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Mesorhizobium rhizophilum sp. nov., a 1-aminocyclopropane-1-carboxylate deaminase producing bacterium isolated from rhizosphere of maize in Northeast China

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Abstract

A novel 1-aminocyclopropane-1-carboxylate deaminase producing bacterium, Gram- stain-negative, aerobic, motile, rod-shaped strain designated YM1C-6-2T was isolated from rhizosphere of maize grown in Northeast China. The 16S rRNA gene sequence analysis indicated that strain YM1C-6-2T belongs to the genus Mesorhizobium and is closely related to Mesorhizobium alhagi CCNWXJ12-2T and M. camelthorni CCNWXJ40-4T with sequence similarities of 98.4% and 97.9%, respectively. Multilocus sequence analysis of other housekeeping genes revealed that the new isolates YM1C-6-2T forms a phylogenetically group with some species in the genus Mesorhizobium. The genome size of strain YM1C-6-2T was 5.51 Mb, comprising 5378 predicted genes with a DNA G+C content of 64.5%. The average nucleotide identity and digital DNA–DNA hybridization comparisons between YM1C-6-2T and the most related type strains showed values below the accepted threshold for species discrimination. The major fatty acids of strain YM1C-6-2T were C19:0 cyclo ω8c (47.5%), summed feature 8 (C18:1ω7c and/or C18:1ω6c) (19.5%) and C16:0 (15.1%), which differed from the closely related reference strains in their relative abundance. The major polar lipids consist of diphosphatidylglycerol, phosphatidylethanolamine, phosphatidylglycerol, phosphatidylcholine and an unidentified aminophospholipid. The predominant ubiquinone was identified as Quinone 10. Phenotypic and biochemical analysis results indicated that strain YM1C-6-2T can be distinguished from closely related type strains. Based on the above results, strain YM1C-6-2T represents a novel species of the genus Mesorhizobium, for which the name Mesorhizobium rhizophilum sp. nov. is proposed with YM1C-6-2T (= CGMCC 1.15487T = DSM 101712T) as the type strain.

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References

  • Bligh EG, Dyer JW (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    Article  CAS  PubMed  Google Scholar 

  • Breznak JA, Costilow RN (2007) Physicochemical factors in growth. In: Beveridge TJ, Breznak JA, Marzluf GA, Schmidt TM, Snyder LR (eds) Methods for general and molecular bacteriology, 3rd edn. American Society for Microbiology, Washington, pp 309–329

    Google Scholar 

  • Chen WM, Zhu WF, Bontemps C, Young PW, Wei GH (2010) Mesorhizobium alhagi sp. nov. isolated from wild Alhagi sparsifolia in north-western China. Int J Syst Evol Microbiol 60:958–962

    Article  CAS  PubMed  Google Scholar 

  • Chen WM, Zhu WF, Bontemps C, Young JP, Wei GH (2011) Mesorhizobium camelthorni sp. nov., isolated from Alhagi sparsifolia. Int J Syst Evol Microbiol 61:574–579

    Article  CAS  PubMed  Google Scholar 

  • Chun J, Oren A, Ventosa A, Christensen H, Arahal DR, da Costa MS, Rooney AP, Yi H, Xu XW, De Meyer S, Trujillo ME (2018) Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 68:461–466

    Article  CAS  PubMed  Google Scholar 

  • Collins MD, Jones D (1980) Lipids in the classification and identification of coryneform bacteria containing peptidoglycans based on 2,4-diaminobutyric acid. J Appl Microbiol 48:459–470

    CAS  Google Scholar 

  • Consden R, Gordon AH (1948) The effect of salt on partition chromatograms. Nature 162:180–181

    Article  CAS  PubMed  Google Scholar 

  • Cowan ST, Steel KJ (1996) Manual for the identification of medical bacteria. Cambridge University Press, London, p 232

    Google Scholar 

  • Delcher AL, Bratke KA, Powers EC, Salzberg SL (2007) Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23:673–679

    Article  CAS  PubMed  Google Scholar 

  • Delory GE, King EJ (1945) A sodium carbonate-bicarbonate buffer for alkaline phosphatases. Biochem J 39:245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376

    Article  CAS  PubMed  Google Scholar 

  • Fu GY, Yu XY, Zhang CY, Zhao Z, Wu D, Su Y, Wang RJ, Han SB, Wu M, Sun C (2017) Mesorhizobium oceanicum sp.nov., isolated from deep seawater. Int J Syst Evol Microbiol 67:2739–2745

    Article  CAS  PubMed  Google Scholar 

  • Gao JL, Yuan M, Wang XM, Qiu TL, Li JW, Liu HC, Li XA, Chen J, Sun JG (2015a) Variovorax guangxiensis sp. nov. an aerobic, 1-aminocyclopropane-1-carboxylate deaminase producing bacterium isolated from banana rhizosphere. Antonie Van Leeuwenhoek 107:65–72

    Article  PubMed  CAS  Google Scholar 

  • Gao M, Zhou JJ, Wang ET, Chen Q, Xu J, Sun JG (2015b) Multiphasic characterization of a plant growth promoting bacterial strain, Burkholderia sp. 7016 and its effect on tomato growth in the field. J Integr Agric 14:1855–1863

    Article  CAS  Google Scholar 

  • Gao JL, Sun P, Wang XM, Cheng ST, Lv FY, Sun JG (2016) Sphingomonas zeicaulis sp. nov., an endophytic bacterium isolated from maize root. Int J Syst Evol Microbiol 66:3755–3760

    Article  CAS  PubMed  Google Scholar 

  • Gao JL, Sun P, Wang XM, Lv FY, Mao XJ, Sun JG (2017) Rhizobium wenxiniae sp. nov. an endophytic bacterium isolated from maize root. Int J Syst Evol Microbiol 67:2798–2803

    Article  CAS  PubMed  Google Scholar 

  • Gao JL, Sun P, Sun XH, Tong S, Yan H, Sun JG (2018) Caulobacter zeae sp. nov. and Caulobacter radicis sp. nov., novel endophytic bacteria isolated from maize root (Zea mays L.). Syst Appl Microbiol 41:604–610

    Article  CAS  PubMed  Google Scholar 

  • Garrity GM, Holt JG (2001) The road map to the Manual. In: Garrity GM, Boone DR, Castenholz RW (eds) Bergey’s manual of systematic bacteriology, vol 1, 2nd edn. Springer, New York, pp 119–166

    Chapter  Google Scholar 

  • Ghosh W, Roy P (2006) Mesorhizobium thiogangeticum sp.nov., a novel sulfur-oxidizing chemolithoautotroph fromrhizosphere soil of an Indian tropical leguminous plant. Int J Syst Evol Microbiol 56:91–97

    Article  CAS  PubMed  Google Scholar 

  • Glick BR, Cheng Z, Czarny J, Duan J (2007) Promotion of plant growth by ACC deaminase-producingsoil bacteria. Eur J Plant Pathol 119:329–339

    Article  CAS  Google Scholar 

  • Hegazi NA, Hamza AM, Osman A, Ali S, Sedik MZ (1998) Modified combined carbon N-deficient medium for isolation, enumeration and biomass production of diazotrophs. In: Kauser MA, Sajjad MM (eds) Nitrogen fixation with nonlegumes. Kluwer Academic Publishers, Dordrecht, pp 247–253

    Chapter  Google Scholar 

  • Jarvis B, Van Berkum P, Chen W, Nour S, Fernandez M, Cleyet-Marel J, Gillis M (1997) Transfer of Rhizobium loti, Rhizobium huakuii, Rhizobium ciceri, Rhizobium mediterraneum, and Rhizobium tianshanense to Mesorhizobium gen.nov. Int J Syst Evol Microbiol 47:895–898

    Article  Google Scholar 

  • Ji ZJ, Yan H, Cui QG, Wang ET, Chen WX, Chen WF (2015) Genetic divergence and gene flow among Mesorhizobium strains nodulating the shrub legume Caragana. Syst Appl Microbiol 38:176–183

    Article  CAS  PubMed  Google Scholar 

  • Komagata K, Suzuki K (1988) Lipid and cell-wall analysis in bacterial systematics. Methods Microbiol 19:161–207

    Article  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lagesen K, Hallin P, Rodland EA, Staerfeldt HH, Rognes T (2007) RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 35:3100–3108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackerandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematic. Wiley, Chichester, pp 115–175

    Google Scholar 

  • Li J, Xin W, Xu ZZ, Xiang FQ, Zhang JJ, Xi LJ, Qu BJ, Liu JG (2019) Mesorhizobium carbonis sp. Nov. isolated from coal bed water. Antonie Van Leeuwenhoek 112:1221–1229

    Article  CAS  PubMed  Google Scholar 

  • Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo R, Liu B, Xie Y, Li Z, Huang W (2012) SOAP denovo 2: an empirically improved memory-efficient short-read de novo assembler. Giga Sci 1:1–6

    Article  Google Scholar 

  • Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M (2013) Genomesequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform 14:60

    Article  Google Scholar 

  • Mergaert J, Swings J (2005) Family IV. Phyllobacteriaceae fam. nov. Bergey’s manual of systematic bacteriology. In: Brenner DJ, Krieg NR, Staley JT, Garrity GM (eds) (The Proteobacteria), Part C (The alpha-, beta-, delta-, and Epsilonproteobacteria, vol 2, 2nd edn. Springer, New York, p 393

    Google Scholar 

  • Miller JH (1972) Experiments in molecular genetics. Cold Spring Harbour Laboratory Press, Cold Spring Harbour

    Google Scholar 

  • Minnikin D, O’Donnell A, Goodfellow M, Alderson G, Athalye M, Schaal A, Parlett JH (1984) An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Appl Bacteriol 2:233–241

    CAS  Google Scholar 

  • Nguyen TM, Pham VHT, Kim J (2015) Mesorhizobium soli sp. nov. a novel species isolated from the rhizosphere of Robinia pseudoacacia L. in South Korea by using a modified culture method. Antonie Van Leeuwenhoek 108:301–310

    Article  CAS  PubMed  Google Scholar 

  • Penrose DM, Glick BR (2003) Methods for isolating and characterizing ACC deaminase-containing plant growth promoting rhizobacteria. Physiol Plant 118:10–15

    Article  CAS  PubMed  Google Scholar 

  • Rai A, Nabti E (2017) Plant growth-promoting bacteria: importance in vegetable production. Microbial strategies for vegetable production. Springer, Berlin

    Google Scholar 

  • Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids, MIDI technical note 101. Microbial ID Inc, Newark

    Google Scholar 

  • Sun YM, Zhang NN, Wang ET, Yuan HL, Yang JS (2009) Influence of intercropping and intercropping plus rhizobial inoculation on microbial activity and community composition in rhizosphere of alfalfa (Medicago sativa L.) and Siberian wild rye (Elymus sibiricus L.). FEMS Microbiol Ecol 70:218–226

    Article  CAS  Google Scholar 

  • Wang Q, Zhu W, Wang ET, Zhang LS, Li X (2016) Genomic identification of rhizobia-related strains and threshold of ANI and core-genome for family, genus and species. Int J Environ Agric Res: IJOEAR 2:76–86

    Google Scholar 

  • Yuan CG, Jiang Z, Xiao M, Zhou EM, Kim CJ, Hozzein WN, Park DJ, Zhi XY, Li WJ (2016) Mesorhizobium sediminum sp. nov., isolated from deep-sea sediment. Int J Syst Evol Microbiol 66:4797–4802

    Article  CAS  PubMed  Google Scholar 

  • Zhang YM, Tian CF, Sui XH, Chen WF, Chen WX (2012) Robust markers reflecting phylogeny and taxonomy of rhizobia. PLoS ONE 7:e44936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We are very grateful to Professor Gehong Wei (North West A & F University) for kindly providing the experimental reference strains: Mesorhizobium alhagi CCNWXJ12-2T and Mesorhizobium camelthorni CCNWXJ40-4T. This research work was supported financially by the National Natural Science Foundation of China (No. 31870003) and Science & Technology Innovation Project of Beijing Academy of Agricultural and Forestry Sciences (KJCX20200519).

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Authors and Affiliations

  1. Beijing Agro-Biotechnology Research Center, Beijing Academy of Agriculture and Forestry/Beijing Key Laboratory of Agricultural Genetic Resources and Biotechnology, Beijing, 100097, People’s Republic of China

    Jun-lian Gao, Jing Xue, Yu-chen Sun, Li-wei Wang & Xiuhai Zhang

  2. Key Laboratory of Microbial Resources, Ministry of Agriculture and Rural Affairs/ Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing, 100081, People’s Republic of China

    Shuai Tong & Jian-guang Sun

  3. Key Laboratory of State Forestry Administration on Forest Protection, Research Institute of Forest Ecology Environment and Protection, Chinese Academy of Forestry, Beijing, 100091, People’s Republic of China

    Han Xue

  4. Departamento de Microbiología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, 11340, Mexico, DF, Mexico

    En Tao Wang

  5. College of Animal Science and Technology, Hebei Agricultural University, Baoding, 071001, People’s Republic of China

    Hui Yan

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  1. Jun-lian Gao
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Contributions

JGS and XHZ designed research and project outline. JLG, YCS, HX and ST performed isolation, deposition and polyphasic taxonomy. JX, HY and ETW performed genome analysis. LWW contributed to the polar lipid analysis. JLG and JGS drafted the manuscript. ETW and XHZ revised the manuscript. All authors read and approved the final manuscript.

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Correspondence to Xiuhai Zhang or Jian-guang Sun.

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10482_2020_1425_MOESM1_ESM.tif

Fig. S1. Two-dimensional thin layer chromatograms of polar lipids for strain YM1C-6-2T, the biomass used for lipids extraction was obtained from cultures grown on YMA plate at 30 ºC for 3 days. The lipids were stained with 5% ethanolic molybdophosphoric acid for total lipids (A), ninhydrin (B) and molybdenum blue(C). Abbreviations: DPG, diphosphatidylglycerol; PG, phosphatidylglycerol; PC, Phosphatidylcholin; PE, Phosphatidylethanolamin; APL, unidentified aminophospholipid. (TIF 107 kb)

10482_2020_1425_MOESM2_ESM.tif

Fig. S2. Scanning electron micrographs of cells of strain YM1C-6-2T showing cells grown in YM broth at 30 ºC for 2 days.

(TIF 155 kb)

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Gao, Jl., Xue, J., Sun, Yc. et al. Mesorhizobium rhizophilum sp. nov., a 1-aminocyclopropane-1-carboxylate deaminase producing bacterium isolated from rhizosphere of maize in Northeast China. Antonie van Leeuwenhoek 113, 1179–1189 (2020). https://doi.org/10.1007/s10482-020-01425-2

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