AT jayeshmdabhi discretecyclicdigmpdependentcontrolofbacterialpredationversusaxenicgrowthinbdellovibriobacteriovorus
AT simonsking discretecyclicdigmpdependentcontrolofbacterialpredationversusaxenicgrowthinbdellovibriobacteriovorus
AT sarahmbasford discretecyclicdigmpdependentcontrolofbacterialpredationversusaxenicgrowthinbdellovibriobacteriovorus
AT kaoruuchida discretecyclicdigmpdependentcontrolofbacterialpredationversusaxenicgrowthinbdellovibriobacteriovorus
AT roberttill discretecyclicdigmpdependentcontrolofbacterialpredationversusaxenicgrowthinbdellovibriobacteriovorus
AT rashidahahmad discretecyclicdigmpdependentcontrolofbacterialpredationversusaxenicgrowthinbdellovibriobacteriovorus
AT shinichiaizawa discretecyclicdigmpdependentcontrolofbacterialpredationversusaxenicgrowthinbdellovibriobacteriovorus
AT markgomelsky discretecyclicdigmpdependentcontrolofbacterialpredationversusaxenicgrowthinbdellovibriobacteriovorus
AT relizabethsockett discretecyclicdigmpdependentcontrolofbacterialpredationversusaxenicgrowthinbdellovibriobacteriovorus
_version_ 1714666099992166400