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Bradyrhizobium Cajani Sp. Nov. Isolated from Nodules of Cajanus Cajan

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Bradyrhizobium Cajani Sp. Nov. Isolated from Nodules of Cajanus Cajan TAXONOMIC DESCRIPTION Araújo et al., Int J Syst Evol Microbiol 2017;67:2236–2241 DOI 10.1099/ijsem.0.001932 Bradyrhizobium cajani sp. nov. isolated from nodules of Cajanus cajan Juan Araújo,1† Jose David Flores-Felix, 2† Jose M. Igual,3,4 Alvaro Peix,3,4 Fernando Gonzalez-Andr es, 5 Cesar Antonio Díaz-Alcantara 1 and Encarna Velazquez 2,4,* Abstract Two slow-growing strains, AMBPC1010T and AMBPC1011, were isolated from nodules of Cajanus cajan in the Dominican Republic. 16S rRNA gene analysis placed these strains within the genus Bradyrhizobium, being phylogenetically equidistant to several species of this genus. Analysis of the recA and atpD genes showed that the strains isolated belong to a cluster containing the strains Bradyrhizobium ottawaense OO99T, ‘Bradyrhizobium americanum’ CMVU44 and Bradyrhizobium daqingense CCBAU 15774T, and presented similarity values lower than 96 % for both genes with respect to the strains nodulating C. cajan. DNA–DNA hybridization analysis showed averages of 36, 40 and 39 % relatedness with respect to the representative strains of Bradyrhizobium ottawaense, ‘Bradyrhizobium americanum’ and Bradyrhizobium daqingense, respectively. Phenotypic characteristics also differed from those of the most closely related species of the genus Bradyrhizobium. Therefore, based on the data obtained in this study, we propose to classify the strains AMBPC1010T (=LMG 29967T=CECT 9227T) and AMBPC1011 into a novel species named Bradyrhizobium cajani sp. nov. The genus Bradyrhizobium comprises Gram-stain-negative, ability to reinfect their host was confirmed according to the aerobic bacteria showing slow growth in media containing method of Araújo et al. [8]. mannitol as a carbon source [1]. This genus currently con- Strains AMBPC1010T and AMBPC1011 were subjected to tains more than 30 species, some of them recently isolated randon amplification of polymorphic DNA (RAPD) finger- – from nodules of American tropical legumes [2 5]. The printing as was previously described [10] using the M13 seeds of some of these legumes have great interest as human primer (5¢-GAGGGTGGCGGTTCT-3¢) and Go Taq G2 foods, particularly for developing countries, such as those Green Master Mix (Promega). The results showed that the from Cajanus cajan L., which establishes nitrogen-fixing two strains have different RAPD profiles between them and symbiosis with strains of the genus Bradyrhizobium [6–8]. with respect to the most closely related type strains (Fig. S1, available in the online Supplementary Material). In this work, we characterized two strains isolated from C. cajan nodules in the Dominican Republic and from the Amplification and sequencing of the complete 16S rRNA results obtained we propose a novel species with the name gene of the newly isolated strains was carried out according Bradyrhizobium cajani sp. nov. to the method of Rivas et al. [11], that of the recA and glnII T genes was performed according to the method of Vinuesa The strains, named AMBPC1010 and AMBPC1011, were et al. [12] and that of the nodC gene was carried out accord- isolated from two effective root nodules (pink colour) of ing to the method of Velazquez et al. [13]. The sequences plants from C. cajan L. cultivated at the site named ‘Monte obtained were compared with those from GenBank using Monito’ located in Azúa province in the Dominican Repub- the BLASTN program [14]. Sequences were aligned using the lic. The isolation was performed on YMA plates following CLUSTAL X software [15]. The distances were calculated the classic methodology described by Vincent [9], and the according to Kimura’s two-parameter model [16]. Author affiliations: 1Facultad de Ciencias Agronómicas y Veterinarias, Universidad Autónoma de Santo Domingo, Santo Domingo, Dominican Republic; 2Departamento de Microbiología y Genetica and Instituto Hispanoluso de Investigaciones Agrarias (CIALE), Universidad de Salamanca, Salamanca, Spain; 3Instituto de Recursos Naturales y Agrobiología de Salamanca, Consejo Superior de Investigaciones Científicas. (IRNASA-CSIC), Salamanca, Spain; 4Unidad Asociada Grupo de Interacción Planta-Microorganismo Universidad de Salamanca-IRNASA-CSIC, Salamanca, Spain; 5Instituto de Medio Ambiente, Recursos Naturales y Biodiversidad, Universidad de León, León, Spain. *Correspondence: Encarna Velazquez, [email protected] Keywords: Bradyrhizobium; Cajanus cajan; Dominican Republic; legume nodules. †These authors contributed equally to this work. The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA, recA and glnII genes of the type strain are KY349447, KY349440 and KY349442, respectively. One supplementary table and two supplementary figures are available with the online Supplementary Material. 001932 ã 2017 IUMS Downloaded from www.microbiologyresearch.org by IP: 161.111.105.1232236 On: Wed, 04 Apr 2018 11:03:00 Araújo et al., Int J Syst Evol Microbiol 2017;67:2236–2241 Phylogenetic trees were inferred using the neighbour-join- fatty acids of the strains isolated from C. cajan were those ing [17] and maximum-likelihood [18] analyses. The topol- from summed feature 8 (C18 : 1!6c/C18 : 1!7c) and C16 : 0 ogies of the trees obtained after the analyses of the (Table 1) in agreement with the results found previously for individual housekeeping genes glnII and recA were similar many species of the genus Bradyrhizobium [28]. The strains and then these genes were concatenated. MEGA5 software from this study showed slight differences in their fatty acid [19] was used for all analyses. profiles and with respect to those of the closely related spe- The 16S rRNA gene sequence of strain AMBPC1011 (acces- cies (Table 1). sion number KY349446) was identical to that of the type The phenotypic characterization was performed as previ- T strain AMBPC1010 and so only this last strain was ously described for species of the genus Bradyrhizobium included in the phylogenetic analysis of this gene. Accord- [25, 26, 29, 30] including API ID32GN and API 20NE ing to the results obtained, this strain belongs to the genus systems (with the addition of MgSO4 up to a final concen- À Bradyrhizobium forming an independent branch equidis- tration of 0.02g l 1). The results were read after 7 days of tant to several species from this genus with similarity values incubation at 28 C (Table S1). The temperature range for ranging from 99 to 99.6 % (Fig. 1). Several species of the growth was determined by incubating cultures in YMA at genus Bradyrhizobium are within this range of similarity 4, 15, 28, 37 and 45 C. The pH range for growth was values and they are distinguishable on the basis of house- determined in the same medium with final pH 4.5, 6, 7, 8, keeping gene sequences, such as those of recA and glnII, 9 and 10. PCA buffer (0.4 M Na2HPO4 and 0.2 M citric available for all species of the genus Bradyrhizobium. acid) was used to adjust to pH 4 and 6, phosphate buffer The analysis of the concatenated recA and glnII genes (0.2 M Na2HPO4 and 0.2 M NaH2PO4) was used for pH 7 showed that the strains isolated from C. cajan nodules and 0.2 M TE buffer was used for pH 8, 9 and 10. Salt tol- formed an independent lineage closely related to the type or erance was tested in the same medium containing 0.5, 1, proposed type strains of Bradyrhizobium ottawaense, Bra- 1.5, 2 and 2.5% (w/v) NaCl. For testing the natural antibi- dyrhizobium daqingense and ‘Bradyrhizobium americanum’ otic resistance, the disc diffusion method on YMA was (Fig. 2). The similarity values for the recA gene were 93, 94 used. The discs contained the following antibiotics: ampi- and 94.5 %, respectively, and those for the glnII gene were cillin (2µg), erythromycin (2µg), ciprofloxacin (5µg), 94.6, 94.4 and 94.8 %, respectively. These values are lower penicillin (10 IU), polymyxin (300 IU), cloxacillin (1µg), than those found among several described species of the tetracycline (30µg), gentamycin (10µg), cefuroxime genus Bradyrhizobium (Fig. 2) suggesting that the strains (30µg) or neomycin (5µg) (Becton Dikinson, BBL). The isolated in this study do not belong to previously described strains B. ottawaense HAMBI 3284T (=LMG 26739T), B. species from this genus. daqingense LMG 26137T (=CCBAU 15774T) and ‘B. americanum’ CMVU44 were included in the phenotypic DNA–DNA hybridization experiments were carried out as study as references. Phenotypic characteristics of the reported previously [20, 21] and showed an average of 82 % novel species are reported below in the species descrip- (±3 %) between strains AMBPC1010T and AMBPC1011, tion, and the differential characteristics with respect to corresponding to strains belonging to the same species. the most closely related species of the genus Bradyrhi- Averages of 36 % (±3 %), 39 (±4 %) and 40 (±4 %) were found between strain AMBPC1010T and B. ottawaense zobium are shown in Table 2. HAMBI 3284T, B. daqingense LMG 26137T and ‘B. ameri- Although symbiotic genes do not offer taxonomic informa- canum’ CMVU44, respectively. Since these percentages are tion because they are located in easily interchangeable below the 70 % threshold value of DNA–DNA relatedness elements (plasmids or symbiotic islands), in this work we for definition of bacterial species [22], the strains isolated in analysed the symbiotic nodC gene, the sequence of which is this study from C. cajan nodules should be assigned to a dif- available for most species of the genus Bradyrhizobium ferent species. allowing differentiation at the symbiovar level [31]. The DNA for analysis of DNA base composition was prepared phylogenetic analysis of this gene placed the newly isolated according to the method of Chun and Goodfellow [23]. The strains into a cluster containing the type strain of Bradyrhi- G+C content (mol%) of DNA was determined using the zobium arachidis isolated in Asia from nodules of Arachis thermal denaturation method [24]. The DNA G+C content hypogeaea [32] (96.5 % similarity) and those of Bradyrhi- of strain AMBPC1010T was 62.7 %, which is within the zobium kavangense [33] and Bradyrhizobium vignae [34] range reported for its most closely related species [3, 25, 26].
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