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Identification of a gene cluster for D-tagatose utilization in Escherichia coli B2 phylogroup.

ABSTRACT: D-Tagatose is a promising low-calorie sugar-substituting sweetener in the food industry. Most ingested D-tagatose is fermented by intestinal microorganisms. Until now, Escherichia coli has been considered incapable of growing on D-tagatose. Here, we discovered a gene cluster involved in D-tagatose utilization in E. coli. The chromosome of the intestinal probiotic E. coli Nissle 1917 contains a six-gene cluster encoding the ABC transporter, D-tagatose kinase, D-tagatose-bisphosphate aldolase, and putative aldose 1-epimerase. The functionality of the gene cluster was experimentally validated. Based on single-gene deletions, D-tagatose dissimilation occurs via D-tagatose 6-phosphate to D-tagatose 1,6-bisphosphate to D-glyceraldehyde 3-phosphate plus dihydroxyacetone phosphate. Remarkably, this gene cluster was located in 93% of the completely sequenced genomes of the E. coli B2 phylogroup, which contains the majority of extraintestinal pathogenic and adherent-invasive E. coli strains prevalent in patients with inflammatory bowel disease. This highlights the importance of understanding the clinical significance of D-tagatose in microbiota alterations.

SUBMITTER: Ha J

PROVIDER: S-EPMC9720028 | biostudies-literature | 2022 Dec

REPOSITORIES: biostudies-literature

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Identification of a gene cluster for D-tagatose utilization in Escherichia coli B2 phylogroup.

Ha Jinyoung J Kim Dohyeon D Yeom Jinho J Kim Youngshin Y Yoo Seung Min SM Yoon Sung Ho SH

iScience 20221122 12

D-Tagatose is a promising low-calorie sugar-substituting sweetener in the food industry. Most ingested D-tagatose is fermented by intestinal microorganisms. Until now, Escherichia coli has been considered incapable of growing on D-tagatose. Here, we discovered a gene cluster involved in D-tagatose utilization in E. coli. The chromosome of the intestinal probiotic E. coli Nissle 1917 contains a six-gene cluster encoding the ABC transporter, D-tagatose kinase, D-tagatose-bisph ...[more]

PMID: 36479150

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Project description:This is a longitudinal study comprising 649 Escherichia coli isolates representing all 7,165 E. coli bloodstream infection (BSI) episodes recorded in a hospital (1996 to 2016). Strain analysis included clonal identification (phylogenetic groups/subgroups, STc131 subclades, pulsed-field gel electrophoresis [PFGE], and whole-genome sequencing [WGS]), antibiotic susceptibility (13 antibiotics), and virulence-associated genes (VAGs; 29 genes). The incidence of E. coli BSI increased from 1996 to 2016 (5.5 to 10.8 BSI episodes/1,000 hospitalizations, average 7 to 8/1,000). B2 isolates predominate (53%), with subgroups B2-I (STc131), B2-II, B2-IX, and B2-VI representing 25%, 25%, 14%, and 9%, respectively. Intertwined waves of community-acquired (CA) plus health care-associated and community-onset health care-associated (HCA) and hospital-acquired (HA) episodes of both B2 and non-B2 phylogroups occurred. A remarkable increase was observed only for B2-I-STc131 (C1/C2 subclades), with oscillations for other B2 subgroups and phylogroups throughout the years. Epidemic and persistent clones (comprising isolates with highly similar/identical PFGE types and genomes differing in 6 to 173 single nucleotide polymorphisms [SNPs]) of B2-I (STc131), B2-II (STc73), B2-III (STc127), B2-IX (STc95), and B2-VI (STc12) were recovered from different patients, most at hospital admission, for long periods (2 to 17 years), and extended-spectrum beta-lactamase (ESBL) producers or resistance to ciprofloxacin in B2 isolates was almost restricted to B2-I (STc131) subclade C. STc131 contributed to increasing the B2 rates but only transiently altered the E. coli population structure. The increase of E. coli BSI was determined by waves of CA+HCA BSI episodes that predate the waves of HA BSI. Besides the risk of hospital transmission that led to temporal increases in BSI, this study suggests that E. coli populations/clones from community-based healthy individuals may occasionally have an epidemic structure and provide a source of transmissible strains influencing the HA BSI incidence. IMPORTANCE Sepsis is the third leading cause of mortality in Western countries and one of the Global Health Threats recognized by the WHO since 2017. Despite Escherichia coli constituting the most common cause of bloodstream infections (BSI), its epidemiology is not fully understood, in part due to the scarcity of local and longitudinal studies. Our work analyzes the long-term dynamics of E. coli causing bacteremia in a single institution and reveals waves of different clonal lineages that emerge periodically and successfully spread afterward in both the community and hospitals. Because the origin of E. coli bloodstream infections is the gut, the microbiota of healthy individuals might occasionally have an epidemic structure, providing a source of E. coli strains to influence the incidence of hospital BSI. The study complements previous fractionated observations focusing on specific E. coli lineages or antibiotic-resistant isolates in the last decades and helps to understand the epidemiology of E. coli BSI and the dynamics of pandemic clones.

Dataset Information

Identification of a gene cluster for D-tagatose utilization in Escherichia coli B2 phylogroup.

Publications

Identification of a gene cluster for D-tagatose utilization in <i>Escherichia coli</i> B2 phylogroup.

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