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1 Division of AIDS, STD, and TB Laboratory Research, National Center for HIV, STD, and TB Prevention, Centers for Disease Control and Prevention, Atlanta, GA 30333, USA
2 Laboratorio de Tuberculosis, Instituto de Biomedicina, Caracas, Venezuela
Correspondence
Robert C. Cooksey
rcooksey{at}cdc.gov
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Published online ahead of print on 9 July 2004 as DOI 10.1099/ijs.0.63238-0.
The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA and hsp65 gene sequences of strain LTA-388T and the 16S rRNA and hsp65 gene sequences of strain 2003-11-06 are AY449728–AY449731, respectively.
A micrograph showing acid-fast bacilli, a photograph showing colonies of strain LTA-388T and photographs showing hsp65 PRA patterns and PFGE and RAPD typing patterns are available as supplementary material in IJSEM Online.
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), only 2 years after Koch reported the tubercle bacillus. Prior to the early 1980s, reports of diseases caused by NTM were somewhat sporadic and the diseases were often associated with environmental sources (Falkingham, 1996). Skin and wound infections following invasive procedures are relatively rare (
5 % of procedures) and NTM are involved only occasionally (Murillo et al., 2000). The most common NTM species associated with primary cosmetic infections are rapidly growing Mycobacterium (RGM) species including Mycobacterium chelonae, Mycobacterium abscessus and Mycobacterium fortuitum. The NTM also appear to be gaining importance as opportunistic pathogens, particularly among immunocompromised patients in developed nations (Falkingham, 1996).
In a recent study involving a nail salon in Atlanta, GA, USA, two cases of furunculosis caused by Mycobacterium mageritense were identified. Three additional NTM isolates from cultures obtained from footbaths and a sink drain were identified as ‘Mycobacterium goodii/Mycobacterium smegmatis’ on the basis of mycolic acid patterns, determined by HPLC, showing features of both species (Gira et al., 2004). A similar pattern was also observed for an isolate from a culture of a granulomatous subdermal lesion of a female patient in Venezuela who was undergoing mesotherapy with an unknown substance(s) for a cosmetic purpose (weight loss). We evaluated these isolates by using a polyphasic approach that included microscopic and macroscopic morphological examination, biochemical and antimicrobial drug-susceptibility patterns, nucleotide sequence analyses of three taxonomically useful regions of the rpoB, hsp65 and 16S rRNA genes and strain typing by random amplified polymorphic DNA (RAPD) electrophoresis and PFGE of large restriction fragments. Our data indicate that the four isolates previously identified as ‘M. goodii/M. smegmatis’ were, in fact, representative of two strains of a novel RGM species.
The isolate taken from a patient was obtained by treating material from the granulomatous lesion with N-acetyl-L-cysteine (0·1875 %, w/v) and NaOH (1 %, w/v) and inoculating Löwenstein–Jensen (LJ) medium as previously described (Kent & Kubica, 1985). The environmental isolates were obtained from swabs of sink and footbath drains, which were placed in 2 ml Middlebrook & Cohn 7H9 broth (Remel) and decontaminated with 0·005 % (w/v) cetylpyridinium chloride. An aliquot (1 ml) of each broth specimen was filtered through 0·45-µm filters that were washed twice with 100 ml 0·00425 % (w/v) monopotassium phosphate buffer, and incubated on Middlebrook 7H10 agar (Remel) plates containing oleic acid albumin dextrose complex enrichment at 35 °C. Mycolic acids derivatized as p-bromophenacyl esters were examined by using a standard UV-HPLC method (Butler et al., 1996) and a model System Gold HPLC system (Beckman Coulter) equipped with a Beckman C18 reverse-phase ultrasphere-XL cartridge and a Beckman model 166 UV detector. Control strains for HPLC included M. smegmatis ATCC 19420T, M. mageritense ATCC 700351T, Mycobacterium wolinskyi ATCC 700010T and M. goodii ATCC 700504T.
Antimicrobial drug-susceptibility testing was performed in cation-supplemented Mueller–Hinton broth by using a microdilution method, and interpretations of MICs were made according to NCCLS standards for organisms that grow aerobically (NCCLS, 2002). Microscopic analysis of acid-fast bacilli following Kenyoun staining, and testing for colonial morphology, pigment production, single-source carbon utilization, growth rate, tolerance of elevated incubation temperature (45 °C) or 5 % (w/v) NaCl, iron uptake, niacin production, nitrate reduction, arylsulfatase production and ability to grow on MacConkey agar without crystal violet were performed as previously described (Kent & Kubica, 1985). Media and reagents for biochemical tests were prepared at the Centers for Disease Control and Prevention (CDC), with the exception of niacin test strips and nitrate-reduction broth and reagents, which were obtained from Remel. The results of biochemical tests were read after 7 and 14 days incubation at 28 °C, except for arylsulfatase, which was read after 3 and 14 days incubation, and ability to grow on MacConkey agar without crystal violet, which was read after 5 and 11 days, as described in a standard protocol for biochemical testing of mycobacteria (Kent & Kubica, 1985). Control strains for biochemical testing included M. smegmatis ATCC 35797, M. fortuitum ATCC 6841T, M. chelonae ATCC 35752T, Mycobacterium avium ATCC 35713 and a BCG strain of Mycobacterium bovis (ATCC 35731), all of which were from the stock collection of the Mycobacteriology Branch of the CDC.
Genotypic tests were performed using DNA extracted from bacteria grown in complete Middlebrook & Cohn 7H9 broth (Remel) with a modified bead-agitation method as previously described (Cooksey et al., 2003). Oligonucleotide primers for PCR restriction analysis (PRA) of the hsp65 gene and for sequencing of regions of the rpoB, hsp65 and 16S rRNA genes are shown in Table 1. Amplification of these regions by PCR was performed in 200 µl, thin-walled, flat-top PCR tubes using 25 µl HotStar Taq polymerase master mix (Qiagen), 100 nM primers, 1 µl DMSO and 1 µl template in a final volume of 50 µl. The PRA was performed using a 441 bp fragment of the hsp65 gene, which was amplified using primers TB11 and TB12 (Telenti et al., 1993). Conditions for PCR thermocycling, restriction with BstEII and HaeIII and electrophoresis were as previously described (Hernandez et al., 1999; Cooksey et al., 2003). Control strains for hsp65 PRA included Mycobacterium hodleri DSM 44183T, Mycobacterium frederiksbergense NRRL B-24126, Mycobacterium neoaurum ATCC 25796, Mycobacterium diernhoferi ATCC 19340T, M. smegmatis ATCC 19420T, M. mageritense ATCC 700351T, M. wolinskyi ATCC 700010T and M. goodii ATCC 700504T. Sequence analysis of the 441 bp region of the hsp65 gene was performed using a 600 bp template obtained under the same PCR conditions as for PRA, except that primers HSPF1 and HSPR1 (Table 1) were used for amplification and for sequence analyses of sense and antisense DNA strands. A 360 bp region of the rpoB gene that was shown to be polymorphic among 26 Mycobacterium species was amplified under conditions that were similar to those used for the hsp65 gene amplification, except that the annealing temperature was 58 °C and primers RPO5' and RPO3' (Lee et al., 2003) were used for amplification and sequencing reactions. A region of the 16S rRNA gene from nucleotide 8 to 1542 (Escherichia coli numbering) was amplified using primers pA and pH, as described previously (Edwards et al., 1989; Floyd et al., 1996), and sequenced by using three forward and three reverse primers (Table 1).
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). The species with the most similarity to the 16S rRNA gene query sequences were selected for phylogenetic analysis. Similarity comparison, multiple sequence alignments and phylogenetic analyses of 16S rRNA gene sequences with pre-compiled aligned RNA sequence data at the RDP-II at Michigan State University (East Lansing, MI, USA) at http://rdp.cme.msu.edu/index.jsp (Cole et al., 2003), were performed by using online phylogenetic programs in PHYLIP version 3.5c (Felsenstein, 1989) at the PHYLIP interface at this web site. RGM species with similar 16S rRNA gene sequences were downloaded from RDP-II for analysis, and a 16S rRNA gene sequence from Mycobacterium tuberculosis was selected as the evolutionary outgroup. A distance matrix was determined with the DNADIST program (Felsenstein, 1989); a phylogenetic relationship inferred with the parameter defined by Jukes & Cantor (1969), an unambiguous alignment mask, was automatically applied and a tree was constructed using the neighbour-joining method (Saitou & Nei, 1987).
The DNA preparations used for PCRs were also utilized for typing the isolates, using RAPD electrophoresis as described previously (Cooksey et al., 2003). The oligonucleotide primer used for RAPD typing was IS986-FP (5'-ACGCTCAACGCCAGAGACCA) (Linton et al., 1994). Typing of isolates by using PFGE of large restriction fragments (>48 kbp) was performed as previously described (Hector et al., 1992), except that DNA samples were restricted with 40 U AseI (Invitrogen). Samples underwent electrophoresis in 1 % (w/v) agarose that was prepared and run in 0·5x TBE buffer (0·445 M Tris/borate, 0·01 M EDTA, pH 8·3) using a contour-clamped homogeneous electric field electrophoresis/direct repeat (CHEF-DR) pulse electrophoresis system (Bio-Rad) set for 5–20 s ramping at 200 V. Thiourea was added to the running buffer (final concentration, 50 mM) to prevent DNA degradation during electrophoresis (Romling & Tummler, 2000).
Microscopic examination of acid-fast bacilli smears revealed that isolates LTA-388T and 2003-11-06 were acid-fast, with no chains and few clumps of bacteria. The dimensions of a typical bacillus were approximately 0·55x1·5 µm by comparison with a microscopic micrometer (Carl Zeiss). Colonies that appeared on Middlebrook 7H10 agar plates or LJ agar slants after aerobic incubation for 3 days at either 28 or 37 °C were smooth, dome-shaped, opaque and possessed a pale-yellow pigment. A micrograph showing acid-fast bacilli and a photograph showing colonies of strain LTA-388T are available as Supplementary Figs A and B in IJSEM Online. The isolates grew on MacConkey agar without crystal violet but not on LJ agar containing 5 % (w/v) NaCl or in Middlebrook 7H9 broth at 45 °C.
Biochemical testing showed that the four isolates were positive for iron uptake, nitrate reduction, 14-day arylsulfatase production and for utilization of D-mannitol, D-xylose, iso-myo-inositol, L-arabinose, D-trehalose and citrate. They were negative for D-sorbitol utilization and for production of niacin and 3-day arylsulfatase.
Mycolic acid patterns determined by using HPLC were identical for the three isolates from the nail salon in the USA, and this pattern was closely similar to that of the isolate of the female patient in Venezuela. The closely similar patterns of the two strains were substantially different from the patterns of other RGM species, but they most closely resembled reference mycolic acid patterns of M. smegmatis, M. goodii, M. wolinskyi and M. mageritense. The type strains of these four species were analysed concurrently with strains LTA-388T and 2003-11-06 (Fig. 1). The most notable similarities in the mycolic acid patterns resided with the study strains. Visual comparison of mycolic acid patterns for the other species revealed major differences in the number of peaks and in peak heights, criteria that are used to distinguish mycobacterial species (Butler & Guthertz, 2001).
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Strain-typing patterns produced by RAPD electrophoresis after amplification using primer IS986-FP and by PFGE after digestion of DNA with AseI matched for isolates 2003-11-06, -24 and -30. The RAPD pattern for these isolates consisted of two prominent bands representing approximately 450 and 320 bp. The RAPD pattern for isolate LTA-388T consisted of multiple bands; the most prominent bands represented approximately 500 and 600 bp. The PFGE pattern for this isolate consisted of six prominent bands between 97 and 242 kbp; only two of these bands were approximately equal in size to any of the eight prominent bands in this size range for the environmental isolates. Therefore, the three isolates obtained from environmental sources at the nail salon were considered to represent one strain, and isolate LTA-388T represented another strain. Photographs of PFGE and RAPD typing patterns are available as Supplementary Fig. D in IJSEM Online.
According to NCCLS interpretive standards, each of the four isolates was susceptible to the eight antimicrobial drugs that were tested. The MICs for the drugs were the same for each of the three isolates from the nail salon: ciprofloxacin, 0·25 µg ml–1; amikacin, 4 µg ml–1; imipenem, 1 µg ml–1; tobramycin, 4 µg ml–1; clarithromycin, 0·25 µg ml–1; sulfamethoxazole, 8 µg ml–1; doxycycline, 0·25 µg ml–1; and cefoxitin, 8 µg ml–1. These MICs were also observed for the isolate from the patient in Venezuela, except that the MIC for sulfamethoxazole was 32 µg ml–1.
Sequences of portions of the rpoB (321 bp), hsp65 (441 bp) and 16S rRNA (1506 bp) genes were identical for isolates LTA-388T and 2003-11-06. The GenBank database was interrogated using a 189 nt sub-sequence of the rpoB gene sequence that corresponded to the 216 nt hypervariable region previously used in a multi-alignment analysis of 26 Mycobacterium species (Lee et al., 2003). We found that our sequence was unique and that the most closely related sequences were from M. fortuitum and M. mageritense (identity score, 88 %). A search of the GenBank database for similarity to the 441 bp hsp65 sequence revealed that the sequence was unique and was most similar to sequences from M. neoaurum and M. diernhoferi (95 %).
A phylogenetic comparison of 16S rRNA gene sequences using 1217 aligned nucleotides is shown in Fig. 2. The sequence of the helix-18 region of the 16S rRNA gene of the study strains matched that of other RGM sequences. Four species shared a common group on the 16S rRNA gene dendrogram, the study strains being separate from the remaining 22 species evaluated (Fig. 2). We therefore compared hsp65 PRA patterns for these four species (M. hodleri, M. frederiksbergense, M. neoaurum and M. diernhoferi) with strain LTA-388T, but no similarities in restriction patterns using either BstEII or HaeIII were observed (Fig. 3).
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; Sniezek et al., 2003; Murillo et al., 2000; Winthrop et al., 2002), and identification of these organisms is warranted.
The inability of the strains we studied to grow at 45 °C or upon media containing 5 % (w/v) NaCl are traits that may be useful for distinguishing them from species belonging to the M. smegmatis complex, which are positive for these tests. Six additional physiological properties that can be used to distinguish strain LTA-388T from those species found to share the greatest 16S rRNA similarities are shown in Table 2. Strain LTA-388T differs from (i) M. frederiksbergense, which does not grow on MacConkey agar containing no crystal violet or on citrate as a sole carbon source, from (ii) M. neoaurum, which is positive for 3-day arylsulfatase production and negative for citrate utilization, from (iii) M. hodleri, which does not grow on MacConkey agar containing no crystal violet, or on citrate or trehalose, but which does grow on sorbitol, as a sole carbon source, and from (iv) M. diernhoferi, which is non-scotochromogenic and does not grow on trehalose, sorbitol or citrate as a sole carbon source. Although the isolates had mycolic acid patterns that most closely resembled those of members of the M. smegmatis group, DNA sequence analysis of three taxonomically useful genes showed dissimilarities with respect to these or other recognized Mycobacterium species. The occurrence of unrelated strains that develop similar mycolic acid patterns has been described (Tortoli et al., 2001). Moreover, the results for HPLC and genetic analysis are not always congruent, and the similarity, or lack of similarity, of HPLC patterns does not reflect phylogenetic relatedness of strains. The standard hsp65 PRA method (Telenti et al., 1993) showed restriction patterns (using BstEII and HaeIII) for the study strains that were easily distinguished from those of other RGM species.
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Description of Mycobacterium cosmeticum sp. nov.
Mycobacterium cosmeticum (cos.me'ti.cum. N.L. neut. adj. cosmeticum referring to cosmetics).
Cells are acid-fast rods (approx. 0·55x1·5 µm) that rarely form cell aggregates in liquid culture. Motility-related structures, spores and cell branching are not present. Colonies on Middlebrook 7H10 or LJ agar have smooth surfaces and edges, are domed and are scotochromogenic. Colonies from a dilute inoculum on LJ agar are visible after 3 days incubation in an aerobic atmosphere at 28 or 35 °C, but no growth is observed at 45 °C. Growth occurs on MacConkey agar without crystal violet but not on LJ agar containing 5 % (w/v) NaCl. Tests for niacin production and 3-day arylsulfatase activity are negative, but tests for 14-day arylsulfatase activity, nitrate reduction and iron uptake are positive. Tests for utilization of D-mannitol, D-xylose, iso-myo-inositol, L-arabinose, D-trehalose and citrate are positive, but that for D-sorbitol utilization is negative. Isolates are susceptible in vitro to ciprofloxacin, amikacin, tobramycin, cefoxitin, clarithromycin, doxycycline, sulfamethoxazole and imipenem. The mycolic acid HPLC pattern consists of two three-peak clusters and is most similar to patterns for M. smegmatis, M. wolinskyi and M. goodii. Partial sequences of the rpoB (321 bp), 16S rRNA (1506 bp) and hsp65 (441 bp) genes are different from those of all currently recognized Mycobacterium species. Characteristics that distinguish this species from other RGM species include the inability to grow at 45 °C or on media containing 5 % (w/v) NaCl, the utilization of trehalose or citrate, but not sorbitol, as a sole carbon source, and a unique banding pattern after restriction of a 441 bp region of the hsp65 gene that includes major fragments of 310 and 130 bp (when BstEII is used) or of 140, 96, 80 and 40 bp (when HaeIII is used).
The type strain, isolate LTA-388T (=ATCC BAA-878T=CIP 108170T), was isolated from a granulomatous lesion of a female patient in Venezuela who was undergoing mesotherapy.
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ACKNOWLEDGEMENTS |
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