A transferable plasticity region in Campylobacter coli allows isolates of an otherwise non‐glycolytic food‐borne pathogen to catabolize glucose

Abstract

Thermophilic Campylobacter species colonize the intestine of agricultural and domestic animals commensally but cause severe gastroenteritis in humans. In contrast to other enteropathogenic bacteria, Campylobacter has been considered to be non-glycolytic, a metabolic property originally used for their taxonomic classification. Contrary to this dogma, we demonstrate that several Campylobacter coli strains are able to utilize glucose as a growth substrate. Isotopologue profiling experiments with (13) C-labeled glucose suggested that these strains catabolize glucose via the pentose phosphate and Entner-Doudoroff (ED) pathways and use glucose efficiently for de novo synthesis of amino acids and cell surface carbohydrates. Whole genome sequencing of glycolytic C. coli isolates identified a genomic island located within a ribosomal RNA gene cluster that encodes for all ED pathway enzymes and a glucose permease. We could show in vitro that a non-glycolytic C. coli strain could acquire glycolytic activity through natural transformation with chromosomal DNA of C. coli and C. jejuni subsp. doylei strains possessing the ED pathway encoding plasticity region. These results reveal for the first time the ability of a Campylobacter species to catabolize glucose and provide new insights into how genetic macrodiversity through intra- and interspecies gene transfer expand the metabolic capacity of this food-borne pathogen.

Glucose Metabolism via the Entner-Doudoroff Pathway in Campylobacter: A Rare Trait that Enhances Survival and Promotes Biofilm Formation in Some Isolates

“…Of these isolates, CV1257, Dg172, and Dg349 all had ED type 1 (the same as in the isolates used by Vorwerk et al, 2015), while B13117 carried ED type 45, which only differed by a single synonymous substitution in pgi2 (471: T- > C). The isolates were grown in minimal media (MCLMAN) without and with glucose supplementation as the main carbon source; a low concentration of L -aspartate (2 mM) was included as a nitrogen source as this was found to greatly aid growth.…”

“…Two phosphoglucose isomerases (Pgi1 and Pgi2) catalyze the same reaction. ED pathway specific enzymes are boxed; Pgi2 is encoded at the glc locus (Vorwerk et al, 2015) and may be required to feed fructose-6-phosphate into the reductive pentose phosphate pathway (RPPP). (B) Organization of the glc locus encoding the ED pathway in Campylobacter jejuni subsp.…”

“…In enteric bacteria like Escherichia coli , the ED pathway enzymes are inducible and serve primarily in gluconate catabolism, with glucose itself being catabolized preferentially by EMP-mediated glycolysis (Conway, 1992). Gluconate is present in the intestine; interestingly, although campylobacters cannot catabolise gluconate (Pajaniappan et al, 2008; Vorwerk et al, 2015), C. jejuni has been shown to use it as an electron donor for respiration via a periplasmic gluconate dehydrogenase (Pajaniappan et al, 2008). A third “cyclic” ED pathway variation is found in Pseudomonas spp.…”

“…Recently, in an elegant and detailed study using mutagenesis, 13 C-isotopolog analysis and enzyme studies, Vorwerk et al (2015) discovered that a functional ED pathway exists in certain C. coli isolates, which enables this pathogen to utilize glucose as a growth substrate. Moreover, the pathway (like that for L -fucose) was found to be encoded on a genomic island or ‘plasticity region,’ designated the glc locus, that could be transferred between ED-positive and ED-negative isolates by natural transformation, suggesting acquisition of the glc -enoded ED pathway could contribute to the expansion of metabolic diversity in campylobacters (Vorwerk et al, 2015).…”

“…Moreover, the pathway (like that for L -fucose) was found to be encoded on a genomic island or ‘plasticity region,’ designated the glc locus, that could be transferred between ED-positive and ED-negative isolates by natural transformation, suggesting acquisition of the glc -enoded ED pathway could contribute to the expansion of metabolic diversity in campylobacters (Vorwerk et al, 2015). However, knowledge of the actual distribution of the ED pathway genes in isolates from a range of different sources is lacking and it is thus not clear what the role or importance of glucose utilization is in the context of the known genomic diversity of campylobacters.…”