Abstract
A Nocardia-like actinobacterial strain, designated YIM TG2190T, was isolated from rhizosphere soil of Psammosilene tunicoides collected from Gejiu, Yunnan province, China. The cells of strain YIM TG2190T were observed to be Gram-stain positive and non-motile. The strain forms extensively branched substrate mycelia that fragments into rod-shaped elements. The 16S rRNA gene sequence analysis showed that strain YIM TG2190T is closely related to Nocardia nova (97.5%), Nocardia jiangxiensis (97.1%) and Nocardia miyunensis (96.8%). Growth occurs at 4–30 °C (optimum 28 °C), pH 6.0–8.0 (optimum pH 7.0) and the strain can tolerate NaCl (w/v) up to 3% (optimum 0–1%). The cell walls were found to contain meso-diaminopimelic acid. The whole-cell sugars were identified as glucose, mannose, ribose, galactose, arabinose and fucose. The polar lipids were identified as diphosphatidylglycerol, phosphatidylethanolamine, phosphatidylinositol mannosides, phosphatidylglycerol and an unidentified phospholipid. The menaquinones detected were MK-9 (H2) and MK-8 (H4). The major fatty acids (> 5%) were found to be C16:0 (33.9%), summed feature 3 (21.7%), C18:0 10-methyl TBSA (13.7%) and C18:1ω9c (7.0%). The DNA G+C content was determined to be 61.1 mol%. DNA-DNA relatedness between the strain YIM TG2190T and N. nova CGMCC 4.1705T, N. jiangxiensis CGMCC 4.1905T and N. miyunensis CGMCC 4.1904T were 46.9 ± 2.6, 36.8 ± 1.3, and 35.7 ± 2.6%, respectively, values which are less than the threshold value (70%) for the delineation of prokaryotic genomic species. The phenotypic, chemotaxonomic and phylogenetic data indicates that strain YIM TG2190T represents a novel species of the genus Nocardia, for which the name Nocardia zhihengii sp. nov. is proposed. The type strain is YIM TG2190T (=KCTC 39596T = DSM 100515T).
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References
Athalye M, Goodfellow M, Lacey J, White R (1985) Numerical classification of Actinomadura and Nocardiopsis. Int J Syst Bacteriol 35:86–98
Bai JL, Wang Y, Qin S, Ding P, Xing K, Yuan B, Cao CL, Huang Y, Zhang YQ, Jiang JH (2016) Nocardia jiangsuensis sp. nov., an actinomycete isolated from coastal soil. Int J Syst Evol Microbiol 66:4633–4638
Christensen H, Angen O, Mutters R, Olsen JE, Bisgaard M (2000) DNA–DNA hybridization determined in micro-wells using covalent attachment of DNA. Int J Syst Evol Microbiol 50:1095–1102
Collins MD, Jones D (1980) Lipids in the classification and identification of coryneform bacteria containing peptidoglycan based on 2,4-diaminobutyric acid. J Appl Bacteriol 48:459–470
Collins MD, Pirouz T, Goodfellow M, Minnikin DE (1977) Distribution of menaquinones in actinomycetes and corynebacteria. J Gen Microbiol 100:221–230
Cui Q, Wang L, Huang Y, Liu Z, Goodfellow M (2005) Nocardia jiangxiensis sp. nov. and nocardia miyunensis sp. nov., isolated from acidic soils. Int J Syst Evol Microbiol 55:1921–1925
Ezaki T, Hashimoto Y, Yabuuchi E (1989) Fluorometric deoxyribonucleic acid-deoxyribonucleic acid hybridization in microdilution wells as an alternative to membrane filter hybridization in which radioisotopes are used to determine genetic relatedness among bacterial strains. Int J Syst Bacteriol 39:224–229
Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–789
Fitch WM (1971) Toward defining the course of evolution: minimum change for a specific tree topology. Syst Zool 20:406–416
Gonzalez C, Gutierrez C, Ramirez C (1978) Halobacterium vallismortis sp. nov., an amylolytic and carbohydratemetabolizing, extremely halophilic bacterium. Can J Microbiol 24:710–715
Goodfellow M, Maldonado LA (2012) Genus I. Nocardia. In: Goodfellow M, Kämpfer P, Busse H-J, Trujillo ME, Suzuki K-I, Ludwig W, Whitman WB (eds) Bergey’s manual of systematic bacteriology, the Actinobacteria, vol 5, 2nd edn. Springer, New York, pp 376–418
Hasegawa T, Takizawa M, Tanida S (1983) A rapid analysis for chemical grouping of aerobic actinomycetes. J Gen Microbiol 29:319–322
Hoshino Y, Watanabe K, Iida S, Suzuki S, Kudo T, Kogure T, Yazawa K, Ishikawa J, Kroppenstedt RM, Mikami Y (2007) Nocardia terpenica sp. nov., isolated from Japanese patients with nocardiosis. Int J Syst Evol Microbiol 57:1456–1460
Hu HY, Lim BR, Goto N, Fujie K (2001) Analytical precision and repeatability of respiratory quinones for quantitative study of microbial community structure in environmental samples. J Microbiol Methods 47:17–24
Kaewkla O, Franco CM (2010) Nocardia callitridis sp. nov., an endophytic actinobacterium isolated from a surface-sterilized root of an australian native pine tree. Int J Syst Evol Microbiol 60:1532–1536
Kageyama A, Yazawa K, Mukai A, Kinoshita M, Takata N, Nishimura K, Kroppenstedt RM, Mikami Y (2004) Nocardia shimofusensis sp. nov., isolated from soil, and Nocardia higoensis sp. nov., isolated from a patient with lung nocardiosis in Japan. Int J Syst Evol Microbiol 54:1927–1931
Kelly KL (1964) Inter-society color council–national bureau of standards color name charts illustrated with centroid colors. US Government Printing Office, Washington
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Kinyoun JJ (1915) A note on Uhlenhuth’s method for sputum examination for tubercle bacilli. Am J Public Health 5:867–870
Kovacs N (1956) Identification of Pseudomonas pyocyanea by the oxidase reaction. Nature 178:703–704
Kroppenstedt RM (1982) Separation of bacterial menaquinones by HPLC using reverse phase (RP18) and a silver loaded ion-exchanger as stationary phases. J Liq Chromatogr 5:2359–2367
Kubica GP, Beam RE (1961) The arylsulfatase activity of acidfast bacilli. II. The differentiation of Mycobacterium avium from the unclassified group III nonphotochromogenic mycobacteria. Am Rev Resp Dis 83:733–736
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
Lamm AS, Khare A, Conville P, Lau PC, Bergeron H, Rosazza JP (2009) Nocardia iowensis sp. nov., an organism rich in biocatalytically important enzymes and nitricoxide synthase. Int J Syst Evol Microbiol 59:2408–2414
Li WJ, Xu P, Schumann P, Zhang YQ, Pukall R, Xu LH, Stackebrandt E, Jiang CL (2007) Georgenia ruanii sp. nov., a novel actinobacterium isolated from forest soil in Yunnan (China) and emended description of the genus Georgenia. Int J Syst Evol Microbiol 57:1424–1428
Li S, Ming H, Duan YY, Huang JR, Zhao ZL, Zhang LY, Ji WL, Meng XL, Li WJ, Nie GX (2017a) Nocardia tengchongensis, sp. nov., isolated from a soil sample. Antonie Van Leewenhoek 110:1149–1155
Li QQ, Han MX, Fang BZ, Jiao JY, Liu L, Yang ZW, Zhang WQ, Wei DQ, Li WJ (2017b) Nocardia cavernae sp. nov., a novel actinobacterium isolated from a karst cave sample. Int J Syst Evol Microbiol 67:2998–3003
Liu C, Guan X, Li Y, Li W, Ye L, Kong X, Song J, Wang X, Xiang W (2016) Nocardia camponoti sp. nov., a novel actinomycete isolated from the head of an ant (Camponotus japonicas Mayr). Int J Syst Evol Microbiol 66:1900–1905
Mesbah M, Premachandran U, Whitman WB (1989) Precise measurement of the G+C content of deoxyribonucleic acid by high-performance liquid chromatography. Int J Syst Bacteriol 39:159–167
Minnikin DE, Collins MD, Goodfellow M (1979) Fatty acid and polar lipid composition in the classification of Cellulomonas, Oerskovia and related taxa. J Appl Bacteriol 47:87–95
Minnikin DE, Hutchinson IG, Caldicott AB, Goodfellow M (1980) Thin layer chromatography of methanolysates of mycolic acid-containing bacteria. J Chromatogr A 188:221–233
Minnikin D, O’donnell A, Goodfellow M, Alderson G, Athalye M, Schaal A, Parlett J (1984) An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 2:233–241
Nie GX, Ming H, Li S, Zhou EM, Cheng J, Tang X, Feng HG, Tang SK, Li WJ (2012) Amycolatopsis dongchuanensis sp. nov., a novel actinobacterium isolated from dry-hot valley in Yunnan, south-west China. Int J Syst Evol Microbiol 62:2650–2656
Nikou MM, Ramezani M, Amoozegar MA, Rasooli M, Harirchi S, Shahzadeh Fazeli SA, Schumann P, Sproer C, Ventosa A (2015) Nocardia halotolerans sp. nov., a halotolerant actinomycete isolated from saline soil. Int J Syst Evol Microbiol 65:3148–3154
Pridham TG, Gottlieb D (1948) The utilization of carbon compounds by some actinomycetales as an aid for species determination. J Bacteriol 56:107–114
Rodríguez-Nava V, Khan ZU, Potter G, Kroppenstedt RM, Boiron P, Laurent F (2007) Nocardia coubleae sp. nov., isolated from oil-contaminated Kuwaiti soil. Int J Syst Evol Microbiol 57:1482–1486
Rosselló-Móra R, Trujillo ME, Sutcliffe IC (2017) Introducing a digital protologue: A timely move towards a database-driven systematics of archaea and bacteria. Syst Appl Microbiol 40(3):121–122
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic tree. Mol Biol Evol 4:406–425
Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids. MIDI Technical Note 101. MIDI, Newark, DE, USA
Schupp T, Traxler P, Auden JA (1981) New rifamycins produced by a recombinant strain of Nocardia mediterranei. J Antibiot (Tokyo) 34:965–970
Shirling EB, Gottlieb D (1966) Methods for characterization of Streptomyces species. Int J Syst Bacteriol 16:313–340
Stackebrandt E, Goebel BM (1994) Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44:846–849
Staneck JL, Roberts GD (1974) Simplified approach to identification of aerobic actinomycetes by thin-layer chromatography. Appl Mirobiol 28:226–231
Tanasupawat S, Phongsopitanun W, Suwanborirux K, Ohkuma M, Kudo T (2016) Nocardia rayongensis sp. nov., isolated from thai peat swamp forest soil. Int J Syst Evol Microbiol 66:1950–1955
Tang SK, Wang Y, Chen Y, Lou K, Cao LL, Xu LH, Li WJ (2009) Zhihengliuella alba sp. nov., and emended description of the genus Zhihengliuella. Int J Syst Evol Microbiol 59:2025–2032
Thawai C, Rungjindamai N, Klanbut K, Tanasupawat S (2016) Nocardia xestospongiae sp. nov., isolated from a marine sponge in the Andaman sea. Int J Syst Evol Microbiol 67:1451–1456
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
Trevisan V (1889) I Generi e le Specie delle Batteriacee. Zanaboni & Gabuzzi, Milan, pp 1–35
Wang Y, Liu W, Feng WW, Zhou XQ, Bai JL, Yuan B, Ju XY, Cao CL, Huang Y, Jiang JH, Lv AJ, Qin S (2015) Nocardia rhizosphaerae sp. nov., a novel actinomycete isolated from the coastal rhizosphere of Artemisia Linn., China. Antonie Van Leeuwenhoek 108:31–39
Xing K, Qin S, Fei SM, Lin Q, Bian GK, Miao Q, Wang Y, Cao CL, Tang SK, Jiang JH, Li WJ (2011) Nocardia endophytica sp. nov., an endophytic actinomycete isolated from the oil-seed plant Jatropha curcas L. Int J Syst Evol Microbiol 61:1854–1858
Xu P, Li WJ, Tang SK, Zhang YQ, Chen GZ, Chen HH, Xu LH, Jiang CL (2005) Naxibacter alkalitolerans gen. nov., sp. nov., a novel member of the family ‘Oxalobacteraceae’ isolated from China. Int J Syst Evol Microbiol 55:1149–1153
Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA and whole genome assemblies. Int J Syst Evol Microbiol 7:1613–1617
Zhao GZ, Li J, Zhu WY, Klenk HP, Xu LH, Li WJ (2011) Nocardia artemisiae sp. nov., an endophytic actinobacterium isolated from a surface-sterilized stem of Artemisia annua L. Int J Syst Evol Microbiol 61:2933–2937
Acknowledgements
The authors are grateful to Prof. Yu-Guang Zhou (CGMCC, China) for his kind providing the reference type strains. This research was supported by Natural Science Foundation of China (No. 31760001), Natural Science Foundation of Guangdong Province, China (No. 2016A030312003), and the Deanship of Scientific Research at Princess Nourah bint Abdulrahman University, through the Research Groups Program Grant no. (RGP-1438-0004). W-J Li was also supported by Guangdong Province Higher Vocational Colleges and Schools Pearl River Scholar Funded Scheme (2014).
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Huang, MJ., Xiao, M., Rao, M.P.N. et al. Nocardia zhihengii sp. nov., an actinobacterium isolated from rhizosphere soil of Psammosilene tunicoides. Antonie van Leeuwenhoek 111, 2149–2156 (2018). https://doi.org/10.1007/s10482-018-1107-8
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DOI: https://doi.org/10.1007/s10482-018-1107-8