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1 Laboratoire de Bactériologie-Virologie, Faculté de Pharmacie, 15 Avenue Charles Flahault, BP 14491, 34060 Montpellier Cedex 5, France
2 Laboratoire de Bactériologie, Hôpital Arnaud de Villeneuve, 371 Avenue du Doyen Gaston Giraud, 34295 Montpellier Cedex 5, France
3 Centre National de Référence des Bactéries Anaérobies et du Botulisme, Institut Pasteur, 25 rue du Dr Roux, 75724 Paris Cedex 15, France
4 National Microbiology Laboratory – Public Health Agency of Canada, 1015 Arlington St, Suite H5040, Winnipeg, MB, Canada R3E 3R2
Correspondence
Hélène Marchandin
h-marchandin{at}chu-montpellier.fr
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The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of D. micraerophilus ADV 04.01T and D. propionicifaciens ADV 1053.03T are AF473837 and AY850119, respectively, and the accession numbers of the dnaK gene sequences of these strains are respectively AY851488 and AY851500.
An evolutionary distance tree, based on partial 16S rRNA gene sequences, and a table of the cellular fatty acid compositions of D. micraerophilus and D. pneumosintes are available as supplementary material in IJSEM Online.
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) was revived by Moore & Moore (1994) to accommodate a rod-shaped Gram-negative bacillus previously classified as Bacteroides pneumosintes (Holdeman & Moore, 1970), and its description was emended in 2003 (Downes et al., 2003). At present, the genus comprises the two species Dialister pneumosintes and Dialister invisus (Downes et al., 2003).
The 28 strains studied were recovered on Columbia sheep-blood agar (bioMérieux) after incubation at 37 °C for 2–5 days in an anaerobic jar with the Anaerogen System (Oxoid Unipath), and are listed in Table 1. It is noteworthy that the pattern of sites of isolation differed from those historically reported for Dialister spp. (Goldstein et al., 1984; Doan et al., 2000; Paster et al., 2001; Rolph et al., 2001; Rousée et al., 2002; Domann et al., 2003; Downes et al., 2003) in that several isolates of this study were grown from infra-diaphragmatic samples (Table 1). All of these isolates were subjected to further polyphasic investigation, but the approaches used on the French and Canadian isolates did not include strictly the same analyses and are presented successively below.
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; Marchandin et al., 2003b). Nearly-complete 16S rRNA gene sequences were matched with the GenBank and EMBL databases by using BLAST program (Altschul et al., 1997): they displayed the highest similarity with sequences of members of the genus Dialister, which is within the family ‘Acidaminococcaceae’ (Willems & Collins, 1995; Garrity & Holt, 2001). Two clusters of nearly-identical sequences could be differentiated on the basis of 16S rRNA gene sequence similarity being below 94·3 % according to LALIGN software (http://www.expasy.org). The first cluster represented by the strain Dialister sp. ADV 04.01T (accession no. AF473837) (Marchandin et al., 2003a) contained 13 isolates sharing at least 99·9 % 16S rRNA gene sequence similarity. Maximum similarity (92·7 %) was found with the sequence of oral strain Dialister sp. GBA27 (accession no. AF287788); sequence similarities with known species are given in Table 2. The second group of clinical isolates included the four strains Dialister sp. ADV 1053.03T, ADV 2463.03, ADV 3202.03 and ADV 4162.03, which shared 16S rRNA gene sequence similarity of at least 99·6 %. The representative strain Dialister sp. ADV 1053.03T showed a maximum similarity of 95·2 % with D. invisus DSM 15470T (Table 2) and with oral clones and isolates. The same distribution of the isolates in two groups was also observed on the basis of dnaK gene sequence similarities being above 97·3 and 97·4 %, respectively (Table 2).
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). Trees were inferred using the PHYLIP suite of programs (Felsenstein, 1993) by maximum likelihood (Olsen et al., 1994), maximum parsimony (Kluge & Farris, 1969) and neighbour joining (algorithm F84 for the distance matrix) (Saitou & Nei, 1987; Kishino & Hasegawa, 1989). The robustness of the trees was evaluated with 1000 bootstrap replications using the SEQBOOT and CONSENSE programs (Felsenstein, 1993). The evolutionary distance tree based on 16S rRNA gene sequences was obtained for members of the genus Dialister, including known species, the strains in this study, oral isolates of unnamed species and oral clones, and is available as a supplementary figure in IJSEM Online. Phylogenetic analysis confirmed that all isolates belonged to the genus Dialister but that they formed two branches distinct from those of D. invisus and D. pneumosintes. These two groups corresponded to two distinct and robust phylogenetic clades supported by bootstrap values of 100 %. Similar branching of the different species was observed whichever algorithm was used to reconstruct phylogenetic trees. The two groups of related strains will be named Dialister micraerophilus sp. nov. and Dialister propionicifaciens sp. nov. The phylogenetic neighbourhood observed between several Dialister sp. oral clones or oral isolates and D. invisus suggested that at least Dialister sp. oral isolate E2_20 E1 could be considered as D. invisus. This suggestion is also supported by both the high level of 16S rRNA gene sequence similarity observed between the corresponding sequences (99·8 %) and the anatomical site reported for this isolate. The dnaK-based phylogeny (Fig. 1) is congruent with that obtained after 16S rRNA gene sequence analysis, there being two well-separated lineages, supported by high bootstrap values, corresponding to D. micraerophilus and D. propionicifaciens. D. invisus and D. pneumosintes formed two other distinct lineages. The branching of the different clusters was identical in trees reconstructed by the different methods. In both the D. micraerophilus cluster and the D. propionicifaciens cluster, subgroups of strains can be distinguished because of the higher variability of the dnaK gene relative to that of the 16S rRNA gene.
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) (Table 2
). The DNA G+C content of strain D. propionicifaciens ADV 1053.03T could not be determined, because the very limited growth of the strain in broth media meant that it was not possible to obtain enough biomass for efficient G+C-content analysis. Therefore, another genomic approach, PFGE, was used to investigate the total DNA content of the strains, since the large-scale chromosome structure was previously described as a sensitive indicator of phylogenetic relationships between bacteria (Liu et al., 1999). The number and sizes of bacterial chromosomes were analysed by PFGE of intact DNAs prepared in agarose plugs as described previously (Marchandin et al., 2001). The PFGE conditions consisted of pulse ramps of 90–300 s for 45 h at 4·5 V cm–1. Mapping experiments with the intron-encoded endonuclease I-CeuI (New England Biolabs) were undertaken to determine the rrn skeletons, as described previously (Marchandin et al., 2003a). PFGE experiments were performed in a CHEF-DRII apparatus (Bio-Rad) on 0·8 % agarose gel in 0·5x TBE. Seven of the 13 French D. micraerophilus strains and the four D. propionicifaciens isolates were studied in comparison with D. pneumosintes ATCC 33048T and D. invisus DSM 15470T. This analysis of genomic organization revealed that all the strains studied possess a unique and circular chromosome (data not shown); chromosome sizes are given in Table 2. Again, two clusters of clinical strains can be distinguished according to chromosomal size. It is interesting to note that the genome size of D. invisus DSM 15470T was about 50 % larger than the genome sizes of D. micraerophilus and D. pneumosintes ATCC 33048T. The size of the D. invisus genome in the context of its relatively high G+C content suggested a recent and massive event of lateral transfer. I-CeuI profiles showed that all the strains tested possess four rrn operons (Table 2). However, each species displayed a specific I-CeuI profile. In particular, the I-CeuI fragments clearly differentiated the genomes of the two species showing similar genome sizes (D. pneumosintes and D. micraerophilus) (data not shown).
All of the isolates formed circular, convex, translucent and tiny colonies on Columbia sheep-blood agar plates. Even after prolonged incubation, the colonies were less than 0·5 mm in diameter, making their recovery in mixed anaerobic cultures relatively difficult. The bacteria stained Gram-negative and were non-sporing, non-motile and coccoid to coccobacillary, occurring as single cells but sometimes in pairs or clumps. They were prepared as described previously for both ultrathin-section observation and negative staining (Marchandin et al., 2003a) with the following modification. Grids were negatively stained with phosphotungstic acid (1 %) for 1 min. Samples were observed under a Hitachi H7100 electron microscope. D. micraerophilus ADV 04.01T and D. propionicifaciens ADV 1053.03T showed similar morphology, being small coccobacilli about 0·2–0·4x0·3–0·6 µm in size. Both strains displayed a very convoluted cell surface after negative staining (Fig. 2) and showed the typical Gram-negative surface layers, in ultrathin sections (Fig. 3), previously described for several members of the family ‘Acidaminococcaceae’ (Jumas-Bilak et al., 2004).
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. Since the majority of the French clinical strains were able to grow under microaerophilic conditions (Table 3), the genus Dialister has to be redefined as including microaerophiles, as previously described for Wolinella (Han et al., 1991), and should be considered as anaerobic and microaerophilic rather than simply anaerobic. For further biochemical characterization, the strains were grown anaerobically in trypticase/glucose/yeast extract broth (Carlier, 1985) and incubated at 37 °C for 72 h in an anaerobic jar containing H2/CO2/N2 (5 : 5 : 90, by vol.). All clinical strains were asaccharolytic and were non-reactive in conventional biochemical tests (nitrate reduction, production of gas, catalase, indole and urease). They also did not modify milk or gelatin. Enzymic profiles obtained with Rapid ID 32A (API bioMérieux) highlighted phenotypic heterogeneity within the genus Dialister (Table 3). The results obtained for D. pneumosintes ATCC 33048T differed from those reported previously by Downes et al. (2003), since only arginine arylamidase activity was detected (Downes et al., 2003). Alanine arylamidase and serine arylamidase activities were found in 64 and 71 % of the D. micraerophilus strains, respectively, and phenylalanine arylamidase and tyrosine arylamidase activities appeared to be specific to this species (Table 3). D. propionicifaciens possessed some physiological characteristics in common with the members of the genus Veillonella. They shared the same metabolic profile, with the production of acetic, propionic and lactic acids, although D. propionicifaciens produced these acids in smaller amounts. Sodium succinate enhanced the growth of D. propionicifaciens isolates, whereas lactate and glutamate did not, and subsequent GC analysis revealed that the four strains produced a large amount of propionate from trypticase/glucose/yeast extract supplemented with sodium succinate. D. propionicifaciens was able to decarboxylate succinate to propionate, similarly to the members of the genus Veillonella. The net yield of the propionate decarboxylation was 1 mol propionate per mol succinate consumed. However, the two types of organism can be easily differentiated. Indeed, Veillonella species ferment lactate to acetate and propionate, produce gas and reduce nitrate (Rogosa, 1984), whereas D. propionicifaciens does not.
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). Eleven clinical isolates of an unidentified Gram-negative coccobacillus isolated in Canada were affiliated to the species D. micraerophilus on the basis of the high levels of 16S rRNA gene sequence similarity (>99·9 %) observed between these isolates and D. micraerophilus ADV 04.01T. The topology of the 16S rRNA gene-based phylogenetic tree reconstructed in a previous unpublished work (Bernard et al., 2003) showed that all the Canadian isolates grouped together with the type strain of D. micraerophilus, ADV 04.01T, without any phylogenetic divergence, as was also observed for the French isolates (data not shown). These isolates were similar to the French D. micraerophilus isolates in terms of all the phenotypic characteristics determined. However, some strains were found to be so fastidious that one or more of the biochemical or chemotaxonomic tests could not be carried out, in spite of repeated attempts. The isolates that yielded sufficient bacterial load after growth in broth were analysed for their cellular fatty acid (CFA) composition as described previously, using the Sherlock system (MIDI) (Bernard et al., 2002); results are available in a supplementary table in IJSEM Online. In some instances, the analysis could only be interpreted after the use of specific techniques to concentrate and maximize the bacterial loads, as found previously for D. pneumosintes (Moore et al., 1994). Anaer1 was used as the Sherlock method, and the profiles generated were compared with the commercial library MOORE, version 3.8. CFA data for D. micraerophilus strains were analysed and stored in a library entry created using LIBRARY GENERATION system software (MIDI) within an in-house library, LCDC2. The D. micraerophilus in-house-entry data were found to be qualitatively consistent with the genus Dialister (Moore et al., 1994; Downes et al., 2003). The Canadian D. pneumosintes isolates were found to have a CFA profile essentially identical to that found previously for D. pneumosintes (Moore et al., 1994). The D. pneumosintes entry demonstrated a reproducible, quantitative difference for the volume of CFAs 3-OH 14 : 0 and 15 : 0 dimethyl acetal (MIDI summed feature 5), which averaged 9 % of total CFAs, whereas this CFA was not detected for D. micraerophilus isolates. Finally, the D. micraerophilus clinical isolates described in this study, whether derived from patients in France or Canada, were essentially identical with respect to the species description.
Emended description of Dialister (ex Bergey et al. 1923) Moore and Moore 1994
The description is as emended by Downes et al. (2003), with the following modifications: species are anaerobic or microaerophilic.
Description of Dialister micraerophilus sp. nov.
Dialister micraerophilus (mic.rae'ro.phi.lus. Gr. adj. mikros small; Gr. n. aer air; N.L. adj. philus from Gr. adj. philos loving; N.L. masc. adj. micraerophilus slightly air-loving, referring to the ability of the species to grow under microaerophilic conditions).
Cells are coccoid to coccobacillary (0·2–0·4x0·3–0·6 µm), occurring singly, in pairs or in clumps. Gram-negative, non-motile, non-sporulating and with a convoluted cell surface. Colonies on Columbia sheep-blood agar are 0·5 mm in diameter, circular, convex and translucent. Anaerobic and microaerophilic. Unreactive in most conventional tests. Among the positive reactions in the Rapid ID 32A profile, phenylalanine arylamidase and tyrosine arylamidase activities are specific for D. micraerophilus. Metabolic end-products are not detected in any significant quantities. Can be differentiated from other species of the genus Dialister by phenylalanine arylamidase and tyrosine arylamidase activity detection and by 16S rRNA gene and dnaK sequencing, and from D. pneumosintes by CFA-composition analysis. The DNA G+C content of the type strain is 36·3 mol%.
The type strain is strain ADV 04.01T (=AIP 25.04T=CIP 108278T=CCUG 48837T), isolated from human clinical samples.
Description of Dialister propionicifaciens sp. nov.
Dialister propionicifaciens (pro.pi.o.ni'ci.fa'ci.ens. N.L. n. acidum propionicum propionic acid; L. v. facio -ere to produce; N.L. part. adj. propionicifaciens propionic acid-producing).
Cells are coccoid to coccobacillary (0·2–0·4x0·3–0·6 µm), occurring singly, in pairs or in clumps. Gram-negative, non-motile, non-sporulating and with a convoluted cell surface. Colonies on Columbia sheep-blood agar are 0·5 mm in diameter, circular, convex and translucent. Anaerobic and microaerophilic. Unreactive in most conventional tests. Metabolic end-products consist of small amounts of acetic acid, propionic acid and lactic acid. Propionate is produced when the growth medium is supplemented with sodium succinate. The net yield of the propionate decarboxylation is 1 mol propionate per mol succinate consumed. Can be differentiated from other species of the genus Dialister by propionic acid production, by 16S rRNA gene and dnaK sequencing and by genome sizing.
The type strain is ADV 1053.03T (=AIP 26.04T=CIP 108336T=CCUG 49291T) and a reference strain is ADV 3202.03 (=AIP 126.04=CIP 108582). Isolated from human clinical samples.
Emended description of Dialister pneumosintes (Olitsky and Gates 1921) Moore and Moore 1994
The description is as emended by Downes et al. (2003), with the following modifications: the type strain shows arginine arylamidase, leucine arylamidase, glycine arylamidase and histidine arylamidase activities in Rapid ID 32A (profile 0000012401). Can be differentiated from other species of the genus Dialister by 16S rRNA gene and dnaK sequencing and from D. micraerophilus by CFA-composition analysis.
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ACKNOWLEDGEMENTS |
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