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Molecular Characterization of the Trichomonas Gallinae Morphologic Complex in the United States Author(S): Richard W

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Molecular Characterization of the Trichomonas Gallinae Morphologic Complex in the United States Author(S): Richard W Molecular Characterization of the Trichomonas gallinae Morphologic Complex in the United States Author(s): Richard W. Gerhold, Michael J. Yabsley, Autumn J. Smith, Elissa Ostergaardi, William Mannan, Jeff D. Cann and John R. Fischer Source: The Journal of Parasitology, Vol. 94, No. 6 (Dec., 2008), pp. 1335-1341 Published by: The American Society of Parasitologists Stable URL: http://www.jstor.org/stable/40059205 . Accessed: 01/08/2014 15:39 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. The American Society of Parasitologists is collaborating with JSTOR to digitize, preserve and extend access to The Journal of Parasitology. http://www.jstor.org This content downloaded from 158.135.136.72 on Fri, 1 Aug 2014 15:39:33 PM All use subject to JSTOR Terms and Conditions J. Parasitol., 94(6), 2008, pp. 1335-1341 © American Society of Parasitologists 2008 MOLECULARCHARACTERIZATION OF THE TRICHOMONAS GALLINAE MORPHOLOGIC COMPLEX IN THE UNITED STATES Richard W. Gerhold, Michael J. Yabsley*, Autumn J. Smithf, Elissa Ostergaardi, William Mannan§, Jeff D. Cann||, and John R. Fischer Southeastern Cooperative Wildlife Disease Study, College of Veterinary Medicine, The University of Georgia, Athens, Georgia 30602. e-mail: [email protected] abstract: Forty-two Trichomonas gallinae isolates were molecularly characterized to determine whether isolates differed in genetic sequence of multiple gene targets depending on host species or geographical location. The 5.8S ribosomal RNA (rRNA) and flanking internal transcribed spacer (ITS) gene regions were amplified by polymerase chain reaction, and the sequences were analyzed phylogenetically. The results of the sequence analysis strongly suggest at least 2 species may exist within the T. gallinae morphologic complex. Based on ITS sequences, one group demonstrated high nucleotide identity to the 3 T. gallinae sequences available in GenBank, whereas the second group was more closely related to T. vaginalis (98%) than to T. gallinae (92%). Two common ground-dove (Columbina passerina) isolates shared a 95% identity with T. vaginalis and a 92% identity with T. gallinae and T. tenax. Sequence analysis of both the 18S rRNA and a-tubulin genes from a subset of the isolates supports the 5.8S-ITS sequence results. All of the T. vaginalis-like isolates originated from Arizona, California, or Texas, whereas T. gallinae isolates were found in all sampled states. Both T. vaginalis-like and T. gallinae isolates were involved in trichomoniasis outbreaks in California and Arizona. Avian trichomoniasis, caused by the protozoan Trichomonas mayeri), numerous passerine species, and a variety of raptors, gallinae, is an acute and often fatal disease that is generally including Cooper's hawk (Accipiter cooperii), barn owl (Tyto manifested as a caseous lesion within the upper digestive tract alba), and the endangered Bonelli's eagle (Hieraaetus fasciatus) of affected birds. The rock pigeon (Columba livid) is an Old (Work and Hale, 1996; Boal et al., 1998; Real et al., 2000; World species and is considered the ultimate source of T. gal- Pennycott et al., 2005; Bunbury et al., 2008). In Tucson, Ari- linae. However, the protozoan may be pathogenic to both Old zona, approximately 85% of Cooper's hawk nestlings tested and New World avian species (Stabler, 1954). Trichomoniasis positive for T. gallinae, and trichomoniasis was the leading has been reported from several continents and is considered a cause of death in nestlings and fledglings (Boal et al., 1998; major disease for numerous avian species in the Columbiformes Estes and Mannan, 2003). and Falconiformes (Stabler, 1954; Forrester and Spalding, 2003; Infectivity studies with T. gallinae have demonstrated a wide Villanua et al., 2006). In the southeastern United States, tricho- spectrum of virulence. With highly virulent isolates, columbids moniasis is considered the most important disease of free-rang- may succumb to infection within 14 days after inoculation with ing mourning doves (Zenaida macroura) (Forrester and Spal- a single trichomonad, whereas with some avirulent isolates, ding, 2003; Gerhold et al., 2007). During a 2-yr outbreak in birds may fail to seroconvert after inoculation with 1 X 106 multiple southeastern states, an estimated 50,000 to 100,000 parasites (Stabler and Kihara, 1954; Honigberg, 1979). Previous mourning doves died of trichomoniasis in Alabama alone (Hau- investigations with clinically virulent and avirulent isolates of gen and Keeler, 1952). The disease occurs annually in mourning T. gallinae suggest that virulence and pathogenicity are con- trolled within doves and other columbids throughout North America, and genetically the organism (Honigberg et al., 1971). virulent and avirulent isolates have not large mortality events are reported frequently (Forrester and However, previously been Spalding, 2003; Rosenstock et al., 2004; Gerhold et al., 2007). analyzed genetically. of the 5.8S ribosomal RNA Recent population census information indicates mourning dove Recently, sequence analysis and internal transcribed 1 and populations have declined over much of the United States, par- (rRNA) flanking spacer regions 2 1 of within Tetratrichomonas dis- ticularly in the eastern United States during the last few decades (ITS , ITS2) organisms spp. closed and associations (Dolton and Rau, 2003), but it is unknown whether trichomo- unexpected diversity host-parasite et al., 2005, 2006). The results indicated that at least niasis is associated with the population decline. (Cepicka 16 distinct exist within the and Trichomoniasis may have an impact on several columbids, monophyletic groups genus, most of these are including the endangered pink pigeon from Mauritius {Columba monophyletic groups host-specific (Cepicka et al., 2006). In contrast, sequence analysis of the ITS1, 5.8S, and ITS2 rRNA regions of 24 T. gallinae isolates from pink Received 1 February 2008; revised 7 April 2008; accepted 8 April pigeons and Madagascar turtle doves (Streptopelia picturata) 2008. from the island of Mauritius disclosed no nucleotide * D. B. Warnell School of and Natural Resources, The Uni- polymor- Forestry of the and were identical versity of Georgia, Athens Georgia, 30602 and Southeastern Coop- phisms among any isolates, sequences erative Wildlife Disease Study, College of Veterinary Medicine, The to T. gallinae isolates from 2 rock pigeons from the United University of Georgia, Athens, Georgia 30602. States (Gaspar da Silva et al., 2007). t Caesar Kleberg Research Institute-Texas A&M University, Kingsville, The goal of the present study was to analyze sequences of Texas 78363. T. gallinae isolates from several avian obtained from a Arizona Game and Fish Tbcson, Arizona 85745. species $ Department, distribution in the United States to § School of Renewable Natural Resources, University of Arizona, TVic- wide-ranging geographic son, Arizona 85721. determine whether T. gallinae isolates differed genetically de- || California Department of Fish and Game, Monterey, California 93940. pending on host species or geographical location. 1335 This content downloaded from 158.135.136.72 on Fri, 1 Aug 2014 15:39:33 PM All use subject to JSTOR Terms and Conditions 1336 THE JOURNAL OF PARASITOLOGY,VOL. 94, NO. 6, DECEMBER2008 MATERIALSAND METHODS GG-3') and trichtubRl (5'-KGGGAAGTGGATACG-3') (Edgcomb et al., were at the Parasite culture 2001). Amplicons sequenced Integrated Biotechnology Laboratories, The University of Georgia, Athens, Georgia. Sequences Isolates collected during this study were acquired from hunter-killed obtained from this study and from other trichomonads stored in birds, necropsy, and arbovirus-testing submissions to the Southeastern GenBank were aligned using the multisequence alignment ClustalX pro- Cooperative Wildlife Disease Study (SCWDS), College of Veterinary gram (Thompson et al., 1994). Phylogenetic analyses were conducted Medicine, The University of Georgia, Athens, Georgia, and from birds using Molecular Evolutionary Genetics Analysis (Center for Evolution- captured in the field (Table I). Oral swabs were initially cultured in In- ary Functional Genomics, Tempe, Arizona), version 3.1 program (Ku- Pouch® TF kits (BioMed Diagnostics, White City, Oregon), incubated mar et al., 1993) using the neighbor-joining and minimum evolution at 37 C, and examined for trichomonad growth for 5 consecutive days. algorithms using the Kimura 2-parameter model and maximum parsi- The In-Pouch TF kit has been shown to be as sensitive as tryptone/ mony using a heuristic search. Bootstrap values were constructed using yeast extract/maltose (TYM) medium for isolating T. gallinae, and the Felsentein's bootstrap test (Felsentein, 1985). The GenBank accession kit has practical advantages for organism isolation, especially in field numbers of sequences obtained in this study are listed in Table I. conditions (Bunbury et al., 2005). Subcultures were performed using TYM (pH 7.0), supplemented with 10% heat-inactivated horse serum RESULTS (HIHS) (Sigma- Aldrich, St. Louis, Missouri) (Diamond, 1983). Initially, subcultures were supplemented
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