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1 Key Laboratory of Agro-Microbial Resource and Application, Ministry of Agriculture/College of Biological Sciences, China Agricultural University, Beijing 100094, China
2 College of Life Science, Henan Agricultural University, Zhengzhou 450002, China
3 Departamento de Microbiología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, 11340 México D. F., Mexico
4 Department of Bioengineering and Biotechnology, College of Chemical Engineering, Qingdao University of Science and Technology, Qingdao 266042, China
5 College of Resources and Environmental Science, Sichuan Agricultural University, Yaan 625000, China
Correspondence
Wen Xin Chen
wenxin_chen{at}263.net
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ABSTRACT |
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, Syst Appl Microbiol 29, 502–517] was further characterized. The seven strains in this group showed similar protein patterns and were different from defined Mesorhizobium species in SDS-PAGE of whole-cell proteins. The representative strain CCBAU 61158T formed a novel Mesorhizobium lineage in phylogenetic analyses of 16S rRNA, atpD, glnII and nifH genes. However, its nodC gene sequence was more similar to that of Rhizobium gallicum R602spT than to those of Mesorhizobium species. DNA–DNA relatedness between CCBAU 61158T and reference strains of defined Mesorhizobium species was lower than 34.1 %. These results indicated that this Mesorhizobium group was a unique genomic species. The subtropical distribution, host origin, PCR-RFLP patterns of 16S rRNA genes, fatty acid profile and a series of phenotypic characteristics could be used as distinctive features of this group. This group is therefore proposed as a novel species, Mesorhizobium albiziae sp. nov., with CCBAU 61158T (=LMG 23507T=USDA 4964T) as the type strain. Strain CCBAU 61158T could form effective nodules on Albizia julibrissin, Glycine max, Leucaena leucocephala and Phaseolus vulgaris.
A dendrogram based on whole-cell protein patterns, an alignment of the insertion within the 16S rRNA genes of the novel strains and results of DNA–DNA hybridization are available as supplementary material with the online version of this paper.
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, 1991, 1997; Gao et al., 2004; Scholla & Elkan, 1984; Tan et al., 2001; van Berkum et al., 1998; Wang et al., 1999; Wei et al., 2002, 2003; Xu et al., 1995; Yao et al., 2002). In addition, novel rhizobial lineages are becoming apparent when further studies are carried out to characterize new isolates with enlarged host ranges and geographical origins.
Trees of the genus Albizia, belonging to the Mimosoideae, are native to Asia and Africa and have many uses. In addition to use as foliage, in gardening/landscaping, as green manure and as a source of timber for furniture production, the bark of Albizia trees is used in herbal medicine and the seeds are a source of oil. There are about 150 species in the genus and 17 of them can be found in the southern regions of China (Wu et al., 1988). Although trees of the genus Albizia are of great importance, little is known about the diversity of their microsymbionts. In our previous study, 31 rhizobial strains isolated from Albizia species were characterized by a polyphasic taxonomic approach and great diversity was found (Wang et al., 2006). Seven strains obtained from nodules of Albizia kalkora grown in Sichuan Province were defined as a novel group (rDNA type 6) belonging to Mesorhizobium by ARDRA (amplified 16S rDNA restriction analysis), SDS-PAGE of whole-cell proteins, numerical taxonomy, rep-PCR and sequencing of 16S rRNA genes (Wang et al., 2006). Interestingly, an insertion sequence of about 80 bp, partially similar to the insertion sequence in the 16S rRNA gene of Rhizobium tropici CFN 299, was found in the 16S rRNA gene of CCBAU 61158T, the representative strain of the novel group. With the intention of verifying the taxonomic position of this novel group, we characterized the seven strains further in this study in comparison with reference strains of defined Mesorhizobium species (Table 1) by SDS-PAGE of whole-cell proteins, cellular fatty acid analysis, DNA–DNA hybridization, sequencing of housekeeping genes (16S rRNA, atpD and glnII) and sequencing of symbiotic genes (nifH and nodC). All strains were maintained on YMA (Vincent, 1970) at 4 °C for temporary storage and in 20 % glycerol at –20 °C for long-term storage.
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) at 28 °C; protein extraction and electrophoretic analysis were performed according to the methods described previously (Tan et al., 1997). Normalized densitometric traces of the electrophoretic protein patterns were grouped by using the Gelcompar II software package. The similarity between each pair of samples (strains) was expressed by the Pearson coefficient and a UPGMA dendrogram was constructed (Vauterin & Vauterin, 1992). Very similar electrophoretic protein patterns were distinguished among the seven strains and they formed a cluster at a similarity level of 95 % (Supplementary Fig. S1 in IJSEM Online). The protein patterns of the reference strains were different from each other and from those of the seven strains.
Tighe et al. (2000) found that similarities derived from fatty acid analysis are in broad agreement with 16S rRNA gene sequence analysis results and appear to distinguish accurately between most species in Agrobacterium, Rhizobium, Sinorhizobium, Mesorhizobium and Bradyrhizobium. In this study, the cellular fatty acid compositions of Mesorhizobium amorphae ACCC 19665T, Mesorhizobium septentrionale SDW014T, Mesorhizobium temperatum SDW018T, Mesorhizobium chacoense LMG 19008T and strains CCBAU 61158T, CCBAU 61162 and CCBAU 61166 from the novel group were analysed. All strains were cultured using methods described previously (Graham et al., 1995; Jarvis & Tighe, 1994) and fatty acid methyl esters were extracted and prepared by the standard protocol of the Microbial Identification System (Microbial ID; MIDI). Extracts were analysed by using a Hewlett Packard model HP6890 gas chromatograph equipped with a flame-ionization detector, an automatic sampler, an integrator and a computer, as described previously (Kämpfer & Kroppenstedt, 1996; Kämpfer et al., 1997). The results obtained were summed and compared with previously reported data (Ghosh & Roy, 2006; Tighe et al., 2000) (Table 2). The novel group could be assigned to Mesorhizobium because they lacked 20 : 3
6,9,12c and summed feature 3 (12 : 0, unknown ECL 10.928, 16 : 1 iso 1/14 : 0 3-OH) and possessed 17 : 0 iso fatty acids (Tighe et al., 2000). The strains of the novel group were separated from Mesorhizobium plurifarium because the former contain 11-methyl 18 : 17c and 15 : 0 iso and lower concentrations of 19 : 0 cyclo 8c and 16 : 0 fatty acids. The strains of the novel group could be distinguished from Mesorhizobium tianshanense group II (Tighe et al., 2000) and Mesorhizobium thiogangeticum based on the lower concentration of summed feature 7 and higher concentrations of 17 : 0 iso and 15 : 0 iso 3-OH fatty acids. The novel group differed from other Mesorhizobium species by the higher concentration of summed feature 7 and 15 : 0 iso and lower concentrations of 19 : 0 cyclo 8c and 15 : 0 iso fatty acids (Table 2).
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) were purified and cloned into the pGEM-T Easy vector (Promega) as recommended by the manufacturer. Almost full-length sequences of the cloned 16S rRNA gene were obtained by the method of Tan et al. (1997). The acquired sequences were aligned using the programs in the CLUSTAL X package (Thompson et al., 1994, 1997). A neighbour-joining tree was reconstructed and bootstrapped with 1000 replications of each sequence using the TREECON programs (Van de Peer & De Wachter, 1994). Similar to strain CCBAU 61158T (Wang et al., 2006), an insertion of about 80 bp at the 5' end was detected in these two strains between positions 75 and 76 of the Escherichia coli 16S rRNA gene sequence (Supplementary Fig. S2). The three strains of the novel group had almost identical 16S rRNA gene sequences and formed a divergent lineage in the genus Mesorhizobium (Fig. 1a). The three strains had similarities of 94.8–96.4 % with M. thiogangeticum SJTT and 98.1–99.2 % with other Mesorhizobium species when the insertion was not considered.
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; Stackebrandt et al., 2002). However, phylogenetic analysis of the 16S rRNA gene has some shortcomings in describing species. For example, the rRNA genes are too highly conserved to allow distinction among closely related species. Mosaicism, recombination and the presence of multiple copies with distinct sequences have been found in the 16S rRNA genes of rhizobia (Hashimoto et al., 2003; Haukka et al., 1996; Martínez-Romero et al., 1991; Ueda et al., 1999; van Berkum et al., 2003). The insertion discovered in the novel group may have been obtained by recombination from other sources. To corroborate the reliability of 16S rRNA gene sequence-based definition of bacterial species, sequence analysis of protein-coding genes has been recommended (Stackebrandt et al., 2002). Core metabolic genes such as atpD, dnaK, glnI, glnII and recA have been used in taxonomic and phylogenetic studies of rhizobia (Gao et al., 2004; Gaunt et al., 2001; Ghosh & Roy, 2006; Parker, 2004; Stepkowski et al., 2003; Turner & Young, 2000; Vinuesa et al., 2005; Wernegreen & Riley, 1999).
In this study, PCR amplification and sequencing of partial atpD and glnII genes of strain CCBAU 61158T was undertaken according to Gaunt et al. (2001) and Turner & Young (2000), respectively, and neighbour-joining trees were reconstructed based on the sequences (Fig. 1b, c
). The phylogenies of partial atpD and glnII sequences showed that CCBAU 61158T was a member of Mesorhizobium, supporting the conclusion from 16S rRNA gene analysis (Fig. 1a). However, slight differences were observed among the phylogenies of these three genes. CCBAU 61158T formed a lineage distantly related to Mesorhizobium species in the 16S rRNA gene phylogeny (Fig. 1a), whereas it formed a subcluster together with M. chacoense in phylogenetic trees of glnII (Fig. 1b) and atpD (Fig. 1c) sequences.
The symbiotic genes (nod and nif) are adaptive genes and in many cases have an evolutionary history independent of the rest of the genome. Comparison of their phylogenies with those derived from housekeeping genes may reveal lateral gene transfer events among rhizobia (Haukka et al., 1998). In this study, partial nodC and nifH sequences of CCBAU 61158T were amplified by using the primers and PCR conditions specified by Laguerre et al. (2001). The purified PCR products were sequenced directly as described previously (Laguerre et al., 2001). In the phylogenetic analysis of nifH (Fig. 1e), CCBAU 61158T formed a subcluster together with an M. plurifarium strain above 93.6 % similarity. The nodC gene of CCBAU 61158T was most similar to that of Rhizobium gallicum bv. gallicum R602spT (Fig. 1d), with 84.3 % similarity, and it had sequence similarity of less than 71.5 % with Mesorhizobium species. These results demonstrated that the nodC and nifH genes of strain CCBAU 61158T had different origins.
Total DNAs extracted from the strains by the method of Marmur (1961) were used for determination of DNA base composition and for DNA–DNA hybridization. The G+C content of DNA was measured using the thermal denaturation method of Marmur & Doty (1962) and E. coli K-12 as a standard. The G+C content of the representative strain CCBAU 61158T was 59 mol%, which is within the range reported for Mesorhizobium (59–64 mol%) (Jarvis et al., 1997). DNA–DNA hybridization was determined by the spectrophotometric method of De Ley (1970) and it showed that the DNA relatedness among CCBAU 61158T and the other six strains in the novel group varied between 88.8 and 100 %, with a mean of 95 % (Supplementary Table S1). With hybridization values of 12.6–34.1 %, none of the defined Mesorhizobium species showed a significant degree of DNA relatedness to the novel group.
The data obtained in this study showed that the seven strains in the novel group were very similar, but were not clones, since their protein patterns and fatty acid compositions were slightly different. Considering the variations observed in the present study and in the previous phenotypic characterization and ARDRA (Wang et al., 2006), we conclude that the seven strains in the novel group cover diverse populations.
No strain of M. thiogangeticum was included in the DNA–DNA hybridization in this work. However, we can estimate that M. thiogangeticum might share low DNA–DNA relatedness based upon the assessment of Vandamme et al. (1996), who concluded that organisms with less than 97 % 16S rRNA gene sequence similarity would not give a DNA relatedness of more than 60 % and suggested that DNA–DNA hybridization might be not necessary when the 16S rRNA gene sequence similarity was below 97 %. In our study, the 16S rRNA gene sequence similarity between the novel group and M. thiogangeticum SJTT was 94.8–96.4 % when the insertion sequence was not considered.
Host range is an important feature for root- and/or stem-nodule bacteria, and cross-nodulation tests with selected hosts are required for the description of novel rhizobial species (Graham et al., 1991). Strain CCBAU 61158T, representing the novel Mesorhizobium group, was used for cross-nodulation tests with 14 legume species. Seed treatment and inoculation were performed using the standard method of Vincent (1970). All the plants were maintained in glass tubes that were half-filled with semi-solid agar and sealed with cotton. Seedlings were grown in a greenhouse under natural daylight and seedlings of the blank control were not nodulated after 1 month. The results showed that strain CCBAU 61158T could nodulate Albizia julibrissin, Glycine max, Leucaena leucocephala and Phaseolus vulgaris, but not Pisum sativum, Astragalus adsurgens, Melilotus suaveolens, Lotus corniculatus, Trifolium repens, Glycyrrhiza glabra, Vigna radiata, Vigna unguiculata, Sesbania sp. or Robinia pseudoacacia.
Based on the results obtained in this study and in our previous work (Wang et al., 2006), we believe that the seven strains represent a novel species in the genus Mesorhizobium. This species could be differentiated by SDS-PAGE of proteins, cellular fatty acid analysis, numerical taxonomy, DNA–DNA hybridization and sequencing of the 16S rRNA, atpD, glnII, nodC and nifH genes. According to the current criteria for rhizobial species description, we propose the name Mesorhizobium albiziae sp. nov. for the seven strains; distinctive features of this species are summarized in Table 3.
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Gram-negative, aerobic, motile, non-spore-forming rods, 0.3–0.5 µm wide by 1–3 µm long. Colonies on YMA are circular, convex, white, opaque and usually 1–2 mm in diameter within 5–7 days at 28 °C. The generation time is 7–8 h in PY broth at 28 °C. Strains of this species can use fructose, lactose, L-malate, maltose, melibiose, D-raffinose, D-sorbose, sucrose, L-xylose and meso-erythritol as sole carbon sources and DL-
-alanine, L-arginine, L-glutamic acid, L-isoleucine and L-phenylalanine as sole nitrogen sources. None of the strains can use L-arabinose, rhamnose, salicin, dulcitol, citrate or L-malonate as sole carbon sources or L-cystine as a sole nitrogen source. Resistant to 300 µg ampicillin (sodium salt) ml–1, 50 µg kanamycin ml–1, 100 µg dihydrostreptomycin ml–1 and 100 µg chloromycetin ml–1. Strains can grow on YMA plates with 0.1 % erythrosin B or 1 % NaCl, but can not grow in LB broth. Alkali is produced when strains are grown in litmus milk. The species can be differentiated at the molecular level from other Mesorhizobium species by PCR-based RFLP of the 16S rRNA gene, phenotypic characterization and numerical taxonomy (Wang et al., 2006), fatty acid composition, SDS-PAGE of whole-cell proteins, total DNA hybridization and 16S rRNA gene sequencing.
The type strain is strain CCBAU 61158T (=LMG 23507T=USDA 4964T). Its G+C content is 59.0 mol% (Tm).
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ACKNOWLEDGEMENTS |
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D. X. Lin, W. F. Chen, F. Q. Wang, D. Hu, E. T. Wang, X. H. Sui, and W. X. Chen Rhizobium mesosinicum sp. nov., isolated from root nodules of three different legumes Int J Syst Evol Microbiol, August 1, 2009; 59(8): 1919 - 1923. [Abstract] [Full Text] [PDF]
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C. Vidal, C. Chantreuil, O. Berge, L. Maure, J. Escarre, G. Bena, B. Brunel, and J.-C. Cleyet-Marel Mesorhizobium metallidurans sp. nov., a metal-resistant symbiont of Anthyllis vulneraria growing on metallicolous soil in Languedoc, France Int J Syst Evol Microbiol, April 1, 2009; 59(4): 850 - 855. [Abstract] [Full Text] [PDF]
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T. X. Han, L. L. Han, L. J. Wu, W. F. Chen, X. H. Sui, J. G. Gu, E. T. Wang, and W. X. Chen Mesorhizobium gobiense sp. nov. and Mesorhizobium tarimense sp. nov., isolated from wild legumes growing in desert soils of Xinjiang, China Int J Syst Evol Microbiol, November 1, 2008; 58(11): 2610 - 2618. [Abstract] [Full Text] [PDF]
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S. H. Guan, W. F. Chen, E. T. Wang, Y. L. Lu, X. R. Yan, X. X. Zhang, and W. X. Chen Mesorhizobium caraganae sp. nov., a novel rhizobial species nodulated with Caragana spp. in China Int J Syst Evol Microbiol, November 1, 2008; 58(11): 2646 - 2653. [Abstract] [Full Text] [PDF]
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T. X. Han, E. T. Wang, L. J. Wu, W. F. Chen, J. G. Gu, C. T. Gu, C. F. Tian, and W. X. Chen Rhizobium multihospitium sp. nov., isolated from multiple legume species native of Xinjiang, China Int J Syst Evol Microbiol, July 1, 2008; 58(7): 1693 - 1699. [Abstract] [Full Text] [PDF]
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D. X. Lin, E. T. Wang, H. Tang, T. X. Han, Y. R. He, S. H. Guan, and W. X. Chen Shinella kummerowiae sp. nov., a symbiotic bacterium isolated from root nodules of the herbal legume Kummerowia stipulacea Int J Syst Evol Microbiol, June 1, 2008; 58(6): 1409 - 1413. [Abstract] [Full Text] [PDF]
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