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Programa de Ecología Molecular y Microbiana, Centro de Investigación sobre Fijación de Nitrógeno, Universidad Nacional Autónoma de México, Apdo. Postal 565-A, Cuernavaca, Morelos, México
Correspondence
Jesús Caballero-Mellado
jesuscab{at}cifn.unam.mx
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Published online ahead of print on 13 April 2004 as DOI 10.1099/ijs.0.02951-0.
The GenBank/EMBL/DDBJ accession numbers for the 16S rDNA sequences of strains MCo-762, MTl-641T and SCCu-23 are AY221955, AY221956 and AY221957, respectively.
A table of restriction patterns of B. unamae genotypes, a fuller phylogenetic tree and a dendrogram to illustrate the genetic relatedness of strains of B. unamae are available as supplementary material in IJSEM Online.
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TOPABSTRACTMAIN TEXTREFERENCES |
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), with Burkholderia cepacia as the type species (Yabuuchi et al., 1992). Burkholderia species of environmental origin that have been described in the last 5 years include Burkholderia graminis (Viallard et al., 1998), Burkholderia thailandensis (Brett et al., 1998), Burkholderia caribensis (Achouak et al., 1999), Burkholderia kururiensis (Zhang et al., 2000), Burkholderia uboniae (Yabuuchi et al., 2000a), which has subsequently been corrected to Burkholderia ubonensis (Yabuuchi et al., 2000b), Burkholderia caledonica and Burkholderia fungorum (Coenye et al., 2001a), Burkholderia ambifaria (Coenye et al., 2001b), Burkholderia sacchari (Brämer et al., 2001), Burkholderia anthina (Vandamme et al., 2002b), Burkholderia terricola and Burkholderia hospita (Goris et al., 2002). Recently, two nodulating strains recovered from legume plants were assigned to the genus Burkholderia as two novel species, Burkholderia tuberum and Burkholderia phymatum (Vandamme et al., 2002a).
For a long time, N2-fixing ability in bacteria of the genus Burkholderia was recognized only in the species Burkholderia vietnamiensis (Gillis et al., 1995). Recently, analysis of maize, sorghum and coffee plants grown under field conditions revealed the richness of the genus Burkholderia in unknown diazotrophs and the N2-fixing ability of B. kururiensis (Estrada-de los Santos et al., 2001). These unknown N2-fixing bacteria showed different amplified 16S rDNA restriction analysis (ARDRA) profiles that corresponded to 14 of the ARDRA genotypes identified, which suggested the existence of at least five novel N2-fixing Burkholderia species. An abundant group of these N2-fixing Burkholderia sp. isolates, identified as ARDRA genotypes 13, 14 and 15, showed almost-identical whole-cell protein patterns, as well as other common phenotypic and genomic features, such as nitrogenase activity with different carbon sources and identical nifHDK hybridization patterns. Very recently, N2-fixing isolates recovered from maize and teosinte plants grown in Mexico, as well as from sugarcane plants cultivated in Brazil and South Africa, were described as ‘Burkholderia tropica’ (Reis et al., 2004).
In the present study, previously identified diazotrophic isolates that corresponded to 16S rDNA genotypes 13, 14 and 15 (Estrada-de los Santos et al., 2001), along with new isolates recovered from diverse plant species, were subjected to a detailed phenotypic and genomic analysis to determine their taxonomic status.
Sources of the 20 Burkholderia isolates that were analysed are shown in Table 1. Seven of these strains, corresponding to ARDRA genotypes 13, 14 and 15, were from a previously described collection (Estrada-de los Santos et al., 2001). New isolates were recovered from the rhizosphere, rhizoplane and surface-sterilized roots and stems of maize and sugarcane plants cultivated in Mexico. Rhizosphere soil and plants were treated as described previously (Estrada-de los Santos et al., 2001). N-free, semi-solid BAz medium was used as an enrichment culture for N2-fixing Burkholderia and BAc agar plates were used for isolation and pure cultures (Estrada-de los Santos et al., 2001). Single colonies were inoculated in N-free, semi-solid BAz medium and assayed for acetylene reduction activity (ARA) as described previously (Estrada-de los Santos et al., 2001). Acetylene-reducing colonies were further verified for culture purity on BAc agar plates. N2-fixing isolates were maintained in 50 % (v/v) glycerol at –80 °C prior to analysis.
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. Each isolate was assigned to one of the ARDRA genotypes described previously (Estrada-de los Santos et al., 2001). For ribotyping, a Southern blot of total EcoRI DNA digest was hybridized by using the conditions described by Caballero-Mellado et al. (1995). In order to obtain the 16S rRNA gene sequence, PCR products were cloned into the vector pCRII (Invitrogen) according to the manufacturer's instructions. 16S rRNA genes were restricted in small fragments (0·6–0·9 kb) by using EcoRI and subcloned into the vector pUC18 (Invitrogen). 16S rRNA gene sequencing was performed by Medigenomix GmbH (Martinsried, Germany). DNA–DNA reassociation was based on relative levels of hybridization to 32P-labelled DNA, as described previously (Estrada-de los Santos et al., 2001).
Multi-locus enzyme electrophoresis (MLEE) and SDS-PAGE of whole-cell proteins were performed as described previously (Caballero-Mellado et al., 1995; Estrada-de los Santos et al., 2001), except that each isolate was grown for 18 h in BSE medium (Estrada-de los Santos et al., 2001) at 29 °C. For determination of cellular fatty acid composition, strains were grown in trypticase soy broth agar at 28 °C for 24 h; the analysis was performed by Microbial ID, Inc. (Newark, DE, USA).
Bacteriological and biochemical characterization was carried out by growing isolates in BSE medium for 12 h at 29 °C (Estrada-de los Santos et al., 2001). Cultures were centrifuged twice and resuspended each time in 10 mM MgSO4, and then adjusted to an OD450 of 0·2 (3x106 c.f.u. ml–1). An aliquot (10 µl) from each culture was streaked onto solid medium and incubated for 72 h at 29 °C unless otherwise indicated, to determine phenotypic features. Colony morphology was examined on BAc agar plates (Estrada-de los Santos et al., 2001) and growth was recorded after 4 days incubation. Effects of temperature and pH on growth were determined in BSE agar medium. Growth on MacConkey agar (Difco) plates and on B. cepacia-selective agar (BCSA) medium, as well as on BCSA/vancomycin (2·5 mg l–1) medium (Henry et al., 1997), was determined. Growth of N2-fixing Burkholderia isolates with 1-aminocyclopropane-1-carboxylic acid (ACC) as the sole nitrogen source was tested on Az–Acc medium (0·2 % azelaic acid, 0·00 3 % ACC, 0·04 % K2HPO4, 0·04 % KH2PO4, 0·02 % MgSO4.7H2O and 1·6 % agarose). The pH was adjusted to 5·7 and the medium was sterilized at 121 °C for 20 min prior to the addition of filter-sterilized ACC (pore size, 0·22 µm). In addition, phenotypic features were assayed with the API 20NE and API 50CH systems, according to the manufacturer's instructions (bioMérieux). The API 20NE system was used to determine nitrate reduction, gelatin liquefaction, aesculin hydrolysis and urease activity. Two colonies grown on BAc agar plates were harvested to determine oxidase reaction, which is a complementary test in the API 20NE system. Results of carbon source assimilation using the API 50CH system were obtained after 4 days incubation at 29 °C. At least two replicates were used for each characteristic examined. Single colonies were inoculated in a modified BAz medium (which lacked azelaic acid, but was supplemented with either 0·5 % succinate or 0·2 % benzoate or propionate) and assayed for ARA as described previously (Estrada-de los Santos et al., 2001). Fresh culture medium with benzoate as the carbon source was used to avoid variable ARA results. Siderophores were detected by using universal chemical assays on chromeazurol-S agar plates (Schwyn & Neilands, 1987).
In the present study, diazotrophic isolates that corresponded to 16S rDNA genotypes 13, 14 and 15 were recovered repeatedly from the rhizospheres and rhizoplanes of maize, sugarcane and coffee (Coffea arabica and Coffea canephora) plants, as well as from the endophyte environment of maize and sugarcane, by using the culture media BAz and BAc. All isolates that corresponded to ARDRA genotypes 13, 14 or 15 formed very thin and fine pellicles at a depth of 5–6 mm below the surface in N-free, semi-solid BAz medium after 24 h. After 72 h, the pellicles become whitish, thick but slightly diffuse and moved up to the surface. Colonies of isolates that corresponded to genotypes 13, 14 or 15, when growing on BAc medium plates, were slightly yellowish, round, smooth and convex, 1–2 mm in diameter with entire margins and turned the colour of the culture medium from green to deep blue after incubation for 4 days at 29 °C.
ARDRA genotypes 13, 14 and 15 showed identical profiles with enzymes AluI, DdeI, HaeIII, HhaI, MspI and RsaI, but they were distinguished by using the enzyme HinfI (see Supplementary Table in IJSEM Online). One isolate showed the same profile as genotype 15 except with enzyme HaeIII; it was therefore designated ARDRA genotype 15a (Table 1
). Genotypes 13, 14, 15 and 15a could be differentiated from other N2-fixing Burkholderia species, as well as from non-diazotrophic Burkholderia species, by their ARDRA profiles (see Supplementary Table in IJSEM Online). For instance, ARDRA profiles obtained with restriction enzymes AluI, DdeI, HaeIII and RsaI can differentiate genotypes 13, 14, 15 and 15a from B. sacchari IPT 101T, a non-diazotrophic species, and the restriction enzymes HinfI and RsaI differentiate genotypes 13, 14, 15 and 15a from ‘B. tropica’ Ppe8. In addition, strains corresponding to genotypes 13, 14, 15 and 15a can be differentiated both from ‘B. tropica’ and B. sacchari by their distinct ribotypes obtained with EcoRI (Fig. 1).
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), strains MTl-641T and SCCu-23, both of which correspond to ARDRA genotype 15, and strain MCo-762 (genotype 13) were chosen for 16S rRNA gene sequencing. The 16S rRNA gene sequences of these strains were compared with available 16S rDNA sequences from Burkholderia species. The phylogenetic tree shown in Fig. 2 illustrates the position of strains MTl-641T, SCCu-23 and MCo-762 relative to the nearest Burkholderia species, as well as to other N2-fixing Burkholderia species. Strains MTl-641T, SCCu-23 and MCo-762 constituted a single, homogeneous cluster with similarity between their 16S rDNA sequences in the range of 99·2–99·6 %. B. sacchari and ‘B. tropica’ were the most closely related species to the cluster that comprised strains MTl-641T, SCCu-23 and MCo-762 (98·5 and 98·2 % sequence similarity, respectively). The N2-fixing strains MCo-762, MTl-641T and SCCu-23 constituted a cluster that was clearly separated from the cluster formed by the diazotrophic species B. kururiensis and B. tuberum, as well as from the diazotroph B. vietnamiensis (95·7 % similarity), which belongs to the B. cepacia complex (Vandamme et al., 1997). A phylogenetic tree based on available 16S rRNA gene sequences of all Burkholderia species is available as supplementary material (see Supplementary Fig. A in IJSEM Online). For clarifying the taxonomic status of strains corresponding to ARDRA genotypes 13, 14, 15 and 15a, a polyphasic taxonomic approach was undertaken, as suggested by Vandamme et al. (1996).
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).
Whole-cell protein extracts were prepared from all 20 isolates corresponding to genotypes 13, 14, 15 and 15a and from several related species. SDS-PAGE protein patterns of some representative strains, corresponding to ARDRA genotypes 13 and 15, are shown in Fig. 3. All 20 strains showed almost-identical protein profiles between themselves, but their protein patterns were clearly different from those of other N2-fixing and non-N2-fixing Burkholderia species (Fig. 3). It is well-known that bacteria with identical or very similar protein patterns possess high genome similarity (Vandamme et al., 1996). On this basis, the SDS-PAGE results suggest strongly that genotypes 13, 14, 15 and 15a represent a novel N2-fixing Burkholderia species.
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5c (0·46±0·06 %), 16 : 1 2-OH (3·41±0·3 %), 17 : 0 cyclo (6·6±1·0 %), 18 : 0 (0·3±0·7 %), 18 : 17c (34·2±1·7 %), 18 : 1 2-OH (1·29±0·07 %), 19 : 08c cyclo (3·6±0·5 %) and summed features 2 (5·5±0·1 %) and 3 (15·6±0·9 %). Summed feature 2 could correspond to 14 : 0 3-OH, iso-16 : 1 I, an unknown fatty acid with equivalent chain-length of 10·928, 12 : 0 ALDE or any combination of these fatty acids, and summed feature 3 could correspond to 16 : 17c or iso-15 : 0 2-OH or both, similar to those fatty acids reported in other Burkholderia species (Vandamme et al., 1997; Coenye et al., 2001b). A comparison of some fatty acids found in strain MTl-641T and other Burkholderia species is shown in Table 2. Strain MTl-641T was identified by the Microbial Identification system as B. cepacia (identification score of 0·568), followed by Burkholderia glathei (identification score of 0·317) and Burkholderia caryophylli (identification score of 0·314). There were only very slight differences in the identification indices between strain MTl-641T and strains MCo-762, SCCu-23 and CGC-72.
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On the basis of the SDS-PAGE protein profiles, electrophoretic mobility patterns of metabolic enzymes and fatty acid profiles, as well as the genomic data described here, we propose the name Burkholderia unamae sp. nov. for the isolates corresponding to ARDRA genotypes 13, 14 and 15, as well as for genotype15a, which was identified in the present work.
All B. unamae strains were Gram-negative and motile in N-free, semi-solid media at 29 °C. Transmission electron microscopy revealed that strain MTl-641T was a straight rod with a single polar flagellum or a tuft of polar flagella (data not shown). The ability of B. unamae strains to grow on different culture media and at different temperatures is reported in the species description (below). B. unamae strains exhibited good growth on BSE medium at pH 4·5–6·5, but poor growth was observed at pH 7·0–7·5. Phenotypic characteristics for the differentiation of B. unamae from other N2-fixing Burkholderia species, as well as from B. sacchari and from the type species of the genus Burkholderia, are shown in Table 2.
Results of the API 20NE biochemical tests for B. unamae strains are reported in the species description (below). These biochemical tests identified the isolates as B. cepacia (67·3 % confidence limits, based on the API analytical profile index), followed by Pseudomonas aureofaciens (confidence limits of 29·9 %). All B. unamae isolates grew and showed the ability to reduce acetylene in N-free, semi-solid BAz medium, as well as with succinate and propionate as carbon sources (Table 2). Hitherto, N2-fixing ability had been described only in B. vietnamiensis (Gillis et al., 1995), B. kururiensis (Estrada-de los Santos et al., 2001) and, recently, in ‘B. tropica’ (Reis et al., 2004), among all known species of the genus Burkholderia. Previously, we reported the ability of Burkholderia isolates corresponding to ARDRA genotypes 13, 14 and 15 to reduce acetylene to ethylene with different carbon sources, and also showed the presence of nifHDK genes in several of these isolates that were recovered from coffee plants (Estrada-de los Santos et al., 2001). These characteristics have been confirmed with 13 new isolates (Table 1) tested in the present study (data not shown), which confirms that the ability to fix nitrogen is a typical feature of the species B. unamae. In this framework, N2-fixing ability can be used as a distinctive feature for the delineation of Burkholderia species. On this basis, B. unamae can be differentiated from the most closely related species, B. sacchari, and from the type species, B. cepacia, by its ability to fix nitrogen. B. unamae can be differentiated from other diazotrophic Burkholderia species, except ‘B. tropica’, by its inability to fix nitrogen using benzoate as a carbon source. The assimilation profile of 49 carbon sources was identical among B. unamae strains (Table 3). B. unamae can be differentiated from the most closely related N2-fixing species, ‘B. tropica’, by its inability to assimilate 
-gentiobiose and ribose, and from B. sacchari by its ability to assimilate cellobiose, rhamnose and trehalose. Differences in the usage of carbon sources by B. unamae strains and other related Burkholderia species are shown in Table 3.
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Cells are straight rods (1·8–2·5 µm long and 0·5–0·8 µm wide) with a single flagellum or a polar tuft of four to eight flagella. Isolates are Gram-negative and oxidase- and catalase-positive. Growth and acetylene reduction to ethylene is observed with different carbon sources in N-free, semi-solid media. B. unamae strains grow on BAc plates, forming colonies that are yellowish, round, smooth and convex with entire margins. Isolates grew on agar media at 29 °C, but not at 42 °C. At 37 °C, they grew on BSE medium, but not on MacConkey agar medium. Strains did not grow on BCSA medium with or without vancomycin. Phenotypic characteristics for the differentiation of B. unamae from other N2-fixing Burkholderia species and related species of the genus Burkholderia are shown in Table 2. Nitrate is reduced to nitrite, but not to N2; there is urease activity, but not aesculin hydrolysis, liquefaction of gelatin or indole production. Additional phenotypic characteristics are listed in Table 3. All isolates showed the ability to produce siderophores. B. unamae can be differentiated phenotypically from all diazotrophic Burkholderia species and from B. sacchari and B. cepacia by its SDS-PAGE protein profile, electrophoretic mobility pattern of metabolic enzymes and fatty acid profile. B. unamae comprises strains with four different ARDRA genotypes and their 16S rDNA sequences show >99·2 % similarity. B. unamae can also be differentiated genomically from all diazotrophic Burkholderia species and from B. sacchari by its ARDRA and ribotype profiles.
The type strain is MTl-641T (=ATCC BAA-744T=CIP 107921T). This strain was isolated from the rhizosphere of maize cultivated in the fields in Tlayacapan, Morelos State, Mexico. Phenotypic and genomic characteristics of the type strain are the same as described above for the species.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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TOPABSTRACTMAIN TEXTREFERENCES |
|---|
Brämer, C. O., Vandamme, P., da Silva, L. F., Gomez, J. G. C. & Steinbüchel, A. (2001). Burkholderia sacchari sp. nov., a polyhydroxyalkanoate-accumulating bacterium isolated from soil of a sugar-cane plantation in Brazil. Int J Syst Evol Microbiol 51, 1709–1713.[Abstract]
Brett, P. J., DeShazer, D. & Woods, D. E. (1998). Burkholderia thailandensis sp. nov., a Burkholderia pseudomallei-like species. Int J Syst Bacteriol 48, 317–320.
Caballero-Mellado, J., Fuentes-Ramirez, L. E., Reis, V. M. & Martinez-Romero, E. (1995). Genetic structure of Acetobacter diazotrophicus populations and identification of a new genetically distant group. Appl Environ Microbiol 61, 3008–3013.[Abstract]
Coenye, T. & Vandamme, P. (2003). Diversity and significance of Burkholderia species occupying diverse ecological niches. Environ Microbiol 5, 719–729.[CrossRef][Medline]
Coenye, T., Laevens, S., Willems, A., Ohlén, M., Hannant, W., Govan, J. R. W., Gillis, M., Falsen, E. & Vandamme, P. (2001a). Burkholderia fungorum sp. nov. and Burkholderia caledonica sp. nov., two new species isolated from the environment, animals and human clinical samples. Int J Syst Evol Microbiol 51, 1099–1107.[Abstract]
Coenye, T., Mahenthiralingam, E., Henry, D., LiPuma, J. J., Laevens, S., Gillis, M., Speert, D. P. & Vandamme, P. (2001b). Burkholderia ambifaria sp. nov., a novel member of the Burkholderia cepacia complex including biocontrol and cystic fibrosis-related isolates. Int J Syst Evol Microbiol 51, 1481–1490.[Abstract]
Estrada-de los Santos, P., Bustillos-Cristales, R. & Caballero-Mellado, J. (2001). Burkholderia, a genus rich in plant-associated nitrogen fixers with wide environmental and geographic distribution. Appl Environ Microbiol 67, 2790–2798.
Gillis, M., Van, T. V., Bardin, R. & 7 other authors (1995). Polyphasic taxonomy in the genus Burkholderia leading to an emended description of the genus and proposition of Burkholderia vietnamiensis sp. nov. for N2-fixing isolates from rice in Vietnam. Int J Syst Bacteriol 45, 274–289.
Goris, J., Dejonghe, W., Falsen, E., De Clerck, E., Geeraerts, B., Willems, A., Top, E. M., Vandamme, P. & De Vos, P. (2002). Diversity of transconjugants that acquired plasmid pJP4 or pEMT1 after inoculation of a donor strain in the A- and B-horizon of an agricultural soil and description of Burkholderia hospita sp. nov. and Burkholderia terricola sp. nov. Syst Appl Microbiol 25, 340–352.[CrossRef][Medline]
Henry, D. A., Campbell, M. E., LiPuma, J. J. & Speert, D. P. (1997). Identification of Burkholderia cepacia isolates from patients with cystic fibrosis and use of a simple new selective medium. J Clin Microbiol 35, 614–619.[Abstract]
Kumar, S., Tamura, K., Jakobsen, I. B. & Nei, M. (2001) MEGA2: molecular evolutionary genetic analysis software. Bioinformatics 17, 1244–1245.
Martínez-Romero, E. & Caballero-Mellado, J. (1996). Rhizobium phylogenies and bacterial genetic diversity. Crit Rev Plant Sci 15, 113–140.
Reis, V. M., Estrada-de los Santos, P., Tenorio-Salgado, S. & 10 other authors (2004). Burkholderia tropica sp. nov., a novel nitrogen-fixing, plant-associated bacterium. Int J Syst Evol Microbiol (in press).
Saitou, N. & Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4, 406–425.[Abstract]
Schwyn, B. & Neilands, J. B. (1987). Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160, 47–56.[CrossRef][Medline]
Thompson, J. D., Higgins, D. G. & Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673–4680.
Vandamme, P., Pot, B., Gillis, M., de Vos, P., Kersters, K. & Swings, J. (1996). Polyphasic taxonomy, a consensus approach to bacterial systematics. Microbiol Rev 60, 407–438.
Vandamme, P., Holmes, B., Vancanneyt, M. & 8 other authors (1997). Occurrence of multiple genomovars of Burkholderia cepacia in cystic fibrosis patients and proposal of Burkholderia multivorans sp. nov. Int J Syst Bacteriol 47, 1188–1200.
Vandamme, P., Goris, J., Chen, W.-M., de Vos, P. & Willems, A. (2002a). Burkholderia tuberum sp. nov. and Burkholderia phymatum sp. nov., nodulate the roots of tropical legumes. Syst Appl Microbiol 25, 507–512.[CrossRef][Medline]
Vandamme, P., Henry, D., Coenye, T., Nzula, S., Vancanneyt, M., LiPuma, J. J., Speert, D. P., Govan, J. R. W. & Mahenthiralingam, E. (2002b). Burkholderia anthina sp. nov. and Burkholderia pyrrocinia, two additional Burkholderia cepacia complex bacteria, may confound results of new molecular diagnostic tools. FEMS Immunol Med Microbiol 33, 143–149.[CrossRef][Medline]
Viallard, V., Poirier, I., Cournoyer, B., Haurat, J., Wiebkin, S., Ophel-Keller, K. & Balandreau, J. (1998). Burkholderia graminis sp. nov., a rhizospheric Burkholderia species, and reassessment of [Pseudomonas] phenazinium, [Pseudomonas] pyrrocinia and [Pseudomonas] glathei as Burkholderia. Int J Syst Bacteriol 48, 549–563.
Yabuuchi, E., Kosako, Y., Oyaizu, H., Yano, I., Hotta, H., Hashimoto, Y., Ezaki, T. & Arakawa, M. (1992). Proposal of Burkholderia gen. nov. and transfer of seven species of the genus Pseudomonas homology group II to the new genus, with the type species Burkholderia cepacia (Palleroni and Holmes 1981) comb. nov. Microbiol Immunol 36, 1251–1275.[Medline]
Yabuuchi, E., Kawamura, Y., Ezaki, T., Ikedo, M., Dejsirilert, S., Fujiwara, N., Naka, T. & Kobayashi, K. (2000a). Burkholderia uboniae sp. nov., L-arabinose-assimilating but different from Burkholderia thailandensis and Burkholderia vietnamiensis. Microbiol Immunol 44, 307–317.[Medline]
Yabuuchi, E., Kawamura, Y., Ezaki, T., Ikedo, M., Dejsirilert, S., Fujiwara, N., Naka, T. & Kobayashi, K. (2000b). Burkholderia ubonensis corrig. (Burkholderia uboniae [sic]). In Validation of the Publication of New Names and New Combinations Previously Effectively Published Outside the IJSB, List No. 75. Int J Syst Bacteriol 50, 1415–1417.[Abstract]
Zhang, H., Hanada, S., Shigematsu, T., Shibuya, K., Kamagata, Y., Kanagawa, T. & Kurane, R. (2000). Burkholderia kururiensis sp. nov., a trichloroethylene (TCE)-degrading bacterium isolated from an aquifer polluted with TCE. Int J Syst Evol Microbiol 50, 743–749.[Abstract]
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| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| INT J SYST EVOL MICROBIOL | MICROBIOLOGY | J GEN VIROL |
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-D-glucoside, 5-ketogluconate, glycogen, inulin, lactose, D-lyxose, maltose, melibiose, melezitose, methyl