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Gut Pathogens
Published in: Gut Pathogens 1/2020

01-12-2020 | Campylobacter | Research

Analyses of energy metabolism and stress defence provide insights into Campylobacter concisus growth and pathogenicity

Authors: Melissa Yeow, Fang Liu, Rena Ma, Timothy J. Williams, Stephen M. Riordan, Li Zhang

Published in: Gut Pathogens | Issue 1/2020

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Abstract

Campylobacter concisus is an emerging enteric pathogen that is associated with inflammatory bowel disease. Previous studies demonstrated that C. concisus is non-saccharolytic and hydrogen gas (H2) is a critical factor for C. concisus growth. In order to understand the molecular basis of the non-saccharolytic and H2-dependent nature of C. concisus growth, in this study we examined the pathways involving energy metabolism and oxidative stress defence in C. concisus. Bioinformatic analysis of C. concisus genomes in comparison with the well-studied enteric pathogen Campylobacter jejuni was performed. This study found that C. concisus lacks a number of key enzymes in glycolysis, including glucokinase and phosphofructokinase, and the oxidative pentose phosphate pathway. C. concisus has an incomplete tricarboxylic acid cycle, with no identifiable succinyl-CoA synthase or fumarate hydratase. C. concisus was inferred to use fewer amino acids and have fewer candidate substrates as electron donors and acceptors compared to C. jejuni. The addition of DMSO or fumarate to media resulted in significantly increased growth of C. concisus in the presence of H2 as an electron donor, demonstrating that both can be used as electron acceptors. Catalase, an essential enzyme for oxidative stress defence in C. jejuni, and various nitrosative stress enzymes, were not found in the C. concisus genome. Overall, C. concisus is inferred to have a non-saccharolytic metabolism in which H2 is central to energy conservation, and a narrow selection of carboxylic acids and amino acids can be utilised as organic substrates. In conclusion, this study provides a molecular basis for the non-saccharolytic and hydrogen-dependent nature of C. concisus energy metabolism pathways, which provides insights into the growth requirements and pathogenicity of this species.
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Literature
1.
Lastovica AJ, On SLW, Zhang L. The family Campylobacteraceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F, editors. The prokaryotes: deltaproteobacteria and epsilonproteobacteria. Berlin: Springer; 2014. p. 307–35.CrossRef
2.
Liu F, Ma R, Wang Y, Zhang L. The clinical importance of Campylobacter concisus and other human hosted Campylobacter species. Front Cell Infect Microbiol. 2018;8:243.PubMedPubMedCentralCrossRef
3.
Hazards EPoB. Scientific opinion on quantification of the risk posed by broiler meat to human campylobacteriosis in the EU. EFSA J. 2010;8(1):1437.CrossRef
4.
Marder ME, Griffin PM, Cieslak PR, et al. Preliminary incidence and trends of infections with pathogens transmitted commonly through food—foodborne diseases active surveillance network, 10 U.S. Sites, 2006–2017. Altanta: Centers for Disease Control and Prevention; 2018.CrossRef
5.
Sammarco ML, Ripabelli G, Fanelli I, Grasso GM, Tamburro M. Prevalence and biomolecular characterization of Campylobacter spp. isolated from retail meat. J Food Prot. 2010;73(4):720–8.PubMedCrossRef
6.
O’Leary MC, Harding O, Fisher L, Cowden J. A continuous common-source outbreak of campylobacteriosis associated with changes to the preparation of chicken liver pâté. Epidemiol Infect. 2009;137(3):383–8.PubMedCrossRef
7.
Rahimi E, Ameri M, Kazemeini HR. Prevalence and antimicrobial resistance of Campylobacter species isolated from raw camel, beef, lamb, and goat meat in Iran. Foodborne Pathog Dis. 2010;7(4):443–7.PubMedCrossRef
8.
Graham C, Whyte R, Gilpin B, Cornelius A, Hudson JA, Morrison D, et al. Outbreak of campylobacteriosis following pre-cooked sausage consumption. Aust N Z J Public Health. 2005;29(6):507–10.PubMedCrossRef
9.
Miller WG, Parker CT, Heath S, Lastovica AJ. Identification of genomic differences between Campylobacter jejuni subsp. jejuni and C. jejuni subsp. doylei at the nap locus leads to the development of a C. jejuni subspeciation multiplex PCR method. BMC Microbiol. 2007;7(1):11.PubMedPubMedCentralCrossRef
10.
Miller WGMR. Prevalence of Campylobacter in the food and water supply: incidence, outbreaks, isolation and detection. In: Konkel MEKJ, editor. Campylobacter: molecular and cellular biology. Norwich: Horizon Scientific Press; 2005. p. 101–63.
11.
Zhang L, Budiman V, Day AS, Mitchell H, Lemberg DA, Riordan SM, et al. Isolation and detection of Campylobacter concisus from saliva of healthy individuals and patients with inflammatory bowel disease. J Clin Microbiol. 2010;48(8):2965–7.PubMedPubMedCentralCrossRef
12.
Mahendran V, Riordan SM, Grimm MC, Tran TAT, Major J, Kaakoush NO, et al. Prevalence of Campylobacter species in adult Crohn’s disease and the preferential colonization sites of Campylobacter species in the human intestine. PLoS ONE. 2011;6(9):e25417-e.CrossRef
13.
Mukhopadhya I, Thomson JM, Hansen R, Berry SH, El-Omar EM, Hold GL. Detection of Campylobacter concisus and other Campylobacter species in colonic biopsies from adults with ulcerative colitis. PLoS ONE. 2011;6(6):e21490.PubMedPubMedCentralCrossRef
14.
Man SM, Zhang L, Day AS, Leach ST, Lemberg DA, Mitchell H. Campylobacter concisus and other Campylobacter species in children with newly diagnosed Crohn’s disease. Inflamm Bowel Dis. 2010;16(6):1008–16.PubMedCrossRef
15.
Liu F, Ma R, Tay CYA, Octavia S, Lan R, Chung HKL, et al. Genomic analysis of oral Campylobacter concisus strains identified a potential bacterial molecular marker associated with active Crohn’s disease. Emerg Microbes Infect. 2018;7(1):64.PubMedPubMedCentral
16.
Kirk KF, Nielsen HL, Thorlacius-Ussing O, Nielsen H. Optimized cultivation of Campylobacter concisus from gut mucosal biopsies in inflammatory bowel disease. Gut Pathog. 2016;8(1):27.PubMedPubMedCentralCrossRef
17.
Nielsen HL, Ejlertsen T, Engberg J, Nielsen H. High incidence of Campylobacter concisus in gastroenteritis in North Jutland, Denmark: a population-based study. Clin Microbiol Infect. 2013;19(5):445–50.PubMedCrossRef
18.
Macfarlane S, Furrie E, Macfarlane GT, Dillon JF. Microbial colonization of the upper gastrointestinal tract in patients with Barrett’s esophagus. Clin Infect Dis. 2007;45(1):29–38.PubMedCrossRef
19.
Man SM, Zhang L, Day AS, Leach ST, Lemberg DA, Mitchell H. Campylobacter concisus and other Campylobacter species in children with newly diagnosed Crohn’s disease. Inflamm Bowel Dis. 2009;16(6):1008–16.CrossRef
20.
Vandamme P, De Ley J. Proposal for a new family, Campylobacteraceae. Int J Syst Bacteriol. 1991;41:451–5.CrossRef
21.
Miller WG. Comparative genomics of Campylobacter species other than Campylobacter jejuni. In: Campylobacter. 3rd edn. American Society of Microbiology; 2008.
22.
Vorwerk H, Huber C, Mohr J, Bunk B, Bhuju S, Wensel O, et al. A transferable plasticity region in Campylobacter coli allows isolates of an otherwise non-glycolytic food-borne pathogen to catabolize glucose. Mol Microbiol. 2015;98(5):809–30.PubMedCrossRef
23.
Muraoka WT, Zhang Q. Phenotypic and genotypic evidence for L-fucose utilization by Campylobacter jejuni. J Bacteriol. 2011;193(5):1065–75.PubMedCrossRef
24.
Stahl M, Friis LM, Nothaft H, Liu X, Li J, Szymanski CM, et al. L-Fucose utilization provides Campylobacter jejuni with a competitive advantage. Proc Natl Acad Sci. 2011;108(17):7194–9.PubMedCrossRefPubMedCentral
25.
Hofreuter D. Defining the metabolic requirements for the growth and colonization capacity of Campylobacter jejuni. Front Cell Infect Microbiol. 2014;4:137.PubMedPubMedCentralCrossRef
26.
Parkhill J, Wren BW, Mungall K, Ketley JM, Churcher C, Basham D, et al. The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature. 2000;403(6770):665–8.PubMedCrossRef
27.
Pearson BM, Gaskin DJ, Segers RP, Wells JM, Nuijten PJ, van Vliet AH. The complete genome sequence of Campylobacter jejuni strain 81116 (NCTC11828). J Bacteriol. 2007;189(22):8402–3.PubMedPubMedCentralCrossRef
28.
Guccione E, Del Rocio Leon-Kempis M, Pearson BM, Hitchin E, Mulholland F, Van Diemen PM, et al. Amino acid-dependent growth of Campylobacter jejuni: key roles for aspartase (AspA) under microaerobic and oxygen-limited conditions and identification of AspB (Cj0762), essential for growth on glutamate. Mol Microbiol. 2008;69(1):77–93.PubMedCrossRef
29.
Leach S, Harvey P, Wait R. Changes with growth rate in the membrane lipid composition of and amino acid utilization by continuous cultures of Campylobacter jejuni. J Appl Microbiol. 1997;82(5):631–40.PubMedCrossRef
30.
Line JE, Hiett KL, Guard-Bouldin J, Seal BS. Differential carbon source utilization by Campylobacter jejuni 11168 in response to growth temperature variation. J Microbiol Methods. 2010;80(2):198–202.PubMedCrossRef
31.
32.
Wright JA, Grant AJ, Hurd D, Harrison M, Guccione EJ, Kelly DJ, et al. Metabolite and transcriptome analysis of Campylobacter jejuni in vitro growth reveals a stationary-phase physiological switch. Microbiology. 2009;155(1):80–94.PubMedCrossRef
33.
Woodall CA, Jones MA, Barrow PA, Hinds J, Marsden GL, Kelly DJ, et al. Campylobacter jejuni gene expression in the chick cecum: evidence for adaptation to a low-oxygen environment. Infect Immun. 2005;73(8):5278–85.PubMedPubMedCentralCrossRef
34.
van der Stel AX, Boogerd FC, Huynh S, Parker CT, van Dijk L, van Putten JPM, et al. Generation of the membrane potential and its impact on the motility, ATP production and growth in Campylobacter jejuni. Mol Microbiol. 2017;105(4):637–51.PubMedCrossRef
35.
36.
Kelly DJ. Complexity and versatility in the physiology and metabolism of Campylobacter jejuni. In: Campylobacter. 3rd edn. American Society of Microbiology; 2008.
37.
Pajaniappan M, Hall JE, Cawthraw SA, Newell DG, Gaynor EC, Fields JA, et al. A temperature-regulated Campylobacter jejuni gluconate dehydrogenase is involved in respiration-dependent energy conservation and chicken colonization. Mol Microbiol. 2008;68(2):474–91.PubMedPubMedCentralCrossRef
38.
Vegge CS, Jansen van Rensburg MJ, Rasmussen JJ, Maiden MCJ, Johnsen LG, Danielsen M, et al. Glucose metabolism via the Entner–Doudoroff pathway in Campylobacter: a rare trait that enhances survival and promotes biofilm formation in some isolates. Front Microbiol. 2016;7:1877.PubMedPubMedCentralCrossRef
39.
Thomas MT, Shepherd M, Poole RK, van Vliet AHM, Kelly DJ, Pearson BM. Two respiratory enzyme systems in Campylobacter jejuni NCTC 11168 contribute to growth on l-lactate. Environ Microbiol. 2011;13(1):48–61.PubMedCrossRef
40.
Mendz GL, Ball GE, Meek DJ. Pyruvate metabolism in Campylobacter spp. Biochim Biophys Acta Gen Subj. 1997;1334(2):291–302.CrossRef
41.
Weerakoon DR, Olson JW. The Campylobacter jejuni NADH: ubiquinone oxidoreductase (complex I) utilizes flavodoxin rather than NADH. J Bacteriol. 2008;190(3):915–25.PubMedCrossRef
42.
Weingarten RA, Taveirne ME, Olson JW. The dual-functioning fumarate reductase is the sole succinate:quinone reductase in Campylobacter jejuni and is required for full host colonization. J Bacteriol. 2009;191(16):5293–300.PubMedPubMedCentralCrossRef
43.
Weerakoon DR, Borden NJ, Goodson CM, Grimes J, Olson JW. The role of respiratory donor enzymes in Campylobacter jejuni host colonization and physiology. Microb Pathog. 2009;47(1):8–15.PubMedCrossRef
44.
Myers JD, Kelly DJ. A sulphite respiration system in the chemoheterotrophic human pathogen Campylobacter jejuni. Microbiology. 2005;151(1):233–42.PubMedCrossRef
45.
Jackson RJ, Elvers KT, Lee LJ, Gidley MD, Wainwright LM, Lightfoot J, et al. Oxygen reactivity of both respiratory oxidases in Campylobacter jejuni: the cydAB genes encode a cyanide-resistant, low-affinity oxidase that is not of the cytochrome bd type. J Bacteriol. 2007;189(5):1604–15.PubMedCrossRef
46.
Guccione EJ, Kendall JJ, Hitchcock A, Garg N, White MA, Mulholland F, et al. Transcriptome and proteome dynamics in chemostat culture reveal how Campylobacter jejuni modulates metabolism, stress responses and virulence factors upon changes in oxygen availability. Environ Microbiol. 2017;19(10):4326–48.PubMedPubMedCentralCrossRef
47.
Pittman MS, Kelly DJ. Electron transport through nitrate and nitrite reductases in Campylobacter jejuni. Biochem Soc Trans. 2005;33(Pt 1):190–2.PubMedCrossRef
48.
Pittman MS, Elvers KT, Lee L, Jones MA, Poole RK, Park SF, et al. Growth of Campylobacter jejuni on nitrate and nitrite: electron transport to NapA and NrfA via NrfH and distinct roles for NrfA and the globin Cgb in protection against nitrosative stress. Mol Microbiol. 2007;63(2):575–90.PubMedCrossRef
49.
Sellars MJ, Hall SJ, Kelly DJ. Growth of Campylobacter jejuni supported by respiration of fumarate, nitrate, nitrite, trimethylamine-N-oxide, or dimethyl sulfoxide requires oxygen. J Bacteriol. 2002;184(15):4187–96.PubMedPubMedCentralCrossRef
50.
Liu YW, Denkmann K, Kosciow K, Dahl C, Kelly DJ. Tetrathionate stimulated growth of Campylobacter jejuni identifies a new type of bi-functional tetrathionate reductase (TsdA) that is widely distributed in bacteria. Mol Microbiol. 2013;88(1):173–88.PubMedCrossRef
51.
Benoit SL, Maier RJ. Site-directed mutagenesis of Campylobacter concisus respiratory genes provides insight into the pathogen’s growth requirements. Sci Rep. 2018;8(1):14203.PubMedPubMedCentralCrossRef
52.
Kirk KF, Méric G, Nielsen HL, Pascoe B, Sheppard SK, Thorlacius-Ussing O, et al. Molecular epidemiology and comparative genomics of Campylobacter concisus strains from saliva, faeces and gut mucosal biopsies in inflammatory bowel disease. Sci Rep. 2018;8(1):1902.PubMedPubMedCentralCrossRef
53.
54.
Flint A, Sun Y-Q, Butcher J, Stahl M, Huang H, Stintzi A. Phenotypic screening of a targeted mutant library reveals Campylobacter jejuni defenses against oxidative stress. Infect Immun. 2014;82(6):2266–75.PubMedPubMedCentralCrossRef
55.
Tanner ACR, Badger S, Lai C-H, Listgarten MA, Visconti RA, Socransky SS. Wolinella gen. nov., Wolinella succinogenes (Vibrio succinogenes Wolin et al.) comb. nov., and Description of Bacteroides gracilis sp. nov., Wolinella recta sp. nov., Campylobacter concisus sp. nov., and Eikenella corrodens from humans with periodontal disease. Int J Syst Evol Microbiol. 1981;31(4):432–45.
56.
Reaney SK, Begg C, Bungard SJ, Guest JR. Identification of the d-tartrate dehydratase genes (ttdA and ttdB) of Escherichia coli and evolutionary relationship with the class I fumarase genes. J Gen Microbiol. 1993;139(7):1523–30.PubMedCrossRef
57.
58.
Hofreuter D, Mohr J, Wensel O, Rademacher S, Schreiber K, Schomburg D, et al. Contribution of amino acid catabolism to the tissue specific persistence of Campylobacter jejuni in a murine colonization model. PLoS ONE. 2012;7(11):e50699-e.CrossRef
59.
Velayudhan J, Kelly DJ. Analysis of gluconeogenic and anaplerotic enzymes in Campylobacter jejuni: an essential role for phosphoenolpyruvate carboxykinase. Microbiology. 2002;148(3):685–94.PubMedCrossRef
60.
Lee H, Ma R, Grimm MC, Riordan SM, Lan R, Zhong L, et al. Examination of the anaerobic growth of Campylobacter concisus strains. Int J Microbiol. 2014;2014:476047.PubMedPubMedCentralCrossRef
61.
Ma R, Liu F, Yap SF, Lee H, Leong RW, Riordan SM, et al. The growth and protein expression of inflammatory bowel disease-associated Campylobacter concisus is affected by the derivatives of the food additive fumaric acid. Front Microbiol. 2018;9:896.PubMedPubMedCentralCrossRef
62.
Axley MJ, Grahame DA, Stadtman TC. Escherichia coli formate-hydrogen lyase. Purification and properties of the selenium-dependent formate dehydrogenase component. J Biol Chem. 1990;265(30):18213–8.PubMed
63.
Pesci EC, Cottle DL, Pickett CL. Genetic, enzymatic, and pathogenic studies of the iron superoxide dismutase of Campylobacter jejuni. Infect Immun. 1994;62(7):2687–94.PubMedPubMedCentralCrossRef
64.
Ohsawa I, Ishikawa M, Takahashi K, Watanabe M, Nishimaki K, Yamagata K, et al. Hydrogen acts as a therapeutic antioxidant by selectively reducing cytotoxic oxygen radicals. Nat Med. 2007;13(6):688–94.PubMedCrossRef
65.
Kern M, Simon J. Electron transport chains and bioenergetics of respiratory nitrogen metabolism in Wolinella succinogenes and other Epsilonproteobacteria. Biochim Biophys Acta Bioenerg. 2009;1787(6):646–56.CrossRef
66.
Nambu T, Wang D, Mashimo C, Maruyama H, Kashiwagi K, Yoshikawa K, et al. Nitric oxide donor modulates a multispecies oral bacterial community—an in vitro study. Microorganisms. 2019;7(9):353.PubMedCentralCrossRef
67.
Cornelius AJ, Miller WG, Lastovica AJ, On SLW, French NP, Vandenberg O, et al. Complete genome sequence of Campylobacter concisus ATCC 33237(T) and draft genome sequences for an additional eight well-characterized C. concisus strains. Genome Announc. 2017;5(29):e00711-17.PubMedPubMedCentralCrossRef
68.
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403–10.PubMedCrossRef
69.
Pearson WR. An introduction to sequence similarity (“Homology”) searching. Curr Protoc Bioinform. 2013;42(1):3.1–3.1.8.CrossRef
70.
71.
Schoneich C. Methionine oxidation by reactive oxygen species: reaction mechanisms and relevance to Alzheimer’s disease. Biochem Biophys Acta. 2005;1703(2):111–9.PubMed
72.
Gundogdu O, Bentley SD, Holden MT, Parkhill J, Dorrell N, Wren BW. Re-annotation and re-analysis of the Campylobacter jejuni NCTC11168 genome sequence. BMC Genomics. 2007;8:162.PubMedPubMedCentralCrossRef
73.
Metadata
Title
Analyses of energy metabolism and stress defence provide insights into Campylobacter concisus growth and pathogenicity
Authors
Melissa Yeow
Fang Liu
Rena Ma
Timothy J. Williams
Stephen M. Riordan
Li Zhang
Publication date
01-12-2020
Publisher
BioMed Central
Keyword
Campylobacter
Published in
Gut Pathogens / Issue 1/2020
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/s13099-020-00349-6

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