Abstract
Strain DKSPLA3T, a novel Gram-negative, catalase-positive, oxidase-positive, non-spore-forming, aerobic, non-nitrogen-fixing, non‐motile bacterium was isolated from Quercus variablis leaf, in Zunyi, Guizhou, China. Growth occurred at 4–37 °C (optimum 28 °C), pH 4.0–9.0 (optimum pH 7.0) and up to 4.0% (w/v) NaCl (optimum under 2.0%, w/v). Phylogeny based on 16S rRNA gene indicated that strain DKSPLA3T was a novel species in the genus Rhizobium, which was supported by average nucleotide identity (ANI) and digital DNA-DNA hybridization (dDDH) values. The predominant fatty acids of strain DKSPLA3T were C16:0, C18:1 ω7c and/or C18:1 ω6c and C18:1 ω7c 11-methyl. The major respiratory quinone was Q-10. Major polar lipids were diphosphatidyl glycerol (DPG), phosphatidyl glycerol (PG), phosphatidylethanolamine (PE), phosphatidylmonomethylethanolamine (PME), phosphatidylcholine (PC), two unidentified phospholipids (PL) and nine unidentified lipids (L). The genomic G + C content was 64.47 mol%. Based on the phenotypic, phylogenetic and genotypic data, DKSPLA3T should be classified as a novel species in the genus Rhizobium, for which the name Rhizobium quercicola sp. nov. (KCTC 82843T = CFCC 16,707T) is proposed.
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Data availability
The GenBank/EMBL/DDBJ accession numbers for the draft genome sequence and the 16S rRNA gene sequence of Rhizobium quercicola DKSPLA3T are NZ_JAJOZR000000000 and OL691139, respectively.
References
Aziz RK, Bartels D, Best AA, Dejongh M, Disz T et al (2008) The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9:75. https://doi.org/10.1186/1471-2164-9-75
Besemer J, Lomsadze A, Borodovsky M (2001) GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions. Nucleic Acids Res 29(12):2607–2618. https://doi.org/10.1093/nar/29.12.2607
Blin K, Shaw S, Steinke K, Villebro R, Yup ZN, LS, (2019) AntiSMASH 5.0: updates to the secondary metabolite genome mining pipeline. Nucleic Acids Res 47:81–87. https://doi.org/10.1093/nar/gkz310
Celador-Lera L, Menendez E, Peix A, Igual JM, Velazquez E, Rivas R (2017) Rhizobium zeae sp. nov., isolated from maize (Zea mays L.) roots. Int J Syst Evol Microbiol 67:2306–2311. https://doi.org/10.1099/ijsem.0.001944
Collins MD (1985) Isoprenoid quinone analysis in classification and identification. In Goodfellow London, pp 267–287.
Chen W, Sheng XF, He LY, Huang Z (2015) Rhizobium yantingense sp. nov., a mineral-weathering bacterium. Int J Syst Evol Microbiol 65:412–417. https://doi.org/10.1099/ijs.0.064428-0
Frank B (1889) Über die Pilzsymbiose der Leguminosen. Ber Dtsch Bot Ges 7:332–3463
Gao J, Sun P, Wang X, Lv FY, Mao XJ, Sun JQ (2017) Rhizobium wenxiniae sp. nov., an endophytic bacterium isolated from maize root. Int J Syst Evol Microbiol 67(8):2798–2803. https://doi.org/10.1099/ijsem.0.002025
Garcia-Fraile P, Rivas R, Willems A, Peix A, Martens M, Martinez-Molina E, Mateos PF, Velazquez E (2007) Rhizobium cellulosilyticum sp. nov., isolated from sawdust of Populus alba. Int J Syst Evol Microbiol 57:844–848. https://doi.org/10.1099/ijs.0.64680-0
Gerhardt P, Costilow RN, Krieg RGE, Nester EW, Phillips GB, Wood WA (1981) Manual of methods for general bacteriology. American Society for Microbiology, Washington, DC
Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM (2007) DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57:81–91. https://doi.org/10.1099/ijs.0.64483-0
Hunter WJ, Kuykendall LD, Manter DK (2007) Rhizobium selenireducens sp. nov.: a selenite-reducing α-Proteobacteria isolated from a bioreactor. Curr Microbiol 55:455–460. https://doi.org/10.1007/s00284-007-9020-9
Kang JP, Huo Y, Kim YJ, Ahn JC, Hurh J, Yang DK, Yang DC (2019) Rhizobium panacihumi sp. nov., an isolate from ginseng-cultivated soil, as a potential plant growth promoting bacterium. Arch Microbiol 201:99–105. https://doi.org/10.1007/s00203-018-1578-z
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Laranjo M, Alexandre A, Oliveira S (2014) Legume growth-promoting rhizobia: an overview on the Mesorhizobium genus. Microbiol Res 169:2–17. https://doi.org/10.1016/j.micres.2013.09.012
Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) In Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 115–175
Li R, Zhu H, Ruan J, Qian WB, Fang XD, Shi ZB, Li YR, Shan G, Kristiansen K, Li SG, Yang HM, Wang J, Wang J (2010) De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 20(2):265–272. https://doi.org/10.1101/gr.097261.109
Li W, Jaroszewski L, Godzik A (2002) Tolerating some redundancy significantly speeds up clustering of large protein databases. Bioinformatics 1:77–82. https://doi.org/10.1093/bioinformatics/18.1.77
Lindström K, Mousavi SA (2020) Effectiveness of nitrogen fixation in rhizobia. Microb Biotechnol 13(5):1314–1335. https://doi.org/10.1111/1751-7915.13517
Liu L, Liang L, Xu LJ, Chi M, Zhang XX, Li LB (2020) Rhizobium deserti sp. nov isolated from biological soil crusts collected at Mu Us sandy land. China Curr Microbiol 77:327–333. https://doi.org/10.1007/s00284-019-01831-4
Liu Y, Wang RP, Ren C, Lai QL, Zeng RY (2015) Rhizobium marinum sp. nov., a malachite-green-tolerant bacterium isolated from seawater. Int J Syst Evol Microbiol 65:449–4454. https://doi.org/10.1099/ijsem.0.000593
Long SR (1989) Rhizobium-legume nodulation: life together in the underground. Cell 56:203–214. https://doi.org/10.1016/0092-8674(89)90893-3
Máthé I, Tóth E, Mentes A, Szabó A, Márialigeti K, Schumann P, Felföldi T (2018) A new Rhizobium species isolated from the water of a crater lake, description of Rhizobium aquaticum sp. nov. Antonie Van Leeuwenhoek 111:2175–2183. https://doi.org/10.1007/s10482-018-1110-0
Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M (2013) Genome sequence–based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 14:60–73. https://doi.org/10.1186/1471-2105-14-60
Minnikin DE, O’Donnell AG, 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 Microbiol Methods 2:233–241
Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids. MIDI, Technical Note 101. MIDI Inc. Newark, Delaware, USA.
Stackebrandt E, Ebers J (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 33:152–155
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882. https://doi.org/10.1093/nar/25.24.4876
Tighe SW, de Lajudie P, Dipietro K, Lindström K, Nick G, Jarvis BD (2000) Analysis of cellular fatty acids and phenotypic relationships of Agrobacterium, Bradyrhizobium, Mesorhizobium, Rhizobium and Sinorhizobium species using the Sherlock microbial identification system. Int J Syst Evol Microbiol 50:787–801. https://doi.org/10.1099/00207713-50-2-787
Tindall BJ (1990) Lipid composition of Halobacterium lacusprofundi. FEMS Microbiol Lett 66:199–202
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 2:76–86
Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017a) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole–genome assemblies. Int J Syst Evol Microbiol 67:1613–1617. https://doi.org/10.1099/ijsem.0.001755
Yoon SH, Ha SM, Lim J, Kwon S, Chun J (2017b) A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Van Leeuwenhoek 110:1281–1286. https://doi.org/10.1007/s10482-017-0844-4
Yoon JH, Kang SJ, Yi HS, Oh TK, Ryu CM (2010) Rhizobium soli sp. nov., isolated from soil. Int J Syst Evol Microbiol 60:1387–1393. https://doi.org/10.1099/ijs.0.013094-0
Young JM, Kuykendall LD, Martínez-Romero E, Kerr A, Sawada H (2001) A revision of Rhizobium Frank 1889, with an emended description of the genus, and the inclusion of all species of Agrobacterium Conn 1942 and Allorhizobium undicola de Lajudie, 1998 as new combinations: Rhizobium radiobacter, R. rhizogenes, R. rubi, R. undicola and R. vitis. Int J Syst Evol Microbiol 51:89–103. https://doi.org/10.1099/00207713-51-1-89
Yuan T, Liu LH, Huang SF, Taher AH, Tan ZY, Wu GJ, Peng GX (2018) Rhizobium wuzhouense sp nov. isolated from roots of oryza officinalis. Int J Syst Evol Microbiol 68(9):2918–2923. https://doi.org/10.1099/ijsem.0.002921
Zhang L, Shi X, Si M, Li C, Zhu L, Zhao L, Shen X, Wang Y (2014) Rhizobium smilacinae sp. nov., an endophytic bacterium isolated from the leaf of Smilacina japonica. Antonie Van Leeuwenhoek 106:715–723. https://doi.org/10.1007/s10482-014-0241-1
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This work was supported by the National Microbial Resource Center of the Ministry of Science and Technology of the People’s Republic of China (NMRC-2022-7).
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LY and WCB collected the material. WCB and BDR performed the experiments. WCB wrote the manuscript. JN, XH, PCG and LY made revisions. All authors read and approved the manuscript.
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Wang, CB., Bian, DR., Jiang, N. et al. Rhizobium quercicola sp. nov., isolated from the leaf of Quercus variablis in China. Arch Microbiol 204, 596 (2022). https://doi.org/10.1007/s00203-022-03188-y
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DOI: https://doi.org/10.1007/s00203-022-03188-y