Evolution of cyclic di-GMP signalling on a short and long term time scale

Römling, Ute; Cao, Lian-Ying; Bai, Fengwu

doi:10.1099/mic.0.001354

Cited by 9 publications

(7 citation statements)

References 179 publications

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“…Pflu0185 is a regulatory protein composed of two enzymatic domains: a diguanylate cyclase (DGC) -responsible for the synthesis of cyclic-di-GMP (c-di-GMP) -and a phosphodiesterase (PDE)responsible for breakdown of c-di-GMP [49]. In P. aeruginosa functional analysis shows the protein to have PDE function, but no DGC activity [8], which is consistent with the genetic analysis reported here.…”

Section: Local Hyper-mutability Underpins Lineage Adaptationsupporting

confidence: 84%

Experimental evolution of evolvability

Barnett,

Zeller,

Rainey

2024

Preprint

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It has been proposed that capacity to generate variation can evolve by natural selection such that mutation becomes biased toward adaptive outcomes. However the idea that selection might drive the evolution of evolvability has remained largely theoretical. Here we detail the de novo evolution of evolvability in experimental populations of bacteria, making explicit the selective processes and molecular events. Key to experimental realisation was a lineage-level birth-death dynamic, where lineage reproductive success was dependent upon capacity to mutate between two target phenotypic states, each optima in a repeating cycle of environments. Fueled by variation in evolutionary potential associated with unique mutational paths, lineages capable of mediating rapid and reliable transitions between states through local mutational bias emerged. The mechanism is analogous to that underpinning highly mutable "contingency loci" in pathogenic bacteria. Drawing upon detailed knowledge of the evolutionary history of lineages, we identify key steps in construction of the locus, including changes to the genotype-phenotype map and input from mutations that elevated transcription and concomitantly, rates of localised frame-shifting. We also document ancillary advantages to rapid phenotype switching, with lineages possessing this ability being more likely to acquire secondary adaptive mutations. Our results provide a mechanistic account of a previously puzzling evolutionary phenomenon and clarify conditions for the adaptive evolution of evolvability.

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Section: Local Hyper-mutability Underpins Lineage Adaptationsupporting

confidence: 84%

Experimental evolution of evolvability

Barnett,

Zeller,

Rainey

2024

Preprint

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“…There may also be other factors that act to inhibit EmaS in the wild-type strain, which could result in higher expression of P emaS in ∆emaS compared to the wild type. A similar scenario has been observed in P. aeruginosa, where it was found that the regulatory protein HapZ interacts with the REC domain of the sensor protein SagS when bound to cyclic di-GMP, thereby inhibiting phosphate transfer between SagS and downstream proteins [26]. Through SMART (Simple Modular Architecture Research Tool) analysis of its secondary structure, we found that the sensor protein EmaS also possesses a REC domain within its C-terminal structure, which can receive signals from sensor proteins and bind with DNA.…”

Section: Kinetic Characterization Of Dj41_2796supporting

confidence: 70%

Gene Expression of Ethanol and Acetate Metabolic Pathways in the Acinetobacter baumannii EmaSR Regulon

Huang,

Shu,

Lin

2024

Microorganisms

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Background: Previous studies have confirmed the involvement of EmaSR (ethanol metabolism a sensor/regulator) in the regulation of Acinetobacter baumannii ATCC 19606 ethanol and acetate metabolism. RNA-seq analysis further revealed that DJ41_568-571, DJ41_2796, DJ41_3218, and DJ41_3568 regulatory gene clusters potentially participate in ethanol and acetate metabolism under the control of EmaSR. Methods: This study fused the EmaSR regulon promoter segments with reporter genes and used fluorescence expression levels to determine whether EmaSR influences regulon expression in ethanol or acetate salt environments. The enzymatic function and kinetics of significantly regulated regulons were also studied. Results: The EmaSR regulons P2796 and P3218 exhibited > 2-fold increase in fluorescence expression in wild type compared to mutant strains in both ethanol and acetate environments, and PemaR demonstrated a comparable trend. Moreover, increases in DJ41_2796 concentration enhanced the conversion of acetate and succinyl-CoA into acetyl-CoA and succinate, suggesting that DJ41_2796 possesses acetate: succinyl-CoA transferase (ASCT) activity. The kcat/KM values for DJ41_2796 with potassium acetate, sodium acetate, and succinyl-CoA were 0.2131, 0.4547, and 20.4623 mM−1s−1, respectively. Conclusions: In A. baumannii, EmaSR controls genes involved in ethanol and acetate metabolism, and the EmaSR regulon DJ41_2796 was found to possess ASCT activity.

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“…Binding of cyclic di-GMP to the elongation factor P facilitates translation of proline tracks in biofilm proteins and to the α-L-glutamate ligase RimK stimulates its enzymatic activity leading to C-terminal glutaminylation of the ribosomal protein RpsF to modulate translation (Guo et al, 2022;Little et al, 2016). On the overall evolutionary time scale equally as the cyclic di-GMP network encoded by genomes, cyclic di-GMP binding sites of individual proteins can rapidly appear and disappear in evolution (Römling, 2023).…”

Section: Iver S It Y and Pl A S Ti Cit Y Of C Yclic Di-g Mp Recep Tor Smentioning

confidence: 99%

“…Cyclic di-AMP signaling seems to have been diminished almost entirely in many phyla though, predominantly in alpha-, beta-, and gamma-proteobacteria. Equally, but by far less frequently, cyclic di-GMP signaling has been reduced or entirely disappeared rapidly in evolutionary terms within Pseudomonadota (previously proteobacteria) and other phyla (Liu et al, 2020;Ojha et al, 2021;Römling et al, 2023). This evolutionary flexibility is remarkable with the number of cyclic di-GMP turnover proteins to span from 0 to 86 for a genome of even minor size within a phylum (http://www-ncbi-nlm-nih-gov.proxy.kib.ki.se/Compl ete_Genom es/c-di-GMP.html).…”

Section: Yclic Di-g Mp a S A Ub I Qu Itous Life S T Yle Reg Ul Ator I...mentioning

confidence: 99%

Cyclic di‐GMP signaling—Where did you come from and where will you go?

Römling

2023

Molecular Microbiology

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Microbes including bacteria are required to respond to their often continuously changing ecological niches in order to survive. While many signaling molecules are produced as seemingly circumstantial byproducts of common biochemical reactions, there are a few second messenger signaling systems such as the ubiquitous cyclic di‐GMP second messenger system that arise through the synthesis of dedicated multidomain enzymes triggered by multiple diverse external and internal signals. Being one of the most numerous and widespread signaling system in bacteria, cyclic di‐GMP signaling contributes to adjust physiological and metabolic responses in all available ecological niches. Those niches range from deep‐sea and hydrothermal springs to the intracellular environment in human immune cells such as macrophages. This outmost adaptability is possible by the modularity of the cyclic di‐GMP turnover proteins which enables coupling of enzymatic activity to the diversity of sensory domains and the flexibility in cyclic di‐GMP binding sites. Nevertheless, commonly regulated fundamental microbial behavior include biofilm formation, motility, and acute and chronic virulence. The dedicated domains carrying out the enzymatic activity indicate an early evolutionary origin and diversification of “bona fide” second messengers such as cyclic di‐GMP which is estimated to have been present in the last universal common ancestor of archaea and bacteria and maintained in the bacterial kingdom until today. This perspective article addresses aspects of our current view on the cyclic di‐GMP signaling system and points to knowledge gaps that still await answers.

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Evolution of cyclic di-GMP signalling on a short and long term time scale

Abstract: Graphical Abstract

Cited by 9 publications

References 179 publications

Experimental evolution of evolvability

Experimental evolution of evolvability

Gene Expression of Ethanol and Acetate Metabolic Pathways in the Acinetobacter baumannii EmaSR Regulon

Cyclic di‐GMP signaling—Where did you come from and where will you go?

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