Growth on glucose decreases cAMP‐CRP activity while paradoxically increasing intracellular cAMP in the light‐organ symbiont Vibrio fischeri

Summary Proteobacteria often co‐ordinate responses to carbon sources using CRP and the second messenger cyclic 3′, 5′‐AMP (cAMP), which combine to control transcription of genes during growth on non‐glucose substrates as part of the catabolite‐repression response. Here we show that cAMP‐CRP is activ...

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Bibliographic Details
Published in:Molecular microbiology 2015-09, Vol.97 (6), p.1114-1127
Main Authors: Colton, Deanna M., Stoudenmire, Julie L., Stabb, Eric V.
Format: Article
Language:English
Subjects:
Aliivibrio fischeri - chemistry
Aliivibrio fischeri - growth & development
Aliivibrio fischeri - metabolism
ATP-Binding Cassette Transporters - metabolism
Bacterial Proteins - genetics
Bacterial Proteins - metabolism
Carrier Proteins - metabolism
Cyclic AMP - metabolism
Glucose
Glucose - metabolism
Glycerol
Gram-negative bacteria
Helicobacter pylori - genetics
Helicobacter pylori - metabolism
Metals - metabolism
Microbiology
Nitric Oxide - metabolism
Transcription factors
Transcription, Genetic
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Summary:Summary Proteobacteria often co‐ordinate responses to carbon sources using CRP and the second messenger cyclic 3′, 5′‐AMP (cAMP), which combine to control transcription of genes during growth on non‐glucose substrates as part of the catabolite‐repression response. Here we show that cAMP‐CRP is active and important in Vibrio fischeri during colonization of its host squid Euprymna scolopes. Moreover, consistent with a classical role in catabolite repression, a cAMP‐CRP‐dependent reporter showed lower activity in cells grown in media amended with glucose rather than glycerol. Surprisingly though, intracellular cAMP levels were higher in glucose‐grown cells. Mutant analyses were consistent with predictions that CyaA was responsible for cAMP generation, that the EIIAGlc component of glucose transport could enhance cAMP production and that the phophodiesterases CpdA and CpdP consumed intracellular and extracellular cAMP respectively. However, the observation of lower cAMP levels in glycerol‐grown cells seemed best explained by changes in cAMP export, via an unknown mechanism. Our data also indicated that cAMP‐CRP activity decreased during growth on glucose independently of crp's native transcriptional regulation or cAMP levels. We speculate that some unknown mechanism, perhaps carbon‐source‐dependent post‐translational modulation of CRP, may help control cAMP‐CRP activity in V. fischeri. CRP combines with the second messenger cAMP to activate the pheromone‐signaling systems in Vibrio fischeri. We now show that cAMP‐CRP is critical for V. fishceri colonization of its host squid, Euprymna scolopes. Moreover, the cAMP‐CRP regulon is induced during growth on non‐glucose carbon sources and in the host. Surprisingly however, we find cAMP levels can be higher in cells grown on glucose, and that cAMP‐independent mechanisms can modulate cAMP‐CRP activity in response to glucose availability.
ISSN:0950-382X
1365-2958
DOI:10.1111/mmi.13087