Cyclic AMP (cAMP) Receptor Protein-cAMP Complex Regulates Heparosan Production in Escherichia coli Strain Nissle 1917

Yan, Huihui; Bao, Feifei; Zhao, Liping; Yu, Yanying; Tang, Jiaqin; Zhou, Xianxuan

doi:10.1128/aem.01814-15

Cited by 17 publications

(13 citation statements)

References 41 publications

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“…S3B). CRP also regulates the K5 N-acetylheparosan-type capsule in the probiotic E. coli Nissle 1917 (39). During a urinary tract infection, cAMP might modulate attachment to the bladder epithelium, epithelial cell invasion, and IBC formation, all by differentially regulating type 1 pili (17), the K1 capsule, and curli/ cellulose.…”

Section: Figmentioning

confidence: 99%

The Catabolite Repressor Protein-Cyclic AMP Complex Regulates csgD and Biofilm Formation in Uropathogenic Escherichia coli

et al. 2016

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The extracellular matrix protects Escherichia coli from immune cells, oxidative stress, predation, and other environmental stresses. Production of the E. coli extracellular matrix is regulated by transcription factors that are tuned to environmental conditions. The biofilm master regulator protein CsgD upregulates curli and cellulose, the two major polymers in the extracellular matrix of uropathogenic E. coli (UPEC) biofilms. We found that cyclic AMP (cAMP) regulates curli, cellulose, and UPEC biofilms through csgD. The alarmone cAMP is produced by adenylate cyclase (CyaA), and deletion of cyaA resulted in reduced extracellular matrix production and biofilm formation. The catabolite repressor protein (CRP) positively regulated csgD transcription, leading to curli and cellulose production in the UPEC isolate, UTI89. Glucose, a known inhibitor of CyaA activity, blocked extracellular matrix formation when added to the growth medium. The mutant strains ⌬cyaA and ⌬crp did not produce rugose biofilms, pellicles, curli, cellulose, or CsgD. Three putative CRP binding sites were identified within the csgD-csgB intergenic region, and purified CRP could gel shift the csgD-csgB intergenic region. Additionally, we found that CRP binded upstream of kpsMT, which encodes machinery for K1 capsule production. Together our work shows that cAMP and CRP influence E. coli biofilms through transcriptional regulation of csgD. IMPORTANCE The catabolite repressor protein (CRP)-cyclic AMP (cAMP) complex influences the transcription of ϳ7% of genes on the Escherichia coli is a multifaceted Gram-negative bacterium that is equipped for survival in disparate environments ranging from the gastrointestinal and urinary tracts to waterways and soil (1). Growth of E. coli can occur with either planktonic or biofilm lifestyles, the transition between which requires a highly organized shift in gene expression. The biofilm lifestyle is characterized by adherence, slow growth, resistance to environmental insults, and production of an extracellular matrix (ECM) (2). CsgD is the major biofilm regulator of E. coli and of many other bacteria of the Enterobacteriaceae family (3-5), and it promotes the production of two E. coli surface appendages, the amyloid fiber curli and the fibrous glycan chain cellulose (2). CsgD represses the transcription of motility-associated genes, while mediating self and surface attachment (6-8).E. coli is found in ϳ80% of urinary tract infections (UTI), more than any other causative agent, and has the ability to thrive in the bladder and urinary tract environments (9). During UTI, uropathogenic E. coli (UPEC) uses various means to evade and colonize the host. Curli and other factors function in establishing an initial bacterial titer (10). Once in the bladder, E. coli utilizes type 1 pili to invade bladder epithelial cells (11). E. coli bacteria then form a biofilm-like structure known as an intracellular bacterial community (IBC), and cells are coated by the ECM component K1 for protection from host cell recognition ...

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Section: Figmentioning

confidence: 99%

The Catabolite Repressor Protein-Cyclic AMP Complex Regulates csgD and Biofilm Formation in Uropathogenic Escherichia coli

et al. 2016

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“…29 Furthermore, the cAMP−CRP complex activates the synthesis of heparosan, a heparin-like polysaccharide, by binding to the region upstream of the region 3 promoter. 30 Cho et al proved that cAMP−CRP is indirectly involved in CPS production by positively affecting the metabolism or growth of Vibrio vulnificus rather than by directly controlling the expression of the CPS operon. 31 However, there are no relevant studies establishing that CRP is involved in polysaccharide synthesis in L. plantarum.…”

Section: ■ Discussionmentioning

confidence: 99%

“…Moreover, the cAMP–CRP complex, which comprises polysaccharides, proteins, and fatty acids, regulates biofilm maintenance . Furthermore, the cAMP–CRP complex activates the synthesis of heparosan, a heparin-like polysaccharide, by binding to the region upstream of the region 3 promoter . Cho et al proved that cAMP–CRP is indirectly involved in CPS production by positively affecting the metabolism or growth of Vibrio vulnificus rather than by directly controlling the expression of the CPS operon .…”

Section: Discussionmentioning

confidence: 99%

Maltose-Enhanced Exopolysaccharide Synthesis of Lactiplantibacillus plantarum through CRP-like Protein

Meng

Lyu

Chen

et al. 2023

J. Agric. Food Chem.

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Carbon sources alter the synthesis of exopolysaccharides (EPS) in Lactiplantibacillus plantarum. Maltose increased the EPS production of L. plantarum 163 6.5-fold. Subsequently, EPS production, transcriptome, and proteome were analyzed using glucose or maltose to further clarify the regulatory mechanism. A cAMP receptor protein (UniProtKB: F9UNI5) has been identified to control EPS synthesis in the presence of cAMP by binding to the EPS synthesis promoter Pcps4A‑J. Overexpression of the cAMP synthesis gene cyaA increased cAMP content and EPS production 4.5- and 2.2-fold, respectively. Furthermore, yogurt produced with L. plantarum 163-cyaA had a similar viscosity to that of commercial Greek yogurt; it had 20 and 83.7% greater viscosity than that produced with L. plantarum 163 with maltose and glucose, respectively. These findings indicated that L. plantarum 163-cyaA has potential applications in the production of functional fermented dairy products.

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“…Hence, this MinC-CRP interplay may be responsible for the cell size reduction, and further details need to be analysed. The crp null mutants of Vibrio cholerae and E. coli showed a reduction in the colony size [21,22]. However, there are no reports on Salmonella spp.…”

Section: Discussionmentioning

confidence: 99%

Role of cAMP receptor protein in phenotype and stress tolerance in Salmonella enterica serovar Typhimurium

Sawant

Shashidhar

2020

J Basic Microbiol

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Salmonella enterica serovar Typhimurium (S. Typhimurium) is exposed to biotic and abiotic stresses. The survival of Salmonella in nature depends on the global regulators like cAMP receptor protein (CRP). The role of CRP in the phenotypic characteristics and stress tolerance was elucidated in S. Typhimurium using a crp gene null mutant (Δcrp). A 1.6‐fold decrease in the cell size, a two‐fold reduction in the colony size, and a 3.5‐fold decrease in motility were observed in the Δcrp compared with the S. Typhimurium wild‐type (WT). H2S production on selective media was affected in the Δcrp. The utilisation of d‐mannose, d‐glycerol and d‐mannitol was completely affected, whereas that of d‐galactose and d‐fructose was partially affected. The utilisation of d‐arabinose was induced in the Δcrp. The growth rate of the Δcrp in Luria Bertani medium was unaffected. However, in the glucose‐containing minimal medium, the growth rate of the Δcrp was reduced by 1.5‐fold compared with the WT. The Δcrp was able to utilise ethanolamine as the sole carbon source similar to the WT. The Δcrp was more tolerant to heat and oxidative stress. Overexpression of heat and oxidative stress‐related genes was observed in the Δcrp in the stationary phase. The Δcrp was less tolerant to radiation stress compared with the WT. The current findings decisively establish the CRP protein as a global regulator. The CRP affects multiple phenotypes, carbon metabolism and stress physiology of S. Typhimurium.

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Cyclic AMP (cAMP) Receptor Protein-cAMP Complex Regulates Heparosan Production in Escherichia coli Strain Nissle 1917

Cited by 17 publications

References 41 publications

The Catabolite Repressor Protein-Cyclic AMP Complex Regulates csgD and Biofilm Formation in Uropathogenic Escherichia coli

The Catabolite Repressor Protein-Cyclic AMP Complex Regulates csgD and Biofilm Formation in Uropathogenic Escherichia coli

Maltose-Enhanced Exopolysaccharide Synthesis of Lactiplantibacillus plantarum through CRP-like Protein

Role of cAMP receptor protein in phenotype and stress tolerance in Salmonella enterica serovar Typhimurium

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