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1 Laboratorium voor Microbiologie, Universiteit Gent, B-9000 Gent, Belgium
2 P. de Ecología Molecular y Microbiana, Centro de Investigación sobre Fijación de Nitrógeno, Universidad Nacional Autónoma de México, Cuernavaca, Morelos, Mexico
3 Center for Microbial Ecology, Michigan State University, East Lansing, MI 48824, USA
4 Culture Collection, Department of Clinical Bacteriology, University of Göteborg, S-413 46 Göteborg, Sweden
Correspondence
Johan Goris
gorisj{at}msu.edu
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ABSTRACT |
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7c, 16 : 17c, 16 : 0, 14 : 0 3OH, 16 : 0 3OH, 17 : 0 cyclo and 14 : 0 being the most abundant fatty acids. The G+C content of the species varies between 62·4 and 62·9 mol%. The type strain of B. xenovorans is LB400T (=LMG 21463T=CCUG 46959T=NRRL B-18064T).
Published online ahead of print on 9 July 2004 as DOI 10.1099/ijs.0.63101-0.
BOX-PCR patterns and ribotype profiles are available as supplementary material in IJSEM Online.
Present address: Center for Microbial Ecology, Michigan State University, East Lansing, MI 48824, USA. 
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MAIN TEXT |
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TOPABSTRACTMAIN TEXTREFERENCES |
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). Several Burkholderia strains have gained interest for their ability to degrade xenobiotic compounds, such as halogenated aromatics. One of the best-studied examples is Burkholderia sp. strain LB400T. This strain co-metabolizes many polychlorinated biphenyl (PCB) congeners when grown on biphenyl (Gibson et al., 1993). The pathways for degradation of PCBs by strain LB400T have been extensively characterized at both the genetic and the molecular level (e.g. Erickson & Mondello, 1992; Hofer et al., 1993) and have become a model system for the bacterial breakdown of these very persistent environmental contaminants (for a recent review on bacterial PCB degradation, see Furukawa, 2000).
Strain LB400T (=LMG 21463T=CCUG 46959T=NRRL B-18064T) was isolated from PCB-contaminated soil collected from a landfill in Moreau, New York, and originally identified as a Pseudomonas species (Bopp, 1986, 1989). It was referred to in more-recent scientific literature as Burkholderia sp. or Burkholderia cepacia (e.g. Bartels et al., 1999; Kumamaru et al., 1998; Seeger et al., 1999). The allocation of strain LB400T to the genus Burkholderia was confirmed in a recent taxonomic characterization by Fain & Haddock (2001). Furthermore, evidence provided by these authors excluded it from the B. cepacia complex. The actual species affiliation of strain LB400T, however, remained unclear.
In the course of a long-term study of the diversity of B. cepacia-like bacteria, two additional strains (CCUG 28445 and CAC-124) exhibited striking similarities with LB400T in SDS-PAGE whole-cell protein patterns. This prompted the polyphasic taxonomic study described below. Strain CCUG 28445 (=LMG 16224) was retrieved in 1991 from a human blood culture specimen, containing blood of a 31-year-old woman in Göteborg, Sweden. Strain CAC-124 (=LMG 21720=CCUG 46958) is a coffee plant rhizosphere isolate from Coatepec, Veracruz State, Mexico (Estrada-de los Santos et al., 2001). All three strains were grown aerobically on tryptic soy agar plates (Oxoid) at 28 °C.
The almost-complete (1466 bases) 16S rRNA gene sequence of strain LB400T was determined previously by P. C. K. Lau and H. Bergeron (unpublished data) and deposited in the EMBL sequence database under accession number U86373. This sequence was compared with those of other Burkholderia species using the BioNumerics software package version 3.0 (Applied Maths). A phylogenetic tree was constructed based on the neighbour-joining method, with bootstrap values based on 1000 resamplings (Fig. 1). As observed by Fain & Haddock (2001), strain LB400T clustered within the ‘Burkholderia graminis group’. Besides B. graminis, this group contains Burkholderia phenazinium, Burkholderia caribensis, several recently described species and a number of partially characterized Burkholderia isolates (Fig. 1). Strain LB400T showed the highest 16S rRNA gene sequence similarity (98·6 %) to the type strains of B. graminis and Burkholderia terricola and to Burkholderia sp. strain N3P2. The latter strain was isolated from soil contaminated with polycyclic aromatic hydrocarbons (Mueller et al., 1997).
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). DNA–DNA hybridization experiments were done in microplates (Willems et al., 2001) at a hybridization temperature of 55 °C. DNA–DNA reassociation experiments were performed with strains LB400T, CCUG 28445, CAC-124 and with the type strains of the closest-related Burkholderia species, as evidenced by 16S rRNA gene sequence data (Table 1). DNA–DNA hybridization values between the former three strains were above 70 %, indicating a relationship at the species level (Stackebrandt et al., 2002; Wayne et al., 1987). In contrast, low to intermediate hybridization values (mean of reciprocal values 
35 %) were obtained in hybridizations of strain LB400T with type strains of other Burkholderia species. The G+C values (mol%) of Burkholderia type strains and DNA–DNA hybridization values (Table 1) were very similar to those reported previously (Achouak et al., 1999; Coenye et al., 2001; Goris et al., 2002; Viallard et al., 1998).
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, with cultivation conditions and analysis parameters as reported by Coenye et al. (2001). Repetitive-element PCR fingerprinting with the BOXA1R primer was performed using the protocol of Rademaker & De Bruijn (1997), with some minor modifications (Goris et al., 2002). For ribotyping, a Southern blot of total EcoRI DNA digests was hybridized with a HindIII–HindIII 700 bp internal fragment from Escherichia coli rrnB 16S rRNA genes cloned in pKK3535 (Brosius et al., 1981). ARDRA and analysis of nifHDK hybridization patterns were performed as described previously (Estrada-de los Santos et al., 2001). Strains CCUG 28445, CAC-124 and LB400T showed striking similarities in their whole-cell protein and ARDRA profiles (data not shown), ribotypes (autoradiogram provided as supplementary material in IJSEM Online) and BOX-PCR patterns (see supplementary material in IJSEM Online). In addition, each of these profile types was useful to distinguish the three strains from their nearest phylogenetic neighbours. The BOX-PCR patterns showed minor differences in DNA fragments at positions corresponding to 1200, 970 and 790 bp (see supplementary material in IJSEM Online). Likewise, the ARDRA profile obtained with enzyme HhaI from strain CCUG 28445 was slightly different from strains LB400T and CAC-124 (data not shown). These differences indicated that the strains represent different genetic clones.
Classical phenotypic tests were performed as described previously (Vandamme et al., 1993). API 20 NE and API ZYM (bioMérieux) microtest galleries were utilized according to the protocol supplied by the manufacturer. Several additional characteristics were determined. Prior to the acetylene reduction activity (ARA) assays (Mascarua-Esparza et al., 1988), strains were grown in nitrogen-free semi-solid BMGM medium (Estrada-de los Santos et al., 2001) for 3 days at 29 °C. The utilization of xenobiotic compounds was examined in a minimal medium (K1), which has been used previously to study degradation of PCBs by bacteria including strain LB400T (Maltseva et al., 1999; Zaitsev & Karasevich, 1985). Growth on naphthalene, toluene and phenol was assessed on K1 agar plates, while growth on benzoate was tested in liquid K1 medium. Growth on biphenyl was evaluated both on K1 agar plates with biphenyl provided as a vapour from solid particles in the lid of the Petri dish and in liquid K1 medium containing 5 mM biphenyl. Plates and liquid medium were incubated for up to 21 days at 30 °C. Degradation of PCBs was evaluated using the resting-cell assay as described by Bedard et al. (1986). Prior to the resting-cell assay, cells were grown in liquid medium containing 5 mM biphenyl, 5 mM benzoate or both. For fatty acid methyl ester (FAME) analysis, cells were grown for 24 h on tryptic soy agar plates (Oxoid) at 28 °C and FAMEs were extracted, prepared, separated and identified using the Microbial Identification System (Microbial ID) as reported previously (Vauterin et al., 1991).
Phenotypic traits useful for the differentiation of strains LB400T, CCUG 28445 and CAC-124 from closely related Burkholderia species are summarized in Table 2. Remarkably, the three strains differed from nearly all Burkholderia strains in their inability to assimilate L-arabinose. All three showed ARA and the presence of nifHDK genes was confirmed (data not shown). The sizes of hybridization bands corresponding to nifHDK genes were identical in the three strains. Previously, ARA assays revealed that strain CAC-124 was capable of fixing N2 with benzoate as the single carbon source (Estrada-de los Santos et al., 2001), and this ability with this carbon source was also observed for strains LB400T and CCUG 28445 (data not shown). Furthermore, the three strains were able to grow on benzoate, with doubling times of approximately 2·5 h. None of the strains grew on naphthalene, toluene or phenol. LB400T was the only strain that grew on biphenyl. PCB degradation was tested for cells grown on K1 medium containing both benzoate and biphenyl and was observed only for strain LB400T. We can therefore conclude that, although strains CAC-124 and CCUG 28445 are highly related to strain LB400T, they do not share the unique biodegrading capacities of this strain.
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Description of Burkholderia xenovorans sp. nov.
Burkholderia xenovorans [xe.no'vo.rans. Gr. adj. xenos foreign; L. part. pres. vorans devouring, digesting; N.L. part. adj. xenovorans digesting foreign (xenobiotic) compounds].
Cells are Gram-negative, motile, non-sporulating, straight rods (1–2 µm long and 0·5 µm wide). The strains grow on nutrient agar at 28 °C, but not at 42 °C. No growth is observed on N-cetyl-N,N,N-trimethylammonium bromide (cetrimide) or on 10 % (w/v) lactose. The strains do not grow in the presence of acetamide or in the presence of 3·0, 4·5 or 6·0 % (w/v) NaCl. Growth in the presence of 0·5 or 1·5 % (w/v) NaCl is strain-dependent (negative for the type strain). All strains grow on blood agar at 30 °C and on Drigalski agar, while growth on blood agar at 37 °C is strain-dependent (negative for the type strain). Haemolysis of horse blood is not observed. Liquefaction of gelatin or hydrolysis of aesculin is not observed. Tween 80 is hydrolysed. No production of acid or H2S in triple-sugar-iron agar, no indole or pigment production. Acetylene is reduced. Nitrate and nitrite reduction is strain-dependent (negative for the type strain). In O–F medium, D-glucose, D-fructose and D-xylose are oxidized, but not maltose or adonitol. D-Glucose is not fermented. Assimilation of D-glucose, DL-norleucine, D-mannose, D-mannitol, N-acetyl-D-glucosamine, D-gluconate, caprate, adipate, L-malate, citrate, phenyl acetate, DL-lactate and DL-lactate with methionine, but not of trehalose, L-arabinose, maltose or sucrose. Assimilation of L-arginine is strain-dependent (positive for the type strain). Catalase, oxidase, alkaline and acid phosphatase, esterase C4, ester lipase C8, leucine arylamidase and phosphoamidase activity is present. Amylase, DNase, lipase C14, tryptophanase, lysine decarboxylase, ornithine decarboxylase, trypsin, chymotrypsin, 
-galactosidase, 
-galactosidase, -glucuronidase, - and -glucosidase, N-acetyl--glucosaminidase, -mannosidase, -fucosidase and arginine dihydrolase activity are not detected. Activities of urease, valine arylamidase and cysteine arylamidase are strain-dependent (enzyme activities are, respectively, absent, present and present in the type strain). The whole-cell fatty acid profile comprises 14 : 0 (4·7 %), 14 : 0 3OH (8·5 %), 16 : 17c (19·1 %), 16 : 0 (18·2 %), 17 : 0 cyclo (5·1 %), 16 : 1 2OH (2·2 %), 16 : 0 2OH (2·2 %), 16 : 0 3OH (7·1 %), 18 : 17c (27·3 %), 18 : 0 (0·5 %), 19 : 0 cyclo 8c (3·6 %) and 18 : 1 2OH (0·9 %) as major components [summed feature 2 (comprising 14 : 0 3OH, 16 : 1 iso I, an unidentified fatty acid with equivalent chain-length value of 10·928 or 12 : 0 ALDE or any combination of these fatty acids) and summed feature 3 (comprising 16 : 17c or 15 iso 2OH or both) are mentioned above as 14 : 0 3OH and 16 : 17c, respectively, as these fatty acid have been reported in Burkholderia species (Stead, 1992)]. The G+C content varies between 62·4 and 62·9 mol%.
The type strain (LB400T=LMG 21463T=CCUG 46959T=NRRL B-18064T) was isolated from a PCB-contaminated soil collected from a landfill in Moreau, New York. The G+C content of the type strain is 62·6 mol%.
Currently, whole-genome sequence analysis of strain LB400T is in progress (http://genome.jgi-psf.org/draft_microbes/burfu/burfu.home.html).
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ACKNOWLEDGEMENTS |
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J. Gescher, W. Ismail, E. Olgeschlager, W. Eisenreich, J. Worth, and G. Fuchs Aerobic Benzoyl-Coenzyme A (CoA) Catabolic Pathway in Azoarcus evansii: Conversion of Ring Cleavage Product by 3,4-Dehydroadipyl-CoA Semialdehyde Dehydrogenase. J. Bacteriol., April 1, 2006; 188(8): 2919 - 2927. [Abstract] [Full Text] [PDF]
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M. Zielinski, S. Kahl, C. Standfuss-Gabisch, B. Camara, M. Seeger, and B. Hofer Generation of Novel-Substrate-Accepting Biphenyl Dioxygenases through Segmental Random Mutagenesis and Identification of Residues Involved in Enzyme Specificity. Appl. Envir. Microbiol., March 1, 2006; 72(3): 2191 - 2199. [Abstract] [Full Text] [PDF]
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M. Sota, H. Yano, Y. Nagata, Y. Ohtsubo, H. Genka, H. Anbutsu, H. Kawasaki, and M. Tsuda Functional Analysis of Unique Class II Insertion Sequence IS1071 Appl. Envir. Microbiol., January 1, 2006; 72(1): 291 - 297. [Abstract] [Full Text] [PDF]
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V. J. Denef, J. A. Klappenbach, M. A. Patrauchan, C. Florizone, J. L. M. Rodrigues, T. V. Tsoi, W. Verstraete, L. D. Eltis, and J. M. Tiedje Genetic and Genomic Insights into the Role of Benzoate-Catabolic Pathway Redundancy in Burkholderia xenovorans LB400 Appl. Envir. Microbiol., January 1, 2006; 72(1): 585 - 595. [Abstract] [Full Text] [PDF]
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V. J. Denef, M. A. Patrauchan, C. Florizone, J. Park, T. V. Tsoi, W. Verstraete, J. M. Tiedje, and L. D. Eltis Growth Substrate- and Phase-Specific Expression of Biphenyl, Benzoate, and C1 Metabolic Pathways in Burkholderia xenovorans LB400 J. Bacteriol., December 1, 2005; 187(23): 7996 - 8005. [Abstract] [Full Text] [PDF]
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A. Ramette, J. J. LiPuma, and J. M. Tiedje Species Abundance and Diversity of Burkholderia cepacia Complex in the Environment Appl. Envir. Microbiol., March 1, 2005; 71(3): 1193 - 1201. [Abstract] [Full Text] [PDF]
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U. Rein, R. Gueta, K. Denger, J. Ruff, K. Hollemeyer, and A. M. Cook Dissimilation of cysteate via 3-sulfolactate sulfo-lyase and a sulfate exporter in Paracoccus pantotrophus NKNCYSA Microbiology, March 1, 2005; 151(3): 737 - 747. [Abstract] [Full Text] [PDF]
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M. Valdes, N.-O. Perez, P. Estrada-de los Santos, J. Caballero-Mellado, J. J. Pena-Cabriales, P. Normand, and A. M. Hirsch Non-Frankia Actinomycetes Isolated from Surface-Sterilized Roots of Casuarina equisetifolia Fix Nitrogen Appl. Envir. Microbiol., January 1, 2005; 71(1): 460 - 466. [Abstract] [Full Text] [PDF]
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