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1 Australian Reference Laboratory for Bovine Tuberculosis, Department of Agriculture Western Australia, 3 Baron-Hay Court, South Perth, WA 6151, Australia
2 CONICET and Departamento de Ciencias Marinas, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, Casilla de Correo 43, (7600) Mar del Plata, Argentina
3 Instituto de Biotecnología, CICVyA, Instituto Nacional de Tecnología Agropecuaria, Los Reseros y Las Cabañas, (1712) Castelar, Argentina
4 Fundación Mundo Marino, Avda Décima 157, (7105) San Clemente del Tuyú, Argentina
5 Bristol Zoo Gardens, Bristol BS8 3HA, UK
6 Pathobiology Group, Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Private Bag 11-222, Palmerston North, New Zealand
7 Centre for DNA Fingerprinting and Diagnostics (CDFD), Nacharam, Hyderabad 500 076, India
8 AgResearch, Wallaceville Animal Research Centre, Upper Hutt, New Zealand
9 Division of AIDS, STD and TB Laboratory Research, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA 30333, USA
10 Mycobacterium Reference Laboratory, Queensland Health Pathology Services, Prince Charles Hospital, Chermside, Qld 4032, Australia
11 Departamento de Micobacterias, DILACOT, Servicio Nacional de Sanidad y Calidad Agroalimentaria (SENASA), Avda A Fleming 1653, (1640) Martínez, Argentina
Correspondence
Debby V. Cousins
dcousins{at}agric.wa.gov.au
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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Published online ahead of print on 24 January 2003 as DOI 10.1099/ijs.0.02401-0.
The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain 6482T is AF502574.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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), but can also cause disease in a wide variety of other animals, including man; M. bovis Bacille Calmette–Guérin (BCG), an attenuated strain that is used for vaccination; Mycobacterium africanum, a heterogeneous group of isolates responsible for human tuberculosis in Africa, which appears to be intermediate between M. tuberculosis and M. bovis (Castets et al., 1969); and Mycobacterium microti, a less frequently isolated pathogen that traditionally causes tuberculosis in voles (Wells & Oxen, 1937; Wells & Robb-Smith, 1946), but has been identified more recently as a cause of disease in immunocompromised humans (van Soolingen et al., 1998). Each member of the M. tuberculosis complex is associated with a specific primary host, although infection is known to occur in various alternative hosts. Although all of these strains effectively share the same 16S rRNA gene sequence (Rogall et al., 1990b) and high DNA–DNA homology (from hybridization studies), they can be separated by some phenotypic characteristics (Grange & Yates, 1994) and, as they have different primary hosts, they have been regarded as separate species (Collins et al., 1982). More recently, two novel strains have been described: ‘Mycobacterium canettii’, a novel smooth variant of M. tuberculosis that was first isolated from a Somali-born patient (van Soolingen et al., 1997) and subsequently from a Swiss patient exposed in Africa (Pfyffer et al., 1998); and ‘Mycobacterium caprae’ (basonym: M. tuberculosis subsp. caprae), a strain that occurs primarily in Spanish goats and has recently been elevated to species level (Aranaz et al., 1999; Niemann et al., 2002; Aranaz et al., 2003). M. tuberculosis, M. africanum, M. microti and M. bovis were accepted as separate species by using a combination of phenotypic characteristics and apparent host specificity. ‘M. canettii’ and ‘M. caprae’ were accepted by virtue of host preference and phenotypic and genetic characteristics.
Previous logical arguments have suggested that all members of the M. tuberculosis complex are sufficiently similar to belong to the species M. tuberculosis (Wayne, 1984; Tsukamura et al., 1985; van Soolingen et al., 1997). Acceptance of such an approach would cause currently accepted species (M. bovis, M. microti and M. africanum) to warrant classification at the subspecies level.
Between 1986 and 1995, M. tuberculosis complex organisms were isolated from cases of tuberculosis in captive or wild Australian sea lions (Neophoca cinerea), New Zealand fur seals (Arctocephalus forsteri), an Australian fur seal (Arctocephalus pusillus doriferus) and a seal trainer who worked with the affected colony in Australia (Forshaw & Phelps, 1991; Thompson et al., 1993; Cousins, 1995; Woods et al., 1995). Similar organisms were recovered from captive Southern sea lions (Otaria flavescens), wild South American fur seals (Arctocephalus australis) and a wild Subantarctic fur seal (Arctocephalus tropicalis) in Uruguay or Argentina during the period 1989–2000 (Bernardelli et al., 1994, 1996; Castro Ramos et al., 1998; Bastida et al., 1999). Between 1996 and 1998, M. tuberculosis complex organisms were recovered from two South American fur seals in a zoological collection in Great Britain and a Brazilian tapir (Tapirus terrestris) housed in an adjacent enclosure, and from two New Zealand fur seals in New Zealand in 1997 and 1998 (Hunter et al., 1998).
Many of the isolates obtained from cases of tuberculosis in Australia, Uruguay and Argentina have been well-characterized (Cousins et al., 1993; Bernardelli et al., 1996; Cousins, 1996; Alito et al., 1999; Zumárraga et al., 1999) and this information, together with preliminary tests on the seal isolates from Great Britain and New Zealand, suggested that the seal bacillus (Cousins et al., 1993), isolated from pinnipeds from all four continents, may be a unique member of the M. tuberculosis complex. A recent study of four Australian and six Argentinian seal isolates by fluorescent amplified fragment length polymorphism (FAFLP) has further substantiated the hypothesis that the seal bacillus occupies a unique taxonomic position within the M. tuberculosis complex (Ahmed et al., 2003). This report consolidates the results of tests performed previously and provides additional information, resulting in a comprehensive comparison of isolates available from pinniped-related cases of tuberculosis, and indicates that the seal bacillus should be considered as a novel species of the M. tuberculosis complex.
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METHODS |
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). Isolates recovered from two guinea pigs and two rabbits after pathogenicity experiments in Australia, a bovine in New Zealand (this isolate had a restriction endonuclease analysis pattern similar to those of the Australian seal isolates) and a Brazilian tapir were also included. Where appropriate, isolates were compared to representative (and reference) strains of M. tuberculosis (H37Rv or Mt14323), M. africanum (TMC3), ‘M. caprae’ (CIP 105776T), M. microti (NCTC 8710T), M. bovis (AN5) and M. bovis BCG (P3) (Table 2).
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). In vitro susceptibility patterns to isoniazid, rifampicin, streptomycin and ethambutol were determined for three isolates from Australia, three from Argentina, one from Uruguay, two from Great Britain and two from New Zealand by using the Mycobacterial Growth Indicator Tube (MGIT; Becton Dickinson) system (Bernardelli et al., 1999; Morcillo et al., 2000).
Pathogenicity studies in guinea pigs and rabbits.
Isolates from two Australian seals (Au-1 and Au-2) were each injected into a guinea pig and a rabbit, and three isolates from Argentina (Ar-1, Ar-2 and Ar-3) and the isolate from Uruguay (U-1) were inoculated into guinea pigs, to examine the pathogenicity of the seal isolates.
Mycolic acid analysis.
Mycolic acid profiles of two representative isolates (Au-1 and Au-2) were examined by HPLC, according to previously published procedures (Butler et al., 1996, 1999).
Tests for MPB70.
All isolates were tested for the presence of the MPB70 antigen either by using the immunoperoxidase test (Corner et al., 1988; Veerman et al., 1990; Liébana et al., 1996) and/or by performing SDS-PAGE on antigen preparations (Cousins et al., 1993; Alito et al., 1999).
16S rDNA sequence determination and PCR-based tests for genetic markers.
PCR-mediated amplification of 16S rDNA was performed by using procedures described previously (Edwards et al., 1989; Kirschner et al., 1993). The nucleotide sequences obtained were compared to all known 16S rDNA mycobacterial sequences in GenBank and the M. bovis sequence (available at the Sanger website, http://www.sanger.ac.uk/Projects/M_bovis/) by using the FastA application. Sequences were aligned with the program PILEUP from the Genetics Computer Group (GCG) version 9 UNIX software package. Phylogenetic analyses of the sequence data were done with programs from the Phylogeny Inference Package (PHYLIP) as described previously (Floyd et al., 1996). The pairwise comparison program GAP, also from the GCG package, was used to determine the position of consensus strand nucleotides, relative to those of Escherichia coli (GenBank number J01859). The 16S rDNA sequence of strain 6482T was deposited in GenBank under accession number AF502574.
PCR-based tests for known genetic markers.
All isolates were tested by PCR for the presence of mycobacterial 16S rDNA, the gene that encodes the MPB70 antigen, the IS6110, IS1081 and mtp40 sequences (Del Portillo et al., 1991) and the PAN promoter region that is present in pathogenic mycobacteria (Gormley et al., 1997) by using previously published methods (Liébana et al., 1996; Zumárraga et al., 1999). Representative isolates were tested for katG and gyrA gene sequence polymorphisms at codons 463 and 95, respectively, by using methods described previously (Zumárraga et al., 1999). Allele-specific polymorphisms were examined at nt 285 of the oxyR gene (Sreevatsan et al., 1996), which differentiates M. bovis and ‘M. caprae’ (adenine) from other members of the M. tuberculosis complex (guanidine), and in codon 57 (nt 169) of the pncA gene, which is responsible for pyrazinamide (PZA) resistance (Espinosa de los Monteros et al., 1998), which is consistent with M. bovis.
Spoligotyping.
All but two isolates were tested for known spacers between direct repeats in the DR allele by using the spoligotyping method developed by Kamerbeek et al. (1997) and performed as described previously (Aranaz et al., 1996; Zumárraga et al., 1999). Spoligotyping results were analysed by electronic scanning of images and converting and analysing them by using GelCompar version 1.3, as described previously (Romano et al., 1995; Cousins et al., 1998a, b). The patterns obtained from the South American isolates were compared to a database that consisted mostly of M. bovis isolates from Argentina. In addition, the patterns obtained from all seal isolates were compared with a large database of patterns that contained approximately 700 M. tuberculosis complex isolates, including approximately 500 M. bovis isolates from cattle, buffalo, deer, wild animals and humans from Australia and other countries (Cousins et al., 1998a); they were also compared to the CDC database (Jack Crawford, personal communication). The seal isolates and representative and reference strains of the M. tuberculosis complex (Table 2
) were included in a dendrogram of spoligotype patterns that were generated by using Dice UPGMA analysis (GelCompar, version 3.1; Applied Maths) to examine the clonal relationships between them.
FAFLP.
Heat-killed cells of isolates from three Australian sea lions, one Australian fur seal and six South American fur seals were digested by using EcoRI/MseI and analysed by FAFLP, using methods described previously (Ahmed et al., 2002, 2003). Analyses were based on the differential amplification of 131 genomic loci. Standard genomic DNA from M. tuberculosis H37Rv, M. bovis AN5, M. africanum and M. microti (NCTC 8710T) was used for comparative FAFLP analysis.
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RESULTS AND DISCUSSION |
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) (Table 3), a fact that led to their initial identification as such in Australia (Forshaw & Phelps, 1991), Argentina (Bernardelli et al., 1996) and Great Britain. In some cases, varying amounts of niacin were produced, which is similar to results reported for M. africanum (Grange & Yates, 1994). In most cases, the seal isolates grew preferentially on media that contained sodium pyruvate, although some (including NZ-2 and NZ-3) also grew on Löwenstein–Jensen medium that contained glycerol. Slight differences from typical M. bovis isolates were noted in Australia and Argentina, in that the cord formation observed after Ziehl–Neelsen staining was loose; further investigations uncovered differences between the seal isolates and M. bovis, including its susceptibility to PZA.
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) and tapirs, suggests that the seal bacillus has the potential for a host range that extends beyond those of M. tuberculosis, M. africanum and M. microti.
Mycolic acid analysis
HPLC chromatograms of isolates Au-1 and Au-2 demonstrated a single cluster pattern that was consistent with species of the M. tuberculosis complex (data not shown) as reported previously (Butler et al., 1991), providing additional evidence that these organisms belonged to the M. tuberculosis complex.
Tests for the MPB70 antigen
All seal isolates were negative when tested for the MPB70 antigen, despite containing the mpb70 gene. The MPB70 antigen is considered to be characteristic of M. bovis (Corner et al., 1988; Liébana et al., 1996) and can be demonstrated by dot-blot immunoperoxidase (Liébana et al., 1996) or SDS-PAGE (Cousins, 1996; Alito et al., 1999). In a previous study, >97 % of M. tuberculosis isolates, 100 % of M. microti isolates and 90 % of M. africanum isolates were negative for the MPB70 antigen, whereas >99 % of M. bovis isolates were positive (Liébana et al., 1996). In this regard, the seal bacillus was more like other members of the M. tuberculosis complex than M. bovis. The reported presence of the MPB70 antigen in a single isolate of M. microti from an alpaca (Alito et al., 1999) was contrary to the findings of Liébana et al. (1996), who tested seven isolates of M. microti (including the reference strain).
16S rDNA sequence determination
16S rDNA sequencing is an accepted method of confirming the species designation of mycobacterial isolates (Böddinghaus et al., 1990; Rogall et al., 1990a, b). The 16S rDNA consensus strand (1400 nt) from the seal isolates demonstrated 99·9 % similarity to those of M. tuberculosis (GenBank number X58890) and M. bovis (available from the Sanger website at http://www.sanger.ac.uk/Projects/M_bovis/). A single nucleotide substitution (C
T) in the consensus strand occurred at E. coli position 1256 (data not shown). Phylogenetic analysis demonstrated that the consensus sequence was on the same branch as that of M. tuberculosis. The 16S rDNA regions of the isolates that were sequenced (1030 bp) were consistent with the sequence of the M. tuberculosis complex.
PCR-based testing of genetic markers
The gyrA and katG gene sequences of all seal isolates were identical (Table 4). These genetic markers are accepted methods of confirming that isolates belong to the M. tuberculosis complex (Thierry et al., 1990, 1993; Collins & Stephens, 1991; Cousins et al., 1991; Groenen et al., 1993; Liébana et al., 1996; Gormley et al., 1997; Sreevatsan et al., 1997). Results from sequencing of the mtp40, pncA and oxyR genes clearly demonstrated that the seal isolates were genetically more consistent with M. tuberculosis and M. africanum than with M. bovis.
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). All of the isolates from Australia and all but one of the Argentinian isolates had a unique but identical pattern, designated seal spoligotype 1 (SS-1). The remaining Argentinian isolate was designated SS-2. The three isolates from Great Britain had identical spoligotypes (SS-3) that differed by one spacer from the other seal spoligotypes. The seal isolates from New Zealand and the isolate from a New Zealand bovine had identical spoligotypes (SS-4) that lacked six spacers that were present in all other seal isolates. When compared to reference (and representative) strains of M. tuberculosis, M. africanum, M. microti, M. bovis, ‘M. canettii’ and ‘M. caprae’, the seal isolates formed a distinct cluster within the M. tuberculosis complex (Fig. 2). Spoligotyping confirmed that the seal isolates from Australia, Argentina, Uruguay and Great Britain were closely related. The finding of three spoligotypes with only minor differences from 29 isolates that originated from these diverse geographical regions indicated a clonal relationship between these isolates, which in turn suggests that the infection may have originated from a single source as a relatively recent event. Considering that these cases were diagnosed over a period of more than 15 years and that many of these populations inhabit geographically separate territories, a more likely explanation is that the DR locus exhibits considerable genetic stability in the seal bacillus. The spoligotype identified in the New Zealand isolates clustered with those of the other seal isolates but was genetically further removed, confirming a closer relationship to the other seal isolates than to other members of the M. tuberculosis complex. Similar small differences in spoligotype were evident among a group of ‘M. caprae’ isolates (Aranaz et al., 1999). Spoligotyping has previously been used to define clonal relationships of the Beijing family of M. tuberculosis (van Soolingen et al., 1995; Qian et al., 1999; Anh et al., 2000) and has been used to trace the global spread of this strain. It has also been proved to be useful in defining populations of M. microti (van Soolingen et al., 1998) and, in this study, demonstrated its usefulness in defining the limited genetic diversity of the seal bacillus.
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that identified deletion events in M. bovis BCG has elicited information on the evolution of BCG strains. Similar evolutionary insights into the origin of the seal bacillus have been gained by using comparative genomic technologies that were described previously (Brosch et al., 2002; Mostowy et al., 2002). In both studies, the seal strain was separated from classical M. bovis by at least six deletions. The seal bacillus has a similar number of deletions to M. microti and Brosch et al. (2002) suggest that, along with M. microti and ‘M. canettii’, the seal bacillus contains a unique deletion. These deletion studies provide further evidence that the seal bacillus should be designated as a separate species within the M. tuberculosis complex.
FAFLP
All 10 seal isolates produced indistinguishable results. When compared to the published sequences of M. tuberculosis strains CDC1551 and H37Rv and M. bovis strain AN5, up to 18 highly polymorphic FAFLP markers for the rapid identification of the seal bacillus were identified. In these studies, three loci appeared to be unique to the seal bacillus, 12 were shared with M. bovis and three were shared with M. tuberculosis. Further studies that include some of these loci may result in the identification of species-specific markers that are potentially useful for the development of PCR-based diagnostics for the seal bacillus. The identical genotype of all seal isolates that were tested by FAFLP confirmed their close clonal relationship, which had been identified by spoligotyping. It also substantiated previous studies that used FAFLP, which suggested that this technique may play a role in discriminating between mycobacterial species, including members of the M. tuberculosis complex (Goulding et al., 2000; Huys et al., 2000).
Description of Mycobacterium pinnipedii sp. nov.
Mycobacterium pinnipedii (pin.ni.pe'di.i. N.L. gen. neut. n. pinnipedii of a pinniped, referring to the host animal from which the organism was first isolated).
Isolates can be recovered from the lung and associated lymph nodes of tuberculous pinnipeds, and occasionally from mesenteric lymph nodes and organs such as the liver. Acid/alcohol-fast, non-spore-forming, non-motile bacilli with loose cord formation. Growth is generally enhanced by sodium pyruvate and usually occurs within 3–6 weeks of incubation on egg-based media at 36–37 °C. Colonies are dysgonic, rough, flat and non-photochromogenic. Isolates are negative for nitrate reduction and generally negative for niacin accumulation; some isolates demonstrate low-to-medium reactions for niacin. Susceptible to 50 µg PZA ml-1 and 1 µg thiophen-2-carboxylic acid hydrazide (TCH) ml-1 (isolates have occasionally demonstrated resistance to 1 µg TCH ml-1, but are susceptible to 10 µg ml-1). Pathogenic in guinea pigs and rabbits; the apparent incidental infection of a human, bovine and tapir indicates that they may have a wide host range. All isolates contain the sequences IS6110, IS1081, mpb70 and mtp40, yet fail to produce detectable MPB70 antigen. The pncA gene contains CAC (His) at codon 57 and the oxyR gene shows G at nt 285, similar to M. tuberculosis, M. microti and M. africanum. The seal isolate spoligotypes form a cluster that is clearly different from those of all other members of the M. tuberculosis complex. The isolates are susceptible to isoniazid, rifampicin, streptomycin, ethambutol and paraminosalicylic acid.
The type strain is 6482T (=ATCC BAA-688T=NCTC 13288T).
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ACKNOWLEDGEMENTS |
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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, Hybridization with spacer; 
, no hybridization with spacer. NCTC, National Collection of Type Cultures; TMC, Trudeau Mycobacterium Collection.