A Subset of Exoribonucleases Serve as Degradative Enzymes for pGpG in c-di-GMP Signaling

Orr, Mona W.; Weiss, Cordelia A; Severin, Geoffrey B.; Turdiev, Husan; Kim, Sang-Yong; Turdiev, Asan; Liu, Kuanqing; Tu, Benjamin P.; Waters, Christopher M.; Winkler, William E.; Lee, Vincent T.

doi:10.1128/jb.00300-18

Cited by 28 publications

(32 citation statements)

References 46 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…We also attempted to quantify intracellular pGpG levels, but levels of pGpG were below the limit of detection for both wild-type and ΔpdeH cells (data not shown). A previous study quantified intracellular pGpG by LC-MS/MS in a B. subtilis mutant devoid of NrnA and NrnB, which are the two exoribonucleases thought to degrade pGpG in Firmicutes and other organisms that do not encode oligoribonuclease (Orn) (41). Similar to our current study, pGpG was undetectable in wild-type cells and could only be detected in the ΔnrnA ΔnrnB double mutant.…”

Section: Resultssupporting

confidence: 86%

“…The second messenger can then bind intracellular effectors to direct physiological changes. EAL or HD-GYP domain-containing phosphodiesterases (PDEs) hydrolyze cyclic di-GMP into the linear dinucleotide 5=-phosphoguanylyl-(3=-5=)-guanosine (pGpG) (29)(30)(31)(32)(33)(34)(35)(36)(37)(38), which is then recycled into nucleoside monophosphate pools through the action of oligoribonucleases (39)(40)(41)). Through bioinformatic analyses, GGDEF, EAL, and HD-GYP domain-containing enzymes have readily been identified in almost all bacterial phyla (35,42).…”

mentioning

confidence: 99%

See 1 more Smart Citation

Single-Cell Microscopy Reveals That Levels of Cyclic di-GMP Vary among Bacillus subtilis Subpopulations

et al. 2019

Self Cite

View full text Add to dashboard Cite

The synthesis of signaling molecules is one strategy bacteria employ to sense alterations in their environment and rapidly adjust to those changes. In Gramnegative bacteria, bis-(3=-5=)-cyclic dimeric GMP (c-di-GMP) regulates the transition from a unicellular motile state to a multicellular sessile state. However, c-di-GMP signaling has been less intensively studied in Gram-positive organisms. To that end, we constructed a fluorescent yfp reporter based on a c-di-GMP-responsive riboswitch to visualize the relative abundance of c-di-GMP for single cells of the Gram-positive model organism Bacillus subtilis. Coupled with cell-type-specific fluorescent reporters, this riboswitch reporter revealed that c-di-GMP levels are markedly different among B. subtilis cellular subpopulations. For example, cells that have made the decision to become matrix producers maintain higher intracellular c-di-GMP concentrations than motile cells. Similarly, we find that c-di-GMP levels differ between sporulating and competent cell types. These results suggest that biochemical measurements of c-di-GMP abundance are likely to be inaccurate for a bulk ensemble of B. subtilis cells, as such measurements will average c-di-GMP levels across the population. Moreover, the significant variation in c-di-GMP levels between cell types hints that c-di-GMP might play an important role during B. subtilis biofilm formation. This study therefore emphasizes the importance of using single-cell approaches for analyzing metabolic trends within ensemble bacterial populations. IMPORTANCE Many bacteria have been shown to differentiate into genetically identical yet morphologically distinct cell types. Such population heterogeneity is especially prevalent among biofilms, where multicellular communities are primed for unexpected environmental conditions and can efficiently distribute metabolic responsibilities. Bacillus subtilis is a model system for studying population heterogeneity; however, a role for c-di-GMP in these processes has not been thoroughly investigated. Herein, we introduce a fluorescent reporter, based on a c-di-GMP-responsive riboswitch, to visualize the relative abundance of c-di-GMP for single B. subtilis cells. Our analysis shows that c-di-GMP levels are conspicuously different among B. subtilis cellular subtypes, suggesting a role for c-di-GMP during biofilm formation. These data highlight the utility of riboswitches as tools for imaging metabolic changes within individual bacterial cells. Analyses such as these offer new insight into c-di-GMP-regulated phenotypes, especially given that other biofilms also consist of multicellular communities.

show abstract

Section: Resultssupporting

confidence: 86%

mentioning

confidence: 99%

Single-Cell Microscopy Reveals That Levels of Cyclic di-GMP Vary among Bacillus subtilis Subpopulations

et al. 2019

Self Cite

View full text Add to dashboard Cite

show abstract

“…Many of these are RNases that normally are not active in growing cells, but are activated under stress conditions as the antitoxins that normally keep them under control are destroyed. These TA systems have been extensively reviewed, but some recent relevant ones are in references (Hall et al 2017; Orr et al 2018; Nikolic 2019). In E. coli , the most well studied RNase toxins are RelE, MazF, and HicA, all of which are endoribonucleases that cleave mRNAs with varying degrees of specificity.…”

Section: Other Rnasesmentioning

confidence: 99%

Bacterial ribonucleases and their roles in RNA metabolism

Bechhofer

Deutscher

2019

Critical Reviews in Biochemistry and Molecular Biology

145

132

View full text Add to dashboard Cite

Ribonucleases (RNases) are mediators in most reactions of RNA metabolism. In recent years, there has been a surge of new information about RNases and the roles they play in cell physiology. In this review, a detailed description of bacterial RNases is presented, focusing primarily on those from Escherichia coli and Bacillus subtilis, the model Gram-negative and Gram-positive organisms, from which most of our current knowledge has been derived. Information from other organisms is also included, where relevant. In an extensive catalog of the known bacterial RNases, their structure, mechanism of action, physiological roles, genetics, and possible regulation are described. The RNase complement of E. coli and B. subtilis is compared, emphasizing the similarities, but especially the differences, between the two. Included are figures showing the three major RNA metabolic pathways in E. coli and B. subtilis and highlighting specific steps in each of the pathways catalyzed by the different RNases. This compilation of the currently available knowledge about bacterial RNases will be a useful tool for workers in the RNA field and for others interested in learning about this area.

show abstract

“…Studies investigating the intracellular concentrations of c-di-GMP in B. subtilis suggested growth phase-dependent differences. While c-di-GMP could not be detected during vegetative growth in standard rich medium (Gao et al 2013), relative high concentrations were detected for cells at the onset of sporulation and for cells grown in biofilm-promoting medium (Diethmaier et al 2014;Orr et al 2018). Therefore, it seems that equivalent to the c-di-GMP signaling in Gram-negative bacteria such as E. coli, the concentration of this second messenger rises at the onset of stationary phase (Sommerfeldt et al 2009).…”

Section: Cyclic Di-guanosinemonophosphate (C-di-gmp) In B Subtilismentioning

confidence: 95%

Physiology of guanosine-based second messenger signaling in Bacillus subtilis

Bange

Bedrunka

2020

Biological Chemistry

View full text Add to dashboard Cite

The guanosine-based second messengers (p)ppGpp and c-di-GMP are key players of the physiological regulation of the Gram-positive model organism B. subtilis. Their regulatory spectrum ranges from key metabolic processes over motility to biofilm formation. Here we review our mechanistic knowledge on their synthesis and degradation in response to environmental and stress signals as well as what is known on their cellular effectors and targets. Moreover, we discuss open questions and our gaps in knowledge on these two important second messengers.

show abstract

A Subset of Exoribonucleases Serve as Degradative Enzymes for pGpG in c-di-GMP Signaling

Cited by 28 publications

References 46 publications

Single-Cell Microscopy Reveals That Levels of Cyclic di-GMP Vary among Bacillus subtilis Subpopulations

Single-Cell Microscopy Reveals That Levels of Cyclic di-GMP Vary among Bacillus subtilis Subpopulations

Bacterial ribonucleases and their roles in RNA metabolism

Physiology of guanosine-based second messenger signaling in Bacillus subtilis

Contact Info

Product

Resources

About