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Burkholderia Ambifaria Sp. Nov., a Novel Member of the Burkholderia Cepacia Complex Including Biocontrol and Cystic fibrosis-Related Isolates

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Burkholderia Ambifaria Sp. Nov., a Novel Member of the Burkholderia Cepacia Complex Including Biocontrol and Cystic fibrosis-Related Isolates International Journal of Systematic and Evolutionary Microbiology (2001), 51, 1481–1490 Printed in Great Britain Burkholderia ambifaria sp. nov., a novel member of the Burkholderia cepacia complex including biocontrol and cystic fibrosis-related isolates 1 Laboratorium voor Tom Coenye,1 Eshwar Mahenthiralingam,2 Deborah Henry,3 Microbiologie, 4 1 1 Universiteit Gent, K. L. John J. LiPuma, Severine Laevens, Monique Gillis, Ledeganckstraat 35, David P. Speert3 and Peter Vandamme1 B-9000 Ghent, Belgium 2 School of Biosciences, Cardiff University, Cardiff, Author for correspondence: Tom Coenye. Tel: j32 9 264 51 14. Fax: j32 9 264 50 92. UK e-mail: Tom.Coenye!rug.ac.be 3 Department of Pediatrics, Division of Infectious and A polyphasic taxonomic study, including amplified fragment length Immunological Diseases, University of British polymorphism (AFLP) fingerprinting, DNA–DNA hybridizations, DNA base-ratio Columbia, Vancouver, determinations, phylogenetic analysis, whole-cell fatty acid analyses and an British Columbia, Canada extensive biochemical characterization, was performed on 19 Burkholderia 4 Department of Pediatrics cepacia-like isolates from the environment and cystic fibrosis (CF) patients. and Communicable Several of the environmental isolates have attracted considerable interest due Diseases, University of Michigan Medical School, to their biocontrol properties. The polyphasic taxonomic data showed that the Ann Arbor, MI, USA strains represent a new member of the B. cepacia complex, for which the name Burkholderia ambifaria sp. nov. is proposed. The type strain is strain LMG 19182T. B. ambifaria can be differentiated from the other members of the B. cepacia complex by means of AFLP fingerprinting, whole-cell fatty acid analysis, biochemical tests (including ornithine and lysine decarboxylase activity, acidification of sucrose and β-haemolysis) and a newly developed recA gene-based PCR assay. 16S rDNA-based RFLP analysis and PCR tests allowed differentiation of B. ambifaria from Burkholderia multivorans, Burkholderia vietnamiensis and B. cepacia genomovar VI, but not from B. cepacia genomovars I and III and Burkholderia stabilis. The finding that this new taxon includes both strains isolated from CF patients and potentially useful biocontrol strains supports the general consensus that the large-scale use of biocontrol strains belonging to the B. cepacia complex would be ill-advised until more is known about their potential pathogenic mechanisms. Keywords: Burkholderia ambifaria, Burkholderia cepacia complex, cystic fibrosis, biocontrol, taxonomy INTRODUCTION least six different genomic species, referred to col- lectively as the B. cepacia complex (Vandamme et al., The taxonomy of Burkholderia cepacia-like organisms 1997; Coenye et al., 2001). One of these genomic has been evolving rapidly and it has been shown that species was identified as the previously described presumed B. cepacia strains isolated from cystic Burkholderia vietnamiensis (Gillis et al., 1995), and the fibrosis (CF) patients and the environment belong to at names Burkholderia multivorans and Burkholderia stabilis have been proposed for strains respectively ................................................................................................................................................. classified previously as B. cepacia genomovars II and Abbreviations: AFLP, amplified fragment length polymorphism; CF, IV (Vandamme et al., 1997, 2000). B. cepacia genom- cystic fibrosis. ovars III and VI still await formal binomial species The GenBank accession numbers for the recA gene sequences of B. ambifaria strains LMG 19182T, R-8863 and R-5142 and B. cepacia genomovar name assignment, pending the availability of differ- VI strain LMG 18943 are AF323985, AF143975, AF143801 and AF323971, ential phenotypic tests (Vandamme et al., 2000; respectively. Coenye et al., 2001). 01692 # 2001 IUMS 1481 T. Coenye and others Originally known as a plant pathogen, B. cepacia has DNA preparation. DNA used for AFLP fingerprinting, emerged as an important opportunistic pathogen and DNA–DNA hybridizations and determination of the DNA plays a significant role in patients with CF and chronic base composition was prepared as described by Pitcher et al. granulomatous disease (Gilligan, 1991; Speert et al., (1989). DNA used for PCR amplification of 16S rRNA and 1994; Govan & Deretic, 1996; Govan et al., 1996; recA genes was prepared by heating one or two colonies (picked from a plate grown overnight) at 95 C for 15 min in LiPuma, 1998a, b). B. cepacia has also attracted m 20 µl lysis buffer containing 0n25% (w\v) SDS and 0n05 M considerable commercial interest as a biological con- NaOH. Following lysis, 180 µl distilled water was added to trol, bioremediation and plant-growth-promoting the lysis buffer and the DNA solutions were stored at agent (Holmes et al., 1998; LiPuma & Mahen- k20 mC. thiralingam, 1999). Field tests have shown that B. AFLP fingerprinting. The preparation of template DNA cepacia-like organisms can colonize the rhizosphere of (using restriction enzymes ApaI and TaqI), amplification several economically important crops, including corn, [using primers A00 and T00 in the pre-selective PCR and maize, rice, pea, sunflower and radish, and can thereby primers B07 (labelled with the fluorescent dye 6-FAM) and increase the crop yield significantly (Parke et al., 1991; T11 in the selective PCR], separation of the fragments using McLoughlin et al., 1992; Bowers & Parke, 1993; an ABI Prism 377 automated DNA sequencer and numerical Hebbar et al., 1998). However, the risks associated analysis were performed as described previously (Coenye et with the use of B. cepacia are not yet clear, and there is al., 1999). a general consensus that the large-scale use of these 16S rRNA gene RFLP. Primers UNI1 and UNI2 were used for organisms would be ill-advised until more is known the amplification of a 1 kb fragment of the 16S rRNA gene about background environmental levels of the various (Mahenthiralingam et al., 2000). Restriction with the re- striction enzyme DdeI (New England Biolabs) and agarose members of the B. cepacia complex, the fate of gel electrophoresis were performed as described before biocontrol strains after environmental release, patho- (Segonds et al., 1999). genic mechanisms, clinical outcomes and the inter- rRNA-based PCR assays. Assays for the identification of action of introduced biocontrol strains with environ- members of the B. cepacia complex based on the rRNA mental and clinical strains (Govan & Vandamme, operon were described previously (LiPuma et al., 1999). The 1998; Holmes et al., 1998; LiPuma & Mahen- following primers were used: RHG-F and RHG-R (specific thiralingam, 1999; Vidaver et al., 1999; Govan et al., for all of the Burkholderia and Ralstonia species), PC-SSF 2000). and PC-SSR (specific for B. cepacia genomovars I and III and B. stabilis), BC-GII and BC-R (specific for B. multi- One of the most studied biocontrol isolates is B. vorans) and BC-V and BC-R (specific for B. multivorans and cepacia AMMD (l LMG 19182). This strain was B. vietnamiensis). isolated from apparently healthy pea plants in Determination of the DNA base composition. DNA was Wisconsin (USA) in 1985. Several studies have shown enzymically degraded into nucleosides as described by that strain LMG 19182 is very effective in controlling Mesbah et al. (1989). The nucleoside mixture obtained was phytopathogenic Pythium species (responsible for pre- then separated by HPLC using a Waters SymmetryShield C8 and post-emergence damping-off in peas) (Parke, column thermostatted at 37 mC. The solvent was 0n02 M 1990; Parke et al., 1991; Xi et al., 1996) and Aphano- NH%H#PO% (pH 4n0) with 1n5% acetonitrile. Non-meth- myces euteiches (responsible for root-rot and the main ylated lambda phage DNA (Sigma) was used as the factor limiting pea production in the American Mid- calibration reference. west) (King & Parke, 1993). DNA–DNA hybridizations. DNA–DNA hybridizations were performed with photobiotin-labelled probes in microplate In an ongoing survey of B. cepacia-like isolates by wells as described by Ezaki et al. (1989), using an HTS7000 means of whole-cell protein analysis, amplified frag- Bio Assay Reader (Perkin-Elmer) for the fluorescence ment length polymorphism (AFLP) fingerprinting and measurements. The hybridization temperature was 50 mC. sequence analysis of the recA gene, 18 isolates from Phylogenetic analysis of 16S rRNA gene sequences. The 16S human clinical and environmental specimens exhibited rDNA sequence of B. ambifaria strain LMG 19182T was similarity towards B. cepacia LMG 19182. This report retrieved from the GenBank database (accession no. describes the polyphasic taxonomic study that was AF043302) and compared with the published 16S rDNA used for the further characterization of these isolates. sequences of other Burkholderia species. A phylogenetic tree The genotypic and phenotypic characteristics allowed was constructed with the 2.1 software package the classification of these strains as a new member of (Applied Maths), based on the neighbour-joining method the B. cepacia complex, for which we propose the name (Saitou & Nei, 1987). Approximately 1460 bases were used Burkholderia ambifaria sp. nov. and all unknown bases were excluded from the calculations. recA gene sequencing and phylogenetic analysis. The sequences of the recA genes of B. ambifaria strains LMG METHODS 19182T, R-5142 and R-8863 were determined as described Bacterial strains and growth conditions. B. ambifaria strains previously
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