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1 Centro Nacional de Pesquisa de Agrobiologia (EMBRAPA-Agrobiologia), km 47, Seropédica, 23851-970, CP 74505, Rio de Janeiro, Brazil
2 Centro de Investigación sobre Fijación de Nitrógeno, Universidad Nacional Autónoma de México, Ap. Postal 565-A, Cuernavaca, Morelos, México
3 SASA Experiment Station, Private Bag X02, Mt Edgecombe, KZN, 4300 South Africa
4 GSF – National Research Center for Environment and Health, Institute of Soil Ecology, Department of Rhizosphere Biology, Ingolstädter Landstr.1, D-85764 Neuherberg/Munich, Germany
5 Ecologie Microbienne, UMR CNRS 5557 Université Claude Bernard Lyon I, 43 Bd du 11 Novembre 1918, 69622 Villeurbanne cedex, France
Correspondence
J. Caballero-Mellado
jesuscab{at}cifn.unam.mx
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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V. M. Reis and P. Estrada-de los Santos contributed equally to this study. 
The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequences of the Burkholderia tropica strains determined in this work are AJ420332, AY128103, AY321306, AY128105 and AY128104.
Detailed Biolog results, ARDRA profiles and an extended 16S rRNA gene-based phylogenetic tree are available as supplementary material in IJSEM Online.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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). 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). This species was isolated from the rhizosphere of young rice plants grown on a Vietnamese soil under laboratory conditions (Trân Van et al., 1994). Concomitant with the creation of the genus Burkholderia in the early 1990s, diazotrophic bacteria were obtained in a survey of root-associated diazotrophs in sugarcane grown in Brazil, and the first indication of their affiliation to the genus Burkholderia was gained from partial 23S rRNA gene sequences (Hartmann et al., 1995). On the basis of the 23S rRNA gene sequence data, an oligonucleotide probe (PPe8) was developed, which was characteristic of these isolates (Kirchhof et al., 1997). Among diazotrophic isolates obtained from the banana and pineapple rhizosphere in Brazil, several grouped within the genus Burkholderia using 23S rRNA gene oligonucleotide probing and phenotypic techniques (Weber et al., 1999). Two isolates from pineapple showed an amplified 16S rDNA restriction analysis (ARDRA) pattern identical to the sugarcane isolate Ppe8T (Cruz et al., 2001). Recently, the analysis of N2-fixing bacteria associated with maize and coffee plants grown under field conditions revealed the presence of B. vietnamiensis, as well as the richness of novel diazotrophic bacterial species belonging to the genus Burkholderia (Estrada-de los Santos et al., 2001; Estrada et al., 2002). These N2-fixing isolates exhibited high diversity in the ARDRA profiles. In addition, two nodulating strains recovered from legume plants were recently assigned to the genus Burkholderia according to their 16S rRNA gene sequences (Moulin et al., 2001). These strains have been formally described as Burkholderia tuberum and Burkholderia phymatum (Vandamme et al., 2002). In this study, a polyphasic approach was undertaken to determine the taxonomic status of bacterial isolates recovered from sugarcane, maize and teosinte plants grown in different geographical and climatic regions of Brazil, Mexico and South Africa. The analysis revealed that these isolates belong to a novel species within the genus Burkholderia, for which the name Burkholderia tropica sp. nov. is proposed.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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. N2-fixing Burkholderia isolates were recovered using three different strategies. In Mexico, the diazotrophic isolates were recovered from the rhizosphere, rhizoplane and inner tissues of maize and teosinte plants using the nitrogen-free semi-solid BAz medium and BAc agar plates as described previously (Estrada-de los Santos et al., 2001). In Brazil, diazotrophic bacteria were isolated from sugarcane in nitrogen-free semi-solid LGI-P medium containing cane juice (Reis et al., 1994). Stems and roots of the sugarcane plants were washed and then macerated and aliquots were inoculated into vials containing semi-solid LGI-P medium. After incubation for 4–5 days at 30 °C, a fine subsurface pellicle was formed. The contents of vials showing pellicles were transferred to semi-solid JMV medium with the following composition (g l–1): 5·0 mannitol, 0·6 K2HPO4, 1·8 KH2PO4, 0·2 MgSO4.7H2O, 0·1 NaCl, 0·02, CaCl2.2H2O, 0·05 yeast extract, 1·6 agar, adjusted to pH 5·5–5·7. New growth was streaked out on JMV or LGI-P solid medium supplemented with yeast extract (100 mg l–1). Grown colonies were inoculated into fresh semi-solid JMV medium and finally transferred to LGI-P solid medium for characterization. Burkholderia strains recovered in South Africa were isolated from the roots of sugarcane. Roots were washed gently with tap water and then blended and aliquots were plated onto PCAT medium (Burbage & Sasser, 1982). After incubation for 48 h, bacterial colonies were transferred to PCAT agar plates once more and purified on tryptic soy agar plates.
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). Cultures were washed twice in 10 mM MgSO4, adjusted to an OD of 0·2 (3x106 c.f.u. ml–1) and each culture was streaked onto solid media. The effects of temperature and pH on growth were determined in BSE agar medium. The effects of temperature and pH on growth and nitrogenase activity of some strains (Ppe5, Ppe6, Ppe7 and Ppe8T) were also evaluated in a nitrogen-free semi-solid JMV medium. The optimal growth temperature was determined indirectly by measuring nitrogenase activity by the acetylene reduction method (Burris, 1972). Growth on MacConkey agar (Difco) plates as well as on BCSA medium (Henry et al., 1997) was determined after 72 h at 29 and 37 °C. Tests such as oxidase, catalase and hydrolysis of gelatin and Tween 80 were performed by the methods of Smibert & Krieg (1981). Strains were analysed with the API 20NE, API 50CH (bioMérieux) and Biolog MicroLog systems. In the case of API 20NE and API 50CH tests, the inoculation was performed according to the recommendations of the manufacturer (bioMérieux). The results for API 20NE were obtained after 24 or 48 h of incubation as recommended by the manufacturer and API 50CH galleries were obtained after 6 days of incubation. When the Biolog system was used, strains were incubated on biological universal growth medium (Biolog) at 30 °C for 24 h. GN2 microplates were inoculated according to the manufacturer's instructions and incubated at 30 °C for 24 h. The quantitative data of carbon source utilization by each strain were transformed to categories using the CategVar module in ADE-4 software (Biolog).
SDS-PAGE of whole-cell proteins and siderophore production.
Preparation of whole-cell proteins as well as SDS-PAGE assays were performed as described previously (Estrada-de los Santos et al., 2001). Siderophores were detected using the universal chemical assays on chromeazurol-S agar plates and in chromeazurol-S solution as described previously (Schwyn & Neilands, 1987). Hydroxamate-type siderophores were identified using the test of Czàky (1948).
ARDRA and sequencing.
Genomic DNA was isolated from bacterial cells using published protocols (Kirchhof et al., 1997; Ausubel et al., 1987). Primers fD1 and rD1 were used for amplification of the 16S rRNA gene (Weisburg et al., 1991) using PCR conditions described previously (Estrada-de los Santos et al., 2001). The amplified 16S rRNA genes were restricted with AluI, DdeI, HaeIII, HhaI, HinfI, MspI and RsaI. The restriction fragments were separated by electrophoresis in 3 % agarose gels and the patterns were compared. Each isolate was assigned to one of the ARDRA genotypes 16, 17 or 19 as described previously (Estrada-de los Santos et al., 2001). For the strain Ppe8T, an almost full-length bacterial 16S rRNA gene fragment was amplified by PCR as described by Juretschko et al. (1998) and sequenced by Sequiserve (Vaterstetten, Germany). For strains MOc-725, MTo-672 and MTo-293, PCR products were cloned first into the pCRII vector (Invitrogen). 16S rRNA genes were restricted into small fragments (0·3–0·8 kb) using EcoRI and subcloned into vector pUC18. 16S rRNA gene sequencing was performed by Medigenomix. The sequences of both strands were determined using universal primers for the pUC18 vector.
DNA base composition and DNA–DNA relatedness analysis.
The mean mol% G+C content of genomic DNA was measured by the DSMZ. DNA–DNA relatedness was based on relative levels of hybridization to 32P-labelled DNA as described previously (Estrada-de los Santos et al., 2001).
Species-specific PCR primers.
Available Burkholderia 16S rRNA gene sequences were aligned to identify regions specific for the novel species; a region corresponding to positions 456–475 of Escherichia coli (GenBank accession no. V00348) was identified. This region was chosen to define the forward primer 5'-TCCCTGGTCCTAATATG-3'. The reverse primer (5'-CAACCCTCTGTTCCGA-3') was identified in a 16S rRNA gene region described previously (Pallud et al., 2001). PCR conditions were as follows: initial denaturation for 7 min at 95 °C followed by 35 cycles of 1 min denaturation at 94 °C, 1 min annealing at 48 °C and 1 min elongation at 72 °C, followed by a final 15 min elongation at 72 °C.
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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). In nitrogen-free LGI-P and BAz enriched semi-solid media, the bacterial growth formed a thin yellowish pellicle approximately 2–4 mm below the surface. When the bacterial growth was transferred to LGI-P solid medium, small colonies were formed with a yellow centre and white margins. Colonies growing on BAc medium plates were yellowish, round, smooth and convex, 1–2 mm in diameter, with entire margins after incubation for 4 days as described previously (Estrada-de los Santos et al., 2001). In terms of morphological features, the novel Burkholderia isolates were characterized as rod-shaped (0·7–0·8x1·5–1·6 µm) Gram-negative bacteria. Cells appeared encapsulated, very motile due to the presence of several (one to four) polar flagella (Fig. 1) and possessed peritrichous fimbriae (data not shown). Spores were not observed but poly-
-hydroxybutyrate granules were viewed under transmission electron microscopy (data not shown). The isolates were oxidase, catalase and urease positive and were able to hydrolyse Tween 80, but not gelatin or starch. Nitrate was reduced to nitrite, but nitrite was not further reduced. The novel isolates grew and showed nitrogenase activity under microaerobic conditions in nitrogen-free semi-solid JMV, LGI-P and BAz media (Table 2), except for strain RASC. Growth and nitrogenase activity were stimulated by the addition of yeast extract (100 mg l–1). Optimum temperature for N2-dependent growth was 30 °C, although they still could fix N2 at 25 and 36 °C; growth at 40 °C was very poor and no growth was observed below 7 °C or above 42 °C. Similarly, all of the isolates grew on BSE agar medium at 37 °C but not at 42 °C. The novel isolates grew well at pH values between 4·5 and 6·5, but poor growth was observed at pH 7·0–7·5; optimal growth was observed between pH 5·0 and 5·8. While strains of B. tropica sp. nov. were found in the rhizosphere and associated with plants growing in soils with a pH in the range 4·5–7·1, isolation from maize plants cultivated on soils with a pH higher than 7·5 was unsuccessful. This result is in accordance with the good growth of the novel isolates on culture media with a pH 4·5–6·5. Bacteria of the genus Burkholderia are considered to be characteristic of neutral pH environments (Liesack et al., 1997), but recent evidence suggests a high abundance of Burkholderia in acidic soils (Nogales et al., 2001).
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), among the hitherto-described species of the genus Burkholderia, N2-fixing ability has only been found in B. vietnamiensis (Gillis et al., 1995) and Burkholderia kururiensis (Estrada-de los Santos et al., 2001). In addition, the presence of the nifH gene encoding dinitrogenase reductase, a key enzyme in N2 fixation, has been detected (Moulin et al., 2001) in the recently described nodulating species B. tuberum (Vandamme et al., 2002). In the present study, diazotrophic Burkholderia isolates recovered from plants grown in Brazil, Mexico and South Africa shared a high similarity in their phenotypic and genomic traits, but exhibited little resemblance to other Burkholderia species. Phenotypic characteristics for the differentiation of B. tropica sp. nov. from other N2-fixing Burkholderia species as well as from related Burkholderia species are shown in Table 2. Differences in the usage of carbon sources by the novel isolates and other related Burkholderia species according to the API 50CH test are shown in Table 3. According to the Biolog carbon source utilization tests, a broad spectrum of sugars and alcohols were used (see supplementary data in IJSEM Online).
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). These protein patterns were clearly different from other N2-fixing and from non-N2-fixing Burkholderia species. All of the isolates corresponding to ARDRA genotypes 16, 17 and 19 showed the ability to produce siderophores. Ninety-two per cent of the strains produced hydroxamates as the main type of siderophore.
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). These genotypes showed identical ARDRA profiles with enzymes AluI, DdeI, HaeIII, HhaI, MspI and RsaI, but could be distinguished by the enzyme HinfI (see Supplementary Fig. A in IJSEM Online). Strain Ppe8T showed an ARDRA profile identical to genotype 19. Strains LM1-376.8, LM2-376.3 and RASC showed the same profiles as genotype 19 except with HaeIII, and therefore they were designated ARDRA genotype 19a (Table 1). When the 16S rRNA gene was restricted with each of the seven different enzymes, the sum of the fragments was approximately 1·5 kb, except in the case of strains corresponding to ARDRA genotype 17, which were greater than 2·0 kb with the HinfI enzyme (see Supplementary Fig. A, lane 8, in IJSEM Online). A possible explanation for the larger size could be the amplification of distinct copies of these genes, some of which lack one of the restriction sites. It is known that bacteria have up to 15 copies of ribosomal operons and that they have internal differences (Klappenbach et al., 2000).
The 16S rRNA gene sequence of strain Ppe8T as well as sequences for isolates MOc-725, MTo-672, MTo-293 and LM2-376.3, representing different ARDRA genotypes, were compared with available 16S rRNA gene sequences from all of the Burkholderia species. The phylogenetic tree shown in Fig. 3 illustrates the position of the novel isolate group, B. tropica sp. nov., relative to other Burkholderia species. Strains Ppe8T, MTo-293, LM2-376.3, MOc-725 and MTo-672 were closely related, forming a cluster with strains BM16 and BM273 described in a previous study (Estrada et al., 2002), as well as with strain AB98 (Cruz et al., 2001). The similarity among the 16S rRNA gene sequences of these strains ranged from 99·2 to 99·9 %. The N2-fixing species B. tropica clearly constituted a well-supported cluster separate from the cluster formed by the diazotrophic species B. kururiensis/B. tuberum. Burkholderia sacchari, a non-diazotrophic bacterium, was the closest species to the B. tropica cluster (97·2 % similarity). The N2-fixing species B. vietnamiensis, which belongs to the second major lineage of Burkholderia comprising the ‘Burkholderia cepacia complex’ (Vandamme et al., 1997), appeared distantly related to B. tropica with a sequence similarity of <96 % (Supplementary Fig. B). Since 97 % is the threshold 16S rRNA gene similarity level for the delineation of bacterial species (Stackebrandt & Goebel, 1994), B. tropica could be clearly differentiated from the closely related species B. sacchari and B. tuberum (96·2 % similarity).
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Species-specific PCR
Results showed that PCR amplification was strictly specific for B. tropica strains. An 800 nt amplicon was obtained with B. tropica strains (Ppe8T, SMi-583, MMi-786, MTo-431, BM16, BM273, MTo-293, LM1-376.8 and LM2-376.3) but not with type strains of other related Burkholderia species such as Burkholderia caledonica, B. caribensis, B. cepacia, Burkholderia fungorum, B. graminis, Burkholderia phenazinium, Burkholderia thailandensis and B. vietnamiensis, nor with six strains of Burkholderia cenocepacia (data not shown).
Taxonomic considerations
Many phenotypic features and all of the genomic characteristics described above agree with similarity criteria recommended for the delineation of bacterial species (Vandamme et al., 1996). Accordingly, we consider that the strains analysed in this work belong to a novel plant-associated N2-fixing bacterial species within the genus Burkholderia and propose the name Burkholderia tropica sp. nov.
Description of Burkholderia tropica sp. nov.
Burkholderia tropica (L. fem. adj. tropica tropical).
Cells are slightly curved rods, approximately 1·5–1·6 µm long and 0·7–0·8 µm wide. They occur singly and possess a capsule. They are motile by means of one to four polar flagella. Isolates are Gram negative and oxidase and catalase positive. On LGI-P solid medium, small colonies are formed with a yellow centre and white margins. Colonies on BAc plates are yellowish, round, smooth and convex with entire margins. Growth and acetylene reduction to ethylene are observed in nitrogen-free semi-solid media. Strains have an aerobic metabolism but fix nitrogen microaerobically. They grow well with ammonium, and nitrate is reduced to nitrite, but nitrite is not further reduced. Nitrate and ammonium inhibit N2 fixation, but small amounts of yeast extract (100 mg l–1) enhance N2 fixation. Several carbon sources support growth, including sugars and organic acids. Growth occurs from 22 to 40 °C and the optimum temperature is 30 °C. No hydrolysis of starch or gelatin is observed, but Tween 40 and Tween 80 are hydrolysed. Characteristics that differentiate B. tropica from other N2-fixing Burkholderia species are listed in Tables 2 and 3. B. tropica can also be differentiated from other N2-fixing and non-N2-fixing Burkholderia species by 16S rRNA gene PCR primers. The species B. tropica comprises four different ARDRA genotypes. It has a G+C content of 63·5 mol%.
The type strain is strain Ppe8T (=ATCC BAA-831T=LMG 22274T=DSM 15359T), isolated from sugarcane var. SP 71-1406 grown in the fields of the Cruangi Sugar factory located in Pernambuco State, Brazil.
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ACKNOWLEDGEMENTS |
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J. Caballero-Mellado, J. Onofre-Lemus, P. Estrada-de los Santos, and L. Martinez-Aguilar The Tomato Rhizosphere, an Environment Rich in Nitrogen-Fixing Burkholderia Species with Capabilities of Interest for Agriculture and Bioremediation Appl. Envir. Microbiol., August 15, 2007; 73(16): 5308 - 5319. [Abstract] [Full Text] [PDF]
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W.-M. Chen, S. M. de Faria, E. K. James, G. N. Elliott, K.-Y. Lin, J.-H. Chou, S.-Y. Sheu, M. Cnockaert, J. I. Sprent, and P. Vandamme Burkholderia nodosa sp. nov., isolated from root nodules of the woody Brazilian legumes Mimosa bimucronata and Mimosa scabrella Int J Syst Evol Microbiol, May 1, 2007; 57(5): 1055 - 1059. [Abstract] [Full Text] [PDF]
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A. Valverde, P. Delvasto, A. Peix, E. Velazquez, I. Santa-Regina, A. Ballester, C. Rodriguez-Barrueco, C. Garcia-Balboa, and J. M. Igual Burkholderia ferrariae sp. nov., isolated from an iron ore in Brazil. Int J Syst Evol Microbiol, October 1, 2006; 56(Pt 10): 2421 - 2425. [Abstract] [Full Text] [PDF]
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W.-M. Chen, E. K. James, T. Coenye, J.-H. Chou, E. Barrios, S. M. de Faria, G. N. Elliott, S.-Y. Sheu, J. I. Sprent, and P. Vandamme Burkholderia mimosarum sp. nov., isolated from root nodules of Mimosa spp. from Taiwan and South America. Int J Syst Evol Microbiol, August 1, 2006; 56(Pt 8): 1847 - 1851. [Abstract] [Full Text] [PDF]
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L. Perin, L. Martinez-Aguilar, G. Paredes-Valdez, J. I. Baldani, P. Estrada-de los Santos, V. M. Reis, and J. Caballero-Mellado Burkholderia silvatlantica sp. nov., a diazotrophic bacterium associated with sugar cane and maize. Int J Syst Evol Microbiol, August 1, 2006; 56(Pt 8): 1931 - 1937. [Abstract] [Full Text] [PDF]
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G. Peng, H. Wang, G. Zhang, W. Hou, Y. Liu, E. T. Wang, and Z. Tan Azospirillum melinis sp. nov., a group of diazotrophs isolated from tropical molasses grass Int J Syst Evol Microbiol, June 1, 2006; 56(6): 1263 - 1271. [Abstract] [Full Text] [PDF]
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L. Perin, L. Martinez-Aguilar, R. Castro-Gonzalez, P. Estrada-de los Santos, T. Cabellos-Avelar, H. V. Guedes, V. M. Reis, and J. Caballero-Mellado Diazotrophic burkholderia species associated with field-grown maize and sugarcane. Appl. Envir. Microbiol., May 1, 2006; 72(5): 3103 - 3110. [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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