Sensory Domains That Control Cyclic di-GMP-Modulating Proteins: A Critical Frontier in Bacterial Signal Transduction

Dayton, Hannah; Smiley, Marina K; Forouhar, F.; Harrison, Joe J.; Price-Whelan, Alexa; Dietrich, Lars E. P.

doi:10.1007/978-3-030-33308-9_9

Cited by 6 publications

(10 citation statements)

References 85 publications

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“…Cellular c-di-GMP levels are modulated by diguanylate cyclases (DGCs), which synthesize c-di-GMP, and phosphodiesterases (PDEs), which degrade it (45). The P. aeruginosa genome encodes 40 proteins with domains implicated in DGC or PDE activity (25,46,47). To identify proteins that could link light sensing to modulation of c-di-GMP levels and therefore biofilm matrix production (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…In this context, it is interesting to note domains in RmcA and DipA with the potential to play sensory roles: RmcA contains an N-terminal, periplasmic arginine-sensing domain (51), followed by four cytoplasmic Per-Arnt-Sim (PAS) domains, while DipA has an N-terminal PAS-GAF-PAS domain architecture. PAS and GAF domains are broadly distributed throughout the tree of life and are frequently involved in sensing stimuli (47,(52)(53)(54). Some of the best-known examples of PAS domain-containing proteins mediate behavioral responses to changes in light exposure, oxygen availability, or the cellular redox state (1,13,(55)(56)(57)(58).…”

Section: Resultsmentioning

confidence: 99%

“…We have previously investigated the role of RmcA in sensing phenazines and inhibiting biofilm wrinkling in the dark (25). Based on sequence analysis and modeling, we have suggested that RmcA's four PAS domains, in order from the N terminus, could bind (i) phenazine, (ii) lipid, (iii) heme, and (iv) FAD, respectively (25,47). A biochemical characterization of purified RmcA provided support for the notion that this protein may bind phenazine and FAD (25).…”

Section: Resultsmentioning

confidence: 99%

“…Although RmcA does not contain a LOV domain, its putative FAD-binding domain PASd shares significant similarities with NifL from Azotobacter vinelandii, which bears resemblance to LOV domains (Fig. S2B) (25,47,59,63). As an initial assessment of the potential involvement of RmcA's PASd domain in light-dependent effects on biofilm development, we grew a ΔrmcA mutant and mutants with deletions in the RmcA PASb ("ΔPASb") and PASd ("ΔPASd") domains in the colony morphology assay and monitored onset of wrinkling in the presence or absence of light.…”

Section: Resultsmentioning

confidence: 99%

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Light-Mediated Decreases in Cyclic di-GMP Levels Inhibit Structure Formation inPseudomonas aeruginosaBiofilms

Kahl¹,

Price-Whelan²,

Dietrich³

2020

J Bacteriol

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Light is known to trigger regulatory responses in diverse organisms, including slime molds, animals, plants, and phototrophic bacteria. However, light-dependent processes in nonphototrophic bacteria, and those of pathogens in particular, have received comparatively little research attention. In this study, we examined the impact of light on multicellular development in Pseudomonas aeruginosa, a leading cause of biofilm-based bacterial infections. We grew P. aeruginosa strain PA14 in a colony morphology assay and found that growth under prolonged exposure to low-intensity blue light inhibited biofilm matrix production and thereby the formation of vertical biofilm structures (i.e., “wrinkles”). Light-dependent inhibition of biofilm wrinkling was correlated with low levels of cyclic di-GMP (c-di-GMP), consistent with the role of this signal in stimulating matrix production. A screen of enzymes with the potential to catalyze c-di-GMP synthesis or degradation identified c-di-GMP phosphodiesterases that contribute to light-dependent inhibition of biofilm wrinkling. One of these, RmcA, was previously characterized by our group for its role in mediating the effect of redox-active P. aeruginosa metabolites called phenazines on biofilm wrinkle formation. Our results suggest that an RmcA sensory domain that is predicted to bind a flavin cofactor is involved in light-dependent inhibition of wrinkling. Together, these findings indicate that P. aeruginosa integrates information about light exposure and redox state in its regulation of biofilm development. IMPORTANCE Light exposure tunes circadian rhythms, which modulate the immune response and affect susceptibility to infection in plants and animals. Though molecular responses to light are defined for model plant and animal hosts, analogous pathways that function in bacterial pathogens are understudied. We examined the response to light exposure in biofilms (matrix-encased multicellular assemblages) of the nonphotosynthetic bacterium Pseudomonas aeruginosa. We found that light at intensities that are not harmful to human cells inhibited biofilm maturation via effects on cellular signals. Because biofilm formation is a critical factor in many types of P. aeruginosa infections, including burn wound infections that may be exposed to light, these effects could be relevant for pathogenicity.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

See 2 more Smart Citations

Light-Mediated Decreases in Cyclic di-GMP Levels Inhibit Structure Formation inPseudomonas aeruginosaBiofilms

Kahl¹,

Price-Whelan²,

Dietrich³

2020

J Bacteriol

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“… 16 , 17 With diverse primary sequences of less than 150 amino acids in size, compact PAS domains possess an interior pocket built characteristically by five antiparallel β-strands and flanked by a few α-helices to host a variety of prosthetic groups and ligands, with few functional amino acids to determine the binding specificity. 16 , 18 …”

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confidence: 99%

A Cyclic di-GMP Network Is Present in Gram-Positive Streptococcus and Gram-Negative Proteus Species

Liu

Lee

et al. 2020

ACS Infect. Dis.

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The ubiquitous cyclic di-GMP (c-di-GMP) network is highly redundant with numerous GGDEF domain proteins as diguanylate cyclases and EAL domain proteins as c-di-GMP specific phosphodiesterases comprising those domains as two of the most abundant bacterial domain superfamilies. One hallmark of the c-di-GMP network is its exalted plasticity as c-di-GMP turnover proteins can rapidly vanish from species within a genus and possess an above average transmissibility. To address the evolutionary forces of c-di-GMP turnover protein maintenance, conservation, and diversity, we investigated a Gram-positive and a Gram-negative species, which preserved only one single clearly identifiable GGDEF domain protein. Species of the family Morganellaceae of the order Enterobacterales exceptionally show disappearance of the c-di-GMP signaling network, but Proteus spp. still retained one diguanylate cyclase. As another example, in species of the bovis, pyogenes, and salivarius subgroups as well as Streptococcus suis and Streptococcus henryi of the genus Streptococcus , one candidate diguanylate cyclase was frequently identified. We demonstrate that both proteins encompass PAS (Per-ARNT-Sim)-GGDEF domains, possess diguanylate cyclase catalytic activity, and are suggested to signal via a PilZ receptor domain at the C-terminus of type 2 glycosyltransferase constituting BcsA cellulose synthases and a cellulose synthase-like protein CelA, respectively. Preservation of the ancient link between production of cellulose(-like) exopolysaccharides and c-di-GMP signaling indicates that this functionality is even of high ecological importance upon maintenance of the last remnants of a c-di-GMP signaling network in some of today’s free-living bacteria.

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Intact and mutated Shigella diguanylate cyclases increase c-di-GMP

Ojha,

Krug,

Jones

et al. 2024

Journal of Biological Chemistry

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Sensory Domains That Control Cyclic di-GMP-Modulating Proteins: A Critical Frontier in Bacterial Signal Transduction

Cited by 6 publications

References 85 publications

Light-Mediated Decreases in Cyclic di-GMP Levels Inhibit Structure Formation inPseudomonas aeruginosaBiofilms

Light-Mediated Decreases in Cyclic di-GMP Levels Inhibit Structure Formation inPseudomonas aeruginosaBiofilms

A Cyclic di-GMP Network Is Present in Gram-Positive Streptococcus and Gram-Negative Proteus Species

Intact and mutated Shigella diguanylate cyclases increase c-di-GMP

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