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Pseudomonas]Phenazinium, [Pseudomonas] Pyrrocinia and [Pseudomonas] Glathei As Burkholderia

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Pseudomonas]Phenazinium, [Pseudomonas] Pyrrocinia and [Pseudomonas] Glathei As Burkholderia international Journal of Systematic Bacteriology (1998), 48, 549-563 Printed in Great Britain Burkholderia graminis sp. nov., a rhizospheric Burkholderia species, and reassessment of [Pseudomonas]phenazinium, [Pseudomonas] pyrrocinia and [Pseudomonas] glathei as Burkholderia Vkronique Viallard,' Isabelle Poirier,' Benoit Cournoyer,' Jacqueline Haurat,' Sue Wiebkin,3 Kathy Ophel-Keller3 and Jacques Balandreaul Author for correspondence : VCronique Viallard. Tel: + 33 4 72 44 80 00. Fax: + 33 4 72 43 12 23. e-mail : lemsl @biomserv.univ-lyonl .fr 1 Laboratoire d'Ecologie In a survey of soil and wheat or maize rhizoplane bacteria isolated using a Microbienne du Sol, medium containing azelaic acid and tryptamine as sole carbon and nitrogen UMR5557 CNRS-Universit6 Lyon I, 43 Bd du 11 sources, respectively, a large proportion of Burkholderia-li ke bacteria were Novembre 1918, 69 622 found. Among them, a homogeneous group of strains was identifiable based Vi Ileurbanne cedex, France on phenotypic properties, fatty acid composition, DNA-DNA hybridizations 2 ENSBANA, Campus and 16s rDNA sequences. According to molecular data, this group belongs to Universitaire de the genus Burkholderia but its weak similarity to previously described species Montmuzard, 2 Bd Gabriel, 21000 Dijon, France suggests that it belongs to a novel species. Closest 16s rDNA phylogenetic neighbours of this species are Burkholderia caryophylli and two previously 3 SARDI Field Crops Pathology Unit, Waite named Pseudomonas species which clearly appear to be part of the Research Precinct, Glen Burkholderia genus and were thus named Burkholderia glathei comb. nov. and Osmond, SA 5064, Burkholderia phenazinium comb. nov. Strains of the new species are oxidase- Austra Iia and catalase-positive, produce indole and gelatinase, and use L-xylose, lactose, rhamnose, trehalose, D-lyxose, L-arabitol, xylitol and D-raff inose as sole carbon source. This novel taxon is named Burkholderia graminis. In the course of this study, [Pseudomonas] pyrrocinia also proved to be a member of the Burkholderia genus. Keywords : Burkholderia graminis sp. nov., genus Burkholderia, phenotypic analysis, genotypic analysis INTRODUCTION by Doudoroff & Palleroni (14), along with other bacteria that utilize arginine and betaine as sole carbon Pseudomonas cepacia was first mentioned by Ballard et source, such as Pseudomonas mallei, Pseudomonas al. (3) in 1970. This term was used for bacteria pseudomallei, Pseudomonas caryophylli and Pseudo- responsible for bulbiferous Aliaceae root rot diseases monas gladioli, formerly Pseudornonas marginata (3 1). which had been described in decaying onions in 1950 This grouping was consistent with that of Ballard et al. by Burkholder (8). In 1966, Stanier et al. (47) had (3) and Palleroni et al. (37) using rRNA-DNA already described a Pseudomonas species (Pseudo- hybridization. rnonas rnultivorans), which later on was recognized to be identical to P. cepacia by Palleroni & Holmes (36), In 1992, Yabuuchi et al. (61) proposed to assign these who validly described P. cepacia in 198 1. bacteria to a new genus, Burkholderia. As well as the above-mentioned species (i.e. Burkholderia caryo- This species was ascribed to section I1 of Pseudomonas phylli, Burkholderia cepacia, Burkholderia gladioli, Burkholderia mallei and Burkholderia pseudornallei), The GenBank accession numbers for the sequences reported in this paper two other [Pseudomonas]species were also included on are U96927-U96941. the basis of 16s rRNA sequences, DNA-DNA hybrid- 00647 0 1998 IUMS 549 V. Viallard and others ization studies, cellular lipids and fatty acids, and of Lyon (France) on an alluvial soil where maize is grown phenotypic properties ; these were Pseudomonas sola- continuously; isolates have been obtained from the soil and nacearum and Pseudomonas pickettii (40). Later on, Li the rhizoplane (washed roots, macerated and diluted) of et al. (60) came to the conclusion that the latter two germinating, flowering or senescent maize root systems. species and [Alcaligenes] eutrophus were a separate Kapunda is an experimental field, 80 km north of Adelaide (South Australia), where wheat is grown either continuously lineage and Gillis et al. (20) proposed that they were a or in rotation with a lupin-based pasture; the soil is an separate genus. In 1995, Yabuuchi et al. (62) validly alphisol. Walpeup is an experimental wheat-growing station, described Ralstonia solanacearum, Ralstonia pickettii situated in Victoria (Australia), on a very poor sandy soil, in and Ralstonia eutropha. Both genera belong to the a fixed sand dune system. Soil samples of the two Australian same rRNA group I1 of [Pseudomonas] as defined by stations have been collected and used for growing wheat (cv. Palleroni et al. (37). Spear) in pots under glasshouse conditions (three plants per pot containing 1.5 kg soil). After 3-4 weeks, wheat plants In 1994, Urakami et al. (53) transferred the [Pseudo- were harvested and used to isolate bacteria from their monas] species Pseudomonas glumae (28) and Pseudo- rhizoplane, as above. A few strains were isolated directly on monas plantarii (2) to the genus Burkholderia and also PCAT medium from salt-affected and hydrophobic soils described a new species, Burkholderia vandii. To these near Adelaide. Also included in Table 1 are 18 reference Burkholderia species, Gillis et al. (20) added a nitrogen- strains of Burkholderia, Pseudomonas, Ralstonia and Alca- fixing bacterium discovered in Vietnam rice fields ligenes. Among the eleven type strains of Burkholderia (49-5 1) known as Burkholderia vietnamiensis. They species, only type strains of B. mallei and B. pseudomallei also transferred to the genus Burkholderia the species were not grown in this laboratory. [Pseudomonas] andropogonis ( = woodsii) (48) and Biochemical characterization. All tests were performed at [Pseudomonas]cocovenenans (see also 63). 28 "C. The Biolog GN system was used as recommended by the manufacturer to test the oxidation of 95 carbon The genus Burkholderia currently comprises eleven substrates. Results were read automatically with a spectro- species ; Burkholderia andropogonis, B. caryophylli, B. photometer after 24 or 48 h incubation at 28 "C. To test the cepacia, Burkholderia cocovenenans, B. gladioli, Burk- reproducibility of the method, eight isolates were run in holderia glumae, B. mallei, Burkholderia plantarii, B. duplicate. Numerical analysis of the results was made using pseudomallei, B. vandii and B. vietnamiensis. This genus the GN Microlog 2N software which calculates Microlog belongs to the P-subclass of the Proteobacteria (59). distances derived from the number of differences between Most of the above-mentioned species appear in section strains. This software also permits clustering analysis using I1 of Pseudomonas in Bergey's Manual (39, whereas the UPGMA (unweighted mean pair group method) al- the others are in section V. The latter section included gorithm of Sneath & Sokal(44). species whose DNA or rRNA relatedness had not been Carbon substrate assimilation tests were performed using characterized in 1984. auxanographic API 50CH strips (bioMCrieux) as recom- mended by the manufacturer. Nine isolates were tested in During a field survey of B. cepacia populations in some duplicate. Numerical analysis was performed on data French and Australian agricultural soils (39), a large obtained after 7 d incubation. Interstrain distances were diversity of strains was isolated on PCAT agar (7), calculated using the coefficient of Dice and a phenogram was which is considered selective for B. cepacia. In com- built using UPGMA. parison with type strains from Burkholderia, Pseudo- The API 20NE microtube system (bioMCrieux) was used as monas and Ralstonia species, these isolates were a standardized method to test oxidase activity, nitrate characterized by phenotypic (Biolog, API, MIDI- reduction, gelatin and aesculin hydrolysis, glucose fermen- FAME) and genotypic (DNA-DNA hybridizations, tation, arginine dihydrolase activity and production of 16s rDNA sequencing) analyses. It became obvious indole, P-galactosidase and urease. that the isolates belonged to at least three, and possibly MIDI-FAME. The MIDI-FAME technique is based on the five or six, different Burkholderia species. One very conversion of fatty acids to methyl esters by mild alkaline homogeneous group (group A) existed among the methanolysis, followed by GLC analysis. Isolates were isolates and could not fit into any of the described grown overnight (1 6-1 8 h) on trypticase soy agar. Cells were Burkholderia or Pseudomonas species ; a novel species, removed from the plate using a plastic inoculating loop, Burkholderia graminis, is proposed. carefully scraped to avoid including medium in the sample. Cells were then transferred to glass tubes. In the first step, cells were saponified; 1 ml methanolic base (45 g NaOH, METHODS 150 ml methanol, 150 ml distilled water) was added before vortexing for 5-10 s and heating to 100 "C for 5 min. After Bacterial strains and medium. Strains used in this study are vortexing again, tubes were heated for a further 25 min at listed in Table 1. Unless otherwise stated, strains were 100 "C. Cells were then methylated as follows: after cooling isolated using PCAT medium [composition (in g 1-l) : in cold water, 2 ml methylation reagent (325 ml hydrochloric MgSO,, 0.1 ; azelaic acid, 2; tryptamine, 0.2; K,HPO,, 4; acid, 275ml methanol) was added and the tubes were KH,PO,, 4; yeast extract, 0.02 (pH 5.7)] (7). Only strains vortexed
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