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Development of a Chlamydophila Psittaci Species-Specific and Genotype-Specific Real-Time PCR Tom Geens, Angelo Dewitte, Nico Boon, Daisy Vanrompay

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Development of a Chlamydophila Psittaci Species-Specific and Genotype-Specific Real-Time PCR Tom Geens, Angelo Dewitte, Nico Boon, Daisy Vanrompay Development of a Chlamydophila psittaci species-specific and genotype-specific real-time PCR Tom Geens, Angelo Dewitte, Nico Boon, Daisy Vanrompay To cite this version: Tom Geens, Angelo Dewitte, Nico Boon, Daisy Vanrompay. Development of a Chlamydophila psittaci species-specific and genotype-specific real-time PCR. Veterinary Research, BioMed Central, 2005,36 (5-6), pp.787-797. 10.1051/vetres:2005035. hal-00903003 HAL Id: hal-00903003 https://hal.archives-ouvertes.fr/hal-00903003 Submitted on 1 Jan 2005 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Vet. Res. 36 (2005) 787–797 787 © INRA, EDP Sciences, 2005 DOI: 10.1051/vetres:2005035 Original article Development of a Chlamydophila psittaci species- specific and genotype-specific real-time PCR Tom GEENSa*, Angelo DEWITTEa, Nico BOONb, Daisy VANROMPAYa a Department of Molecular Biotechnology, Faculty of Bioscience Engineering, Ghent University, Coupure Links 653, 9000 Ghent, Belgium b Laboratory of Microbial Ecology and Technology (LabMET), Faculty of Bioscience Engineering, Ghent University, Coupure Links 653, 9000 Ghent, Belgium (Received 12 October 2004; accepted 22 March 2005) Abstract – A Chlamydophila psittaci species-specific real-time PCR targeting the rDNA ribosomal spacer was developed as well as a genotype-specific real-time PCR targeting the Cp. psittaci outer membrane protein A (ompA) gene. The SYBR Green-based species-specific real-time PCR detected Cp. psittaci genotypes A to F, and the recently discovered E/B genotype. The genotype-specific real-time PCR could easily distinguish genotypes C, D, F by use of TaqMan probes. Genotypes A, B and E could not be distinguished from each other by simply using TaqMan probes. For this purpose, non-fluorescent competitor oligonucleotides, had to be used next to the TaqMan probes. Genotype E/B could only be detected by use of a minor groove binder (MGB) probe. Both real-time PCR assays allowed reproducible, sensitive (10 rDNA or ompA copies/µL DNA extract) and specific detection of Cp. psittaci DNA. The genotype-specific real-time PCR was compared to ompA sequencing and ompA restriction fragment length polymorphism (RFLP) analysis using five Cp. psittaci field isolates (99, 61/8, 7344/2, 8615/1 and 7778B15) each consisting of two different genotypes. The currently developed real-time PCR assays were used in a case study on a veterinary school and a turkey farm. In the veterinary school, Cp. psittaci genotypes D, E/B and F infection were detected in all five groups of turkeys, and one veterinarian who was taking care of all these turkeys. On the turkey farm, the presence of two Cp. psittaci genotype B infection waves was demonstrated in one randomly selected turkey, the first wave at the age of 6 weeks, and the second at the age of 12 weeks. Chlamydophila psittaci / real-time PCR / species-specific / genotype-specific / diagnosis 1. INTRODUCTION zoonotic disease in humans. Human psittaco- Chlamydiaceae are Gram-negative obli- sis mostly originates from exposure to infected gate intracellular bacteria replicating in psittacines, pigeons or poultry, mainly tur- mucosal epithelial cells and macrophages, keys [11] or ducks [14, 18]. Symptoms in causing disease in birds, humans, other man vary from asymptomatic to severe sys- mammals and marsupials. Chlamydophila temic disease [3]. psittaci (formerly Chlamydia psittaci) is a Cp. psittaci in birds and man still repre- respiratory avian pathogen able to cause sents a diagnostic challenge. Isolation is * Corresponding author: [email protected] Article published by EDP Sciences and available at http://www.edpsciences.org/vetres or http://dx.doi.org/10.1051/vetres:2005035 788 T. Geens et al. Table I. Cp. psittaci strains used for developing species- and genotype-specific primers and probes as well as inhibition control plasmids. Strain Reference Country Host Genotype Control plasmid 90/1051 [9] Belgium Amazona sp. A pGemT::CpPsGAS 41A12 [9] Belgium Meleagris gallopavo B pGemT::CpPsGBS GD [15] Gemany Anas platyrhyncos C pGemT::CpPsGCS 7344/2 [9] Italy Columba livia D pGemT::CpPsGDS 3759/2 [9] Italy Columba livia E pGemT::CpPsGES pGemT::CpPsSS 7778B15 [9] Belgium Meleagris gallopavo F pGemT::CpPsGFS WS/RT/E30 [9] Germany Anas platyrhyncos E/B pGemT::CpPsGE/BS labour-intensive, relatively insensitive and tive post PCR detection methods and are not without danger. In birds, serology is not quantitative or only semi-quantitative. used and is nowadays mostly performed by In addition, genotyping still needs to be per- an enzyme linked immunosorbent assay [6, formed by ompA restriction fragment length 21]. However the interpretation of the polymorphism (RFLP) analysis and ompA results is often difficult since most birds sequencing, and both techniques often have pre-existing antibodies from previous require bacterial culture, since amplifica- exposures, and antibodies can persist for up tion of full length ompA can mostly not be to several months. In man, the complement carried out directly from clinical specimens. binding assay (CBA) is often used. How- The present study describes the develop- ever, the CBA cannot distinguish Cp. psit- ment of a Cp. psittaci species-specific real- taci specific antibodies from antibodies time PCR. Additionally, we describe the against other chlamydial human pathogens, development of a genotype-specific real- like Cp. pneumoniae and Chlamydia tra- time PCR allowing the identification of all chomatis. As a result, the CBA is more and avian Cp. psittaci genotypes including the more often replaced by the micro-immun- recently discovered new E/B genotype [9]. ofluorescence (MIF) test. The MIF test dis- The performance of the genotype-specific tinguishes all chlamydial species and real-time PCR was compared to ompA measures IgG as well as IgM titres, allow- ing the detection of recent infections. How- RFLP analysis and ompA sequencing. The ever, early antibiotic treatment can interfere species- and genotype-specific real-time with antibody formation and in some PCR assays were used in a case study in a patients, antibody responses can develop veterinary school and on a turkey farm. rather slowly. Moreover, obligatory exam- ination of paired sera removes serology from immediate clinical relevance. There- 2. MATERIALS AND METHODS fore, several commercial antigen detection methods were developed for both birds and 2.1. Bacterial cultures man but they are either insensitive and/or less specific [21, 25]. Due to these short- Cp. psittaci genotypes A to F plus E/B comings, nucleic acid amplification methods strains 90/1051, 41A12, GD, 7344/2, 3759/2, have been designed. However, currently 7778B15 and WS/RT/E30 (Tab. I) were described polymerase chain reaction (PCR) used for the development of the species- and assays use labour-intensive and/or insensi- genotype-specific real-time PCR assays. Chlamydophila psittaci species/genotype real-time PCR 789 Bacteria were grown in cycloheximide fied using Qiagen spin columns (Westburg, treated Buffalo Green Monkey (BGM) cells Leusden, The Netherlands) and cloned into as described previously [26]. For each pGem®-T (Promega, Madison, WI, USA) strain, an infected monolayer of 300 cm2 following the manufacturer’s protocol. was disrupted by freezing and thawing, fol- Sequence analyses were performed by the lowed by ultrasonic treatment for 1 min in a VIB Genetic Service Facility (University of tabletop sonicator (Bransonic 12, BIOMEDe- Antwerp, Antwerp, Belgium) using vector vice, San Pablo, CA, USA). A two-hundred associated T7 and SP6 priming sites. millilitre cell culture harvest was centri- Sequence alignment using ClustalX soft- fuged for 10 min (1 000 × g, 4 °C) and sub- ware [22] allowed us to select a Cp. psittaci sequently concentrated by ultracentrifugation species-specific inhibition control plasmid for 1 h (45 000 × g, 4 °C). Bacteria were (pGemT::CpPsSS, Tab. I). resuspended in 2 mL sucrose phosphate glutamate buffer (SPG, 218 mM sucrose, 2.4. Species-specific real-time PCR 38 mM KH2PO4, 7 mM K2HPO4, 5 mM L-glutamic acid) and stored at –80 °C until use. Real-time PCR was performed with the LightCycler 2.0 Instrument (Roche, Applied 2.2. Preparation of genomic DNA Science, Penzberg, Germany) using the LightCycler FastStart DNA MasterPLUS Genomic DNA for real-time PCR assays SYBR Green I kit and LightCycler Capil- was prepared as described by Wilson et al. laries. The reaction mixture (20 µL) was [34]. DNA samples were further purified by prepared according to the manufacturer’s extracting them twice with 200 µL phenol- protocol: 11 µL PCR grade water, 2 µL of chlorophorm (1:1). Precipitation was per- primer mixture (300 nM CpPsSSfor and formed (1 h, –80 °C) by adding 20 µL sodi- CpPsSSrev), 2 µL 10× Master Mix, 5 µL of umacetate (3M) and 400 µL of 100% DNA template. The cycling conditions ethanol. The pellets obtained following were as follows: 50 cycles of 95 °C for 10 s, centrifugation (20 min, 4 °C, 16 060 × g) 63 °C for 10 s and 72 °C for 8 s. All default were washed for 5 min with 500 µL of 70% program settings were used. Standard graphs ethanol (4 °C, 16 060 × g) and were finally of the Cycle threshold (Ct) values, obtained resuspended in 30 µL bidest. by testing tenfold serial dilutions (108 to 101) of the purified species-specific inhibi- tion control plasmid, were used for quanti- 2.3. Species-specific primers fication. Ct-values were automatically and inhibition control plasmid converted into initial template quantities Published ribosomal spacer sequences (N0) using the LightCycler Software 4.0.
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