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1 Universidade Federal Rural do Rio de Janeiro, km 45, BR 465, C.P. 74505, Seropédica, Rio de Janeiro, Brazil
2 Embrapa Agrobiology, km 47, BR 465, C.P. 74505, Seropédica, Rio de Janeiro, Brazil
3 Centro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Ap. Postal 565-A, Cuernavaca, Morelos, Mexico
Correspondence
J. Caballero-Mellado
jesuscab{at}cifn.unam.mx
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The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of strains SRMrh-20T, SRCL-18, SRMrh-85 and PPCR-2 are AY965240–AY965243, respectively.
A dendrogram derived from MLEE and SDS-PAGE showing whole-cell protein profiles for the novel strains, N2-fixing Burkholderia species and B. sacchari are available as supplementary figures in IJSEM Online.
These authors contributed equally to this work. 
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). Coenye & Vandamme (2003) reported that the genus Burkholderia included over 30 species, but N2-fixing species were poorly represented in the genus until recently. Nitrogen fixation, the reduction of atmospheric N2 to ammonia, was reported only for Burkholderia vietnamiensis (Gillis et al., 1995) of all the species of the genus. Nevertheless, a study by Estrada-de los Santos et al. (2001) showed that Burkholderia could be a genus rich in plant-associated nitrogen-fixers. In that study, Burkholderia kururiensis (Zhang et al., 2000) was identified as a diazotrophic species, and many N2-fixing isolates recovered from different plants (maize, coffee and sorghum) or their rhizospheres have subsequently been classified within novel Burkholderia species, including Burkholderia unamae (Caballero-Mellado et al., 2004), Burkholderia xenovorans (Goris et al., 2004) and Burkholderia tropica (Reis et al., 2004). Concomitantly, two nodulating N2-fixing strains recovered from legume plants were assigned to the genus Burkholderia according to their 16S rRNA gene sequences (Moulin et al., 2001), and later they were formally classified as Burkholderia phymatum and Burkholderia tuberum (Vandamme et al., 2002). The ability of several as yet unnamed strains to form nodules on Macroptilium atropurpureum, on Mimosa species (including Mimosa pigra) and on other mimosoid legumes probably indicates that these micro-organisms represent novel Burkholderia species (Barrett & Parker, 2005, 2006; Chen et al., 2005). It is worth noting that the diazotrophic Burkholderia species, with the exception of B. vietnamiensis, comprise a group of closely related species that are distant from the group of opportunistic pathogens referred to as the Burkholderia cepacia complex, which includes B. vietnamiensis (Coenye & Vandamme, 2003).
In the present study, a polyphasic approach was undertaken to determine the taxonomic status of diazotrophic isolates tentatively designated as the Burkholderia NAR group. These include isolates from sugar-cane and maize plants reported by Perin et al. (2006) together with novel strains isolated from other sugar-cane varieties grown in different geographical regions of Brazil. A detailed analysis confirmed that these isolates belong to a novel species within the genus Burkholderia.
The sources of the 21 N2-fixing Burkholderia isolates that were analysed are shown in Table 1. Eleven of these strains were described previously (Perin et al., 2006); they correspond to those tentatively named as Burkholderia NAR isolates. In a previous study, diazotrophic isolates were obtained using both nitrogen-free semi-solid BAz and JMV media for enrichment, and BAc agar plates for the isolation and purification of isolates as described previously (Perin et al., 2006). In the present study, nitrogen-free semi-solid JMV (pH 5.2) and LGI (pH 6.0) media (Perin et al., 2006) were used for enriching diazotrophic bacteria, and the strains were purified in JMV and LGI agar plates containing yeast extract (100 and 20 mg l–1, respectively). Nitrogenase activity (N2 fixation) was confirmed in pure cultures by the acetylene-reduction method (Burris, 1972). The presence of nifH genes was determined with primers IGK (Poly et al., 2001) and NDR-1 (Valdés et al., 2005), using PCR-amplification conditions as described by Perin et al. (2006). Although many novel N2-fixing Burkholderia isolates from each sample (rhizosphere or plant tissues) were obtained, only one representative strain, based on amplified rDNA restriction analysis (ARDRA) as described below, from each sample was included in the present study. Earlier, we had reported that the Burkholderia NAR isolates reduce acetylene to ethylene and also that nifH genes were present in several of these isolates recovered from maize and sugar-cane plants (Perin et al., 2006). These characteristics are confirmed in the novel isolates examined in the present study (data not shown), thereby confirming that they all possess the ability to fix nitrogen.
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. Each isolate was assigned to one ARDRA genotype as described previously (Estrada-de los Santos et al., 2001). Many isolates had an ARDRA profile that was identical (data not shown) to those of micro-organisms designated as Burkholderia NAR strains (Perin et al., 2006), thus confirming the prevalence of this N2-fixing group in association with sugar cane in Brazil. Previously, 16S rRNA gene sequences were obtained from strains SRMrh-20T, SRMrh-85 and SRCL-318 (Perin et al., 2006) and deposited in the GenBank/EMBL database (accession numbers are shown in Fig. 1). In the present study, the 16S rRNA gene sequence was obtained from a novel isolate, strain PPCR-2. Remarkably, the 16S rRNA gene sequence of strain PPCR-2, isolated from the roots of sugar cane var. RB 85-5113, grown in Paraná State (1100 km from Rio de Janeiro), showed 100 % similarity with those of strains SRMrh-20T and SRMrh-85, both of which had been isolated from maize cultivated in Rio de Janeiro (Perin et al., 2006), and with the sequence from an unidentified strain designated AB48 (GenBank accession no. AF164043), originally isolated from pineapple (Ananas comosus) in Bahia (Cruz et al., 2001). This confirmed that all of these strains belong to the same species. In addition, this result suggests that ARDRA profiles can be used successfully to differentiate the novel isolates from other Burkholderia species. A neighbour-joining phylogenetic tree based on available 16S rRNA gene sequences from Burkholderia species is shown in Fig. 1. It illustrates the position of five of the novel strains recovered during different seasons and from diverse plants and geographical regions of Brazil. Burkholderia sacchari, a non-diazotrophic species, and B. unamae and B. tropica, two N2-fixing bacteria, were closely related to the cluster constituted by the novel strains (97.1, 96.9 and 96.8 % identity, respectively). The novel strains constituted a cluster that is significantly distant from the cluster formed by the diazotroph B. vietnamiensis (<96 % identity) and other species included in the B. cepacia complex (Fig. 1).
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) for 12 h at 29 °C. Thereafter, the cultures were centrifuged and resuspended in fresh medium and the cell number was adjusted as described previously (Caballero-Mellado et al., 2004). An aliquot (10 µl) from each culture was streaked on solid medium and incubated for 72 h at 29 °C, unless otherwise indicated. The temperature effects on growth were determined on BSE agar medium. Growth on BAc agar plates (Estrada-de los Santos et al., 2001), MacConkey agar (Difco) plates and on B. cepacia selective agar medium (Henry et al., 1997) was also determined. Growth of Burkholderia isolates using 1-aminocyclopropane-1-carboxylic acid as the sole nitrogen source was examined on Az-Acc medium as described previously (Caballero-Mellado et al., 2004). In addition, phenotypic tests to determine nitrate reduction, gelatin liquefaction, aesculin hydrolysis and urease activity were performed with the API 20NE system, according to the instructions of the manufacturer (bioMérieux). The oxidase reaction was assayed as described by Caballero-Mellado et al. (2004). The assimilation of 49 carbon sources was determined with the API 50 CH system and CHB medium (bioMérieux), and the results were obtained after 5 days at 29 °C. Acetylene-reduction activity with succinate, benzoate and propionate as single carbon sources was assayed as described previously (Estrada-de los Santos et al., 2001). Two replicates were used in each test. MLEE and SDS-PAGE assays 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 at 29 °C.
Colonies produced by the novel isolates on JMV agar plates were round, cream-coloured with yellow in the centre, smooth, convex with entire margins and were 2–3 mm in diameter. Phenotypic characteristics useful for differentiating the novel strains from the most closely related species, B. sacchari, and from diazotrophic Burkholderia species are summarized in Table 2. The novel strains differ from B. sacchari in their ability to reduce acetylene to ethylene and they differ from all diazotrophic Burkholderia species by their poor ability to fix nitrogen when using propionate as a carbon source. All of the novel strains showed the same assimilation profile for 49 carbon sources. Differences in the utilization of carbon sources among N2-fixing Burkholderia species and B. sacchari are summarized in Table 3. Notably, the novel strains differ from all diazotrophic Burkholderia species (except B. vietnamiensis) by their ability to use sucrose as a carbon source; they differ from B. vietnamiensis by their ability to use adonitol and rhamnose.
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).
The SDS-PAGE protein patterns of some representative novel strains isolated from different plants and geographical regions are shown in Supplementary Fig. S2 (available in IJSEM Online). The 21 strains analysed showed almost identical protein profiles, but strains AB-48 and SRCL-318 (having identical profiles) showed slight differences with respect to the other strains. However, the protein profiles of the novel strains were clearly distinct from those of the N2-fixing Burkholderia species examined and from that of their closest relative, B. sacchari (Supplementary Fig. S2). It is well established that bacteria with identical or very similar protein patterns possess high levels of genome similarity (Vandamme et al., 1996). On this basis, the SDS-PAGE results confirm that the novel isolates represent a novel diazotrophic species.
Three strains were analysed for their cellular fatty acid compositions. The strains were grown in trypticase soy broth agar at 28 °C for 24 h and the analysis was performed by Microbial ID, Inc. (Newark, DE, USA). Strains SRMrh-20T, SRCL-318 and PPCR-2 had almost identical fatty acid profiles, but slight quantitative variations were observed. The major fatty acid components (means and standard deviations based on the profiles of three strains) were as follows: 14 : 0 (4.6±0.4 %), 16 : 0 (26.5±1.9 %), 16 : 0 2-OH (2.7±0.1 %), 16 : 0 3-OH (4.9±0.7 %), 16 : 1 2-OH (1.9±0.3 %), 17 : 0 cyclo (17.2±3.5 %), 18 : 1
7c (14.0±4.5 %), 18 : 1 2-OH (1.0±0.2 %), 19 : 0 cyclo 8c (11.7±2.0 %), summed feature 2 (5.8±0.7 %) and summed feature 3 (5.3±2.0 %). Summed feature 2 corresponds to 14 : 0 3-OH, 16 : 1 iso I (an unknown fatty acid with an equivalent chain-length of 10.947) or 12 : 0 alde or any combination of these fatty acids. Summed feature 3 corresponds to 16 : 17c and/or 16 : 16c. These profiles are similar to the fatty acids reported for other Burkholderia species (Vandamme et al., 1997; Coenye et al., 2001b), except for the component 16 : 16c. The fatty acid profile of the novel strains showed clear quantitative differences from those of N2-fixing Burkholderia species, and from that of the phylogenetically closest species, B. sacchari (Table 2
). For example, the novel isolates contain relatively small amounts of 18 : 17c and summed feature 3 and relatively large amounts of 19 : 0 cyclo 8c in comparison with diazotrophic Burkholderia species and B. sacchari. This could be useful for identification of the species represented by the novel strains.
DNA–DNA reassociation experiments were based on relative levels of hybridization to 32P-labelled DNA from novel strain SRMrh-20T, as described previously (Estrada-de los Santos et al., 2001). DNA–DNA relatedness assays were performed with eight novel strains as well as with the type strain of B. sacchari, the most closely related Burkholderia species (as indicated by 16S rRNA gene sequence data), and other N2-fixing Burkholderia species. The DNA–DNA reassociation values between strain SRMrh-20T and other novel strains were in the range 75–102 % (SRMrh-85, 102 %; SRCL-327, 99 %; PPCrh-15, 96 %; SRMrh-77, 86 %; AB48, 83 %; SRCL-18, 79 %; PPCR-2, 78 %; PPCR-3, 75 %), indicating a relationship at the species level (Stackebrandt et al., 2002; Vandamme et al., 1996). In contrast, low reassociation values (below 30 %) were obtained in hybridizations of strain SRMrh-20T with B. sacchari LMG 19450T (=IPT101T) (30 %) and N2-fixing Burkholderia species such as B. unamae MTl-641T (28 %), B. tropica Ppe8T (27 %), B. kururiensis KP23T (22 %), B. xenovorans LMG 21463T (=LB-400T) (21 %), B. vietnamiensis TVV75T (19 %), B. tuberum STM678T (14 %) and B. phymatum STM815T (13 %). These DNA–DNA reassociation data, together with the 16S rRNA gene sequence analyses, SDS-PAGE protein patterns, MLEE assay data and fatty acid profiles, support the notion that diazotrophic isolates previously and tentatively named as the Burkholderia NAR group (Perin et al., 2006) belong to a novel species within the genus Burkholderia, for which we propose the name Burkholderia silvatlantica sp. nov.
Description of Burkholderia silvatlantica sp. nov.
Burkholderia silvatlantica (sil.vat.lan'ti.ca. L. n. silva wood, forest; L. fem. adj. Atlantica pertaining to the Atlas Mountains and by extension to the Atlantic Ocean; N.L. fem. adj. silvatlantica pertaining to the Atlantic forest of Brazil).
Cells are straight rods (1.6–1.9 µm long and 0.8–0.9 µm wide), each having a polar tuft of flagella. Isolates are Gram-negative and oxidase- and catalase-positive. Growth and nitrogenase activity are observed with different carbon sources in nitrogen-free LGI, JMV and BAz semi-solid media. Strains grown on JMV agar plates produce colonies that are round, cream-coloured with yellow in the centre, smooth, convex with entire margins and that are 2–3 mm in diameter. Grows on BSE medium at 29 and 37 °C, but not at 42 °C. Does not grow on MacConkey agar or B. cepacia selective agar medium at 29 or 37 °C. Phenotypic characteristics useful for differentiation from other N2-fixing Burkholderia species and the most closely related species, B. sacchari, are shown in Table 2. Nitrate is reduced to nitrite but not to N2; there is urease activity and aesculin hydrolysis, but not liquefaction of gelatin or indole production. Additional phenotypic characteristics are listed in Table 3. Can be differentiated phenotypically from all diazotrophic Burkholderia species and from B. sacchari on the basis of SDS-PAGE protein profiles, the electrophoretic mobility patterns of metabolic enzymes and fatty acid profiles. Strains SRMrh-20T, SRMrh-85, PPCR-2 and AB48 show 100 % similarity among their 16S rRNA gene sequences and show 99.77 % similarity to strain SRCL-318. Can also be differentiated genomically from all diazotrophic Burkholderia species, and from B. sacchari, by ARDRA profiles.
The type strain, SRMrh-20T (=LMG 23149T=ATCC BAA-1244T), was isolated from the rhizosphere of maize var. Avantis A2345, cultivated in the Experimental Campus of Embrapa Agrobiology in Seropédica, Rio de Janeiro, Brazil. The phenotypic and genomic characteristics of the type strain are the same as those described above for the species.
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ACKNOWLEDGEMENTS |
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-D-glucoside, 2-ketogluconate, 5-ketogluconate, glycogen, inulin, lactose, D-lyxose, maltose,melibiose, melezitose, methyl