Bradyrhizobium huanghuaihaiense sp. nov., an effective symbiotic bacterium isolated from soybean (Glycine max L.) nodules

Zhang, Yan Ming; Li, Ying Jr; Chen, Wen Feng; Wang, En Tao; Sui, Xin; Li, Qin Qin; Zhang, Yun Zeng; Zhou, Yu

doi:10.1099/ijs.0.034546-0

Cited by 61 publications

(33 citation statements)

References 47 publications

(51 reference statements)

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“…Non-methylated lambda phage (Sigma) and Escherichia coli DNA were used as a calibration reference and a control, respectively. The DNA G+C content of our strain was 63.8 mol% (Table 1), which is within the range reported for species of the genus Bradyrhizobium and was different to the closest type strain, CCBAU 23303 T , for which the DNA G+C content was 61.5 mol% (Zhang et al, 2012).…”

Section: Bradyrhizobium Manausense Br3310supporting

confidence: 78%

Bradyrhizobium manausense sp. nov., isolated from effective nodules of Vigna unguiculata grown in Brazilian Amazonian rainforest soils

Silva

Meyer

Simões‐Araújo³

et al. 2014

International Journal of Systematic and Evolutionary Microbiology

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Root nodule bacteria were trapped within cowpea (Vigna unguiculata) in soils with different cultivation histories collected from the Amazonian rainforest in northern Brazil. Analysis of the 16S rRNA gene sequences of six strains (BR 3351 T , BR 3307, BR 3310, BR 3315, BR 3323 BR and BR 3361) isolated from cowpea nodules showed that they formed a distinct group within the genus Bradyrhizobium, which was separate from previously identified type strains. Phylogenetic analyses of three housekeeping genes (glnII, recA and rpoB) revealed that Bradyrhizobium huanghuaihaiense CCBAU 23303 T was the most closely related type strain (96 % sequence similarity or lower). Chemotaxonomic data, including fatty acid profiles (predominant fatty acids being C 16 : 0 and summed feature 8), the slow growth rate and carbon compound utilization patterns supported the assignment of the strains to the genus Bradyrhizobium. The results of DNA-DNA hybridizations, antibiotic resistance and physiological tests differentiated these novel strains from the most closely related species of the genus Bradyrhizobium with validly published names. Symbiosis-related genes for nodulation (nodC) and nitrogen fixation (nifH) grouped the novel strains of the genus Bradyrhizobium together with Bradyrhizobium iriomotense strain EK05 T , with 94 % and 96 % sequence similarity, respectively. Based on these data, these six strains represent a novel species for which the name Brabyrhizobium manausense sp. nov. (BR 3351 T 5HAMBI 3596 T ), is proposed.The family Leguminosae is one of the most abundant plant families in the Amazonian rainforest (AR) with more than 1240 species and 140 genera of all three subfamilies (Caesalpinioideae, Mimosoideae and Papilionoideae) catalogued (Ducke, 1949;Silva et al., 1988). This family is ecologically and economically important to the biome, because it contains pioneer species that revegetate bare soils, species that produce grain for food and species used for timber production. Many legume species are capable of forming root (or sometimes stem) nodules, which contain nitrogen-fixing bacterial symbionts, collectively known as 'rhizobia ' (Sprent, 1995). The capacity to nodulate appears to be the rule for leguminous plants within the AR, since more than 80 % of species of the subfamilies Papilionoideae and Mimosoideae do it; however, only about 20 % of the Caesalpinioideae are capable of forming nodules (de Faria, et al., 1989(de Faria, et al., , 2010Moreira, et al., 1993). Legumes contribute significantly to the AR N-balance, with more than 1006 10 8 kg of nitrogen being fixed annually (Salati et al., 1982;Martinelli et al., 1992;Gehring, et al., 2005).Bacteria of the genus Bradyrhizobium have been reported to comprise the majority of root nodule bacteria isolated from The GenBank/EMBL/DDBJ accession number for the 16S rRNA, glnII, recA, rpoB, dnaK, gyrB, nodC and nifH gene sequences of BR3351 T are HQ641226, KF785986, KF785992, KF785998, KF786000, KF786001, KF786002 and KF786003, respectively. Abbreviation: AR, Amazonian ra...

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Section: Bradyrhizobium Manausense Br3310supporting

confidence: 78%

Bradyrhizobium manausense sp. nov., isolated from effective nodules of Vigna unguiculata grown in Brazilian Amazonian rainforest soils

Silva

Meyer

Simões‐Araújo³

et al. 2014

International Journal of Systematic and Evolutionary Microbiology

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“…Menna et al, Chang et al, 2011;Zhang et al, 2012), and our results support the use of this methodology for such purposes. Group Ia strains formed distinct and well-supported clades in single-gene phylogenies of atpD, recA and glnII, for which sequences of all described Bradyrhizobium species are available (data not shown).…”

supporting

confidence: 87%

Polyphasic evidence supporting the reclassification of Bradyrhizobium japonicum group Ia strains as Bradyrhizobium diazoefficiens sp. nov.

Delamuta

Ribeiro

Ormeño‐Orrillo

et al. 2013

International Journal of Systematic and Evolutionary Microbiology

227

122

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Polyphasic evidence supporting the reclassification of Bradyrhizobium japonicum group Ia strains as Bradyrhizobium diazoefficiens sp. nov. Embrapa Meio Ambiente, C.P. 69, 13820-000 Jaguariú na, Sã o Paulo, BrazilBradyrhizobium japonicum was described from soybean root-nodule bacterial isolates. Since its description, several studies have revealed heterogeneities among rhizobia assigned to this species. Strains assigned to B. japonicum group Ia have been isolated in several countries, and many of them are outstanding soybean symbionts used in inoculants worldwide, but they have also been isolated from other legume hosts. Here, we summarize published studies that indicate that group Ia strains are different from the B. japonicum type strain USDA 6 T and closely related strains, and present new morphophysiological, genotypic and genomic evidence to support their reclassification into a novel species, for which the name Bradyrhizobium diazoefficiens sp. nov. is proposed. The type strain of the novel species is the well-studied strain USDA 110 T (5IAM Biological fixation is the main source of nitrogen for natural and agricultural ecosystems. In agriculture, the symbioses of nitrogen-fixing bacteria, collectively known as rhizobia, with crops belonging to the family Leguminosae (5Fabaceae) are the most studied. Relatively high contributions to nitrogen nutrition have been demonstrated in pulses, fodders, green manures and trees (Ormeño-Orrillo et al., 2013). Members of the genus Bradyrhizobium constitute an important group of rhizobia, some of which form symbioses with economically important crops, such as soybean [Glycine max (L.) Merr.].A first systematic classification of rhizobia was proposed by Fred et al. (1932), based on the cross-inoculation concept with respect to the host legume, resulting in six species of Rhizobium: Rhizobium meliloti, R. trifolii, R. phaseoli, R. lupini, R. leguminosarum and R. japonicum, the last of which is a symbiont of soybean. Fifty years later, the taxonomy was redefined using numerical criteria, including several morphophysiological and genetic properties. A new genus was created, Bradyrhizobium, to accommodate rhizobia with the typical property of slow growth rates in culture media, with only one defined species, Bradyrhizobium japonicum (Jordan, 1982). It is noteworthy that the division of rhizobia into fast and slow growers in vitro had been proposed earlier by Löhnis & Hansen (1921).It has been suggested that Bradyrhizobium is the ancestor of the alpha-rhizobia, probably originating in the tropics (Lloret & Martínez-Romero, 2005;Norris, 1965;Provorov & Vorob'ev, 2000). However, despite its evolutionary position, significantly fewer species have been described in Bradyrhizobium in comparison with Rhizobium. One possible explanation is that the 'backbone' of modern taxonomy relies on the analysis of 16S rRNA gene sequences (Woese, 1987), which are highly conserved inAbbreviations: DDH, DNA-DNA hybridization; ITS, intergenic transcribed spacer; MLSA, multilocus sequencing analys...

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“…The 272 Bradyrhizobium strains used in this study (see Table S1 and Fig. S1 in the supplemental material) were previously collected from soybean nodules in four ecoregions of China (South China, Huanghuaihai, Northeast China, and Xinjiang) (2,3,6,8,10,33). These strains were grown in TY medium at 28°C.…”

Section: Methodsmentioning

confidence: 99%

“…It has been recurrently reported that Bradyrhizobium japonicum, Bradyrhizobium elkanii, Bradyrhizobium liaoningense, Bradyrhizobium yuanmingense, and Sinorhizobium fredii could nodulate soybeans (2)(3)(4)(5). Recently, Bradyrhizobium huanghuaihaiense, Bradyrhizobium daqingense, Sinorhizobium sojae, and several unnamed species were also found to be effective microsymbionts of soybeans (2,3,(6)(7)(8). Strain USDA110 represents a widely distributed type formerly known as B. japonicum Ia, but it has recently been proposed as a member of the new species Bradyrhizobium diazoefficiens (9).…”

mentioning

confidence: 99%

“…In contrast to the highly conserved rrs sequences in Bradyrhizobium, sequence analyses of housekeeping genes (atpD, recA, glnII, gyrB, rpoB, dnaK, etc.) have been found to be very useful in this scenario, especially when these genes were concatenated (5,6,8,(14)(15)(16). Although the phylogeny of the concatenated housekeeping genes was usually considered to represent the species tree, these housekeeping loci showed high rates of intergenic recombination and a limited gap between interspecies and intraspecies sequence similarities (15,16).…”

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confidence: 99%

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Genetic Divergence of Bradyrhizobium Strains Nodulating Soybeans as Revealed by Multilocus Sequence Analysis of Genes Inside and Outside the Symbiosis Island

Zhang

Guo

Wang

et al. 2014

Appl Environ Microbiol

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The genus Bradyrhizobium has been considered to be a taxonomically difficult group. In this study, phylogenetics and evolutionary genetics analyses were used to investigate divergence levels among Bradyrhizobium strains nodulating soybeans in China. Eleven genospecies were identified by sequence analysis of three phylogenetic and taxonomic markers (SMc00019, thrA, and truA). This was also supported by analyses of eight genes outside the symbiosis island ("off-island" genes; SMc00019, thrA, truA, fabB, glyA, phyR, exoN, and hsfA). However, seven genes inside the symbiosis island ("island" genes; nifA, nifH, nodC, nodV, fixA, trpD, and rhcC2) showed contrasting lower levels of nucleotide diversity and recombination rates than did off-island genes. Island genes had significantly incongruent gene phylogenies compared to the species tree. Four phylogenetic clusters were observed in island genes, and the epidemic cluster IV (harbored by Bradyrhizobium japonicum, Bradyrhizobium diazoefficiens, Bradyrhizobium huanghuaihaiense, Bradyrhizobium liaoningense, Bradyrhizobium daqingense, Bradyrhizobium sp. I, Bradyrhizobium sp. III, and Bradyrhizobium sp. IV) was not found in Bradyrhizobium yuanmingense, Bradyrhizobium sp. II, or Bradyrhizobium elkanii. The gene flow level of island genes among genospecies is discussed in the context of the divergence level of off-island genes. Soybeans (Glycine max L.) were first domesticated in China and then introduced into different parts of the planet (1), now with an annual harvest area of 100 million hectares around the world (FAO, 2011). Ninety percent of their production comes from the United States, Brazil, Argentina, China, and India (FAO, 2007(FAO, to 2011. One of the key features of soybean is its ability to form symbiotic nitrogen-fixing nodules with diverse rhizobial species (2, 3), implying its important role in sustainable agriculture. It has been recurrently reported that Bradyrhizobium japonicum, Bradyrhizobium elkanii, Bradyrhizobium liaoningense, Bradyrhizobium yuanmingense, and Sinorhizobium fredii could nodulate soybeans (2-5). Recently, Bradyrhizobium huanghuaihaiense, Bradyrhizobium daqingense, Sinorhizobium sojae, and several unnamed species were also found to be effective microsymbionts of soybeans (2, 3, 6-8). Strain USDA110 represents a widely distributed type formerly known as B. japonicum Ia, but it has recently been proposed as a member of the new species Bradyrhizobium diazoefficiens (9).Recent studies not only suggested differences in the biogeographic distribution of rhizobial species nodulating soybeans but also demonstrated a biased selection of rhizobial species by different genotypes of soybeans (2,4,10,11). Consistent with these findings, comparative genomics of rhizobia revealed that the phyletic distribution of rhizobial functional genes involved in environmental adaptations and symbiotic interactions generally agrees with the phylogeny of rhizobial species (7). Therefore, it is important to distinguish different rhizobial species and even subdivis...

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Bradyrhizobium huanghuaihaiense sp. nov., an effective symbiotic bacterium isolated from soybean (Glycine max L.) nodules

Abstract: Bradyrhizobium huanghuaihaiense sp. nov., an effective symbiotic bacterium isolated from soybean (Glycine max L.) nodules

Cited by 61 publications

References 47 publications

Bradyrhizobium manausense sp. nov., isolated from effective nodules of Vigna unguiculata grown in Brazilian Amazonian rainforest soils

Bradyrhizobium manausense sp. nov., isolated from effective nodules of Vigna unguiculata grown in Brazilian Amazonian rainforest soils

Polyphasic evidence supporting the reclassification of Bradyrhizobium japonicum group Ia strains as Bradyrhizobium diazoefficiens sp. nov.

Genetic Divergence of Bradyrhizobium Strains Nodulating Soybeans as Revealed by Multilocus Sequence Analysis of Genes Inside and Outside the Symbiosis Island

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