Abstract
During the investigation of exploring potential sources of novel species and natural bioactives, a novel actinomycete, designated strain HIT-DPA4T, was isolated from a soil sample, which was collected from Nanjing, Jiangsu Province, PR China and characterized using a polyphasic approach. On the basis of 16S rRNA gene sequence similarities and the result of phylogenetic analysis, strain HIT-DPA4T was most closely related to Streptomyces cyaneus CGMCC 4.1671 T, and shared the highest sequence similarity of 98.76%. In addition, the cell walls of the species HIT-DPA4T contained LL-diaminopimelic acid as the diagnostic diamino acid and the whole-cell hydrolysates were identified as glucose and ribose, and the principal phospholipids were found to be diphosphatidylglycerol, phosphatidylethanolamine, phosphatidylinositol mannoside and phosphatidylmonomethylethanolamine. MK-9(H6) and MK-9(H4) were predominant menaquinones; and C16:0, anteiso-C15:0 and C15:0 as major cellular fatty acids of the organism HIT-DPA4T. Gene Ontology database analysis and antiSMASH server predicted results displayed that strain HIT-DPA4T was a promising classification units, which has various types of functions and contains multiple biosynthetic gene clusters with the similarity more than 80%. Multilocus sequence analysis (MLSA) of five housekeeping genes (atpD, gyrB, recA, rpoB and trpB) illustrated that Streptomyces luteolifulvus formed a separate branch in the genus Streptomyces. However, a combination of low level of DNA-DNA relatedness and physiological properties indicated that strain HIT-DPA4T can be distinguished from its phylogenetically related species Streptomyces cyaneus CGMCC 4.1671 T. Moreover, gene synteny research could be further differed organism HIT-DPA4T from similarity species. Therefore, the strain is concluded to represent a novel species of the genus Streptomyces, for which the name Streptomyces luteolifulvus sp. nov. is proposed. The type strain is HIT-DPA4T (= CGMCC 4.7558 T = TISTR 2751 T).
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References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. Nat Genet 25:25–29
Atlas RM (1993) Handbook of Microbiological Media.Edited by Parks LC. Boca Raton, FL: CRC Press
Chung B, Kwon OS, Shin J, Oh KB (2020) Antibacterial activity and mode of action of lactoquinomycin a from streptomyces bacillaris. Mar Drugs 19:7. https://doi.org/10.3390/md19010007
Collins MD (1985) Isoprenoid quinone analyses in bacterial classification and identification. In: Goodfellow M, Minnikin DE (eds) Chemical methods in bacterial systematics. AcademicPress, London, pp 267–284
Collins MD, Jones D (1980) Lipids in the classification and identification of coryneform bacteria containing peptidoglycan based on 2, 4-diaminobutyric acid. Appl Bacteriol 48:459–470. https://doi.org/10.1111/j.1365-2672.1980.tb01036.x
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/10.1111/j.1558-5646.1985.tb00420.x
Galperin MY, Makarova KS, Wolf YI, Koonin EV (2015) Expanded microbial genome coverage and improved protein family annotation in the COG database. Nucleic Acids Res 43:261–269
Gao RX, Liu CX, Zhao JW, Jia FY, Yu C, Yang LY, Wang XJ, Xiang WS (2014) Micromonospora jinlongensis sp. nov., isolated from muddy soil in China and emended description of the genus micromonospora. Antonie Van Leeuwenhoek 105:307–315. https://doi.org/10.1007/s10482-013-0074-3
Gordon RE, Barnett DA, Handerhan JE, Pang C (1974) Nocardiacoeliaca, nocardiaautotrophica, and the nocardin strain. Int J Syst Bacteriol 24:54–63. https://doi.org/10.1099/00207713-24-1-54
Guan XJ, Liu CX, Zhao JW, Fang BZ, Zhang YJ, Li LJ, Jin PJ, Wang XJ, Xiang WS (2015) Streptomyces maoxianensis sp. nov., a novel actinomyceteisolated from soil in maoxian. China Antonie Van Leeuwenhoek 107:1119–1126. https://doi.org/10.1007/s10482-015-0403-9
Jia FY, Liu CX, Wang XJ, Zhao JW, Liu QF, Zhang J, Gao RX, Xiang WS (2013) Wangella harbinensis gen. nov., sp. nov., a new member of the family micromonosporaceae. Antonie Van Leeuwenhoek 103:399–408
Jones KL (1949) Fresh isolates of actinomycetes in which the presence of sporogenous aerial mycelia is a fluctuating characteristic. J Bacteriol 57:141–145. https://doi.org/10.1128/JB.57.2.141-145.1949
Kämpfer P, Labeda DP (2006) International committee on systematics of prokaryotes; subcommittee on the taxonomy of the Streptomycetaceae: minutes of the meeting, 25 July 2005, San Francisco, CA, USA. Int J Syst Evol Microbiol 56 495. http://ijs.sgmjournals.org/cgi/doi/https://doi.org/10.1099/ijs.0.64136-0
Kelly KL (1964) Inter-society color council-national bureau of standards color-name charts illustrated with centroid colors published in US
Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park SC, Jeon YS, Lee JH, Yi H, Won S, Chun J (2012) Introducing EzTaxon-e: a prokaryotic 16SrRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721. https://doi.org/10.1099/ijs.0.038075-0
Kim YH, Park BS, Bhatia SK, Seo HM, Jeon JM, Kim HJ, Yi DH, Lee JH, Choi KY, Park HY, Kim YG, Yang YH (2014) Production of rapamycin in streptomyces hygroscopicus from glycerol-bases media optimized by systematic methodology. J Microbiol Biotechnol 24:1319–1326. https://doi.org/10.4014/jmb.1403.03024
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. https://doi.org/10.1007/BF01731581
Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C, Salzberg SL (2004) Versatile and open software for comparing large genomes. Genome biology 5(2): 12. http://genomebiology.com/2004/5/2/R12
Lechevalier MP, Lechevalier HA (1980) The chemotaxonomy of actinomycetes. In: Dietz A, Thayer DW (eds) Actinomycete taxonomy special publication, vol 6. Society of Industrial Microbiology, Arlington, pp 227–291
Lee YK, Kim HW, Liu CL, Lee HK (2003) A simple method for DNA extraction from marine bacteria that produce extracellular materials. J Microbiol Methods 52:245–250. https://doi.org/10.1016/S0167-7012(02)00180-X
Li R, Li Y, Kristiansen K, Wang J (2008) Soap: short oligonucleotide alignment program. Bioinformatics 24:713–714
Li RQ, Zhu HM, Ruan J, Qian WB, Fang XD, Shi ZB, Li YR, Li ST, Shan G, Kristiansen K (2010) De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 20:265–272. https://doi.org/10.1101/gr.097261.109
Loqman S, Barka EA, Clément C, Ouhdouch Y (2009) Antagonistic actinomycetes from moroccan soil to control the grapevine gray mold. World J Microbiol Biotechnol 25:81–91. https://doi.org/10.1007/s11274-008-9864-6
Mandel M, Marmur J (1968) Use of ultraviolet absorbance temperature profile for determining the guanine plus cytosine content of DNA. Methods Enzymol 12B:195–206. https://doi.org/10.1016/0076-6879(67)12133-2
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 39:339–346
Meier-Kolthoff JP, Göker M, Spröer C, Klenk H-P (2013) When should a DDH experiment be mandatory in microbial taxonomy? Arch Microbiol 195:413–418
McKerrow J, Vagg S, McKinney T, Seviour EM, Maszenan AM, Brooks P, Seviou RJ (2000) A simple HPLC method for analyzing diaminopimelic acid diastereomers in cell walls of gram-positive bacteria. Lett Appl Microbiol 30:178–182. https://doi.org/10.1046/j.1472-765x.2000.00675.x
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 quinines and polar lipids. J Microbiol Methods 2:233–241. https://doi.org/10.1016/0167-7012(84)90018-6
Nie GX, Ming H, Li S, Zhou EM, Cheng J, Tang X, Feng HG, Tang SK, Li WJ (2012) Amycolatopsis dongchuanensis sp. nov., an actinobacterium isolated from soil. Int J Syst Evol Microbiol 62:2650–2656. https://doi.org/10.1099/ijs.0.038125-0
Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 106:19126–19131. https://doi.org/10.1073/pnas.0906412106
Rong X, Huang Y (2012) Taxonomic evaluation of the Streptomyces hygroscopicus clade using multilocus sequence analysis and DNA-DNA hybridization, validating the MLSA scheme for systematics of the whole genus. Syst Appl Microbiol 35:7–18. https://doi.org/10.1016/j.syapm.2011.10.004
Saini A, Aggarwal NK (2018) Enhanced endoglucanase production by soil inhabiting Streptomyces sp. strain NAA9 using lignocellulosic biomass. Energy Sources Part A Recovery Util Environ Eff 41:1–10. https://doi.org/10.1080/15567036.2018.1549138
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
Shirling EB, Gottlieb D (1966) Methods for characterisation of streptomyces species. Int J Syst Bacteriol 16:313–340. https://doi.org/10.1099/00207713-16-3-313
Smibert RM, Krieg NR (1994) Phenotypiccharacterisation. In: Gerhardt P, Murray RGE, Wood WA, Krieg NR (eds) Methods for generaland molecular bacteriology. American Society for Microbiology, Washington DC
Staneck JL, Roberts GD (1974) Simplified approach to identification of aerobic actinomycetes by thin-layer chromatography. Appl Microbiol 28:226–231
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.06. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197
Trujillo ME, Fernández-Molinero C, Velázquez E, Kroppenstedt RM, Schumann P, Mateos PF, Martínez-Molina E (2005) Micromonospora mirobrigensis sp. nov. Int J Syst Evol Microbiol 55:877–880. https://doi.org/10.1099/ijs.0.63361-0
Trujillo ME, Kroppenstedt RM, Fernández-Molinero C, Schumann P, Martínez-Molina E (2007) Micromonospora lupini sp. nov. and micromonospora saelicesensis sp. nov., isolated from root nodules of lupinus angustifolius. Int J Syst Evol Microbiol 57:2799–2804. https://doi.org/10.1099/ijs.0.65192-0
Tom V, Sarah L, Stien B, Martine M, Sofie G (2016) Streptomyces as a plant’s best friend? FEMS Microbiol Ecol 92:fiw119. https://doi.org/10.1093/femsec/fiw119
Waksman AS, Henrici AT (1943) The nomenclature and classification of the actinomycetes. J Bacteriol 46:337–341. https://doi.org/10.1128/JB.46.4.337-341.1943
Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703. https://doi.org/10.1128/jb.173.2.697-703.1991
Wu C, Lu X, Qin M, Wang Y, Ruan J (1989) Analysis of menaquinone compound in microbial cells by HPLC. Microbiology [English translation of Microbiology (Beijing)] 16:176–178
Xiang WS, Liu CX, Wang XJ, Du J, Xi LJ, Huang Y (2011) Actinoalloteichus nanshanensis sp. nov., isolated from the rhizosphere of a fig tree (Ficusreligiosa). Int J Syst Evol Microbiol 61:1165–1169. https://doi.org/10.1099/ijs.0.023283-0
Xu J, Yang Q (2010) Isolation and characterization of rice straw degrading streptomyces griseorubens C-5. Biodegradation 21:107. https://doi.org/10.1007/s10532-009-9285-8
Yokota A, Tamura T, Hasegawa T, Huang LH (1993) Catenuloplanes japonicas gen. nov., sp. nov., nom. rev., a new genus of the order actinomycetales. Int J Syst Bacteriol 43:805–812. https://doi.org/10.1099/00207713-43-4-805
Yoon SH, Ha SM, Lim J, Kwon S, Chun J (2017) 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
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This work was supported in part by grant from the Harbin science and technology project (No. 2016AB3AP042). We are also grateful to Professor Aharon Oren for helpful advice on the specific epithet.
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SZ and QY conceived the idea of the study; SZ, MC, CL and ZW analysed the data; SZ, HL, KZ and SS interpreted the results. SZ wrote the paper; all authors discussed the results and revised the manuscript.
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Zhao, S., Cheng, M., Lin, C. et al. Streptomyces luteolifulvus sp. nov., a novel actinomycete isolated from soil in Nanjing, China. Antonie van Leeuwenhoek 114, 1829–1839 (2021). https://doi.org/10.1007/s10482-021-01643-2
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DOI: https://doi.org/10.1007/s10482-021-01643-2