The ever-expanding world of bacterial cyclic oligonucleotide second messengers

Yoon, Soo Hun; Waters, Christopher M.

doi:10.1016/j.mib.2021.01.017

Cited by 45 publications

(42 citation statements)

References 76 publications

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“…In most bacteria, the switch from planktonic growth to the sessile biofilm lifestyle is induced in response to a common second messenger cyclic di-guanosine monophosphate (c-di-GMP) (Simm et al, 2004;Hengge et al, 2016;Yoon and Waters, 2021). Responses to the intracellular concentration of c-di-GMP have been implicated in all phases of biofilm formation from initial attachment, through proliferation, and dispersal (Figure 1A; Davey and O'Toole, 2000;Joo and Otto, 2012), and promote the production of numerous EPS components involved in biofilm assembly, including extracellular DNA, protein adhesin, and exopolysaccharide (Römling, 2012).…”

Section: Introductionmentioning

confidence: 99%

“…Since the discovery of c-di-GMP, additional cyclic-dinucleotides, including cyclic-di-adenosine monophosphate (cdi-AMP) and the mixed nucleotide second messenger cyclicadenosine monophosphate-guanosine monophosphate (c-AMP-GMP), have been identified (Witte et al, 2008;Corrigan et al, 2011;Davies et al, 2012;Dias da et al, 2020;Xiong et al, 2020;Yoon and Waters, 2021). C-di-AMP was originally identified in Bacillus subtilis where it was shown to play a role in sporulation (Witte et al, 2008), and has since been identified in other Gram-positive bacteria including Staphylococcus aureus, where it is implicated in controlling cell size (Corrigan et al, 2011), and Streptococcus mutans, where it is implicated in the regulation of glucan biosynthesis (Cheng et al, 2015;Peng et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

“…The primary mechanism by which c-di-GMP regulates cell cycle progression, bacterial motility, and biofilm formation involves the interaction of c-di-GMP with a wide assortment of effectors, including riboswitches, DNA-binding proteins, protein complexes, and enzymes whose activities are allosterically regulated through binding of c-di-GMP (Valentini and Filloux, 2019). Several recent reviews thoroughly describe how c-di-GMP binding to these effectors influences transcriptional regulation, signaling, and bacterial virulence (Valentini and Filloux, 2019;Yi et al, 2019;Kunz and Graumann, 2020;Ma et al, 2020;Yoon and Waters, 2021). This review will specifically focus on how c-di-GMP post-translationally regulates biofilm formation through allosteric activation of enzyme complexes involved in the biosynthesis and export of biofilm exopolysaccharides that serve as key structural components of the biofilm EPS.…”

Section: Introductionmentioning

confidence: 99%

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Regulation of Biofilm Exopolysaccharide Production by Cyclic Di-Guanosine Monophosphate

Poulin

Kuperman

2021

Front. Microbiol.

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Many bacterial species in nature possess the ability to transition into a sessile lifestyle and aggregate into cohesive colonies, known as biofilms. Within a biofilm, bacterial cells are encapsulated within an extracellular polymeric substance (EPS) comprised of polysaccharides, proteins, nucleic acids, lipids, and other small molecules. The transition from planktonic growth to the biofilm lifecycle provides numerous benefits to bacteria, such as facilitating adherence to abiotic surfaces, evasion of a host immune system, and resistance to common antibiotics. As a result, biofilm-forming bacteria contribute to 65% of infections in humans, and substantially increase the energy and time required for treatment and recovery. Several biofilm specific exopolysaccharides, including cellulose, alginate, Pel polysaccharide, and poly-N-acetylglucosamine (PNAG), have been shown to play an important role in bacterial biofilm formation and their production is strongly correlated with pathogenicity and virulence. In many bacteria the biosynthetic machineries required for assembly of these exopolysaccharides are regulated by common signaling molecules, with the second messenger cyclic di-guanosine monophosphate (c-di-GMP) playing an especially important role in the post-translational activation of exopolysaccharide biosynthesis. Research on treatments of antibiotic-resistant and biofilm-forming bacteria through direct targeting of c-di-GMP signaling has shown promise, including peptide-based treatments that sequester intracellular c-di-GMP. In this review, we will examine the direct role c-di-GMP plays in the biosynthesis and export of biofilm exopolysaccharides with a focus on the mechanism of post-translational activation of these pathways, as well as describe novel approaches to inhibit biofilm formation through direct targeting of c-di-GMP.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Regulation of Biofilm Exopolysaccharide Production by Cyclic Di-Guanosine Monophosphate

Poulin

Kuperman

2021

Front. Microbiol.

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“…Biofilms are often promoted by cyclic-di-GMP (c-di-GMP), a ubiquitous second messenger in bacteria ( 17 – 20 ). High levels of c-di-GMP induce a sessile biofilm state, and low levels of c-di-GMP promote motility and/or switch cells to a planktonic state.…”

Section: Introductionmentioning

confidence: 99%

Para-Aminobenzoic Acid, Calcium, and c-di-GMP Induce Formation of Cohesive, Syp-Polysaccharide-Dependent Biofilms in Vibrio fischeri

Dial

Speare

Sharpe

et al. 2021

mBio

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“…In addition, many DNA binding proteins other than sigma factors are known to influence promoter activities. Several pathways that activate sigma factors or other transcription factors in response to environmental signals have been unraveled in the past (e.g., [ 5 , 6 , 7 ]). sRNAs make important contributions to post-transcriptional regulation.…”

Section: Introductionmentioning

confidence: 99%

A Complex Network of Sigma Factors and sRNA StsR Regulates Stress Responses in R. sphaeroides

Eisenhardt

Remes

Grützner

et al. 2021

IJMS

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Adaptation of bacteria to a changing environment is often accompanied by remodeling of the transcriptome. In the facultative phototroph Rhodobacter sphaeroides the alternative sigma factors RpoE, RpoHI and RpoHII play an important role in a variety of stress responses, including heat, oxidative stress and nutrient limitation. Photooxidative stress caused by the simultaneous presence of chlorophylls, light and oxygen is a special challenge for phototrophic organisms. Like alternative sigma factors, several non-coding sRNAs have important roles in the defense against photooxidative stress. RNAseq-based transcriptome data pointed to an influence of the stationary phase-induced StsR sRNA on levels of mRNAs and sRNAs with a role in the photooxidative stress response. Furthermore, StsR also affects expression of photosynthesis genes and of genes for regulators of photosynthesis genes. In vivo and in vitro interaction studies revealed that StsR, that is under control of the RpoHI and RpoHII sigma factors, targets rpoE mRNA and affects its abundance by altering its stability. RpoE regulates expression of the rpoHII gene and, consequently, expression of stsR. These data provide new insights into a complex regulatory network of protein regulators and sRNAs involved in defense against photooxidative stress and the regulation of photosynthesis genes.

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The ever-expanding world of bacterial cyclic oligonucleotide second messengers

Cited by 45 publications

References 76 publications

Regulation of Biofilm Exopolysaccharide Production by Cyclic Di-Guanosine Monophosphate

Regulation of Biofilm Exopolysaccharide Production by Cyclic Di-Guanosine Monophosphate

Para-Aminobenzoic Acid, Calcium, and c-di-GMP Induce Formation of Cohesive, Syp-Polysaccharide-Dependent Biofilms in Vibrio fischeri

A Complex Network of Sigma Factors and sRNA StsR Regulates Stress Responses in R. sphaeroides

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