Abstract
Strain C17T, a novel strain belonging to the phylum Actinobacteria, was isolated from a thermal power plant in Yantai, Shandong Province, China. Cells of strain C17T were Gram stain positive, aerobic, pink, non-motile and round with neat edges, showing optimum growth at 28 °C. Phylogenetically, strain C17T was a member of the class Actinobacteria, order Mycobacteriales, family Gordoniaceae. Phylogenetic analysis based on 16S rRNA gene sequence comparisons revealed that the related strains were Williamsia faeni JCM 17784 T and Williamsia limnetica KCTC 19981 T with pairwise sequence similarity of 98.5% for both strains. According to the draft genome sequence, the DNA G + C content was 64.7%. The average amino acid identity (AAI), average nucleotide identity (ANI) and digital DNA–DNA hybridization (dDDH) values between genome sequences of strain C17T and the closest type strain W. faeni JCM 17784 T were 77.5, 77.9, and 20.7%, respectively. Predominant fatty acids were C16:0 (31.7%) and C18:1ω9c (26.8%). The major menaquinone was MK-9. The diagnostic phospholipids were phosphatidylethanolamine (PE), diphosphatidylglycerol (DPG), and phosphatidylinositol (PI). Therefore, the combined phenotypic, chemotaxonomic and phylogenetic data indicated that strain C17T was considered to represent a novel species of the genus Williamsia. Williamsia soli sp. nov. was proposed for strain C17T (= KCTC 49567 T = MCCC 1K04355T).
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References
Afonso De Menezes CB, Afonso RS, Souza WR, Parma M, Melo IS, Zucchi TD, Fantinatti-Garboggini F (2017) Williamsia spongiae sp. nov., an actinomycete isolated from the marine sponge Amphimedon viridis. Int J Syst Evol Microbiol 67:1260–1265. https://doi.org/10.1099/ijsem.0.001796
Aziz RK, Bartels D, Best AA, Dejongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, Mcneil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O (2008) The RAST Server: rapid annotations using subsystems technology. BMC Genom 9:75. https://doi.org/10.1186/1471-2164-9-75
Blin K, Shaw S, Steinke K, Villebro R, Ziemert N, Lee SY, Medema MH, Weber T (2019) antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline. Nucleic Acids Res 47:W81–W87. https://doi.org/10.1093/nar/gkz310
Bowman J (2000) Description of Cellulophaga algicola sp. Nov,, isolated from the surfaces of Antarctic algae, and reclassification of Cytophaga uliginosa (ZoBell and Upham 1944) Reichenbach 1989 as Cellulophaga uliginosa comb nov. Int J Syst Evol Microbiol 50(Pt 5):1861–1868. https://doi.org/10.1099/00207713-50-5-1861
Chen L, Yang J, Yu J, Yao Z, Sun L, Shen Y, Jin Q (2005) VFDB: a reference database for bacterial virulence factors. Nucleic Acids Res 33:D325–D328. https://doi.org/10.1093/nar/gki008
De Menezes CBA, Afonso RS, De Souza WR, Parma MM, De Melo IS, Fugita FLS, Moraes LAB, Zucchi TD, Fantinatti-Garboggini F (2019) Williamsia aurantiacus sp. nov. a novel actinobacterium producer of antimicrobial compounds isolated from the marine sponge. Arch Microbiol 201:691–698. https://doi.org/10.1007/s00203-019-01633-z
Fang XM, Su J, Wang H, Wei YZ, Zhang T, Zhao LL, Liu HY, Ma BP, Klenk HP, Zhang YQ, Yu LY (2013) Williamsia sterculiae sp. nov., isolated from a Chinese medicinal plant. Int J Syst Evol Microbiol 63:4158–4162. https://doi.org/10.1099/ijs.0.052688-0
Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376. https://doi.org/10.1007/BF01734359
Felsenstein J (1985) Confidence-limits on phylogenies - an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.2307/2408678
Hiraishi A, Ueda Y, Ishihara J, Mori T (1996) Comparative lipoquinone analysis of influent sewage and activated sludge by high-performance liquid chromatography and photodiode array detection. J Gen Appl Microbiol 42:457–469. https://doi.org/10.2323/jgam.42.457
Jones AL, Payne GD, Goodfellow M (2010) Williamsia faeni sp. nov., an actinomycete isolated from a hay meadow. Int J Syst Evol Microbiol 60:2548–2551. https://doi.org/10.1099/ijs.0.015826-0
Kämpfer P, Andersson MA, Rainey FA, Kroppenstedt RM, Salkinoja-Salonen M (1999) Williamsia muralis gen. nov., sp. nov., isolated from the indoor environment of a children’s day care centre. Int J Syst Evol Microbiol 49:681–687. https://doi.org/10.1099/00207713-49-2-681
Kämpfer P, Wellner S, Lohse K, Lodders N, Martin K (2011) Williamsia phyllosphaerae sp. nov., isolated from the surface of Trifolium repens leaves. Int J Syst Evol Microbiol 61:2702–2705. https://doi.org/10.1099/ijs.0.029322-0
Kämpfer P, Busse HJ, Horn H, Abdelmohsen UR, Hentschel U, Glaeser SP (2016) Williamsia herbipolensis sp. nov., isolated from the phyllosphere of Arabidopsis thaliana. Int J Syst Evol Microbiol 66:4609–4613. https://doi.org/10.1099/ijsem.0.001398
Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M (2016) KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res 44:D457–D462. https://doi.org/10.1093/nar/gkv1070
Kim M, Oh HS, Park SC, Chun J (2014) Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 64:346–351. https://doi.org/10.1099/ijs.0.059774-0
Klimke W, Agarwala R, Badretdin A, Chetvernin S, Ciufo S, Fedorov B, Kiryutin B, O’neill K, Resch W, Resenchuk S, Schafer S, Tolstoy I, Tatusova T (2009) The national center for biotechnology information’s protein clusters database. Nucleic Acids Res 37:D216–D223. https://doi.org/10.1093/nar/gkn734
Konstantinidis KT, Tiedje JM (2005) Towards a genome-based taxonomy for prokaryotes. J Bacteriol 187:6258–6264. https://doi.org/10.1128/JB.187.18.6258-6264.2005
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
Lefort V, Desper R, Gascuel O (2015) FastME 2.0: a comprehensive, accurate, and fast distance-based phylogeny inference program. Mol Biol Evol 32:2798–2800. https://doi.org/10.1093/molbev/msv150
Luo R, Liu B, Xie Y, Li Z, Huang W, Yuan J, He G, Chen Y, Pan Q, Liu Y, Tang J, Wu G, Zhang H, Shi Y, Liu Y, Yu C, Wang B, Lu Y, Han C, Cheung DW, Yiu SM, Peng S, Xiaoqian Z, Liu G, Liao X, Li Y, Yang H, Wang J, Lam TW, Wang J (2012) SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 1:18. https://doi.org/10.1186/2047-217X-1-18
Medema MH, Blin K, Cimermancic P, De Jager V, Zakrzewski P, Fischbach MA, Weber T, Takano E, Breitling R (2011) antiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences. Nucleic Acids Res 39:W339–W346. https://doi.org/10.1093/nar/gkr466
Meier-Kolthoff JP, Göker M (2019) TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 10:2182. https://doi.org/10.1038/s41467-019-10210-3
Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform. https://doi.org/10.1186/1471-2105-14-60
Minnikin DE, Alshamaony L, Goodfellow M (1975) Differentiation of Mycobacterium, Nocardia, and related taxa by thin-layer chromatographic analysis of whole-organism methanolysates. J Gen Microbiol 88:200–204. https://doi.org/10.1099/00221287-88-1-200
Minnikin D, O’Donnell A, Goodfellow M, Alderson G, Athalye M, Schaal A, Parlett JH (1984) Fatty acid, polar lipid and wall amino acid composition of Gardnerella vaginalis. Arch Microbiol 138:68–71. https://doi.org/10.1007/BF00425410
Parte AC, Sarda Carbasse J, Meier-Kolthoff JP, Reimer LC, Göker M (2020) List of prokaryotic names with standing in nomenclature (LPSN) moves to the DSMZ. Int J Syst Evol Microbiol 70:5607–5612. https://doi.org/10.1099/ijsem.0.004332
Pathom-Aree W, Nogi Y, Sutcliffe IC, Ward AC, Horikoshi K, Bull AT, Goodfellow M (2006) Williamsia marianensis sp. nov., a novel actinomycete isolated from the Mariana Trench. Int J Syst Evol Microbiol 56:1123–1126. https://doi.org/10.1099/ijs.0.64132-0
Rodriguez-R L, Konstantinidis K (2014) Bypassing cultivation to identify bacterial species: culture-independent genomic approaches identify credibly distinct clusters, avoid cultivation bias, and provide true insights into microbial species. Microbe Magazine. https://doi.org/10.1128/microbe.9.111.1
Saitou N, Nei M (1987) The neighbor-joining method - a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids. USFCC Newsl 20:1–6
Sazak A, Sahin N (2012) Williamsia limnetica sp. nov., isolated from a limnetic lake sediment. Int J Syst Evol Microbiol 62:1414–1418. https://doi.org/10.1099/ijs.0.032474-0
Smibert RM (1994) Krieg NR (1994) Phenotypic characterization. In: Gerhardt P, Murray RGE, Wood WA, Krieg NR (eds) Methods for General and Molecular Bacteriology. American Society for Microbiology, Washington, pp 607–654
Stach JEM, Maldonado LA, Ward AC, Bull AT, Goodfellow M (2004) Williamsia maris sp. nov., a novel actinomycete isolated from the Sea of Japan. Int J Syst Evol Microbiol 54:191–194. https://doi.org/10.1099/ijs.0.02767-0
Staneck JL, Roberts GD (1974) Simplified approach to identification of aerobic actinomycetes by thin-layer chromatography. Appl Microbiol 28:226–231. https://doi.org/10.1128/am.28.2.226-231.1974
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
Tindall BJ, Sikorski J, Smibert R, Krieg N (2007) Phenotypic charaterization and the principles of comparative systematics. In: Reddy CA, Beveridge TJ, Breznak JA, Marzluf GA, Schmidt TM, Snyder LR (Eds). Methods for General and Molecular Microbiology 330–393. https://doi.org/10.1128/9781555817497.ch15
Tippmann HF (2004) Analysis for free: comparing programs for sequence analysis. Brief Bioinform 5:82–87. https://doi.org/10.1093/bib/5.1.82
Yang SJ, Cho JC (2008) Gaetbulibacter marinus sp nov., isolated from coastal seawater, and emended description of the genus Gaetbulibacter. Int J Syst Evol Microbiol 58:315–318. https://doi.org/10.1099/ijs.0.65382-0
Yassin AF, Hupfer H (2006) Williamsia deligens sp. nov., isolated from human blood. Int J Syst Evol Microbiol 56:193–197. https://doi.org/10.1099/ijs.0.63856-0
Yassin AF, Young CC, Lai WA, Hupfer H, Arun AB, Shen FT, Rekha PD, Ho MJ (2007) Williamsia serinedens sp. nov., isolated from an oil-contaminated soil. Int J Syst Evol Microbiol 57:558–561. https://doi.org/10.1099/ijs.0.64691-0
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
Acknowledgements
The authors thank the expert Aharon Oren for helping to view and modify the name of the new species.
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This work was supported by the National Natural Science Foundation of China (31700116), the Natural Science Foundation of Shandong Province (ZR2017MC019), the China Postdoctoral Science Foundation (2017M62218), and the Key Science and Technology Program of Weihai (1070413421511).
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XHL and ZCL contributed to the sample collection and biochemical characterization. MJZ analyzed the data and drafted the manuscript. STY and LYP contributed to genome analyses. YXZ designed the experiments and revised the manuscript. All authors read and approved the final manuscript.
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Zhang, MJ., Li, XH., Peng, LY. et al. Williamsia soli sp. nov., an actinobacterium isolated from soil at a thermal power plant in Yantai, China. Arch Microbiol 204, 102 (2022). https://doi.org/10.1007/s00203-021-02714-8
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DOI: https://doi.org/10.1007/s00203-021-02714-8