Sugar-mediated regulation of a c-di-GMP phosphodiesterase in Vibrio cholerae

Heo, Kyoo; Park, Young-Ha; Lee, Kyung‐Ah; Kim, Joonwon; Ham, Hyeong-In; Kim, Byung‐Gee; Lee, Won–Jae; Seok, Yeong‐Jae

doi:10.1038/s41467-019-13353-5

Cited by 19 publications

(22 citation statements)

References 66 publications

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“…Thus, the phosphorylation states of the PTS components are modulated in response to the available carbon source (Deutscher et al ., 2014). PTS components are also important as they play physiological roles by interacting with their cognate partners in a phosphorylation‐dependent manner (Deutscher et al ., 2006; Park et al ., 2013; Kim et al ., 2015; Park et al ., 2016; Choe et al ., 2017; Heo et al ., 2019). Furthermore, in Gram‐positive bacteria, it is known that the ATP‐dependent phosphorylation of HPr on the Ser‐46 residue by HPr kinase/phosphorylase (HPrK/P) (Mijakovic et al ., 2002) is involved in physiological regulation, such as carbon catabolite repression, by binding to the global transcription regulator, catabolite control protein A (CcpA) (Singh et al ., 2008).…”

Section: Introductionmentioning

confidence: 99%

Functional dissection of the phosphotransferase system provides insight into the prevalence of Faecalibacterium prausnitzii in the host intestinal environment

Kang

Ham

Lee

et al. 2021

Environmental Microbiology

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Summary Faecalibacterium prausnitzii is a dominant member of healthy human colon microbiota, regarded as a beneficial gut bacterium due to its ability to produce anti‐inflammatory substances. However, little is known about how F. prausnitzii utilizes the nutrients present in the human gut, influencing its prevalence in the host intestinal environment. The phosphoenolpyruvate (PEP):carbohydrate phosphotransferase system (PTS) is a widely distributed and highly efficient carbohydrate transport system found in most bacterial species that catalyses the simultaneous phosphorylation and import of cognate carbohydrates; its components play physiological roles through interaction with other regulatory proteins. Here, we performed a systematic analysis of the 16 genes encoding putative PTS components (2 enzyme I, 2 HPr, and 12 enzyme II components) in F. prausnitzii A2‐165. We identified the general PTS components responsible for the PEP‐dependent phosphotransfer reaction and the sugar‐specific PTS components involved in the transport of two carbohydrates, N‐acetylglucosamine and fructose, among five enzyme II complexes. We suggest that the dissection of the functional PTS in F. prausnitzii may help to understand how this species outcompetes other bacterial species in the human intestine.

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Section: Introductionmentioning

confidence: 99%

Functional dissection of the phosphotransferase system provides insight into the prevalence of Faecalibacterium prausnitzii in the host intestinal environment

Kang

Ham

Lee

et al. 2021

Environmental Microbiology

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“…Each of the carbohydrate genes specific to E. lacertideformus encoded various subunits of sugar phosphotransferase system (PTS) transporters. Sugar phosphotransferase system transporters are involved in signal transduction and in the transport and metabolism of sugars, all essential for modulating biofilm formation and EPS synthesis ( Loo et al, 2003 ; Lazazzera, 2010 ; Kawada-Matsuo et al, 2016 ; Heo et al, 2019 ). An additional E. lacertideformus -specific COG; glycerol-3-phosphate cytidylyltransferase (COG0615) may further correlate with the biofilm-forming capacity of this bacterium.…”

Section: Discussionmentioning

confidence: 99%

Genomic Insights Into the Pathogenicity of a Novel Biofilm-Forming Enterococcus sp. Bacteria (Enterococcus lacertideformus) Identified in Reptiles

et al. 2021

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Whole genome analysis of a novel species of enterococci, Enterococcus lacertideformus, causing multi-systemic and invariably fatal disease in critically endangered Christmas Island reptiles was undertaken to determine the genetic elements and potential mechanisms conferring its pathogenic nature, biofilm-forming capabilities, immune recognition avoidance, and inability to grow in vitro. Comparative genomic analyses with related and clinically significant enterococci were further undertaken to infer the evolutionary history of the bacterium and identify genes both novel and absent. The genome had a G + C content of 35.1%, consisted of a circular chromosome, no plasmids, and was 2,419,934 bp in length (2,321 genes, 47 tRNAs, and 13 rRNAs). Multi-locus sequence typing (MLST), and single nucleotide polymorphism (SNP) analysis of multiple E. lacertideformus samples revealed they were effectively indistinguishable from one another and highly clonal. E. lacertideformus was found to be located within the Enterococcus faecium species clade and was closely related to Enterococcus villorum F1129D based on 16S rDNA and MLST house-keeping gene analysis. Antimicrobial resistance (DfreE, EfrB, tetM, bcrRABD, and sat4) and virulence genes (Fss3 and ClpP), and genes conferring tolerance to metals and biocides (n = 9) were identified. The detection of relatively few genes encoding antimicrobial resistance and virulence indicates that this bacterium may have had no exposure to recently developed and clinically significant antibiotics. Genes potentially imparting beneficial functional properties were identified, including prophages, insertion elements, integrative conjugative elements, and genomic islands. Functional CRISPR-Cas arrays, and a defective prophage region were identified in the genome. The study also revealed many genomic loci unique to E. lacertideformus which contained genes enriched in cell wall/membrane/envelop biogenesis, and carbohydrate metabolism and transport functionality. This finding and the detection of putative enterococcal biofilm determinants (EfaAfs, srtC, and scm) may underpin the novel biofilm phenotype observed for this bacterium. Comparative analysis of E. lacertideformus with phylogenetically related and clinically significant enterococci (E. villorum F1129D, Enterococcus hirae R17, E. faecium AUS0085, and Enterococcus faecalis OG1RF) revealed an absence of genes (n = 54) in E. lacertideformus, that encode metabolic functionality, which potentially hinders nutrient acquisition and/or utilization by the bacterium and precludes growth in vitro. These data provide genetic insights into the previously determined phenotype and pathogenic nature of the bacterium.

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“…PTS components play multiple regulatory roles in enteric bacteria 53 . In V. cholerae , EIIA of glucose PTS influences biofilm formation via modulating the activity of cyclic di-GMP phosphodiesterase PdeS and regulating the decay of CsrB/C sRNA 54 , 55 . In this study, we showed that in response to the low O 2 signal in animal small intestine, V. cholerae turns off fruT and uptakes fructose via PTS, leading to the decrease of intracellular cAMP level and the enhanced expression of virulence genes.…”

Section: Discussionmentioning

confidence: 99%

A fructose/H+ symporter controlled by a LacI-type regulator promotes survival of pandemic Vibrio cholerae in seawater

Liu

et al. 2021

Nat Commun

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The bacterium Vibrio cholerae can colonize the human intestine and cause cholera, but spends much of its life cycle in seawater. The pathogen must adapt to substantial environmental changes when moving between seawater and the human intestine, including different availability of carbon sources such as fructose. Here, we use in vitro experiments as well as mouse intestinal colonization assays to study the mechanisms used by pandemic V. cholerae to adapt to these environmental changes. We show that a LacI-type regulator (FruI) and a fructose/H+ symporter (FruT) are important for fructose uptake at low fructose concentrations, as those found in seawater. FruT is downregulated by FruI, which is upregulated when O2 concentrations are low (as in the intestine) by ArcAB, a two-component system known to respond to changes in oxygen levels. As a result, the bacteria predominantly use FruT for fructose uptake under seawater conditions (low fructose, high O2), and use a known fructose phosphotransferase system (PTS, Fpr) for fructose uptake under conditions found in the intestine. PTS activity leads to reduced levels of intracellular cAMP, which in turn upregulate virulence genes. Our results indicate that the FruT/FruI system may be important for survival of pandemic V. cholerae in seawater.

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Sugar-mediated regulation of a c-di-GMP phosphodiesterase in Vibrio cholerae

Cited by 19 publications

References 66 publications

Functional dissection of the phosphotransferase system provides insight into the prevalence of Faecalibacterium prausnitzii in the host intestinal environment

Functional dissection of the phosphotransferase system provides insight into the prevalence of Faecalibacterium prausnitzii in the host intestinal environment

Genomic Insights Into the Pathogenicity of a Novel Biofilm-Forming Enterococcus sp. Bacteria (Enterococcus lacertideformus) Identified in Reptiles

A fructose/H+ symporter controlled by a LacI-type regulator promotes survival of pandemic Vibrio cholerae in seawater

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