Identification of Campylobacter jejuni and Campylobacter coli genes contributing to oxidative stress response using TraDIS analysis.
Aerobic stress
Campylobacter coli
Campylobacter jejuni
Oxidative stress
TraDIS
Journal
BMC microbiology
ISSN: 1471-2180
Titre abrégé: BMC Microbiol
Pays: England
ID NLM: 100966981
Informations de publication
Date de publication:
01 Feb 2024
01 Feb 2024
Historique:
received:
13
09
2023
accepted:
21
01
2024
medline:
2
2
2024
pubmed:
2
2
2024
entrez:
2
2
2024
Statut:
epublish
Résumé
Campylobacter jejuni and Campylobacter coli are the major causative agents of bacterial gastroenteritis worldwide and are known obligate microaerophiles. Despite being sensitive to oxygen and its reduction products, both species are readily isolated from animal food products kept under atmospheric conditions where they face high oxygen tension levels. In this study, Transposon Directed Insertion-site Sequencing (TraDIS) was used to investigate the ability of one C. jejuni strain and two C. coli strains to overcome oxidative stress, using H This is the first study to investigate gene fitness in both C. jejuni and C. coli under oxidative stress conditions and highlights both similar roles for certain genes for both species and highlights other genes that have a role under oxidative stress.
Sections du résumé
BACKGROUND
BACKGROUND
Campylobacter jejuni and Campylobacter coli are the major causative agents of bacterial gastroenteritis worldwide and are known obligate microaerophiles. Despite being sensitive to oxygen and its reduction products, both species are readily isolated from animal food products kept under atmospheric conditions where they face high oxygen tension levels.
RESULTS
RESULTS
In this study, Transposon Directed Insertion-site Sequencing (TraDIS) was used to investigate the ability of one C. jejuni strain and two C. coli strains to overcome oxidative stress, using H
CONCLUSIONS
CONCLUSIONS
This is the first study to investigate gene fitness in both C. jejuni and C. coli under oxidative stress conditions and highlights both similar roles for certain genes for both species and highlights other genes that have a role under oxidative stress.
Identifiants
pubmed: 38302896
doi: 10.1186/s12866-024-03201-y
pii: 10.1186/s12866-024-03201-y
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
46Subventions
Organisme : Biotechnology and Biological Sciences Research Council
ID : Institute Strategic Programme Microbes in the Food Chain [BB/R012504/1 and its constituent project BBS/E/F000PR10349 (Theme 2, Microbial Survival in the Food Chain]; and the Quadram Institute Bioscience funded Core Capability Grant [BB/CCG1860/1]; BBSRC Institute Strategic Programme Microbes and Food Safety BB/X011011/1 and its partner project BB/X018814/
Pays : United Kingdom
Informations de copyright
© 2024. The Author(s).
Références
Gillespie IA, O’Brien SJ, Frost JA, Tam C, Tompkins D, Neal KR, et al. Investigating vomiting and/or bloody diarrhoea in Campylobacter jejuni infection. J Med Microbiol. 2006;55:741–6.
doi: 10.1099/jmm.0.46422-0
pubmed: 16687593
Daniel N, Casadevall N, Sun P, Sugden D, Aldin V. The Burden of Foodborne Disease in the UK 2018. 2020.
Thépault A, Méric G, Rivoal K, Pascoe B, Mageiros L, Touzain F, et al. Genome-wide identification of host-segregating epidemiological markers for source attribution in Campylobacter jejuni. Appl Environ Microbiol. 2017;83:e03085–16.
doi: 10.1128/AEM.03085-16
pubmed: 28115376
pmcid: 5359498
Park SF. The physiology of Campylobacter species and its relevance to their role as foodborne pathogens. Int J Food Microbiol. 2002;74:177–88.
doi: 10.1016/S0168-1605(01)00678-X
pubmed: 11981968
Kaakoush NO, Miller WG, De Reuse H, Mendz GL. Oxygen requirement and tolerance of Campylobacter jejuni. Res Microbiol. 2007;158:644–50.
doi: 10.1016/j.resmic.2007.07.009
pubmed: 17890061
Ugarte-Ruiz M, Domínguez L, Corcionivoschi N, Wren BW, Dorrell N, Gundogdu O. Exploring the oxidative, antimicrobial and genomic properties of Campylobacter jejuni strains isolated from poultry. Res Vet Sci. 2018;119:170–5.
doi: 10.1016/j.rvsc.2018.06.016
pubmed: 29957495
Kim J-C, Oh E, Hwang S, Ryu S, Jeon B. Non-selective regulation of peroxide and superoxide resistance genes by PerR in Campylobacter jejuni. Front Microbiol. 2015. https://doi.org/10.3389/fmicb.2015.00126 .
doi: 10.3389/fmicb.2015.00126
pubmed: 26793181
pmcid: 4639627
Palyada K, Sun Y-Q, Flint A, Butcher J, Naikare H, Stintzi A. Characterization of the oxidative stress stimulon and PerR regulon of Campylobacter jejuni. BMC Genomics. 2009;10:481.
doi: 10.1186/1471-2164-10-481
pubmed: 19835633
pmcid: 2772861
Lee J-W, Helmann JD. The PerR transcription factor senses H
doi: 10.1038/nature04537
pubmed: 16541078
Hwang S, Kim M, Ryu S, Jeon B. Regulation of oxidative stress response by CosR, an essential response regulator in Campylobacter jejuni. PLoS ONE. 2011;6:e22300.
doi: 10.1371/journal.pone.0022300
pubmed: 21811584
pmcid: 3139631
Gundogdu O, da Silva DT, Mohammad B, Elmi A, Wren BW, van Vliet AHM, et al. The Campylobacter jejuni oxidative stress Regulator RrpB is associated with a genomic hypervariable region and altered oxidative stress resistance. Front Microbiol. 2016;7. https://doi.org/10.3389/fmicb.2016.02117 .
Gundogdu O, da Silva DT, Mohammad B, Elmi A, Mills DC, Wren BW, et al. The Campylobacter jejuni MarR-like transcriptional regulators RrpA and RrpB both influence bacterial responses to oxidative and aerobic stresses. Front Microbiol. 2015;6. https://doi.org/10.3389/fmicb.2015.00724 .
Atack JM, Kelly DJ. Oxidative stress in Campylobacter jejuni: responses, resistance and regulation. Future Microbiol. 2009;4:677–90.
doi: 10.2217/fmb.09.44
pubmed: 19659424
Grant KA, Park SF. Molecular characterization of katA from Campylobacter jejuni and generation of a catalase-deficient mutant of Campylobacter coli by interspecific allelic exchange. Microbiol (N Y). 1995;141:1369–76.
Baillon M-LA, van Vliet AHM, Ketley JM, Constantinidou C, Penn CW. An iron-regulated alkyl hydroperoxide reductase (AhpC) confers aerotolerance and oxidative stress resistance to the microaerophilic pathogen Campylobacter jejuni. J Bacteriol. 1999;181:4798–804.
doi: 10.1128/JB.181.16.4798-4804.1999
pubmed: 10438747
pmcid: 93964
Wood ZA, Schröder E, Robin Harris J, Poole LB. Structure, mechanism and regulation of peroxiredoxins. Trends Biochem Sci. 2003;28:32–40.
doi: 10.1016/S0968-0004(02)00003-8
pubmed: 12517450
Atack JM, Kelly DJ. Contribution of the stereospecific methionine sulphoxide reductases MsrA and MsrB to oxidative and nitrosative stress resistance in the food-borne pathogen Campylobacter jejuni. Microbiol (N Y). 2008;154:2219–30.
Seaver LC, Imlay JA. Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J Bacteriol. 2001;183:7173–81.
doi: 10.1128/JB.183.24.7173-7181.2001
pubmed: 11717276
pmcid: 95566
Rodrigues RC, Haddad N, Chevret D, Cappelier J-M, Tresse O. Comparison of Proteomics profiles of Campylobacter jejuni strain bf under Microaerobic and Aerobic conditions. Front Microbiol. 2016;7:1596.
doi: 10.3389/fmicb.2016.01596
pubmed: 27790195
pmcid: 5061731
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;82:2266–75.
doi: 10.1128/IAI.01528-13
pubmed: 24643543
pmcid: 4019188
Langridge GC, Phan M-D, Turner DJ, Perkins TT, Parts L, Haase J, et al. Simultaneous assay of every Salmonella Typhi gene using one million transposon mutants. Genome Res. 2009;19:2308–16.
doi: 10.1101/gr.097097.109
pubmed: 19826075
pmcid: 2792183
Stoakes E, Turner K, Baker DJ, Suau Sans M, Yasir M, Kalmar L, et al. Application of TraDIS to define the core essential genome of Campylobacter jejuni and Campylobacter coli. BMC Microbiol. 2023;23:97.
doi: 10.1186/s12866-023-02835-8
pubmed: 37024800
pmcid: 10077673
Kendall JJ, Barrero-Tobon AM, Hendrixson DR, Kelly DJ. Hemerythrins in the microaerophilic bacterium Campylobacter jejuni help protect key iron–sulphur cluster enzymes from oxidative damage. Environ Microbiol. 2014;16:1105–21.
doi: 10.1111/1462-2920.12341
pubmed: 24245612
Van Vliet AHM, Baillon M-LA, Penn CW, Ketley JM. Campylobacter jejuni contains two fur homologs: characterization of iron-responsive regulation of peroxide stress defense genes by the PerR repressor. J Bacteriol. 1999;181:6371–6.
doi: 10.1128/JB.181.20.6371-6376.1999
pubmed: 10515927
pmcid: 103772
Paysan-Lafosse T, Blum M, Chuguransky S, Grego T, Pinto BL, Salazar GA, et al. InterPro in 2022. Nucleic Acids Res. 2023;51:D418–27.
doi: 10.1093/nar/gkac993
pubmed: 36350672
Sun F, Liang H, Kong X, Xie S, Cho H, Deng X et al. Quorum-sensing agr mediates bacterial oxidation response via an intramolecular disulfide redox switch in the response regulator AgrA. Proceedings of the National Academy of Sciences 2012; 109: 9095–9100.
Schwengers O, Jelonek L, Dieckmann MA, Beyvers S, Blom J, Goesmann A. Bakta: rapid and standardized annotation of bacterial genomes via alignment-free sequence identification. Microb Genom. 2021;7:000685.
pubmed: 34739369
pmcid: 8743544
Barnawi H, Masri N, Hussain N, Al-Lawati B, Mayasari E, Gulbicka A, et al. RNA-based thermoregulation of a Campylobacter jejuni zinc resistance determinant. PLoS Pathog. 2020;16:e1009008.
doi: 10.1371/journal.ppat.1009008
pubmed: 33064782
pmcid: 7592916
Gao B, Vorwerk H, Huber C, Lara-Tejero M, Mohr J, Goodman AL, et al. Metabolic and fitness determinants for in vitro growth and intestinal colonization of the bacterial pathogen Campylobacter jejuni. PLoS Biol. 2017;15:e2001390.
doi: 10.1371/journal.pbio.2001390
pubmed: 28542173
pmcid: 5438104
de Vries S, Gupta S, Baig A, Wright E, Wedley A, Jensen AN, et al. Genome-wide fitness analyses of the foodborne pathogen Campylobacter jejuni in in vitro and in vivo models. Sci Rep. 2017;7:1251.
doi: 10.1038/s41598-017-01133-4
pubmed: 28455506
pmcid: 5430854
Imlay JA. Diagnosing oxidative stress in bacteria: not as easy as you might think. Curr Opin Microbiol. 2015;24:124–31.
doi: 10.1016/j.mib.2015.01.004
pubmed: 25666086
pmcid: 4380616
Gardner SP, Olson JW. Interaction of copper toxicity and oxidative stress in Campylobacter jejuni. J Bacteriol. 2018;200:e00208–18.
doi: 10.1128/JB.00208-18
pubmed: 30150230
pmcid: 6182239
Wai SN, Nakayama K, Umene K, Moriya T, Amako K. Construction of a ferritin-deficient mutant of Campylobacter jejuni: contribution of ferritin to iron storage and protection against oxidative stress. Mol Microbiol. 1996;20:1127–34.
doi: 10.1111/j.1365-2958.1996.tb02633.x
pubmed: 8809765
Feng Y, Wang Z, Chien K-Y, Chen H-L, Liang Y-H, Hua X, et al. Pseudo-pseudogenes in bacterial genomes: Proteogenomics reveals a wide but low protein expression of pseudogenes in Salmonella enterica. Nucleic Acids Res. 2022;50:5158–70.
doi: 10.1093/nar/gkac302
pubmed: 35489061
pmcid: 9122581
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;403:665–8.
doi: 10.1038/35001088
pubmed: 10688204
Pearson BM, Rokney A, Crossman LC, Miller WG, Wain J, van Vliet AHM. Complete genome sequence of the Campylobacter coli clinical isolate 15-537360. Genome Announc. 2013;1:e01056–13.
doi: 10.1128/genomeA.01056-13
pubmed: 24336384
pmcid: 3861437
van Vliet AHM, Pearson BM, Williams NJ, Pascoe B, Meric G, Ashton P et al. Generating tools for the molecular epidemiology of Campylobacter coli by next generation genome sequencing. 2017.
Lambert RJW, Pearson J. Susceptibility testing: accurate and reproducible minimum inhibitory concentration (MIC) and non-inhibitory concentration (NIC) values. J Appl Microbiol. 2000;88:784–90.
doi: 10.1046/j.1365-2672.2000.01017.x
pubmed: 10792538
Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 2011;17:10–2.
doi: 10.14806/ej.17.1.200
Barquist L, Mayho M, Cummins C, Cain AK, Boinett CJ, Page AJ, et al. The TraDIS toolkit: sequencing and analysis for dense transposon mutant libraries. Bioinformatics. 2016;32:1109–11.
doi: 10.1093/bioinformatics/btw022
pubmed: 26794317
pmcid: 4896371
de Vries SPW, Gupta S, Baig A, L’Heureux J, Pont E, Wolanska DP, et al. Motility defects in Campylobacter jejuni defined gene deletion mutants caused by second-site mutations. Microbiol (Reading). 2015;161:2316–27.
doi: 10.1099/mic.0.000184