Genomic analysis of Escherichia coli strains isolated from diseased chicken in the Czech Republic

. 2020 Jun 10 ; 16 (1) : 189. [epub] 20200610

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid32522212

Grantová podpora
107/2017/FVL Veterinární a Farmaceutická Univerzita Brno
QK1810462 Ministerstvo Zemědělství

Odkazy

PubMed 32522212
PubMed Central PMC7286222
DOI 10.1186/s12917-020-02407-2
PII: 10.1186/s12917-020-02407-2
Knihovny.cz E-zdroje

BACKGROUND: Avian pathogenic Escherichia coli (APEC) can cause various extraintestinal infections in poultry, resulting in massive economic losses in poultry industry. In addition, some avian E. coli strains may have zoonotic potential, making poultry a possible source of infection for humans. Due to its extreme genetic diversity, this pathotype remains poorly defined. This study aimed to investigate the diversity of colibacillosis-associated E. coli isolates from Central European countries with a focus on the Czech Republic. RESULTS: Of 95 clinical isolates subjected to preliminary characterization, 32 were selected for whole-genome sequencing. A multi resistant phenotype was detected in a majority of the sequenced strains with the predominant resistance to β-lactams and quinolones being associated with TEM-type beta-lactamase genes and chromosomal gyrA mutations respectively. The phylogenetic analysis confirmed a great diversity of isolates, that were derived from nearly all phylogenetic groups, with predominace of B2, B1 and C phylogroups. Clusters of closely related isolates within ST23 (phylogroup C) and ST429 (phylogroup B2) indicated a possible local spread of these clones. Besides, the ST429 cluster carried blaCMY-2, - 59 genes for AmpC beta-lactamase and isolates of both clusters were generally well-equipped with virulence-associated genes, with considerable differences in distribution of certain virulence-associated genes between phylogenetically distant lineages. Other important and potentially zoonotic APEC STs were detected, incl. ST117, ST354 and ST95, showing several molecular features typical for human ExPEC. CONCLUSIONS: The results support the concept of local spread of virulent APEC clones, as well as of zoonotic potential of specific poultry-associated lineages, and highlight the need to investigate the possible source of these pathogenic strains.

Zobrazit více v PubMed

Nolan LK, Barnes HJ, Vaillancourt JP, Abdul-Aziz T, Logue CM, et al. Colibacillosis. In: Swayne DE, Glisson JR, et al., editors. Diseases of poultry. Ames: Wiley; 2013. pp. 751–805.

La Ragione RM, Woodward MJ. Virulence factors of Escherichia coli serotypes associated with avian colisepticaemia. Res Vet Sci. 2002;73:27–35. PubMed

Johnson TJ, Wannemuehler Y, Doetkott C, Johnson SJ, Rosenberger SC, Nolan LK. Identification of minimal predictors of avian pathogenic Escherichia coli virulence for use as a rapid diagnostic tool. J Clin Microbiol. 2008;46:3987–3996. PubMed PMC

Rodriguez-Siek KE, Giddings CW, Doetkott C, Johnson TJ, Nolan LK. Characterizing the APEC pathotype. Vet Res. 2005;36:241–256. PubMed

Stromberg ZR, Johnson JR, Fairbrother JM, Kilbourne J, Van Goor A, Curtiss R, 3rd, Mellata M. Evaluation of Escherichia coli isolates from healthy chickens to determine their potential risk to poultry and human health. PLoS One. 2017;12:e0180599. PubMed PMC

Collingwood C, Kemmett K, Williams N, Wigley P. Is the concept of avian pathogenic Escherichia coli as a single pathotype fundamentally flawed? Front Vet Sci. 2014;1(5):1–4. PubMed PMC

Ewers C, Antão EM, Diehl I, Philipp HC, Wieler LH. Intestine and environment of the chicken as reservoirs for extraintestinal pathogenic Escherichia coli strains with zoonotic potential. Appl Environ Microbiol. 2009;75:184–192. PubMed PMC

Kemmett K, Humphrey T, Rushton S, Close A, Wigley P, Williams NJ. A longitudinal study simultaneously exploring the carriage of APEC virulence associated genes and the molecular epidemiology of faecal and systemic E. coli in commercial broiler chickens. PLoS One. 2013;8:e67749. PubMed PMC

Maturana VG, de Pace F, Carlos C, Mistretta Pires M, Amabile de Campos T, Nakazato G, Guedes Stheling E, Logue CM, Nolan LK, Dias da Silveira Subpathotypes of avian pathogenic Escherichia coli (APEC) exist as defined by their syndromes and virulence traits. Open Microbiol J. 2011;5:55–64. PubMed PMC

Jordan FTW, Williams NJ, Wattret A, Jones T. Observations on salpingitis, peritonitis and salpingoperitonitis in a layer breeder flock. Vet Rec. 2005;157:573–577. PubMed

Olsen RH, Thøfner ICN, Pors SE, Pires dos Santos T, Christensen JP. Experimental induced avian E coli salpingitis: significant impact of strain and host factors on the clinical and pathological outcome. Vet Microbiol. 2016;188:59–66. PubMed

Pires-dos-Santos T, Bisgaard M, Christensen H. Genetic diversity and virulence profiles of Escherichia coli causing salpingitis and peritonitis in broiler breeders. Vet Microbiol. 2013;162:873–880. PubMed

Mellata M. Human and avian extraintestinal pathogenic Escherichia coli: infections, zoonotic risks, and antibiotic resistance trends. Foodborne Pathog Dis. 2013;10:916–932. PubMed PMC

Johnson JR, Russo TA. Extraintestinal pathogenic Escherichia coli: “The other bad E coli”. J Lab Clin Med. 2002;139:155–162. PubMed

Guabiraba R, Schouler C. Avian colibacillosis: still many black holes. FEMS Microbiol Lett. 2015;362:fnv118. PubMed

Zhu Ge X, Jiang J, Pan Z, Hu L, Wang S, Wang H, Leung FC, Dai J, Fan H. Comparative genomic analysis shows that avian pathogenic Escherichia coli isolate IMT5155 (O2:K1:H5; ST complex 95, ST140) shares close relationship with ST95 APEC O1:K1 and human ExPEC O18:K1 strains. PLoS One. 2014;9:e112048. PubMed PMC

Moulin-Schouleur M, Répérant M, Laurent S, Brée A, Mignon-Grasteau S, Germon P, Rasschaert D, Schouler C. Extraintestinal pathogenic Escherichia coli strains of avian and human origin: link between phylogenetic relationships and common virulence patterns. J Clin Microbiol. 2007;45:3366–3376. PubMed PMC

Tivendale KA, Logue CM, Kariyawasam S, Jordan D, Hussein A, Li G, Wannemuehler Y, Nolan LK. Avian-pathogenic Escherichia coli strains are similar to neonatal meningitis E. coli strains and are able to cause meningitis in the rat model of human disease. Infect Immun. 2010;78:3412–3419. PubMed PMC

Riley LW. Pandemic lineages of extraintestinal pathogenic Escherichia coli. Clin Microbiol Infect. 2014;20:380–390. PubMed

Cunha MPV, Saidenberg AB, Moreno AM, Ferreira AJP, Vieira MAM, Gomes TAT, Knöbl T. Pandemic extra-intestinal pathogenic Escherichia coli (ExPEC) clonal group O6-B2-ST73 as a cause of avian colibacillosis in Brazil. PLoS One. 2017;12:e0178970. PubMed PMC

Liu CM, Stegger M, Aziz M, Johnson TJ, Waits K, Nordstrom L, Gauld L, Weaver B, Rolland D, Statham S, Horwinski J, Sariya S, Davis GS, Sokurenko E, Keim P, Johnson JR, Price LB. Escherichia coli ST131-H22 as a foodborne uropathogen. mBio. 2018;9(4):e00470–e00418. PubMed PMC

Maluta RP, Logue CM, Casas MRT, Meng T, Guastalli EAL, Rojas TCG, Montelli AC, Sadatsune T, de Carvalho Ramos M, Nolan LK, da Silveira WD. Overlapped sequence types (STs) and serogroups of avian pathogenic (APEC) and human extra-intestinal pathogenic (ExPEC) Escherichia coli isolated in Brazil. PLoS One. 2014;9:e105016. PubMed PMC

Manges AR. Escherichia coli and urinary tract infections: the role of poultry-meat. J Clin Microbiol Infect. 2016;22:122–129. PubMed

Mora A, Viso S, López C, Alonso MP, García-Garrote F, Dabhi G, Mamani R, Herrera A, Marzoa J, Blanco M, Blanco JE, Moulin-Schouleur M, Schouler C, Blanco J. Poultry as reservoir for extraintestinal pathogenic Escherichia coli O45:K1:H7-B2-ST95 in humans. Vet Microbiol. 2013;167:506–512. PubMed

Pietsch M, Irrgang A, Roschanski N, Brenner Michael G, Hamprecht A, Rieber H, Käsbohrer A, Schwarz S, Rösler U, Kreienbrock L, Pfeifer Y, Fuchs S, Werner G, RESET Study Group Whole genome analyses of CMY-2-producing Escherichia coli isolates from humans, animals and food in Germany. BMC Genomics. 2018;19:601. PubMed PMC

Cordoni G, Woodward MJ, Wu H, Alanazi M, Wallis T, La Ragione RM. Comparative genomics of European avian pathogenic E. coli (APEC) BMC Genomics. 2016;17:960. PubMed PMC

Paudel S, Stessl B, Hess C, Zloch A, Hess M. High genetic diversity among extraintestinal Escherichia coli isolates in pullets and layers revealed by a longitudinal study. BMC Vet Res. 2016;12(1):221. PubMed PMC

Clermont O, Christenson JK, Denamur E, Gordon DM. The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups. Environ Microbiol Rep. 2013;5:58–65. PubMed

Johnson TJ, Siek KE, Johnson SJ, Nolan LK. DNA sequence of a ColV plasmid and prevalence of selected plasmid-encoded virulence genes among avian Escherichia coli strains. J Bacteriol. 2006;188:745. PubMed PMC

Mellata M, Dho-Moulin M, Dozois CM, Curtiss R, 3rd, Brown PK, Arné P, Brée A, Desautels C, Fairbrother JM. Role of virulence factors in resistance of avian pathogenic Escherichia coli to serum and in pathogenicity. Infect Immun. 2003;71:536–540. PubMed PMC

Tenaillon O, Skurnik D, Picard B, Denamur E. The population genetics of commensal Escherichia coli. Nat Rev Microbiol. 2010;8:207–217. PubMed

Mokady D, Gophna U, Ron EZ. Extensive gene diversity in septicemic Escherichia coli strains. J Clin Microbiol. 2005;43:66–73. PubMed PMC

Escobar-Parámo P, Blanc-Potard AB, Bui H, Le Bouguénec C, Denamur E. A specific genetic background is required for acquisition and expression of virulence factors in Escherichia coli. Mol Biol Evol. 2004;21:1085–1094. PubMed

Solà-Ginés M, Cameron-Veas K, Badiola I, Dolz R, Majó N, Dahbi G, Viso S, Mora A, Blanco J, Piedra-Carrasco N, González-López JJ, Migura-Garcia L. Diversity of multi-drug resistant avian pathogenic Escherichia coli (APEC) causing outbreaks of colibacillosis in broilers during 2012 in Spain. PLoS One. 2015;10:e0143191. PubMed PMC

Projahn M, Daehre K, Roesler U, Friese A. Extended-spectrum-beta-lactamase- and plasmid-encoded cephamycinase-producing enterobacteria in the broiler hatchery as a potential mode of pseudo-vertical transmission. J Appl Environ Microbiol. 2016;83:e02364–e02316. PubMed PMC

Cummins ML, Reid CJ, Roy Chowdhury P, Bushell RN, Esbert N, Tivendale KA, Noormohammadi AH, Islam S, Marenda MS, Browning GF, Markham PF, Djordjevic SP. Whole genome sequence analysis of Australian avian pathogenic Escherichia coli that carry the class 1 integrase gene. Microb Genom. 2019;5:e000250. PubMed PMC

Dziva F, Hauser H, Connor TR, van Diemen PM, Prescott G, Langridge GC, Eckert S, Chaudhuri RR, Ewers C, Mellata M, Mukhopadhyay S, Curtiss R, 3rd, Dougan G, Wieler LH, Thomson NR, Pickard DJ, Stevens MP. Sequencing and functional annotation of avian pathogenic Escherichia coli serogroup O78 strains reveal the evolution of E. coli lineages pathogenic for poultry via distinct mechanisms. Infect Immun. 2013;81:838–849. PubMed PMC

Ideses D, Gophna U, Paitan Y, Chaudhuri RR, Pallen MJ, Ron EZ. A degenerate type III secretion system from septicemic Escherichia coli contributes to pathogenesis. J Bacteriol. 2005;187:8164–8171. PubMed PMC

Dissanayake DRA, Octavia S, Lan R. Population structure and virulence content of avian pathogenic Escherichia coli isolated from outbreaks in Sri Lanka. Vet Microbiol. 2014;168:403–412. PubMed

Projahn M, Daehre K, Semmler T, Guenther S, Roesler U, Friese A. Environmental adaptation and vertical dissemination of ESBL−/pAmpC-producing Escherichia coli in an integrated broiler production chain in the absence of an antibiotic treatment. Microb Biotechnol. 2018;11:1017–1026. PubMed PMC

Ronco T, Stegger M, Olsen RH, Sekse C, Nordstoga AB, Pohjanvirta T, Lilje B, Lyhs U, Andersen PS, Pedersen K. Spread of avian pathogenic Escherichia coli ST117 O78:H4 in Nordic broiler production. BMC Genomics. 2017;18:13. PubMed PMC

Vincent C, Boerlin P, Daignault D, Dozois CM, Dutil L, Galanakis C, Reid-Smith RJ, Tellier PP, Tellis PA, Ziebell K, Manges AR. Food reservoir for Escherichia coli causing urinary tract infections. Emerg Infect Dis. 2010;16:88–95. PubMed PMC

Guo S, Wakeham D, Brouwers HJM, Cobbold RN, Abraham S, Mollinger JL, Johnson JR, Chapman TA, Gordon DM, Barrs VR, Trott DJ. Human-associated fluoroquinolone-resistant Escherichia coli clonal lineages, including ST354, isolated from canine feces and extraintestinal infections in Australia. Microbes Infect. 2015;17:266–274. PubMed

Vangchhia B, Abraham S, Bell JM, Collignon P, Gibson JS, Ingram PR, Johnson JR, Kennedy K, Trott DJ, Turnidge JD, Gordon DM. Phylogenetic diversity, antimicrobial susceptibility and virulence characteristics of phylogroup F Escherichia coli in Australia. Microbiology. 2016;162:1904–1912. PubMed

Jørgensen SL, Stegger M, Kudirkiene E, Lilje B, Poulsen LL, Ronco T, Pires Dos Santos T, Kiil K, Bisgaard M, Pedersen K, Nolan LK, Price LB, Olsen RH, Andersen PS, Christensen H. Diversity and population overlap between avian and human Escherichia coli belonging to sequence type 95. mSphere. 2019;4:e00333–e00318. PubMed PMC

Mora A, López C, Dabhi G, Blanco M, Blanco JE, Alonso MP, Herrera A, Mamani R, Bonacorsi S, Moulin-Schouleur M, Blanco J. Extraintestinal pathogenic Escherichia coli O1:K1:H7/NM from human and avian origin: detection of clonal groups B2 ST95 and D ST59 with different host distribution. BMC Microbiol. 2009;9:132. PubMed PMC

Johnson TJ, Wannemuehler Y, Kariyawasam S, Johnson JR, Logue CM, Nolan LK. Prevalence of avian-pathogenic Escherichia coli strain O1 genomic islands among extraintestinal and commensal E. coli isolates. J Bacteriol. 2012;194:2846–2853. PubMed PMC

Johnson JR, Murray AC, Gajewski A, Sullivan M, Snippes P, Kuskowski MA, Smith KE. Isolation and molecular characterization of nalidixic acid-resistant extraintestinal pathogenic Escherichia coli from retail chicken products. Antimicrob Agents Chemother. 2003;47:2161–2168. PubMed PMC

van Hoek AHAM, Stalenhoef JE, van Duijkeren E, Franz E. Comparative virulotyping of extended-spectrum cephalosporin-resistant E. coli isolated from broilers, humans on broiler farms and in the general population and UTI patients. Vet Microbiol. 2016;194:55–61. PubMed

Dolejska M, Villa L, Poirel L, Nordmann P, Carattoli A. Complete sequencing of an IncHI1 plasmid encoding the carbapenemase NDM-1, the ArmA 16S RNA methylase and a resistance–nodulation–cell division/multidrug efflux pump. J Antimicrob Chemother. 2013;68:34–39. PubMed

Dolejska M, Duskova E, Rybarikova J, Janoszowska D, Roubalova E, Dibdakova K, Maceckova G, Kohoutova L, Literak I, Smola J, Cizek A. Plasmids carrying blaCTX-M−1 and qnr genes in Escherichia coli isolates from an equine clinic and a horseback riding centre. J Antimicrob Chemother. 2011;66:757–764. PubMed

Johnson TJ, Nolan LK. Pathogenomics of the virulence plasmids of Escherichia coli. Microbiol Mol Biol Rev. 2009;73:750–774. PubMed PMC

Kao CY, Chen JW, Liu TL, Yan JJ, Wu JJ. Comparative genomics of Escherichia coli sequence type 219 clones from the same patient: evolution of the IncI1 blaCMY-carrying plasmid in vivo. Front Microbiol. 2018;9:1518. PubMed PMC

Royden A, Ormandy E, Pinchbeck G, Pascoe B, Hitchings MD, Sheppard SK, Williams NJ. Prevalence of faecal carriage of extended-spectrum β-lactamase (ESBL)-producing Escherichia coli in veterinary hospital staff and students. Vet Rec Open. 2019;6:e000307. PubMed PMC

Clinical and Laboratory Standards Institute (CLSI) Performance standards for antimicrobial susceptibility testing; twenty-fifth informational supplement. CLSI document M100-S25. Wayne: Clinical and Laboratory Standards Institute; 2015.

Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–2120. PubMed PMC

Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19:455–477. PubMed PMC

Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O, Aarestrup FM, Larsen MV. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother. 2012;67:2640–2644. PubMed PMC

Carattoli A, Zankari E, García-Fernández A, Voldby Larsen M, Lund O, Villa L, Møller Aarestrup F, Hasman H. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother. 2014;58:3895–3903. PubMed PMC

Joensen KG, Tetzschner AM, Iguchi A, Aarestrup FM, Scheutz F. Rapid and easy in silico serotyping of Escherichia coli using whole genome sequencing (WGS) data. J Clin Microbiol. 2015;53(8):2410–2426. PubMed PMC

Larsen MV, Cosentino S, Rasmussen S, Friis C, Hasman H, Marvig RL, Jelsbak L, Sicheritz-Pontén T, Ussery DW, Aarestrup FM, Lund O. Multilocus sequence typing of total-genome-sequenced bacteria. J Clin Microbiol. 2012;50:1355–1361. PubMed PMC

Liu B, Zheng D, Jin Q, Chen L, Yang J. VFDB 2019: a comparative pathogenomic platform with an interactive web interface. Nucleic Acids Res. 2019;47(D1):D687–D692. PubMed PMC

Beghain J, Bridier-Nahmias A, Le Nagard H, Denamur E, Clermont O. ClermonTyping: an easy-to-use and accurate in silico method for Escherichia genus strain phylotyping. Microb Genom. 2018;4:e000192. PubMed PMC

Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30(14):2068–2069. PubMed

Page JA, Cummins CA, Hunt M, Wong VK, Reuter S, Holden MTG, Fookes M, Falush D, Keane JA, Parkhill J. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics. 2015;15(31):3691–3693. PubMed PMC

Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30(9):1312–1313. PubMed PMC

Letunic I, Bork P. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res. 2016;44:W242–W245. PubMed PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...