Genome-Based Comparison of Cyclic Di-GMP Signaling in Pathogenic and Commensal Escherichia coli Strains

Povolotsky, Tatyana L.; Hengge, Regine

doi:10.1128/jb.00520-15

Cited by 60 publications

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References 79 publications

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“…Genes involved in c-di-GMP signaling have also been studied in pathogenic E. coli, i.e., in uropathogenic E. coli (UPEC) (42), and two additional genes encoding PDEs have been detected in an enterohemorrhagic E. coli (EHEC) strain (38) and a meningitis-associated E. coli strain (39). Together with a recent analysis of genome sequences of 61 E. coli strains (29), which included commensal as well as pathogenic strains of the major pathotypes and phylogroups, a total of two additional GGDEF domain proteins and four more EAL domain proteins have been identified that are not found in E. coli K-12. On the basis of the presence of the key residues involved in enzymatic activities, these proteins should be active DGCs and PDEs (see an accompanying paper [29] in this issue).…”

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“…However, on the basis of the finding that the DGC YdeH is regulated by zinc, it was recently renamed "DgcZ" (23). Also, the newly identified genes encoding DGCs and PDEs in non-K-12 E. coli strains had to be given names, and it seemed obvious to use a dgc and pde nomenclature (29).…”

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“…Together with a recent analysis of genome sequences of 61 E. coli strains (29), which included commensal as well as pathogenic strains of the major pathotypes and phylogroups, a total of two additional GGDEF domain proteins and four more EAL domain proteins have been identified that are not found in E. coli K-12. On the basis of the presence of the key residues involved in enzymatic activities, these proteins should be active DGCs and PDEs (see an accompanying paper [29] in this issue).Being aware that a systematic nomenclature of the many E. coli genes encoding DGCs and PDEs might eventually be useful, most researchers have refrained from renaming single genes and proteins involved in c-di-GMP signaling in E. coli and have used the preliminary y designations instead, even though these were difficult to memorize and certainly not popular in oral scientific presentations. However, on the basis of the finding that the DGC YdeH is regulated by zinc, it was recently renamed "DgcZ" (23).…”

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Systematic Nomenclature for GGDEF and EAL Domain-Containing Cyclic Di-GMP Turnover Proteins of Escherichia coli

et al. 2016

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hIn recent years, Escherichia coli has served as one of a few model bacterial species for studying cyclic di-GMP (c-di-GMP) signaling. The widely used E. coli K-12 laboratory strains possess 29 genes encoding proteins with GGDEF and/or EAL domains, which include 12 diguanylate cyclases (DGC), 13 c-di-GMP-specific phosphodiesterases (PDE), and 4 "degenerate" enzymatically inactive proteins. In addition, six new GGDEF and EAL (GGDEF/EAL) domain-encoding genes, which encode two DGCs and four PDEs, have recently been found in genomic analyses of commensal and pathogenic E. coli strains. As a group of researchers who have been studying the molecular mechanisms and the genomic basis of c-di-GMP signaling in E. coli, we now propose a general and systematic dgc and pde nomenclature for the enzymatically active GGDEF/EAL domain-encoding genes of this model species. This nomenclature is intuitive and easy to memorize, and it can also be applied to additional genes and proteins that might be discovered in various strains of E. coli in future studies. More than 10 years ago, it was demonstrated that GGDEF domains can produce and EAL domains can degrade the bacterial second messenger cyclic di-GMP (c-di-GMP) (1-4). With these assignments, it also became clear that bacterial genomes-in particular, those of gammaproteobacteria-usually contain multiple genes encoding these diguanylate cyclases (DGC) and c-di-GMP phosphodiesterases (PDE) (5, 6). Crystal structures of GGDEF and EAL domains have been elucidated, and studies of structure-function relationships have identified the key amino acid residues required for substrate and cation binding and catalysis (7). This also allowed identification of a subset of GGDEF and EAL (GGDEF/EAL) domain proteins, in which these key amino acids are not conserved, as "degenerate" and enzymatically inactive. In a few cases, it could be demonstrated that these degenerate GGDEF/EAL domain proteins have alternative functions based on direct interactions with other macromolecules (8-11). A subset of proteins combine GGDEF and EAL domains in a single polypeptide, where one domain is usually enzymatically active and the other is degenerate and plays a regulatory role in these "composite" proteins (3). Most GGDEF/EAL domain proteins also contain N-terminal sensory input domains that control their output activities, and a majority are localized or anchored in the cytoplasmic membrane via their membrane-intrinsic or periplasmic sensory domains (12).In studies of the molecular principles and physiological functions of c-di-GMP signaling, Escherichia coli has served as one of a few model species (13,14). The commonly used E. coli K-12 laboratory strain has a total of 29 proteins with GGDEF and/or EAL domains, including 12 and 10 proteins featuring the GGDEF and EAL domains alone, respectively, and 7 composite proteins carrying both domains. Based on direct measurements of purified proteins and/or the presence of key conserved amino acids and their elimination by point mutations, DGC and PDE activities can ...

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Systematic Nomenclature for GGDEF and EAL Domain-Containing Cyclic Di-GMP Turnover Proteins of Escherichia coli

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“…An EAL-only-encoding gene, sfaY II , is part of a pathogenicity island in a newborn meningitis E. coli isolate and its expression in Vibrio cholerae has been shown to affect biofilm formation (37). Similar EAL-only proteins PdeW, PdeX, and PdeY have been found encoded in the genomes of various enteropathogenic and enterotoxigenic strains of E. coli (38).…”

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Stand-Alone EAL Domain Proteins Form a Distinct Subclass of EAL Proteins Involved in Regulation of Cell Motility and Biofilm Formation in Enterobacteria

et al. 2017

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The second messenger cyclic dimeric GMP (c-di-GMP) is almost ubiquitous among bacteria as are the c-di-GMP turnover proteins, which mediate the transition between motility and sessility. EAL domain proteins have been characterized as c-di-GMP-specific phosphodiesterases. While most EAL domain proteins contain additional, usually N-terminal, domains, there is a distinct family of proteins with stand-alone EAL domains, exemplified by Salmonella enterica serovar Typhimurium proteins STM3611 (YhjH/PdeH), a c-di-GMP-specific phosphodiesterase, and the enzymatically inactive STM1344 (YdiV/CdgR) and STM1697, which regulate bacterial motility through interaction with the flagellar master regulator, FlhDC. We have analyzed the phylogenetic distribution of EAL-only proteins and their potential functions. Genes encoding EAL-only proteins were found in various bacterial phyla, although most of them were seen in proteobacteria, particularly enterobacteria. Based on the conservation of the active site residues, nearly all stand-alone EAL domains encoded by genomes from phyla other than proteobacteria appear to represent functional phosphodiesterases. Within enterobacteria, EAL-only proteins were found to cluster either with YhjH or with one of the subfamilies of YdiV-related proteins. EAL-only proteins from Shigella flexneri, Klebsiella pneumoniae, and Yersinia enterocolitica were tested for their ability to regulate swimming and swarming motility and formation of the red, dry, and rough (rdar) biofilm morphotype. In these tests, YhjH-related proteins S4210, KPN_01159, KPN_03274, and YE4063 displayed properties typical of enzymatically active phosphodiesterases, whereas S1641 and YE1324 behaved like members of the YdiV/STM1697 subfamily, with Yersinia enterocolitica protein YE1324 shown to downregulate motility in its native host. Of two closely related EAL-only proteins, YE2225 is an active phosphodiesterase, while YE1324 appears to interact with FlhD. These results suggest that in FlhDC-harboring beta-and gammaproteobacteria, some EAL-only proteins evolved to become catalytically inactive and regulate motility and biofilm formation by interacting with FlhDC.IMPORTANCE The EAL domain superfamily consists mainly of proteins with cyclic dimeric GMP-specific phosphodiesterase activity, but individual domains have been classified in three classes according to their functions and conserved amino acid signatures. Proteins that consist solely of stand-alone EAL domains cannot rely on other domains to form catalytically active dimers, and most of them fall into one of two distinct classes: catalytically active phosphodiesterases with well-conserved residues of the active site and the dimerization loop, and catalytically inactive YdiV/ CdgR-like proteins that regulate bacterial motility by binding to the flagellar master

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Alterations of c‐di‐GMP turnover proteins modulate semi‐constitutive rdar biofilm formation in commensal and uropathogenic Escherichia coli

Cimdins

Simm

et al. 2017

MicrobiologyOpen

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Agar plate‐based biofilm of enterobacteria like Escherichia coli is characterized by expression of the extracellular matrix components amyloid curli and cellulose exopolysaccharide, which can be visually enhanced upon addition of the dye Congo Red, resulting in a red, dry, and rough (rdar) colony morphology. Expression of the rdar morphotype depends on the transcriptional regulator CsgD and occurs predominantly at ambient temperature in model strains. In contrast, commensal and pathogenic isolates frequently express the csgD‐dependent rdar morphotype semi‐constitutively, also at human host body temperature. To unravel the molecular basis of temperature‐independent rdar morphotype expression, biofilm components and c‐di‐GMP turnover proteins of seven commensal and uropathogenic E. coli isolates were analyzed. A diversity within the c‐di‐GMP signaling network was uncovered which suggests alteration of activity of the trigger phosphodiesterase YciR to contribute to (up)regulation of csgD expression and consequently semi‐constitutive rdar morphotype development.

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Genome-Based Comparison of Cyclic Di-GMP Signaling in Pathogenic and Commensal Escherichia coli Strains

Cited by 60 publications

References 79 publications

Systematic Nomenclature for GGDEF and EAL Domain-Containing Cyclic Di-GMP Turnover Proteins of Escherichia coli

Systematic Nomenclature for GGDEF and EAL Domain-Containing Cyclic Di-GMP Turnover Proteins of Escherichia coli

Stand-Alone EAL Domain Proteins Form a Distinct Subclass of EAL Proteins Involved in Regulation of Cell Motility and Biofilm Formation in Enterobacteria

Alterations of c‐di‐GMP turnover proteins modulate semi‐constitutive rdar biofilm formation in commensal and uropathogenic Escherichia coli

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