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Bradyrhizobium Daqingense Sp. Nov., Isolated from Soybean Nodules

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Bradyrhizobium Daqingense Sp. Nov., Isolated from Soybean Nodules International Journal of Systematic and Evolutionary Microbiology (2013), 63, 616–624 DOI 10.1099/ijs.0.034280-0 Bradyrhizobium daqingense sp. nov., isolated from soybean nodules Jing Yu Wang,13 Rui Wang,13 Yan Ming Zhang,1 Hong Can Liu,2 Wen Feng Chen,1 En Tao Wang,1,3 Xin Hua Sui1 and Wen Xin Chen1 Correspondence 1State Key Laboratory for Agro-Biotechnology, College of Biological Sciences, China Agricultural Xinhua Sui University, Beijing 100193, PR China [email protected] 2Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, PR China 3Departamento de Microbiologı´a, Escuela Nacional de Ciencias Biolo´gicas, Instituto Polite´cnico Nacional, 11340 Me´xico DF, Mexico Thirteen slow-growing rhizobial strains isolated from root nodules of soybean (Glycine max L.) grown in Daqing city in China were classified in the genus Bradyrhizobium based on 16S rRNA gene sequence analysis. Multilocus sequence analysis of IGS, atpD, glnII and recA genes revealed that the isolates represented a novel clade in this genus. DNA–DNA relatedness lower than 42.5 % between the representative strain CCBAU 15774T and the type strains of the closely related species Bradyrhizobium liaoningense USDA 3622T, Bradyrhizobium yuanmingense CCBAU 10071T and Bradyrhizobium betae LMG 21987T, further confirmed that this group represented a novel species. CCBAU 15774T shared seven cellular fatty acids with the three above-mentioned species, but the fatty acids 15 : 0 iso and summed feature 5 (18 : 2v6,9c and/or 18 : 0 anteiso) were unique for this strain. The respiratory quinone in CCBAU 15774T was ubiquinone-10 and the cellular polar lipids were phosphatidylethanolamine, phosphatidylglycerol, phosphatidylcholine, cardiolipin and unknown aminolipid, polar lipid and phospholipid. In addition, some phenotypic features could be used to differentiate the novel group from the related species. On basis of these results, we propose the name Bradyrhizobium daqingense sp. nov., with CCBAU 15774T (5LMG 26137T5HAMBI 3184T5CGMCC 1.10947T) as the type strain. The DNA G+C content of the type strain is 61.2 mol% (Tm). The genus Bradyrhizobium was proposed by Jordan (1982) incubation at 28 uC. At the time of writing, the genus for the slow-growing root nodule bacteria, in which contained 12 defined species: Bradyrhizobium japonicum colonies are generally less than or equal to 1 mm on yeast (Jordan, 1982), B. elkanii (Kuykendall et al., 1992), B. extract-mannitol agar (YMA) medium after 5–10 days liaoningense (Xu et al., 1995), B. yuanmingense (Yao et al., 2002), B. betae (Rivas et al., 2004), B. canariense (Vinuesa et al., 2005a), B. denitrificans (van Berkum et al., 2006), B. 3These authors contributed equally to this work. iriomotense (Islam et al., 2008), B. jicamae, B. pachyrhizi Abbreviations: AL, aminolipid; BOX-PCR, BOX-repeat-based PCR; CL, (Ramı´rez-Bahena et al., 2009), B. lablabi (Chang et al., cardiolipin; GL, glycolipid; IGS, 16S–23S rRNA intergenic spacer; MLSA, 2011) and B. cytisi (Chahboune et al., 2011). With the multilocus sequence analysis; MP, maximum parsimony; NJ, neighbour- exception of B. betae, all species are symbiotic nitrogen- joining; NP, unknown phospholipid; PC, phosphatidylcholine; PE, phosphatidylethanolamine; PG, phosphatidylglycerol; PL, polar lipid. fixing bacteria associated with different legumes. The GenBank sequence accession numbers of 16S rRNA, IGS, atpD, Soybean [Glycine max (L.) Merrill] originated in China and glnII, recA, nodC and nifH are: HQ231274, HQ231312, HQ231289, has been planted for over 5000 years (Liu et al., 2008) as HQ231301, HQ231270, HQ231326 and HQ231323 for CCBAU one of the most important crops for edible oil and protein T 15774 ; HQ664956, HQ664959, HQ664967, HQ664973, production. Previously, B. japonicum, B. elkanii, B. HQ664970, HQ664988 and HQ664977 for CCBAU 15772; HQ664955, HQ664958, HQ664966, HQ664972, HQ664969, liaoningense, B. yuanmingense, Ensifer fredii and Ensifer HQ664989 and HQ664976 for CCBAU 15768; and HQ664954, sojae (Han et al., 2009; Li et al., 2011a; Man et al., 2008; HQ664957, HQ664960, HQ664971, HQ664968, HQ664978 and Wang et al., 2009; Xu et al., 1995) have been isolated from HQ664974 for CCBAU 15779, respectively. root nodules of soybean grown in different regions of Seven supplementary figures and two supplementary tables are China. Clear biogeographic patterns have been revealed in available with the online version of this paper. the soybean rhizobia and soil types seemed to be the main 616 034280 G 2013 IUMS Printed in Great Britain Bradyrhizobium daqingense sp. nov. determinant of the biogeography of these bacteria (Han Gram-negative, non-spore-forming rods. Colonies on et al., 2009; Li et al., 2011b; Man et al., 2008; Zhang et al., YMA medium were mucoid, white, translucent and 2011). circular, 1 mm in diameter after 7 days of incubation at 28 uC and they produced an alkaline pH on YMA medium Heilongjiang Province, in the north-east of China, is the supplied with bromothymol blue (0.025 %), indicating main soybean-producing area, accounting 44 % (4.01 that these isolates belonged to the genus Bradyrhizobium million ha) of the culturing area and 40 % of the yield in (Vincent, 1970). China in 2009 (http://zzys.agri.gov.cn/nongqing.aspx). In general, Heilongjiang has extremely fertile black soil with Similar to other studies (Cho & Tiedje, 2000; Healy et al., low acidity or neutral pH, in which B. japonicum is the 2005; Rademaker et al., 2000), BOX-PCR fingerprinting predominant microsymbiont of soybean, whereas B. was used to reveal the genetic diversity of the nodule elkanii, B. liaoningense and Ensifer fredii have been isolates. In this study, the BOXAIR primer (Versalovic et al., occasionally isolated (Wang et al., 2009; Xu et al., 1995). 1994) and method of Nick & Lindstrom (1994) were used In contrast to other places in Heilongjiang Province, in analysis of BOX-PCR. The PCR products were subjected Daqing city, in the south-west of the province, has saline, to electrophoresis in agarose gel (1.5 %, w/v) supplied with alkaline soil, high precipitation and lower terrain, making ethidium bromide. Four BOX-PCR patterns were obtained it possible to harbour soybean rhizobia that differ from among the 13 isolates (Fig. S1, Table 1), which shared more those in other places of Heilongjiang. than 84 % similarity. From them, isolates CCBAU 15768, CCBAU 15772, CCBAU 15774T and CCBAU 15779, In a study of bradyrhizobia associated with soybean in representing four BOX fingerprints, were chosen for the Heilongjiang province, a group of 13 isolates (Table 1) subsequent analyses. originating from Daqing city showed same 16S–23S rRNA intergenic spacer (IGS)-RFLP patterns and differed from The 16S rRNA genes of the four representative strains were the defined species of Bradyrhizobium (data not shown), amplified with the primers P1 and P6 by the PCR protocol implying that they may represent a novel species of the of Tan et al. (1997). The IGS fragments were amplified with genus. To clarify their taxonomic position, we performed the primers FGPS1490 and FGPL132 (Laguerre et al., 1996) the present study and a novel species, Bradyrhizobium as described by Kwon et al. (2005). The atpD, recA and glnII genes were amplified by using the method of Vinuesa daqingense, was defined based upon the results. et al. (2005b), with primer sets atpD255F/atpD782R, These 13 isolates were obtained from surface-sterilized root recA41F/recA640R and glnII12F/glnII689R, respectively. nodules collected in August 2009 on YMA medium as The amplification of partial nodC and nifH genes were described elsewhere (Bergersen, 1961). All the isolates were performed with the primers nodC540/nodC1160 (Sarita Table 1. Sequence similarities of 16S rRNA gene, combined atpD, recA and glnII, IGS, nifH and nodC, DNA relatedness among CCBAU 15774T and related strains, DNA G+C contents and BOX types 2, Not done. Strain Similarity with CCBAU 15774T (%) DNA G+C content (mol%; Tm) 16S rRNA MLSA* IGS nifH nodC DNA–DNA relatedness (%) B. daqingense sp. nov.D CCBAU 15774T (BOX type I) 100 100 100 100 100 100 61.2 CCBAU 15772 (BOX type II) 100 99.8 99.9 92.6 92.9 94.3±1.78 61.4 CCBAU 15768 (BOX type III) 100 100 100 100 100 94.0±2.05 60.1 CCBAU 15779 (BOX type IV) 100 100 100 99.7 100 93.6±1.69 60.6 B. liaoningense USDA 3622T 99.9 94.4 89.9 100 2 42.5±2.06 B. yuanmingense CCBAU 10071T 99.5 94.2 93.3 91.5 92.1 26.8±2.48 B. betae LMG 21987 T 99.3 94.1 88.8 22 22.37±1.93 B. canariense BTA-1T 99.5 92.4 89.7 78.5 68.6 2 B. japonicum USDA 6T 99.7 92.6 89.4 100 100 2 B. cytisi CTAW 11T 98.9 91.2 2 77.7 70.1 2 B. iriomotense LMG 24129T 98.8 91.9 92.4 79.8 66.8 2 B. denitrificans LMG 8443T 98.7 89.4 72.3 80.3 22 *atpD, recA and glnII sequences were included in MLSA. DNine other strains were also defined in this group: CCBAU 15766, 15769, 15775, 15776, 15777 and 15778 in BOX type I; CCBAU 15767 in BOX type II; and CCBAU 15770 and 15910 in BOX type IV. http://ijs.sgmjournals.org 617 J. Y. Wang and others et al., 2005) and nifH1F/nifH1R (Laguerre et al., 2001), criteria employed in the recent description of respectively. All the amplified fragments were directly Bradyrhizobium species (Ramı´rez-Bahena et al., 2009; sequenced as described previously (Hurek et al., 1997) and Rivas et al., 2004; Vinuesa et al., 2005a). Rhizobium the acquired sequences were aligned with those of defined lupini DSM 30140T described by Ludwig et al. (1995) Bradyrhizobium species using the CLUSTAL W program in should be reclassified in the genus Bradyrhizobium and the MEGA 4.0 software package (Kumar et al., 1994, 2008).
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