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Gopherus Agassizii) and the Gopher Tortoise (Gopherus Polyphemus)

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Gopherus Agassizii) and the Gopher Tortoise (Gopherus Polyphemus) International Journal of Systematic and Evolutionary Microbiology (2001), 51, 413–418 Printed in Great Britain Mycoplasma agassizii sp. nov., isolated from NOTE the upper respiratory tract of the desert tortoise (Gopherus agassizii) and the gopher tortoise (Gopherus polyphemus) M. B. Brown,1 D. R. Brown,1 P. A. Klein,3 G. S. McLaughlin,1 I. M. Schumacher,3 E. R. Jacobson,2 H. P. Adams4 and J. G. Tully5† Author for correspondence: M. B. Brown. Tel: j1 352 392 4700 ext. 3970. Fax: j1 352 846 2781. e-mail: mbbrown!nersp.nerdc.ufl.edu 1,2,3 Departments of Biochemical, serological and molecular genetic studies were performed on 1 Pathobiology and seven mycoplasma isolates that were recovered from the upper respiratory Small Animal Clinical Sciences2 , College of tract of clinically ill desert tortoises. The isolates were serologically related to Veterinary Medicine, each other but serologically distinct from previously described species. Unique and Department of mycoplasma species-specific 16S rRNA nucleotide sequences were found in the Pathology and Laboratory Medicine, proposed type strain. The name Mycoplasma agassizii is proposed for these College of Medicine3 , isolates. The type strain is PS6T (l ATCC 700616T) which caused upper University of Florida, respiratory tract disease (URTD) in experimentally infected tortoises. Gainesville, FL 32610, USA 4 Department of Cell Biology, Baylor College Keywords: mycoplasma, tortoise, upper respiratory tract disease of Medicine, Houston, TX 77030, USA 5 Mycoplasma Section, National Institute of Allergy and Infectious Diseases, Frederick, MD 21702, USA Recent dramatic population declines in the desert mycoplasmas have also been isolated from the trachea tortoise (Gopherus agassizii) in California have resulted and lung. Antibody to the mycoplasma species was in the listing by the United States Federal Government found in 15 of 16 tortoises with respiratory lesions of this animal as a threatened species in areas north (Schumacher et al., 1993). In a serological survey of and west of the Colorado River (Department of desert tortoises in Nevada, 84% of animals with Interior, 1990). In addition to habitat degradation, clinical signs of URTD tested positive by ELISA drought and predation, an upper respiratory tract (Schumacher et al., 1997). In experimental infection disease (URTD) was identified as a major contributory studies (Brown et al., 1994, 1999) clinical isolates of the factor in population declines. We initially demon- new mycoplasma caused URTD in both the desert and strated by electron microscopy the presence of classical gopher tortoise (Gopherus polyphemus), fulfilling the mycoplasma-like organisms attached to the respir- majority of the Koch–Henle–Evans postulates and atory surface, often between the cilia (Jacobson et al., demonstrating the pathogenic potential of the species 1991). These observations led to attempts to culture (Evans, 1976). The isolates from the desert tortoise did and isolate the mycoplasmal species. In conjunction not react with antisera against other known myco- with a detailed pathology study, we have isolated plasmal species. In this study we describe the charac- mycoplasmas from 5 of 9 (56%) ill tortoises and 4 of teristics of the isolates and propose that these strains 12 (33%) apparently healthy tortoises, some of which should be classified as a new species in the genus had microscopic lesions. The most common sites of Mycoplasma, Mycoplasma agassizii sp. nov. The type isolation were the choana and nasal passages, but strain of this species is PS6T which was used in the ................................................................................................................................................. experiments to demonstrate an aetiologic role for the † Present address: 16400 Black Rock Road, Germantown, MD 20874, USA. mycoplasma in URTD. Abbreviation: URTD, upper respiratory tract disease. Desert tortoises used in this study were obtained under The GenBank accession number for the 16S rRNA gene sequence of special permit from the US Fish and Wildlife Service. Mycoplasma agassizii is U09786. Tortoises had been collected in the Las Vegas Valley, 01633 # 2001 IUMS 413 M. B. Brown and others Table 1 Chelonian species from which Mycoplasma agassizii has been recovered by culture or detected by PCR Scientific name Common name Status* Geochelone chilensis Chaco tortoise Captive Geochelone pardalis Leopard tortoise Captive Geochelone elegans Indian star tortoise Captive Geochelone forstenii Travancore tortoise Captive Geochelone sulcata African spurred tortoise Captive Gopherus agassizii Desert tortoise Wild and captive Gopherus polyphemus Gopher tortoise Wild and captive Indotestudo sp. Unnamed tortoise Captive Terrapene carolina bauri Florida box turtle Wild and captive Testudo graeca graeca Spur-thighed tortoise Captive Testudo graeca ibera Spur-thighed tortoise Captive * Wild status refers to tortoises which were captured and sampled in the field. Captive status refers to tortoises which were part of a private collection or housed under captive conditions. Las Vegas, NV, USA, and were held at the Desert arginine, 10B, A8 and SP-4 (ATCC medium 988) Tortoise Conservation Center. Clinically ill and ap- (Freundt, 1983; Tully et al., 1979). Both horse serum parently clinically healthy animals were sent to the and fetal bovine serum were used as supplements. University of Florida for intensive pathology studies. Initial incubation temperatures included 20, 25, 30 and Isolates designated PS were cultured from these 35 mC. Cultures were incubated in both ambient air animals at necropsy. Additional samples, designated and 5% CO#. The only successful initial isolations as numerals only, were submitted as nasal washes from were obtained with SP-4 containing 20% fetal bovine tortoises in a relocation study. Nasal washes were serum. Optimal primary isolation rates were obtained obtained in the field by gently flushing the nares of the at 30 mC. Primary isolations required 3–6 weeks for tortoise with 1 ml sterile tryptose broth via a catheter growth in broth or on agar. Single colonies were attached to a 1 ml syringe. The broth was placed in expanded in broth, replated and the procedure re- cryotubes, frozen in liquid nitrogen and sent to the peated two times. Strains recovered under these University of Florida on dry ice. conditions were then purified by conventional filter- cloning procedures through three consecutive passages All strains described in this study were isolated from T (Tully, 1983). Subsequent broth passages could be tortoises with URTD. Strains PS6 , PS10, 553 and 111 adapted to grow at 37 mC. were isolated from the nares of desert tortoises with clinical signs of URTD. Strain PS13T was isolated Morphology was examined by conventional darkfield from the trachea of a tortoise with URTD; strain and electron microscopy. Ultrathin sections of micro- PS13C was isolated from the choana of that same organisms from broth cultures were prepared by tortoise. The micro-organism has been demonstrated techniques described by Deines & Bullivant (1968). in the upper respiratory tract of a number of other The morphology of strain PS6T cultivated in SP-4 captive chelonians (Table 1), but the pathogenic broth at 30 mC for 48 h was examined under darkfield potential in these species has not been confirmed microscopy at a magnification of i1250. Agar col- although clinical signs compatible with URTD have onies of strain PS6T were obtained on SP-4 agar after been observed in some of these species. Reference incubation at 30 mC under anaerobic conditions in the strains and antisera used in the serological cross- Gaspak system (BBL Microbiology Systems). reaction tests were from the Mycoplasma Reference Laboratory Collection, NIAID, Frederick, MD, USA All strains recovered from the tortoises that showed a (Table 2). Most, if not all, of these reference reagents colour change in broth were subjected to six passages are available from the Mollicutes Culture Collection, in broth without bacterial inhibitors. At each passage, University of Florida, Gainesville, FL, USA. Myco- subcultures were made on blood agar, brain heart plasma testudinis, the only other described myco- infusion agar and in brain heart infusion broth to determine if reversion to bacterial forms had occurred. plasmal species of chelonian origin (Hill, 1985), was T obtained from the American Type Culture Collection The ability of strain PS6 and other tortoise isolates to (ATCC), Manassas, VA, USA. Rabbit antiserum was pass through filters was determined by passage through T 0n45 and 0n22 µm porosity membrane filters (Tully, prepared to Mycoplasma agassizii PS6 and Myco- T plasma testudinis. 1983). The ability of strain PS6 and other tortoise isolates to ferment glucose, hydrolyse arginine and Initial isolation attempts were made using a wide urea, and produce phosphatase was tested using variety of media, including Frey’s, modified Hayflick’s, standard methods (Aloutto et al., 1970). Haemag- 414 International Journal of Systematic and Evolutionary Microbiology 51 Mycoplasma agassizii sp. nov. Table 2 Mycoplasma species tested by growth inhibition and epi-immunofluorescence for cross-reactivity with Mycoplasma agassizii Mycoplasma adleri G145T Mycoplasma edwardii PG24T Mycoplasma meleagridis 17529T Mycoplasma agalactiae PG2T Mycoplasma elephantis E42T Mycoplasma moatsii MK405T Mycoplasma alkalescens D12T Mycoplasma equigenitalium T37T Mycoplasma mobile 163KT Mycoplasma alvi IlsleyT Mycoplasma equirhinis M432\72T
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