Glucose metabolism via the Entner-Doudoroff pathway in Campylobacter: A rare trait that enhances survival and promotes biofilm formation in some isolates

Isolates of the zoonotic pathogen Campylobacter are generally considered to be unable to metabolize glucose due to lack of key glycolytic enzymes. However, the Entner-Doudoroff (ED) pathway has been identified in Campylobacter jejuni subsp. doylei and a few C. coli isolates. A systematic search for...

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Main Authors: Christina S Vegge, Melissa J Jansen van Rensburg, Janus J Rasmussen, Martin Christopher James Maiden, Lea G Johnsen, Morten Danielsen, Sheila MacIntyre, Hanne Ingmer, David J Kelly
Format: Article
Language:English
Published: Frontiers Media S.A. 2016-11-01
Series:Frontiers in Microbiology
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fmicb.2016.01877/full
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spelling doaj-a13b3fed20224470b2349a1c85c913c72020-11-24T21:43:04ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2016-11-01710.3389/fmicb.2016.01877233689Glucose metabolism via the Entner-Doudoroff pathway in Campylobacter: A rare trait that enhances survival and promotes biofilm formation in some isolatesChristina S Vegge0Melissa J Jansen van Rensburg1Janus J Rasmussen2Martin Christopher James Maiden3Lea G Johnsen4Morten Danielsen5Sheila MacIntyre6Hanne Ingmer7David J Kelly8University of CopenhagenUniversity of OxfordUniversity of CopenhagenUniversity of OxfordMS-OmicsMS-OmicsUniversity of ReadingUniversity of CopenhagenThe University of SheffieldIsolates of the zoonotic pathogen Campylobacter are generally considered to be unable to metabolize glucose due to lack of key glycolytic enzymes. However, the Entner-Doudoroff (ED) pathway has been identified in Campylobacter jejuni subsp. doylei and a few C. coli isolates. A systematic search for ED pathway genes in a wide range of Campylobacter isolates and in the C. jejuni/coli PubMLST database revealed that 1.7% of >6,000 genomes encoded a complete ED pathway, including both C. jejuni and C. coli from diverse clinical, environmental and animal sources. In rich media, glucose significantly enhanced stationary phase survival of a set of ED-positive C. coli isolates. Unexpectedly, glucose massively promoted floating biofilm formation in some of these ED-positive isolates. Metabolic profiling by gas chromatography-mass spectrometry revealed distinct responses to glucose in a low biofilm strain (CV1257) compared to a high biofilm strain (B13117), consistent with preferential diversion of hexose-6-phosphate to polysaccharide in B13117. We conclude that while the ED pathway is rare amongst Campylobacter isolates causing human disease (the majority of which would be of agricultural origin), some glucose-utilizing isolates exhibit specific fitness advantages, including stationary-phase survival and biofilm production, highlighting key physiological benefits of this pathway in addition to energy conservation.http://journal.frontiersin.org/Journal/10.3389/fmicb.2016.01877/fullGlycolysispolysaccharideCapsuleStationary-phasehexose sugarPubMLST database
collection DOAJ
language English
format Article
sources DOAJ
author Christina S Vegge
Melissa J Jansen van Rensburg
Janus J Rasmussen
Martin Christopher James Maiden
Lea G Johnsen
Morten Danielsen
Sheila MacIntyre
Hanne Ingmer
David J Kelly
spellingShingle Christina S Vegge
Melissa J Jansen van Rensburg
Janus J Rasmussen
Martin Christopher James Maiden
Lea G Johnsen
Morten Danielsen
Sheila MacIntyre
Hanne Ingmer
David J Kelly
Glucose metabolism via the Entner-Doudoroff pathway in Campylobacter: A rare trait that enhances survival and promotes biofilm formation in some isolates
Frontiers in Microbiology
Glycolysis
polysaccharide
Capsule
Stationary-phase
hexose sugar
PubMLST database
author_facet Christina S Vegge
Melissa J Jansen van Rensburg
Janus J Rasmussen
Martin Christopher James Maiden
Lea G Johnsen
Morten Danielsen
Sheila MacIntyre
Hanne Ingmer
David J Kelly
author_sort Christina S Vegge
title Glucose metabolism via the Entner-Doudoroff pathway in Campylobacter: A rare trait that enhances survival and promotes biofilm formation in some isolates
title_short Glucose metabolism via the Entner-Doudoroff pathway in Campylobacter: A rare trait that enhances survival and promotes biofilm formation in some isolates
title_full Glucose metabolism via the Entner-Doudoroff pathway in Campylobacter: A rare trait that enhances survival and promotes biofilm formation in some isolates
title_fullStr Glucose metabolism via the Entner-Doudoroff pathway in Campylobacter: A rare trait that enhances survival and promotes biofilm formation in some isolates
title_full_unstemmed Glucose metabolism via the Entner-Doudoroff pathway in Campylobacter: A rare trait that enhances survival and promotes biofilm formation in some isolates
title_sort glucose metabolism via the entner-doudoroff pathway in campylobacter: a rare trait that enhances survival and promotes biofilm formation in some isolates
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2016-11-01
description Isolates of the zoonotic pathogen Campylobacter are generally considered to be unable to metabolize glucose due to lack of key glycolytic enzymes. However, the Entner-Doudoroff (ED) pathway has been identified in Campylobacter jejuni subsp. doylei and a few C. coli isolates. A systematic search for ED pathway genes in a wide range of Campylobacter isolates and in the C. jejuni/coli PubMLST database revealed that 1.7% of >6,000 genomes encoded a complete ED pathway, including both C. jejuni and C. coli from diverse clinical, environmental and animal sources. In rich media, glucose significantly enhanced stationary phase survival of a set of ED-positive C. coli isolates. Unexpectedly, glucose massively promoted floating biofilm formation in some of these ED-positive isolates. Metabolic profiling by gas chromatography-mass spectrometry revealed distinct responses to glucose in a low biofilm strain (CV1257) compared to a high biofilm strain (B13117), consistent with preferential diversion of hexose-6-phosphate to polysaccharide in B13117. We conclude that while the ED pathway is rare amongst Campylobacter isolates causing human disease (the majority of which would be of agricultural origin), some glucose-utilizing isolates exhibit specific fitness advantages, including stationary-phase survival and biofilm production, highlighting key physiological benefits of this pathway in addition to energy conservation.
topic Glycolysis
polysaccharide
Capsule
Stationary-phase
hexose sugar
PubMLST database
url http://journal.frontiersin.org/Journal/10.3389/fmicb.2016.01877/full
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