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1 Respiratory and Systemic Infection Laboratory, Health Protection Agency, Specialist and Reference Microbiology Division, 61 Colindale Avenue, London NW9 5HT, UK
2 Mycoplasma Experience Ltd, 1 Norbury Road, Reigate, Surrey RH2 9BY, UK
3 Department of Veterinary Pathology, University of Liverpool, Leahurst, Neston, South Wirral CH64 7TE, UK
4 Staten Serum Institut, Mycoplasma Laboratory, Artillerivej 5, Copenhagen DK-2300, Denmark
5 Department of Microbiology, Royal Free Hospital, Pond Street, London NW3 2QG, UK
6 Department of Clinical Immunology, Royal Free Hospital, Pond Street, London NW3 2QG, UK
Correspondence
D. G. Pitcher
dave.pitcher2{at}btopenworld.com
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The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene and internally transcribed spacer sequences are AY531655 and AY531657, respectively, for strain A39T and AY531656 and AY531658, respectively, for strain M5572.
Details of the antisera used for the serological reactions and figures showing the colonial appearance and electron micrographs of cells of Mycoplasma amphoriforme A39T, SDS-PAGE separation of proteins of Mycoplasma species, agarose gel separation of ITS and M. amphoriforme-specific 16S rRNA gene sequence amplicons, and PFGE of strain A39T and Mycoplasma pneumoniae M129 are available as supplementary material in IJSEM Online.
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). Subsequently, similar isolates were cultured from three other patients with bronchial symptoms.
Primary isolation of strains A39T, A55 and A84 was made in ME broth and agar medium (Hannan et al., 1997) at the Mycoplasma Experience Laboratory, Reigate, UK. Strain M5572 (=ATCC BAA-993) was isolated from the sputum of a patient with bronchitis on modified Friis medium, as used for the isolation of Mycoplasma genitalium (Jensen et al., 1996), at the Staten Serum Institute, Copenhagen, Denmark.
Growth on modified Hayflicks medium (Freundt, 1983) and SP4 medium (Tully, 1995) was also tested. Agar cultures were incubated at 37 °C in gas jars (95 % N2, 5 % CO2) or with CampyGen gas packs (8 % CO2, 9 % O2; Oxoid). Strains grew aerobically, but anaerobic growth was more rapid.
The organism was fastidious; it did not grow on modified Hayflicks medium. Growth was poor on conventional SP4 media, but better growth was obtained on SP4 containing 20 % porcine serum instead of fetal bovine serum. The best growth was obtained on ME medium. On all media, approximately 7–14 days incubation was required before growth was detected.
Colonies on agar media lacked the characteristic ‘fried egg’ appearance of most mycoplasmas. The colonies were small (<1 mm), translucent and convex, with a glistening ‘ground glass' appearance and lacking a central spot (Supplementary Fig. S1 in IJSEM Online). It is possible that the colonial appearance could be confused on occasion with that of other species from the human respiratory tract, as colonies of some freshly isolated cultures of Mycoplasma pneumoniae and M. genitalium have been reported as not having a central spot. The apparently related species Mycoplasma testudinis (from tortoise cloaca), Mycoplasma alvi (from bovine rumen) and Mycoplasma pirum (from laboratory cell lines) are described as having colonies typical of mycoplasmas (Hill, 1985; Gourlay et al., 1977; Del Giudice et al., 1985).
To ensure purity, strain A39T was cultured in broth that was filtered through a 0·2 µm filter, cloned and passaged three times by colony isolation on agar medium.
The optimum growth temperature was 37 °C; growth did not occur at 30 or 40 °C within 14 days.
For transmission electron microscopy studies, cells of strain A39T were pelleted from a 100 ml mid-exponential phase broth culture, fixed in buffered glyceraldehyde, post-fixed in osmium tetroxide, dehydrated in graded alcohols and embedded in Lemix epoxy resin and sectioned.
Electron micrographs (EMs) of ultrathin sections revealed ‘flask-shaped’ cells approximately 0·5 µm in length with a trilaminar cell membrane, similar to M. pneumoniae, M. genitalium and M. pirum. Cells of strain A39T differed from those of these species, however, in containing dense granules (Supplementary Fig. S2 in IJSEM Online). Although the nature of the granules could not be ascertained, they did not appear to be artefacts introduced by the EM processing, as cells of M. pneumoniae FHT that were treated identically did not show granules. The cells did not appear to possess electron-dense material in the tip (bleb) structure, as described for M. pneumoniae, M. genitalium and Mycoplasma gallisepticum.
It has been suggested (S. Razin, personal communication) that the granules in the cytoplasm of cells of strain A39T resemble in their organization structures that were first reported in M. gallisepticum by Maniloff (1971, 1994), and interpreted as representing aggregations of polyribosomal helices. However, Korolev et al. (1994a, b) later reinterpreted them as representing tubular structures rather than ribosomes. At present the nature of these structures is not known.
The sterol requirement of strain A39T was determined indirectly using the digitonin disc method (Poveda, 1998) and, directly, by measuring the growth response to cholesterol in broth using the method of Razin & Tully (1970), except that a final inoculum of 7·5 % (v/v) was used instead of 3 %. Strain A39T required sterol for growth. It hydrolysed glucose, but not arginine, and reduced tetrazolium, but did not possess urease or phosphatase activity. Film and spot were not evident (Aluotto et al., 1970). On the basis of biochemical activity alone, strain A39T could not be distinguished from M. pneumoniae or M. genitalium; however, M. pirum and M. alvi differ in hydrolysing arginine (Del Giudice et al., 1985; Gourlay et al., 1977) and M. testudinis in not reducing tetrazolium (Hill, 1985).
Haemadsorption of cells of strain A39T to chicken, guinea pig and sheep erythrocytes and haemolysis of sheep erythrocytes were observed (Gardella & Del Giudice, 1983). SDS-PAGE of whole-cell proteins was carried out on washed deposits from 20 ml late-exponential phase broth cultures using the method of Laemmli (1970). Gels were stained with Coomassie blue. Visual examination of the gels revealed that the four novel isolates had very similar patterns that could be easily distinguished from those of other species known to infect humans, M. pneumoniae (three strains), M. genitalium (two strains), M. pirum (two strains), M. gallisepticum (one strain), M. alvi (one strain) and M. testudinis (one strain) (Supplementary Fig. S3 in IJSEM Online).
Serological reactions were performed using growth inhibition and immunofluorescence methods (Bradbury, 1998; Poveda & Nicholas, 1998) with antisera to 110 Mycoplasma species (see supplementary material in IJSEM Online) against strain A39T antigen. Rabbit polyclonal antiserum was prepared against strain A39T (Senterfit, 1983) and reciprocal tests were carried out against cultures of other species where cross-reactions were observed. A few (13 growth inhibition and 10 immunofluorescence) weak reactions to the 110 mycoplasma antisera tested against A39T cells were observed, but they were all confirmed as negative by reciprocal testing. Reciprocal tests with A39T antiserum were also carried out with the type strains of members of the pneumoniae group (M. alvi, M. gallisepticum, M. genitalium, Mycoplasma imitans, M. pirum, M. pneumoniae and M. testudinis), with negative results. Isolates A55, A84 and M5572 gave positive reactions when tested by immunofluorescence with anti-A39T rabbit antiserum, indicating a close antigenic relationship.
Purified DNA was prepared by extraction from centrifuged deposits of late-exponential phase 50 ml broth cultures (Pitcher et al., 1989). Templates for PCR were prepared from centrifuged deposits from 5 ml broth cultures with Chelex 100 (InstaGene kit; Bio-Rad).
The nucleotide sequences of both strands of the 16S rRNA gene of strains A39T, A55, A84 and M5572 were determined using primers described by Johansson et al. (1998), but without solid-phase sequencing. Sequence reactions were carried out using a dye terminator cycle sequencing quick-start kit (Beckman Coulter) and the products were analysed on a CEQ 8000 genetic analysis system (Beckman Coulter).
In a BLAST search of the GenBank database (Altschul et al., 1990), the 16S rRNA gene sequence of strain A39T showed greatest similarity to Mycoplasma species of the pneumoniae group. Sequences of Mycoplasma strains A39T, M5572 and the eight most closely related 16S rRNA gene sequences of other species were subjected to phylogenetic analysis. Mycoplasma penetrans GTU-54-6A1T was included as an outlier.
16S rRNA gene sequences of approximately 1476 bases from positions 34 to 1510 (Escherichia coli numbering; Brosius et al., 1978) were subjected to multiple alignment and phylogenetic trees were constructed using neighbour-joining and maximum-parsimony algorithms with the Kimura 2 adjustment provided in the Kodon version 1.0 software package (Applied Maths). Bootstrap resampling analysis for 500 replicates was performed to estimate the confidence of the tree topology. It is generally accepted that strains with 16S rRNA gene sequence similarity of less than 97 % are members of different species (Stackebrandt & Goebel, 1994). The 16S rRNA gene sequences of isolates A55, A84 and M5572 shared >98 % sequence similarity with strain A39T. However, the sequence similarity between M. pneumoniae FHT and A39T or M5572 was only 93·0 %. These strains appeared to be more closely related to M. testudinis (96·8 %) and M. alvi (96·6 %), based on the 16S rRNA gene alone (Fig. 1), but not when other criteria were considered (Table 1).
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, 2004). The PCR product was sequenced in both directions using internal primers proposed by Harasawa et al. (1993, 2004). The length of the 16S–23S ITS sequence (368 bp) was greater than those of other Mycoplasma species in the clade, with the exception of M. gallisepticum (645 bp) and M. imitans (2488 bp, which contains a putative transposase gene; Harasawa et al., 2004). (Table 1
and Supplementary Fig. S4 in IJSEM Online). Pairwise alignments of the ITS sequences of A39T (GenBank accession no. AY531657) and M5572 (GenBank accession no. AY531658) showed that these two strains had 98 % sequence similarity, but the results of pairwise alignments of the ITS sequence of strain A39T with those of other species related according to the 16S rRNA gene sequence were 62 % (M. testudinis 01008T; GenBank accession no. AY785378), 58 % (M. alvi IlsleyT; AY779745), 56 % (M. pirum HRC 70-159T; AY757364), 53 % (M. pneumoniae FHT; AF132740), 47 % (M. genitalium G-37T; D14526) and 38 % (M. gallisepticum PG31T; AB098504).
The G+C content of the DNA of strain A39T was determined by using the fluorescence monitoring method described by Xu et al. (2000) with a LightCycler (Roche Diagnostics). Reference DNA from M. pneumoniae M129 was used for comparison (G+C content 40 mol%; Himmelreich et al., 1996). The G+C content of the DNA of strain A39T was 34 mol%.
Genome size was estimated by using PFGE. DNA plugs were prepared from suspensions of strain A39T in TE buffer (Neimark & Carle, 1995). Restriction enzymes used were ApaI, BamHI, BglI, BssHI, KspI, NaeI, NarI, NheI, NotI, SacI, SalI, SfiI, SmaI, XbaI and XhoI.
PFGE was carried out using a CHEF-DR II apparatus (Bio-Rad) with 1 % PFGE-quality agarose gels in 0·5x TBE running buffer at 200 V for 26 h. Pulse times were 3–95 s. The mobility of fragments was compared to size standards consisting of a concatenated ladder of bacteriophage 
DNA and yeast chromosome DNA size markers (Bio-Rad). The gel was visualized with ethidium bromide and photographed. Only two restriction enzymes, NotI and SfiI, cut the genomic DNA into useable fragments. Photographs of the gels were scanned and fragment lengths were estimated using BioNumerics software (Applied Maths).
PFGE of restriction fragments of the A39T genome cut with SfiI revealed two fragments of 741 and 439 kbp, and two fragments of 1173 and 89 kbp with NotI (Supplementary Fig. S5 in IJSEM Online). Therefore, the genome size of strain A39T was estimated to be 1180–1260 kbp. As a control, the same enzymes were used to cut the DNA of M. pneumoniae M129; fragments obtained were 554 and 441 kbp (SfiI) and 847 and 164 kbp (NotI) (Supplementary Fig. S5 in IJSEM Online), giving genome size estimations of between 995 and 1011 kbp. These values are high compared with the known genome size for M. pneumoniae M129 of 816 394 bp determined from the complete genome sequence (Himmelreich et al. 1996). It has been observed that estimates based on the summation of restriction-fragment sizes may on occasion be higher than those estimated using other methods and might vary under different electrophoretic conditions (Neimark & Lange, 1990). Therefore, each value for strain A39T was adjusted using the actual genome size of M. pneumoniae M129 as a standard, and sizes of 968 kbp (SfiI) and 1018 kbp (NotI) were obtained, giving a mean value of 993 kbp.
The G+C content (34 mol%) and genome size (993 kbp) of strain A39T contrast with those of the related species M. pneumoniae (40 mol% and 816 kbp), M. genitalium (32 mol% and 580 kbp) and M. gallisepticum (31 mol% and 996 kbp). The G+C contents of M. pirum, M. alvi and M. testudinis were 26, 26 and 35 mol%, respectively, but the genome sizes are not available (Himmelreich et al., 1996; Fraser et al., 1995; Papazisi et al., 2003; Del Giudice et al., 1985; Gourlay et al., 1977; Hill, 1985).
Specific PCRs for M. pneumoniae and M. genitalium were carried out (Cadieux et al., 1993), but were negative for all four isolates.
PCR based on unique primer sequences at positions 441 and 991 of the 16S rRNA gene of strain A39T was developed to identify other isolates belonging to the same putative species. The forward primer used was amph-F (5'-AAGCTAGTAAAGGAAATGTTATT-3') and the reverse primer was amph-R (5'-TCGACTATATTTCTATAGTTTTG -3'). Reaction mixtures (50 µl) contained 50 mM KCl, 2·5 mM MgCl2, 15 mM Tris/HCl (pH 8·0), 200 µM of each dNTP, 20 pmol of each primer and 1·5 U Taq DNA polymerase (Gibco-BRL). Broth culture deposits were extracted using an InstaGene kit (Bio-Rad). Samples (10 µl) were added to the reaction mixtures. Following an initial denaturation step of 96 °C for 3 min, 35 cycles of 94 °C for 30 s, 56 °C for 30 s and 72 °C for 40 s were carried out, followed by an extension step of 72 °C for 5 min. Reactions were performed using an MR DNA engine thermocycler (Genetic Research Ltd).
A 550 bp product was detected by electrophoresis in 1·5 % agarose at 80 V for 2 h. Gels were stained with ethidium bromide (1 µg l–1) for 30 min and photographed under UV illumination at 254 nm. All four A39T-like isolates had this product, but other species in the M. pneumoniae group and other human mycoplasma species failed to amplify (Supplementary Fig. S6a, b in IJSEM Online).
Conclusions
When Tully (1993) reviewed the status of the mollicute flora of humans, 15 species were reported as having been isolated from human tissues on more than one occasion. Since then, no isolates have been described that could be confirmed as novel species. We believe that strain A39T represents an undescribed member of the human microflora that might have implications for human health, because it exhibits metabolic synapomorphy with the pneumoniae group of mycoplasmas. Therefore, from a clinical diagnostic viewpoint, it is crucial that this strain can be distinguished from M. pneumoniae and other human mycoplasmas. To date, the acquisition of strains by patients and its role as a pathogen remain unclear. The species is fastidious and could easily be missed. Zoonotic infections with mycoplasmas have been reported in immunocompromised patients, but no one animal species has been linked to more than one patient. Therefore, it appears that this species is part of the human microflora, although it is not known at present whether the respiratory tract is its primary habitat.
At the time of writing, the minimal standards for descriptions of novel species of Mollicutes from 1995 apply (International Committee on Systematic Bacteriology Subcommittee on the Taxonomy of Mollicutes, 1995). We believe that this description of a novel species of Mycoplasma conforms to these standards.
Description of Mycoplasma amphoriforme sp. nov.
Amphoriforme (am.pho'ri.for'me. L. n. amphora -ae amphora; L. adj. suffix -formis -is -e like, of the shape of; N.L. neut. adj. amphoriforme having the form of an amphora, amphora-shaped).
Cells are flask-shaped with a trilaminar membrane and contain electron-dense granules. Aerobic or anaerobic growth occurs slowly on conventional mycoplasma media at the optimum temperature for growth of 37 °C. Colonies have a glistening ‘ground glass' appearance and do not possess the typical ‘fried egg’ appearance common to most mycoplasmas. Requires serum or sterol for growth. Acid is produced from glucose. Arginine and urea are not hydrolysed. Tetrazolium is reduced. Phosphatase activity is negative. Cells adhere to chicken, guinea pig and sheep erythrocytes. Haemolytic on sheep erythrocytes. Serological tests show a lack of relatedness to the type strains of previously established Mycoplasma species.
The type strain is A39T (=NCTC 11740T=ATCC BAA-992T). The 16S rRNA gene and the 16S–23S rRNA ITS sequences are unique and the SDS-PAGE whole-cell protein profiles are distinctive. All strains so far isolated were cultured from the human respiratory tract. The pathogenic status is not known. The G+C content of the type strain is 34 mol% and the genome size is 993 kbp.
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