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Associated Mycoplasma Gallisepticum Identified in Lesser Goldfinch

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Associated Mycoplasma Gallisepticum Identified in Lesser Goldfinch DOI: 10.7589/2017-04-079 Journal of Wildlife Diseases, 54(1), 2018, pp. 180–185 Ó Wildlife Disease Association 2018 House Finch (Haemorhous mexicanus)–Associated Mycoplasma gallisepticum Identified in Lesser Goldfinch (Spinus psaltria) and Western Scrub Jay (Aphelocoma californica) using Strain-Specific Quantitative PCR Catherine R. Allen,1 Arlind Mara,1 Edan R. Tulman,1 David H. Ley,2 and Steven J. Geary1,3 1Department of Pathobiology and Veterinary Science and Center of Excellence for Vaccine Research, University of Connecticut, 61 N Eagleville Road, Unit 3089, Storrs, Connecticut 06269, USA; 2Department of Population Health and Pathobiology, College of Veterinary Medicine, North Carolina State University, 1060 William Moore Drive, Raleigh, North Carolina 27607, USA; 3Corresponding author (email: [email protected]) ABSTRACT:In1994Mycoplasma gallisepticum North American House Finch (Haemorhous was found to be the etiologic agent of House mexicanus) in Virginia, US in 1994 (Ley et al. Finch (Haemorhous mexicanus) conjunctivitis, a 1996), and this novel House Finch disease rapidly expanding epidemic caused by a geneti- cally discrete, House Finch–associated strain of spread into a North American epidemic. M. gallisepticum (HFMG). While most prominent Bacterial genomic sequencing (Tulman et al. in House Finches, HFMG has been reported in 2012) and multi-locus genetic analysis (Ho- other members of the family Fringillidae, includ- chachka et al. 2013) revealed the novel ing American Goldfinches (Spinus tristis), Purple epidemic to be caused by a discrete strain of Finches (Haemorhous purpureus), Pine Gros- beaks (Pinicola enucleator), and Evening Gros- M. gallisepticum (the House Finch–associated beaks (Coccothraustes vespertinus). Herein we Mycoplasma gallisepticum [HFMG] strain) report two new potential host species of HFMG which likely became established and spread strain, the Lesser Goldfinch (Spinus psaltria), in the House Finch population following a belonging to the Fringillidae family, and the single introduction. The epidemic spread Western (California) Scrub Jay (Aphelocoma californica), belonging to the Corvidae family. quickly across the eastern states (Dhondt et The latter is one of only two reports of HFMG al. 1998) and eventually throughout the native being found outside the Fringillidae family, and of House Finch range in the western US (Duck- these is the only one reported outside of captivity. worth et al. 2003; Ley et al. 2006). The Furthermore, non-HFMG M. gallisepticum was HFMG strain has been associated with a identified in an American Crow (Corvus brachyr- substantial decrease in the House Finch hynchos), indicating presence of additional strains in wild birds. Strain typing of M. gallisepticum population, especially in the eastern range isolates was done via HFMG-specific quantitative (Dhondt et al. 1998, 2005). PCR analysis and validated using random ampli- House Finches are the wild birds best fied polymorphic DNA analysis. Our results known to be impacted by M. gallisepticum,in suggested an expanded host range of HFMG particular by the HFMG strain that is found strain, and further suggested that the host range of HFMG was not limited to members of the nearly exclusively in finches (Hochachka et al. family Fringillidae. 2013). However, recent studies have identi- Key words: Corvidae, House Finch, Lesser fied M. gallisepticum in other wild bird Goldfinch, Mycoplasma gallisepticum, mycoplas- species (Ley et al. 2016). While most reports mal conjunctivitis, qPCR, RAPD, Western Scrub do not strain type M. gallisetpictum from wild Jay. birds, HFMG specifically has been reported in American Goldfinch (Spinus tristis), Purple Mycoplasma gallisepticum is a bacterial Finch (Haemorhous purpureus; Hartup et al. pathogen primarily associated with acute and 2000), Evening Grosbeak (Coccothraustes chronic respiratory disease in domestic poul- vespertinus), and Pine Grosbeak (Pinicola try (Raviv and Ley 2013). It was first reported enucleator; Mikaelian et al. 2001). In addition, as the etiologic agent of conjunctivitis in a non-HFMG strain (NY2001-var, ADRL House Finches when it was isolated from a 2001.035-16) of M. gallisepticum has been 180 SHORT COMMUNICATIONS 181 identified in a subclinical House Finch USA) to be between 4 ng/lL and 15 ng/lL (Cherry et al. 2006; Hochachka et al. 2013), and diluted with nuclease-free water 1:10 indicating that independent introduction of (0.4–1.5 ng/lL) for qPCR analysis. M. gallisepticum into House Finches may For HFMG-specific PCR design, reference occur and that additional strains may be genome sequences from multiple strains of M. circulating in the wild. To more fully under- gallisepticum were analyzed to identify sites stand its distribution and host range in wild suitable for discrimination of HFMG from bird populations, it is important to distinguish other strains. These included published and the genetically unique HFMG strain from unpublished data from HFMG (GenBank other strains of M. gallisepticum. Strain typing accession nos. CP003506–CP003513, of M. gallisepticum isolates is commonly done CA2009, GA2001, NY1998) and non-HFMG using randomly amplified polymorphic DNA strains low-passage R strain (AE015450), F (RAPD) fingerprinting, which yields distinct (CP001873), S6 (CP006916), TS-11, 6/85, and banding profiles when the RAPD products are NY2001-variant. The following forward and resolved electrophoretically (Geary et al. reverse primers were designed following 1994; Ley et al. 1997). Pure cultures of M. published suggestions (Dieffenbach et al. gallisepticum are essential for consistent and 1993), here with HFMG-specific bases high- accurate strain identification using a RAPD- lighted in bold text: SG2307, forward, 50- based technique. Due to the difficulties AGATAATCATAAACTTTGACACGGT-30 associated with acquiring pure cultures from and SG2327, reverse, 50-GATGAACTTT- wild birds and to make the process of TATTTAGTTCTTTACTG-30. These targeted identifying HFMG from wild bird isolates the 30 end of the HFMG thioredoxin reduc- quick, sensitive, and specific, we designed an tase locus (HFMG94VAA_3550) to produce HFMG-specific quantitative real-time PCR an amplicon of 274 base pairs in length. The (qPCR) assay that differentiates HFMG from qPCR reaction master mix per sample con- other M. gallisepticum strains in wild birds. sisted of 6.25 lL of Applied Biosystems Power Mycoplasma gallisepticum isolates from a SYBR Green PCR reagent (Roche Molecular variety of wild birds were initially speciated Systems, Pleasanton, California, USA), 0.5 lL and inventoried as part of the Avian Diagnos- working stock (10 lM) of each primer, and tic Research Laboratory collection at North 3.25 lL of nuclease-free water. Master mix Carolina State University. Conjunctival swabs (10 lL) and diluted DNA template (2.5 lL) were taken from both eyes, inoculated into was added in optical qPCR tubes to reach a mycoplasma transport media that was then reaction volume of 12.5 lL per sample. The stored at 4 C and shipped to the laboratory qPCR was run on the Bio-Rad CFX96TM overnight on cold packs. For analysis, 0.5 mL Real-Time PCR Detection System (Bio-Rad, of sample in transport medium was inoculated Hercules, California, USA) with the following into either 10 mL of Frey’s medium supple- conditions: 94 C for 3 min, followed by 40 mented with 15% swine serum or complete cycles of 94 C for 30 sec, 61.5 C for 30 sec, Hayflick’s broth and incubated at 37 C until and 72 C for 1 min, with fluorescence color change indicated growth. Bacterial measured once every extension. Under these concentration was estimated using measure- conditions and after analysis using the Bio- ment of optical density at 620 nm. Genomic Rad CFX Manager (Bio-Rad), known HFMG DNA was extracted from up to 23109 isolates consistently amplified at low cycle bacterial cells resuspended in 20 lL phos- threshold values (18.32–27.65), while known phate buffered saline per extraction using a non-HFMG isolates yielded no amplification gram-negative bacteria DNA extraction pro- or late-stage amplification. Melt-curve analysis tocol (GeneJET Genomic, Life Technologies, indicated one peak at 75.5 C in HFMG Carlsbad, California, USA). We quantified samples, suggesting primer specificity and a DNA concentrations using the Qubit dsDNA single amplicon. Given data using reference HS Assay (Invitrogen, Carlsbad, California, strains, cycle threshold values of less than 30 182 JOURNAL OF WILDLIFE DISEASES, VOL. 54, NO. 1, JANUARY 2018 at a constant baseline threshold value were be infected with HFMG (Ley et al. 1996) and considered positive for HFMG strain-specific M. gallisepticum has been detected in West- amplification under these qPCR conditions. ern Scrub Jays, but the infections in corvids To further validate the qPCR assay as were all suspected to be obtained nosocomi- HFMG-specific, a panel of isolates previously ally at rehabilitation facilities housing infected typed by RAPD fingerprinting was subjected House Finches. The Western Scrub Jay to qPCR and again typed by RAPD. Results hosting HFMG here had a field description indicated that our qPCR assay was fully stated as ‘‘consistent with ocular mycoplas- congruent with RAPD typing (Table 1 and mosis’’ including apparent sightlessness, and it Fig. 1). was euthanized for humane reasons on We examined currently untyped M. galli- accession to the wildlife facility, thus preclud- septicum isolates from non–House Finch ing nosocomial infection and suggesting nat- species to gain insight as to the host range urally
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