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Int J Syst Evol Microbiol 56 (2006), 1823-1829; DOI  10.1099/ijs.0.64256-0
© 2006 International Union of Microbiological Societies

Description of Pseudochrobactrum gen. nov., with the two species Pseudochrobactrum asaccharolyticum sp. nov. and Pseudochrobactrum saccharolyticum sp. nov.

Peter Kämpfer1, Ramon Rosselló-Mora2, Holger C. Scholz3, Christina Welinder-Olsson4, Enevold Falsen4 and Hans-Jürgen Busse5

1 Institut für Angewandte Mikrobiologie, Justus-Liebig-Universität Giessen, Heinrich-Buff-Ring 26–32, D-35392 Giessen, Germany
2 Institut Mediterrani d'Estudis Avancats (CSIC-UIB), E-07190 Esporles, Mallorca, Spain
3 Bundeswehr Institute of Microbiology, D-80937 Munich, Germany
4 Culture Collection University of Göteborg, Department of Clinical Bacteriology, S-41346 Göteborg, Sweden
5 Institut für Bakteriologie, Mykologie und Hygiene, Veterinärmedizinische Universität, A-1210 Wien, Austria

Correspondence
Peter Kämpfer
peter.kaempfer{at}agrar.uni-giessen.de


   ABSTRACT
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Two Gram-negative, rod-shaped, oxidase-positive, non-spore-forming, non-motile bacteria (CCUG 46016T and CCUG 33852T), isolated from a knee aspirate of a 66-year-old man and an industrial glue, respectively, were studied for their taxonomic position. On the basis of chemotaxonomic data [i.e. major ubiquinone (Q-10), major polar lipids (phosphatidylethanolamine, phosphatidylglycerol and phosphatidylcholine) and major fatty acids (C18 : 1{omega}7c and C19 : 0 cyclo {omega}8c)] and 16S rRNA gene sequence similarity, both strains belong to the Alphaproteobacteria. The presence of spermidine and putrescine as the predominant polyamines in CCUG 46016T were in agreement with its phylogenetic affiliation in the vicinity of the genus Ochrobactrum. 16S rRNA gene sequence similarities between both strains and established species within the genera Bartonella, Ochrobactrum and Brucella were less than 95 %. Although both organisms showed highest 16S rRNA gene sequence similarity to members of Brucella, phenotypic features (including chemotaxonomic features) were more like those of members of the genus Ochrobactrum. Sequence comparison of the recA genes confirmed the separate phylogenetic position of the two strains. On the basis of DNA–DNA pairing results and physiological and biochemical data, the two strains can be clearly differentiated from each other and from all known Ochrobactrum species. It is evident that these organisms represent two novel species in a new genus, Pseudochrobactrum gen. nov., for which the names Pseudochrobactrum asaccharolyticum sp. nov. (the type species, type strain CCUG 46016T=CIP 108977T) and Pseudochrobactrum saccharolyticum sp. nov. (type strain CCUG 33852T=CIP 108976T) are proposed.

Abbreviations: PME, phosphatidylmonomethylethanolamine

The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of strains CCUG 46016T and CCUG 33852T are AM180485 and AM180484, respectively, and those of the partial recA sequences of strains CCUG 46016T and CCUG 33852T are AM118081 and AM118082.

A multiple sequence alignment of partial recA gene sequences and a two-dimensional TLC of the polar lipids of CCUG 46016T are available as supplementary material in IJSEM Online.


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The genus Ochrobactrum was first described by Holmes et al. (1988)Go. At present, the genus comprises five species: Ochrobactrum anthropi Holmes et al. 1988Go, Ochrobactrum intermedium Velasco et al. 1998Go, Ochrobactrum tritici Lebuhn et al. 2000Go, Ochrobactrum grignonense Lebuhn et al. 2000Go and Ochrobactrum gallinifaecis Kämpfer et al. 2003Go. The status of ‘Ochrobactrum lupini’ (Trujillo et al., 2005Go) is not yet clear.

On the basis of 16S rRNA gene sequence data, members of the genus Brucella are most closely related to members of the genus Ochrobactrum; however, they clearly differ on the basis of serology, Western blot profiles and protein patterns (Velasco et al., 1998Go). An overview of the genus Brucella is provided by Moreno & Moriyon (2001)Go. Bacteria of the genus Bartonella are aerobic, fastidious, oxidase-negative, slow-growing organisms. Currently, 19 species are recognized, all of which are associated with mammalian hosts and can be differentiated on the basis of genetic analyses (Breitschwerdt & Kordick, 2000Go; Bermond et al., 2002Go; Pitulle et al., 2002Go; Zeaiter et al., 2002Go). Based on 16S rRNA gene sequence comparisons, members of the genus Bartonella also fall into the Alphaproteobacteria, with species of Brucella, Rhizobium and Agrobacterium as closest relatives. In general, the genus Bartonella is relatively homogeneous, with members exhibiting greater than 95 % similarity among aligned 16S rRNA gene sequences.

Strain CCUG 46016T was isolated on blood agar at 37 °C from a knee aspirate of a 66-year-old man in Uddevalla, Sweden. Strain CCUG 33852T was isolated on blood agar at 37 °C from an industrial glue in Göteborg, Sweden. Both strains formed beige-coloured colonies on blood agar. Subcultivation was done on tryptone soy agar (TSA) at 28 °C for 48 h. On this agar, both organisms were able to grow at 15–45 °C, but not at 10 or 50 °C. Growth at 30 °C was also observed on nutrient agar, MacConkey agar and R2A agar (all from Oxoid).

Gram-staining was performed as described by Gerhardt et al. (1994)Go. Cell morphology was observed under a Zeiss light microscope at x1000, with cells grown for 3 days at 28 °C on TSA. The 16S rRNA gene was analysed as described by Kämpfer et al. (2003)Go. Phylogenetic analysis was performed using the ARB (Strunk et al., 2000Go; Ludwig et al., 2004Go) and MEGA version 2.1 (Kumar et al., 2001Go) software packages after multiple alignment of data by CLUSTAL X (Thompson et al., 1997Go). The sequenced lengths of the 16S rRNA genes of strains CCUG 46016T and CCUG 33852T were 1457 bp and 1401 bp, respectively (GenBank accession nos AM180485 and AM180484, respectively). Nucleotide sequence similarities were below 95 % with all species of the genera Bartonella (94.2 and 94.3 %, respectively), Brucella (94.6–94.8 %) and Ochrobactrum (93.8–94.6 %) with validly described names. The phylogenetic tree shown in Fig. 1Go results from a neighbour-joining reconstruction modified after comparison with maximum-parsimony and maximum-likelihood trees and with the use of different datasets as reported previously (Albert et al., 2005Go). The multifurcation shown in the tree represents branching orders that could not be resolved by the multiple reconstructions as recommended by Ludwig et al. (1998)Go. In all calculations, both sequences appeared on a single phylogenetic branch, indicating their independent affiliation.


Figure 1
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  		Fig. 1. 16S rRNA gene sequence phylogenetic neighbour-joining tree reconstruction showing the affiliation of Pseudochrobactrum species to their closest relatives. The tree topology shows the consensus of neighbour-joining, maximum-parsimony and maximum-likelihood algorithms with different datasets, as implemented in the ARB software package (Ludwig et al.,2004Go). In cases where the branching order was irresolvable, a multifurcation was drawn (Ludwig et al., 1998Go). Bar, 5 % sequence dissimilarity.

 
Partial recA sequences of some Ochrobactrum type strains and strains of Brucella species were amplified by PCR with primers recA-BrucOchro-f (5'-ATGTCTCAAAATTCATTGCGAC-3') and recA-BrucOchro-r (5'-AGCATCTTCTTCCGGTCCGC-3') to generate a 1065 bp fragment. Partial recA sequences (909 bp) of strains CCUG 46016T and CCUG 33852T were amplified by PCR with primers RecA-PsOchro-f (5'-AAGGCTCTGGACGCGGCACT-3') and RecA-PsOchro-r (5'-CGCAAGGTCAGTTCAATCTCAT-3').

Subsequent sequencing and sequence comparison analyses of the recA genes revealed multiple sequence variations within recA among the investigated strains (see the multiple sequence alignment available as Supplementary Fig. S1 in IJSEM Online). The similarity between recA sequences of CCUG 46016T and CCUG 33852T was 91 % over 909 nt. Lower similarity values were observed with species of Brucella (80.1–81.0 %), Ochrobactrum (80.7–81.4 %) and Bartonella (76.3 %). CCUG 46016T and CCUG 33852T shared several motifs within recA that were absent from sequences in species of Bartonella, Brucella and Ochrobactrum (Supplementary Fig. S1).

Strains CCUG 46016T and CCUG 33852T were found as separate branches in the phylogenetic tree of recA sequences (909 nt) (Fig. 2Go). The tree was constructed using the online accessible bioinformatics tools of HUSAR (available from http://genius.embnet.dkfz-heidelberg.de/menu/w2h/w2hdkfz) from CLUSTAL W using CLUSTREE neighbour-joining and the Kimura two-parameter model; 1000 bootstrap resamplings were performed. The tree was rooted using the sequence of Mesorhizobium loti MAFF 303099 as an outgroup.


Figure 2
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  		Fig. 2. Phylogenetic tree reconstruction with recA sequences (909 nt) using CLUSTREE neighbour-joining analysis and the Kimura two-parameter model. Bar, 0.1 divergent residues per site. The significance of each branch is indicated by a bootstrap value from 1000 repetitions. The tree was rooted using the sequence of Mesorhizobium loti MAFF 303099 as an outgroup.

 
Results of chemotaxonomic analyses are given in the genus description. The following compounds were analysed: respiratory quinones (Tindall, 1990Go; Altenburger et al., 1996Go), polyamines (Busse & Auling, 1988Go; Busse et al., 1997Go), polar lipids (Ventosa et al., 1993Go) and fatty acids (Kämpfer & Kroppenstedt, 1996Go). The presence of the quinone system ubiquinone Q-10 (97 %) supports affiliation of CCUG 46016T and CCUG 33852T to the Alphaproteobacteria, where the majority of species have Q-10 as the major quinone (Lechner et al., 1995Go; Yokota et al., 1992Go). In addition, CCUG 46016T contained small amounts of Q-9 (3 %). Strain CCUG 46016T contained the following polyamines [in µmol (g dry weight)–1]: spermidine, 63.8; putrescine, 11.6; diaminopropane, 3.8; spermine, 0.5; and cadaverine, 0.1. This profile is similar to those reported for species of Ochrobactrum (Lechner et al., 1995Go; Hamana & Takeuchi, 1998Go; Kämpfer et al., 2003Go), but distinct from the polyamine patterns of members of the genera Rhizobium, Mesorhizobium, Sinorhizobium, Aminobacter, Pseudaminobacter, Phyllobacterium and Mycoplana, which have been shown to contain sym-homospermidine in at least minor amounts (Busse & Auling, 1988Go; Hamana & Takeuchi, 1998Go; Kämpfer et al., 1999Go). The polar lipid profiles of CCUG 46016T (TLC available as Supplementary Fig. S2 in IJSEM Online) and CCUG 33852T (not shown) were almost identical and were similar to those of species of the related genera Aminobacter, Pseudaminobacter, Ochrobactrum (Kämpfer et al., 1999Go, 2003Go), Brucella (Thiele et al., 1971Go; H.-J. Busse, unpublished results), Sinorhizobium (Geiger et al., 1999Go) and Mesorhizobium (Choma & Komaniecka, 2002Go). The absence of unknown aminolipid AL2 shown to be present in O. gallinifaecis Iso 196T, O. anthropi LMG 7991 (Kämpfer et al., 2003Go), O. anthropi CCUG 24695T and O. intermedium LMG 3301T (B. Huber and H.-J. Busse, unpublished results) distinguishes CCUG 46016T and CCUG 33852T from Ochrobactrum species. Phosphatidyldimethylethanolamine shared almost identical chromatographic behaviour with the unknown aminolipid AL1. The existence of two lipids at almost the same position in the two-dimensional TLC (spot between phosphatidylglycerol and phosphatidylethanolamine; available as supplementary material in IJSEM Online) could be clearly identified when the plate was first sprayed with ninhydrin reagent and afterwards with molybdenum blue reagent. Only the lower part of the ninhydrin-positive spot stained blue with molybdenum blue reagent. Polar lipid profiles did not clearly distinguish CCUG 46016T and CCUG 33852T from two analysed Brucella strains (results not shown). However, the content of phosphatidylmonomethylethanolamine (PME) might be a distinguishing characteristic. In Brucella species, this lipid was not detectable or was present only in minor amounts, whereas it was a major compound in the polar lipid profiles of CCUG 46016T and CCUG 33852T. However, the suitability of PME as a distinguishing trait would have to be substantiated by analysis of additional strains. Unfortunately, no information is available on polar lipids in Bartonella nor could strains of this genus be made available for our study. The fatty acid profiles of strains CCUG 46016T and CCUG 33852T (Table 1Go) revealed mainly C19 : 0 cyclo {omega}8c (7.3–14.3 %), C18 : 1{omega}7c (74.6–74.9 %), C16 : 0 (1.9–5.6 %) and C18 : 0 (7.4–10.9 %). The presence of C19 : 0 cyclo {omega}8c appears to be useful for differentiation of CCUG 46016T and CCUG 33852T from Brucella and Bartonella species. Whereas Brucella species were shown to contain this fatty acid either only in traces (Brucella canis; Dees et al., 1981Go) or as a predominant compound (>34 % in the four other species; Dees et al., 1980Go; 1981Go; Coloe et al., 1984Go), it was completely absent in fatty acid profiles of Bartonella species (Welch et al., 1992Go; Regnery et al., 1992Go; Daly et al., 1993Go). However, this observation has to be considered with care because the data for Brucella and Bartonella species were obtained from biomass grown on blood-supplemented media.


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  		Table 1. Major fatty acid composition (%) of strains CCUG 46016T and CCUG 33852T and type strains of the genus Ochrobactrum

Strains: 1, CCUG 46016T; 2, CCUG 33852T; 3, O. gallinifaecis Iso 196T; 4, O. intermedium LMG 3301T; 5, O. anthropi LMG 3331T; 6, O. grignonense DSM 13338T; 7, O. tritici LMG 18957T, 8, ‘O.lupini’ LUP21 (data from Trujillo et al. 2005Go). All strains were grown on TSA at 28 °C for 48 h prior to fatty acid analysis. For unsaturated fatty acids, the position of the double bond is located by counting from the methyl ({omega}) end of the carbon chain; cis and trans isomers are indicated by the suffixes c and t, respectively. –, Not detected.

 
Results of the physiological characterization are given in the species description and in Table 2Go. Methods used have been described previously (Kämpfer et al., 1991Go). Both organisms can be clearly differentiated on the basis of several tests. A comparison with the physiological profiles of Bartonella species is difficult. As pointed out by Breitschwerdt & Kordick (2000)Go, biochemical profiles of Bartonella species are fairly neutral. Members of the genus Brucella are biochemically quite heterogeneous.


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  		Table 2. Physiological characteristics of strains CCUG 46016T and CCUG 33852T and type strains of the genus Ochrobactrum

Strains: 1, CCUG 46016T; 2, CCUG 33853T; 3, O. gallinifaecis Iso 196T; 4, O. intermedium LMG 3301T; 5, O. anthropi LMG 3331T; 6, O. grignonense DSM 13338T; 7, O. tritici LMG 18957T. +, Positive; –, negative; (+), weakly positive; pNA, para-nitroanilide; pNP, para-nitrophenyl. All strains were positive for hydrolysis of L-alanine pNA and weak hydrolysis of bis-pNP phosphate. All strains were negative for hydrolysis of aesculin, pNP beta-D-galactopyranoside, pNP beta-D-glucuronide, pNP {alpha}-D-glucopyranoside, pNP beta-D-glucopyranoside, pNP phosphorylcholine and 2-deoxythymidine-5'-pNP phosphate. All strains were also positive for assimilation of acetate, oxoglutarate, L-alanine, L-proline and L-serine. All strains were negative for assimilation of p-arbutin, salicin, putrescine, L-phenylalanine, L-tryptophan, 3-hydroxybenzoate, adipate, itaconate, mesaconate, phenylacetate, {alpha}-D-melibiose and azelate. Hydrolysis of aesculin and pNP beta-D-galactopyranoside and assimilation of oxoglutarate, L-serine, phenylacetate and {alpha}-D-melibiose were also tested using a different method by Holmes et al. (1988)Go with O. anthropi; results were in agreement with those of this study. Adipate assimilation was also tested using a different method by Velasco et al. (1998)Go with O. intermedium; results were in agreement with those of this study.

 
The G+C content for strain CCUG 46016T was determined as described by Ziemke et al. (1998)Go. DNA–DNA hybridization experiments were performed with CCUG 46016T and type strains of all Ochrobactrum species using the method described by Ziemke et al. (1998)Go, except that, for nick translation, 2 µg DNA was labelled during a 3 h incubation at 15 °C. Strain CCUG 46016T showed relatively low DNA–DNA relatedness to O. anthropi LMG 3331T (46 %), O. intermedium LMG 3301T (42 %), O. tritici LMG 18957T (47 %), O. grignonense DSM 13338T (53 %) and O. gallinifaecis Iso 196T (38 %). DNA–DNA hybridization values between strains CCUG 46016T and CCUG 33852T were 41.9 %. Pooled standard deviations of all hybridization experiments were between 3.9 and 7.9 %.

From the results of 16S rRNA gene and recA sequencing and from the physiological characteristics, it is evident that strains CCUG 46016T and CCUG 33852T differ from each other and from all species of the genera Bartonella, Brucella and Ochrobactrum. For this reason, a new genus with two novel species is proposed.

Description of Pseudochrobactrum gen. nov.
Pseudochrobactrum (Pseud.och.ro.bac'trum. Gr. adj. pseudes false; N.L. neut. n. Ochrobactrum a bacterial genus name; N.L. neut. n. Pseudochrobactrum false Ochrobactrum).

Cells are non-motile, non-spore-forming rods (approx. 2 µm in length). Gram-negative and oxidase-positive, showing an oxidative metabolism. The quinone system consists mainly of Q-10. Polyamine patterns comprise spermidine and putrescine as major compounds and 1,3-diaminopropane and spermine in minor amounts. Predominant polar lipids are phosphatidylethanolamine, phosphatidylmonomethylethanolamine, phosphatidylglycerol, diphosphatidylglycerol and phosphatidylcholine. Additionally, moderate amounts of phosphatidyldimethylethanolamine and unknown aminolipid AL1 and small amounts of unknown phospholipid PL1 and five unknown lipids (L1–L5) are detected. Fatty acid profiles contain large amounts of C18 : 1{omega}7c and moderate amounts of C18 : 0 and C19 : 0 cyclo {omega}8c. Negative for a Brucella abortus- and Brucella melitensis-specific antigen (according to the assay of Baily et al., 1992Go). In recA sequence analyses, most closely related to species of Brucella (80 %) and Ochrobactrum (81 %), followed by Bartonella (76 %). Species of the genus can be differentiated from Bartonella species by a positive oxidase reaction, non-fastidious growth and utilization of several organic acids (Table 2Go). The type species is Pseudochrobactrum asaccharolyticum.

Description of Pseudochrobactrum asaccharolyticum sp. nov.
Pseudochrobactrum asaccharolyticum (a.sac.cha.ro.ly'ti.cum. Gr. pref. a not; Gr. n. saccharon sugar; N.L. neut. adj. lyticum able to lyse from Gr. adj. lutikos able to loose; N.L. neut. adj. asaccharolyticum not digesting sugar).

Shares all characteristics listed in the genus description. Good growth occurs on R2A agar, TSA, nutrient agar and MacConkey agar at 25–30 °C. Beige, translucent and shiny colonies with entire edges form within 24 h on blood agar, with a diameter of approximately 2 mm. Carbon source utilization (none of the sugars were utilized) and hydrolysis of chromogenic substrates (including differentiating characters for all Ochrobactrum species) are indicated in Table 2Go.

Type strain is CCUG 46016T (=CIP 108977T), isolated from a knee aspirate of a 66-year-old man. The G+C content of strain CCUG 46016T is 50.9 mol%.

Description of Pseudochrobactrum saccharolyticum sp. nov.
Pseudochrobactrum saccharolyticum (sac.cha.ro.ly'ti.cum. Gr. n. saccharon sugar; N.L. neut. adj. lyticum able to lyse from Gr. adj. lutikos able to loose; N.L. neut. adj. saccharolyticum digesting sugar).

Good growth occurs on R2A agar, TSA, nutrient agar and MacConkey agar at 25–30 °C. Beige, translucent and shiny colonies with entire edges form within 24 h on blood agar, with a diameter of approximately 2 mm. Carbon source utilization (several sugars were utilized) and hydrolysis of chromogenic substrates (including differentiating characters for all Ochrobactrum species) are indicated in Table 2Go.

The type strain is CCUG 33852T (=CIP 108976T), isolated from an industrial glue.


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