Analysis of Campylobacter jejuni infection in the gnotobiotic piglet and genome-wide identification of bacterial factors required for infection

Vries, Stefan P. W. de; Linn, Aileen; Macleod, Kareen; MacCallum, Amanda; Hardy, Simon P.; Douce, Gill; Watson, E.D.; Dagleish, Mark P.; Thompson, H.; Stevenson, Andy; Kennedy, David J.; Baig, Abiyad; Coward, Chris; Maskell, Duncan J.; Smith, David George Emslie; Grant, A.; Everest, Paul

doi:10.1038/srep44283

Cited by 16 publications

(20 citation statements)

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“…Genome sequencing of numerous strains has revealed genomic flexibility in C. jejuni and C. coli and has indicated possible host-specific genotypes but has not yet identified possible virulence determinants (Van Putten et al 2009 ; Yahara et al 2017 ). Similarly, genome-wide functional screening (using mutant panels) is beginning to provide evidence for fitness, colonisation and virulence determinants besides flagella and glycosylation systems (de Vries et al 2017a , b ). To date, C. jejuni has been subject to metabolomics studies where novel glycosylation events of flagella were observed (McNally et al 2007 , 2006 ; Logan et al 2009 ), resistance to antibiotic (Li et al 2015 ), metabolic mutant differentiation (Howlett et al 2014 ), and preferential utilisation of amino acids was shown through NMR analysis of depletion from complex growth medium (Wright et al 2009 ).…”

Section: Discussionmentioning

confidence: 99%

Unexpected differential metabolic responses of Campylobacter jejuni to the abundant presence of glutamate and fucose

et al. 2018

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IntroductionCampylobacter jejuni is the leading cause of foodborne bacterial enteritis in humans, and yet little is known in regard to how genetic diversity and metabolic capabilities among isolates affect their metabolic phenotype and pathogenicity.ObjectivesFor instance, the C. jejuni 11168 strain can utilize both l-fucose and l-glutamate as a carbon source, which provides the strain with a competitive advantage in some environments and in this study we set out to assess the metabolic response of C. jejuni 11168 to the presence of l-fucose and l-glutamate in the growth medium.MethodsTo achieve this, untargeted hydrophilic liquid chromatography coupled to mass spectrometry was used to obtain metabolite profiles of supernatant extracts obtained at three different time points up to 24 h.ResultsThis study identified both the depletion and the production and subsequent release of a multitude of expected and unexpected metabolites during the growth of C. jejuni 11168 under three different conditions. A large set of standards allowed identification of a number of metabolites. Further mass spectrometry fragmentation analysis allowed the additional annotation of substrate-specific metabolites. The results show that C. jejuni 11168 upon l-fucose addition indeed produces degradation products of the fucose pathway. Furthermore, methionine was faster depleted from the medium, consistent with previously-observed methionine auxotrophy.ConclusionsMoreover, a multitude of not previously annotated metabolites in C. jejuni were found to be increased specifically upon l-fucose addition. These metabolites may well play a role in the pathogenicity of this C. jejuni strain.Electronic supplementary materialThe online version of this article (10.1007/s11306-018-1438-5) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 99%

Unexpected differential metabolic responses of Campylobacter jejuni to the abundant presence of glutamate and fucose

et al. 2018

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“…Induction of formate dehydrogenase is observed when C. jejuni is grown in a rabbit ileal‐loop ex vivo (Stintzi et al ., ), but not during chicken colonization (Woodall et al ., ; Taveirne et al ., ). Moreover, formate utilization is crucial for piglet colonization (Vries et al ., ), efficient colonization of chickens (Weerakoon et al ., ) and pathology in mouse models (Bereswill et al ., ; Kassem et al ., ). Formate also acts as invasion signal for the pathogenic bacterium Salmonella enterica serovar Enteritidis (Van Immerseel et al ., ; Huang et al ., ).…”

Section: Discussionmentioning

confidence: 99%

Generation of the membrane potential and its impact on the motility, ATP production and growth in Campylobacter jejuni

Stel

Boogerd²,

Huynh

et al. 2017

Molecular Microbiology

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The generation of a membrane potential (Δψ), the major constituent of the proton motive force (pmf), is crucial for ATP synthesis, transport of nutrients and flagellar rotation. Campylobacter jejuni harbors a branched electron transport chain, enabling respiration with different electron donors and acceptors. Here, we demonstrate that a relatively high Δψ is only generated in the presence of either formate as electron donor or oxygen as electron acceptor, in combination with an acceptor/donor respectively. We show the necessity of the pmf for motility and growth of C. jejuni. ATP generation is not only accomplished by oxidative phosphorylation via the pmf, but also by substrate-level phosphorylation via the enzyme AckA. In response to a low oxygen tension, C. jejuni increases the transcription and activity of the donor complexes formate dehydrogenase (FdhABC) and hydrogenase (HydABCD) as well as the transcription of the alternative respiratory acceptor complexes. Our findings suggest that in the gut of warm-blooded animals, C. jejuni depends on at least formate or hydrogen as donor (in the anaerobic lumen) or oxygen as acceptor (near the epithelial cells) to generate a pmf that sustains efficient motility and growth for colonization and pathogenesis.

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“…Campylobacter infection is one of the main bacterial causes of diarrhea and of ‘environmental enteropathy’ and body growth failure. Campylobacter species like Campylobacter jejuni and Campylobacter concisus could cause human diarrhea diseases which originate from piglets via consumption of contaminated meat products ( de Vries et al., 2017 ; Rosner et al., 2017 ). Also, PCV2 infection is widespread in swine industry ( Baró et al., 2015 ).…”

Section: Introductionmentioning

confidence: 99%

Porcine circovirus type 2 (PCV2) and Campylobacter infection induce diarrhea in piglets: Microbial dysbiosis and intestinal disorder

et al. 2020

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Diarrhea is considered to be associated with microbial dysbiosis caused by infection of pathogens but poorly understood. We herein characterized the colonic microbiota of diarrheal early-weaning piglets infected with porcine circovirus type 2 (PCV2) and Campylobacter . Campylobacter infection significantly decreased species richness and Shannon diversity index of colonic microbiota together with a significant increase in the proportion of Campylobacter and Enterobacteriaceae, whereas no significant difference on the above indexes was observed in piglets infected with PCV2 compared with healthy piglets. PCV2 and Campylobacter infection could disturb the homeostasis of colonic microbiota through deterioration of ecological network within microbial community, and specially Campylobacter performed as a module hub in ecological networks. The microbial dysbiosis caused metabolic dysfunction and led to a remarkable reduction in production of short chain fatty acids, following by a higher pH level in colon cavity. Campylobacter infection disturbed the function of colonic tract barrier observed in terms of significant lower relative expression of claudin-1, occluding, and zonula occludens protein-1 genes, and PCV2 infection induced intestinal inflammation together with a higher permeability of colon. Generally, these results suggested that PCV2 and Campylobacter infection could induce microbial dysbiosis and metabolic dysfunction, and cause intestinal disorder, all of which finally were associated to contribute to the diarrhea of early-weaning piglets.

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Analysis of Campylobacter jejuni infection in the gnotobiotic piglet and genome-wide identification of bacterial factors required for infection

Cited by 16 publications

References 49 publications

Unexpected differential metabolic responses of Campylobacter jejuni to the abundant presence of glutamate and fucose

Unexpected differential metabolic responses of Campylobacter jejuni to the abundant presence of glutamate and fucose

Generation of the membrane potential and its impact on the motility, ATP production and growth in Campylobacter jejuni

Porcine circovirus type 2 (PCV2) and Campylobacter infection induce diarrhea in piglets: Microbial dysbiosis and intestinal disorder

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