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1 Université Montpellier 1, Laboratoire de Bactériologie-Virologie, EA3755, Faculté de Pharmacie, 15 Avenue Charles Flahault, BP 14491, F-34093 Montpellier Cedex 5, France
2 CHU de Montpellier, Laboratoire de Bactériologie, Hôpital Arnaud de Villeneuve, 371 Avenue du doyen Gaston Giraud, -34295 Montpellier Cedex 5, France
Correspondence
Corinne Teyssier
corinne.teyssier{at}univ-montp1.fr
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ABSTRACT |
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A phylogenetic tree based on concatenated dnaK and rpoB gene sequences of strains ADV31T, AD41 and AD43 and other members of the genera Ochrobactrum and Brucella, a schematic representation of the rrn skeleton of the two chromosomes of strain ADV31T and a two-dimensional thin-layer chromatogram of the polar lipids of strain ADV31T are available as supplementary figures in IJSEM Online.
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TOPABSTRACTMAIN TEXTREFERENCES |
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), as well as from plants (Trujillo et al., 2005; Tripathi et al., 2006), animals (Kämpfer et al., 2003) and humans (Holmes et al., 1988; Velasco et al., 1998). To date, Ochrobactrum anthropi and Ochrobactrum intermedium are the only species to be recovered from human clinical samples (Teyssier et al., 2005a). In this study, we characterized three strains of an Ochrobactrum sp. that were isolated from two patients hospitalized in intensive-care units of the Montpellier University Hospital, France. We used genetic, phylogenetic, genomic and phenotypic analyses to compare these strains with known Ochrobactrum species. This study led to the description of a novel species in the genus Ochrobactrum.
The three isolates were recovered from samples taken during the standard procedure for the detection of multi-resistant bacilli carriage in patients hospitalized in intensive-care units. The strains grew after incubation for 24–48 h at 37 °C on Drigalski agar (Difco), supplemented with 4 mg ceftazidime l–1, a medium that is selective for multi-resistant, non-exigent, Gram-negative bacteria. Strain ADV31T was isolated in 2002 from an axillary swab from a 20-year-old man. Isolates ADV41 and ADV43 were recovered in 2003 from rectal swabs taken 48 h apart from a 25-year-old man hospitalized in a different intensive-care unit. PFGE of SpeI-restricted DNA performed as described previously (Teyssier et al., 2003a) showed that strains ADV41 and ADV43 were not related (data not shown).
Genomic DNA used for PCR was obtained using an AquaPure genomic DNA isolation kit (Bio-Rad). Amplification of the 16S rRNA gene was performed using the universal primers 27f and 1492r (Teyssier et al., 2003a) or primers F4 and R2 that are described as being specific for Brucella spp. and O. intermedium (Romero et al., 1995; Velasco et al., 1998). Partial dnaK (encoding the 70 kDa heat-shock protein) and rpoB (encoding the DNA-dependent RNA polymerase 
-subunit) gene amplifications were carried out with primers 289f (5'-ATCGTCAAGGGCGACAATGGC-3')/1142r (5'-CGTCCTTGACGTCGCCCTGCA-3') and 453f (5'-ATCGTTTCGCAGATGCACCG-3')/1232r (5'-CGCATGTTCATCTTCACGCGGCC-3'), respectively. The PCR reactions were all performed as described previously for 16S rRNA gene amplification (Teyssier et al., 2003a). Sequencing was done in both directions with forward and reverse primers using an Applied Biosystems Automatic Sequencer (Genome Express). Partial 16S rRNA gene sequences of about 1400 bp were compared with sequences deposited in GenBank/EMBL/DDBJ using the standard BLAST program (www.ncbi.nlm.nih.gov/blast) and LALIGN software (www.expasy.org). The three isolates, ADV31T, ADV41 and ADV43, shared more than 99.8 % of their nucleotide positions. The highest 16S rRNA gene sequence similarity was obtained with the type strain of O. intermedium (97.48 %). However, PCR using primers F4 and R2 was negative for strains ADV31T, ADV41 and ADV43, clearly differentiating these strains from O. intermedium (Velasco et al., 1998). The dnaK and rpoB sequences also distinguished strain ADV31T from other members of the genus Ochrobactrum, as the maximum similarity levels were 95.5 % with O. intermedium for dnaK and 93.6 % with O. anthropi for rpoB. The similarity levels among strains ADV31T, ADV41 and ADV43 were greater than 98.9 and 97.5 % for dnaK and rpoB, respectively. 16S rRNA gene-, dnaK- and rpoB-based phylogenies were used to analyse the relationships between the three clinical isolates and members of the genera Ochrobactrum and Brucella. A single dnaK- and rpoB-based tree was reconstructed using a concatenation of dnaK and rpoB sequences. A distance matrix was calculated using the F84 algorithm (Kishino & Hasegawa, 1989) in the DNADIST program after sequence alignment with CLUSTAL_X (Thompson et al., 1997). The neighbour-joining method (Saitou & Nei, 1987) was used to reconstruct distance trees. The results were compared with trees obtained using parsimony (Kluge & Farris, 1969) and maximum-likelihood (Olsen et al., 1994) with the programs DNAPARS and fastDNAml, respectively. The robustness of the trees was evaluated by bootstrap analysis of 1000 replicates using the programs SEQBOOT and CONSENSE. All the phylogenetic programs used were from PHYLIP package 3.66 (Felsenstein, 1993). Independent of methods and markers, strains ADV31T, ADV41 and ADV43 were grouped in a lineage that was distinct from other species of the genus Ochrobactrum and supported by high bootstrap values (Fig. 1 and Supplementary Fig. S1 in IJSEM Online). The phylogenetic analysis showed that isolates ADV31T, ADV41 and ADV43 should be considered as representing a novel species in the genus Ochrobactrum. Independent lineages, each corresponding to a single Ochrobactrum species, were observed in all the trees reconstructed, except for Ochrobactrum lupini, which formed a monophyletic group with O. anthropi ATCC 49188T (Fig. 1 and Supplementary Fig. S1 in IJSEM Online). The relative branching of O. intermedium and Ochrobactrum grignonense differed between 16S rRNA- and dnak–rpoB-based trees. The dnak–rpoB-based tree displayed higher bootstrap values than those obtained in the 16S rRNA gene-based tree. This confirmed that the evolutionary relationships among members of the genus Ochrobactrum cannot be resolved using the 16S rRNA gene alone. In addition to recA (Scholz et al., 2006), the two markers proposed herein are useful for studying species diversity in the genus Ochrobactrum. Additional comparative sequence analysis showed that 16S rRNA gene sequences deposited in databases for strains that have not been identified to the species level matched the sequences of the clinical isolates studied. These sequences were used to reconstruct a 16S rRNA gene-based tree (data not shown). The tree showed that Ochrobactrum strain CGL-X (GenBank accession no. DQ305290) might represent another member of the novel species, as well as strain TKW2 (AY631061) deposited as Rhizobium sp. and strain YBJCA-1 (DQ305284) deposited as Brucella sp.
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).
DNA–DNA hybridization between O. intermedium LMG 3301T and strain ADV31T was performed, according to the methods of De Ley et al. (1970) with the modifications of Huß et al. (1983), at the Identification Service of the Deutsche Sammlung von Mikroorganismen und Zellkulturen (DSMZ; Germany). The values obtained in duplicate experiments were 37.7 and 48.2 %, confirming that isolate ADV31T does not belong to the species O. intermedium. The DNA G+C content of strain ADV31T, determined by HPLC (Mesbah et al., 1989), was 54.5 mol%, a value that was different from those reported for other members of the genus Ochrobactrum (Table 1).
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). The rrn skeleton was constructed as described previously (Teyssier et al., 2003b, 2005b). The genomes of the three clinical strains harboured two circular chromosomes of about 2.8 and 1.78 Mb. In addition, strain ADV31T possessed a plasmid of 0.44 Mb. I-CeuI digestion led to four restriction fragments, indicating the presence of four rrn copies in the genome of the three strains. Two rrn copies were located on each chromosome (see Supplementary Fig. S2 in IJSEM Online). These results were in agreement with the affiliation of the isolates to the genus Ochrobactrum. Indeed, the bipartite organization of the genome and the rrn skeleton of the large chromosome have been described previously as being characteristic of this genus (Teyssier et al., 2005b). The rrn organization of the small chromosome was identical to that of O. anthropi, O. grignonense, O. tritici and O. lupini, but was different from that of O. intermedium and O. gallinifaecis (Teyssier et al., 2005b).
Cells of strains ADV31T, ADV41 and ADV43 were Gram-negative, straight or slightly curved short rods, with one flame-shaped end. The cells appeared to be motile under microscopic observation and after culture on mannitol motility nitrate broth medium (Bio-Rad). Electron microscopy after negative staining, performed as described previously (Marchandin et al., 2003) and observed with a Hitachi H7100 electron microscope, showed the presence of one or two flagella in a subterminal position. Cells were 0.65–0.75x1.5–1.7 µm in size. The strains were cultivated on tryptic soy agar (Difco) at 25, 30, 37 and 45 °C. Colonies were non-pigmented, mucoid and opaque. The three strains grew on MacConkey medium (Difco) only at 37 °C and did not grow on cetrimid agar (Difco), independent of the incubation temperature. General metabolic characteristics were common to those of all members of the genus Ochrobactrum: aerobic respiration, presence of catalase and cytochrome oxidase, oxidative metabolism and acids not being produced from carbohydrates on the API 20E system (bioMérieux). Eighty-one biochemical characteristics were determined using the API 20E and API 20NE systems and VITEK 2 with ID-GN card version WSVT2-R04.01 (bioMérieux), according to the manufacturer's instructions. A comparison of the data obtained for strains ADV31T, ADV41 and ADV43 and those for the type strains of other Ochrobactrum species is given in Table 1
. The antimicrobial susceptibility pattern was determined by using the disc-diffusion assay on Mueller–Hinton agar, according to the recommendations of the SFM antibiogram committee for Gram-negative non-fermenters (Members of the SFM Antibiogram Committee, 2003). Antibiotic susceptibility patterns for strains ADV31T, ADV41 and ADV43 and other Ochrobactrum species are compared in Table 1. As generally observed for the genus Ochrobactrum, the three isolates were resistant to all -lactams except imipenem (10 µg) (Teyssier et al., 2005a). They were also resistant to colistin (50 µg) and susceptible to tobramycin (10 µg) and netilmicin (30 µg). This pattern differentiated strains ADV31T, ADV41 and ADV43 from the two other Ochrobactrum species recovered from human clinical samples (Teyssier et al., 2005a). Indeed, O. anthropi strains were susceptible to colistin, tobramycin and netilmicin, whereas O. intermedium strains were resistant to these three antibiotics (Teyssier et al., 2005a). Moreover, strains ADV31T, ADV41 and ADV43 were resistant to tetracycline (30 µg), unlike other Ochrobactrum species.
Chemotaxonomic analyses of strain ADV31T, including fatty acid methyl esters, respiratory quinones and polar lipids, were performed at the Identification Service of the DSMZ, according to Tindall (1990a, b) and Kämpfer et al. (1994). Predominant cellular fatty acids were C19 : 0 cyclo 
8c and C18 : 17c, constituting 39.8 and 29.3 % of the total fatty acid methyl esters, respectively. Other fatty acids were present at moderate or low amounts (Table 2). This profile was most similar to that of O. gallinifaecis, but differed from those of the type strains of other Ochrobactrum species (Kämpfer et al., 2003; Trujillo et al., 2005; Tripathi et al., 2006). Two respiratory lipoquinones, ubiquinone 10 and ubiquinone 9, were detected, at peak area ratios of 96 and 4 %, respectively. The presence of ubiquinone 10 as the dominant respiratory lipoquinone is characteristic of members of the Alphaproteobacteria (Lechner et al., 1995). The major polar lipids were phosphatidylglycerol, phosphatidylethanolamine and phosphatidylcholine. In addition, diphosphatidylglycerol, aminophospholipid and an unidentified aminolipid were detected in moderate amounts (see Supplementary Fig. S3 in IJSEM Online). The unidentified aminophospholipid in the profile of strain ADV31T exhibited the same RF value as that of phosphatidylmonomethylethanolamine in the polar lipid profile of O. gallinifaecis (Kämpfer et al., 2003). Consequently, we could not show any obvious differences between the polar lipid profiles of strain ADV31T and O. gallinifaecis.
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) were common to strains ADV31T, ADV41 and ADV43 and O. intermedium (mucoid colonies, ability to grow on tryptic soy agar at 45 °C, absence of urease activity and resistance to colistin). In addition, genotyping data and phylogeny showed that the novel species was related to O. intermedium, supporting its denomination as Ochrobactrum pseudintermedium sp. nov. However, the 16S rRNA gene-, dnaK- and rpoB-phylogenies, DNA–DNA hybridization, G+C content, rrn skeleton of the small chromosome, PCR specific for Brucella spp. and O. intermedium, phenotype and chemotaxonomy clearly differentiated strains ADV31T, ADV41 and ADV43 from O. intermedium. Together, the results support the creation of a novel species to accommodate isolates ADV31T, ADV41 and ADV43 and its denomination as Ochrobactrum pseudintermedium sp. nov. is proposed.
Description of Ochrobactrum pseudintermedium sp. nov.
Ochrobactrum pseudintermedium (pseud.in'ter.med'i.um. Gr. adj. pseudos false; L. neut. adj. intermedium intermediate, and a specific epithet of the genus Ochrobactrum; N.L. neut. adj. pseudintermedium a false Ochrobactrum intermedium).
Cells are Gram-negative, non-spore forming, short rods, and motile by subpolar flagella. Cells are 0.65–0.75x1.5–1.7 µm in size. Growth occurs at 25–45 °C on tryptic soy agar. Grows on MacConkey agar and R2A agar at 37 °C. Colonies are non-pigmented, mucoid and opaque. Aerobic respiration, oxidative metabolism, nitrate reduction and catalase and oxidase are positive. Positive for glycine arylamidase, L-proline arylamidase, tyrosine arylamidase and L-pyrrolidonyl arylamidase activities, assimilation of glucose, arabinose, mannose, malate, potassium gluconate, D-mannitol, N-acetylglucosamine, D-maltose and capric acid, acidification of adonitol and D-tagatose, and alkalinization of L-lactate and succinate. Negative for activities of DNase, urease, phenylalanine deaminase, tryptophan deaminase, Glu-Gly-Arg arylamidase and -alanine arylamidase p-nitroanilide (pNA), arginine dihydrolase, Ala-Phe-Pro arylamidase, glutamyl arylamidase pNA, -xylosidase, lipase, N-acetyl--galactosaminidase, 
-galactosidase, -galactosidase (ONPG), N-acetyl--glucosaminidase, phosphatase, ornithine decarboxylase, lysine decarboxylase, -glucuronidase and -glucosidase (aesculin hydrolysis). Negative for acidification of D-glucose, D-mannose, L-arabitol, D-cellobiose, D-mannitol, D-trehalose, malonate, 5-keto-D-gluconate and coumarate, production of indole, acetoin and H2S, hydrolysis of gelatin, assimilation of adipic acid, phenylacetic acid, L-histidine and L-lactate, and fermentation of carbohydrates. Resistant to -lactams except imipenem, and to chloramphenicol, tetracycline, fosfomycin and colistin. Susceptible to aminoglycosides (gentamicin, tobramycin, netilmicin, isepamicin, amikacin), fluoroquinolones (pefloxacin, ofloxacin, ciprofloxacin), nalidixic acid, rifampicin and trimethoprim-sulfamethoxazole. Major fatty acids are C19 : 0 cyclo 8c and C18 : 17c. Ubiquinone 10 is the dominant respiratory lipoquinone. Polar lipids mainly comprise phosphatidylglycerol, phosphatidylethanolamine and phosphatidylcholine. 16S rRNA gene amplification is not obtained with primers F4 and R2 (Velasco et al., 1998). Genome is constituted of two chromosomes of about 2.8 and 1.8 Mb comprising four rrn copies with two rrn operons in divergent orientation on the small chromosome. The G+C content of the DNA of the type strain is 54.5 mol%. Can be differentiated from other species of the genus Ochrobactrum by 16S rRNA, dnaK and rpoB gene sequencing.
The type strain is ADV31T (=CIP 109116T=DSM 17490T), which was isolated from a human clinical sample.
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ACKNOWLEDGEMENTS |
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