1887

Abstract

The fungal pathogen is the causal agent of devastating gray mold diseases in many economically important fruits, vegetables, and flowers, leading to serious economic losses worldwide. In this study, a novel actinomycete NEAU-LD23 exhibiting antifungal activity against was isolated, and its taxonomic position was evaluated using a polyphasic approach. Based on the genotypic, phenotypic and chemotaxonomic data, it is concluded that the strain represents a novel species within the genus , for which the name sp. nov. is proposed. The type strain is NEAU-LD23 (=CCTCC AA 2019029=DSM 109824). In addition, strain NEAU-LD23 showed a strong antagonistic effect against (82.6±2.5%) and varying degrees of inhibition on nine other phytopathogenic fungi. Both cell-free filtrate and methanol extract of mycelia of strain NEAU-LD23 significantly inhibited mycelial growth of . To preliminarily explore the antifungal mechanisms, the genome of strain NEAU-LD23 was sequenced and analyzed. AntiSMASH analysis led to the identification of several gene clusters responsible for the biosynthesis of bioactive secondary metabolites with antifungal activity, including 9-methylstreptimidone, echosides, anisomycin, coelichelin and desferrioxamine B. Overall, this research provided us an excellent strain with considerable potential to use for biological control of tomato gray mold.

Funding
This study was supported by the:
  • the National Natural Science Foundation of China (Award 31972291)
    • Principle Award Recipient: WangXiangjing
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2021-09-14
2021-09-24
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References

  1. Sautua FJ, Baron C, Pérez-Hernández O, Carmona MA. First report of resistance to carbendazim and procymidone in Botrytis cinerea from strawberry, blueberry and tomato in Argentina. Crop Protection 2019; 125:104879 [View Article]
    [Google Scholar]
  2. Fillinger S, Elad Y. Botrytis – the Fungus, the Pathogen and its Management in Agricultural Systems Cham: Springer International Publishing; 2016 [View Article]
    [Google Scholar]
  3. Soylu EM, Kurt S, Soylu S. In vitro and in vivo antifungal activities of the essential oils of various plants against tomato grey mould disease agent Botrytis cinerea. Int J Food Microbiol 2010; 143:183–189 [View Article]
    [Google Scholar]
  4. Wei CL, Zhang F, Song LL, Chen XF, Meng XH. Photosensitization effect of curcumin for controlling plant pathogen Botrytis cinerea in postharvest apple. Food Control 2020; 123:107683 [View Article]
    [Google Scholar]
  5. Williamson B, Tudzynski B, Tudzynski P, Van Kan JA. Botrytis cinerea: the cause of grey mould disease. Mol Plant Pathol 2007; 8:561–580 [View Article]
    [Google Scholar]
  6. Ciliberti N, Fermaud M, Roudet J, Rossi V. Environmental conditions affect Botrytis cinerea infection of mature grape berries more than the strain or transposon genotype. Ecol Epidemiol 2015; 105:1090–1096 [View Article]
    [Google Scholar]
  7. Torres-Ossandón MJ, Vega-Gálvez A, Salas CE, Rubio J, Silva-Moreno E et al. Antifungal activity of proteolytic fraction (P1G10) from (Vasconcellea cundinamarcensis) latex inhibit cell growth and cell wall integrity in Botrytis cinerea. Int J Food Microbiology 2019; 289:7–16 [View Article]
    [Google Scholar]
  8. Adnan M, Hamada MS, Li GQ, Luo CX. Detection and molecular characterization of resistance to the dicarboximide and benzamide fungicides in Botrytis cinerea from tomato in Hubei Province, China. Plant Disease 2018; 102:1299–1306 [View Article]
    [Google Scholar]
  9. Boukaew S, Prasertsan P, Troulet C, Bardin M. Biological control of tomato gray mold caused by Botrytis cinerea by using Streptomyces spp. BioControl 2017; 62:793–803 [View Article]
    [Google Scholar]
  10. Sarven MS, Hao QY, Deng JB, Yang F, Wang GF et al. Biological control of tomato gray mold caused by Botrytis Cinerea with the entomopathogenic fungus Metarhizium Anisopliae. Pathogens 2020; 9:213 [View Article]
    [Google Scholar]
  11. Li XJ, Xie XF, Xing FG, Xu L, Zhang J et al. Glucose oxidase as a control agent against the fungal pathogen Botrytis cinerea in postharvest strawberry. Food Control 2019; 105:277–284 [View Article]
    [Google Scholar]
  12. Waksman SA, Henrici AT. The nomenclature and classification of the actinomycetes. J Bacteriol 1943; 46:337–341 [View Article]
    [Google Scholar]
  13. Vargas Hoyos HA, Nobre Santos S, Da Silva LJ, Paulino Silva FS, Bonaldo Genuário D et al. Streptomyces rhizosphaericola sp. nov., an actinobacterium isolated from the wheat rhizosphere. Int J Syst Evol Microbiol 2019; 69:2431–2439 [View Article]
    [Google Scholar]
  14. Williams ST, Goodfellow M, Alderson G, Wellington EM, Sneath PH et al. Numerical classification of Streptomyces and related genera. J Gen Microbiol 1983; 129:1743–1813 [View Article]
    [Google Scholar]
  15. She W, Sun Z, Yi L, Zhao S, Liang Y. Streptomyces alfalfae sp. nov. and comparisons with its closest taxa Streptomyces silaceus, Streptomyces flavofungini and Streptomyces intermedius. Int J Syst Evol Microbiol 2016; 66:44–49 [View Article]
    [Google Scholar]
  16. Zhang QY, Liu CF, Wang Y, Xia ZF, Huang YJ et al. Streptomyces roseicoloratus sp. nov., isolated from cotton soil. Int J Syst Evol Microbiol 2020; 70:738–743 [View Article]
    [Google Scholar]
  17. Bérdy J. Thoughts and facts about antibiotics: where we are now and where we are heading. J Antibiot 2012; 65:385–395 [View Article]
    [Google Scholar]
  18. Ribeiro I, Girão M, Alexandrino DAM, Ribeiro T, Santos C et al. Diversity and bioactive potential of actinobacteria isolated from a coastal marine sediment in northern Portugal. Microorganisms 2020; 8:1691 [View Article]
    [Google Scholar]
  19. Xu Y, He J, Tian XP, Li J, Yang LL et al. Streptomyces glycovorans sp. nov., Streptomyces xishensis sp. nov. and Streptomyces abyssalis sp. nov., isolated from marine sediments. Int J Syst Evol Microbiol 2012; 62:2371–2377 [View Article]
    [Google Scholar]
  20. Zhao J, Duan LP, Qian LL, Cao P, Tian YY et al. Kribbella jiaozuonensis sp. nov., a novel actinomycete isolated from soil. Int J Syst Evol Microbiol 2019; 69:3500–3507 [View Article]
    [Google Scholar]
  21. Atlas RM. Handbook of microbiological media. Parks L. eds In Microbiology Boca Raton: CRC Press; 1993
    [Google Scholar]
  22. Shirling ET, Gottlieb D. Methods for characterization of Streptomyces species. Int J Syst Evol Microbiol 1966; 16:313–340
    [Google Scholar]
  23. Smibert RM, Krieg NR. Phenotypic characterization. In Methods for General and Molecular Bacteriology American Society for Microbiology; 1994 pp 607–654
    [Google Scholar]
  24. Jin LY, Zhao Y, Song W, Duan LP, Jiang SW et al. Streptomyces inhibens sp. nov., a novel actinomycete isolated from rhizosphere soil of wheat (Triticum aestivum L. Int J Syst Evol Microbiol 2019; 69:688–695 [View Article]
    [Google Scholar]
  25. Berdy J. Are actinomycetes exhausted as a source of secondary metabolites?. Biotechnologia 1995 13–34
    [Google Scholar]
  26. Waksman SA. The Actinomycetes. A Summary of Current Knowledge New York: Ronald; 1967
    [Google Scholar]
  27. Jones KL. Fresh isolates of actinomycetes in which the presence of sporogenous aerial mycelia is a fluctuating characteristic. J Bacteriol 1949; 57:141–145 [View Article]
    [Google Scholar]
  28. Waksman SA. The Actinomycetes, vol. 2, Classification, Identification and Descriptions of Genera and Species Baltimore: Williams and Wilkins; 1961
    [Google Scholar]
  29. Kelly KL. Inter-Society Color Council-National Bureau of Standards Color-Name Charts U.S. National Bureau of Standards; 1964
    [Google Scholar]
  30. Cao P, Li CX, Tan KF, Liu CZ, Xu X et al. Characterization, phylogenetic analyses and pathogenicity of Enterobacter cloacae on rice seedlings in Heilongjiang Province, China. Plant Dis 2020; 104:1601–1609 [View Article]
    [Google Scholar]
  31. Zhao J, Han L, Yu M, Cao P, Li D et al. Characterization of Streptomyces sporangiiformans sp. nov., a novel soil actinomycete with antibacterial activity against Ralstonia solanacearum. Microorganisms 2019; 7:360 [View Article]
    [Google Scholar]
  32. Gordon RE, Barnett DA, Handerhan JE, Pang C. Nocardia coeliaca, Nocardia autotrophica, and the nocardin strain. Int J Syst Bacteriol 1974; 24:54–63 [View Article]
    [Google Scholar]
  33. Yokota A, Tamura T, Hasegawa T, Huang LH. Catenuloplanes japonicas gen. nov., sp. nov., nom. rev., a new genus of the order Actinomycetales. Int J Syst Bacteriol 1993; 43:805–812 [View Article]
    [Google Scholar]
  34. Smibert RM, Krieg NR. Phenotypic characterization. Gerhardt P, Murray R, Wood W, Krieg N. eds In Methods for General and Molecular Bacteriology Washington, DC: American Society for Microbiology; 1994 pp 607–654
    [Google Scholar]
  35. McKerrow J, Vagg S, McKinney T, Seviour EM, Maszenan AM et al. A simple HPLC method for analysing diaminopimelic acid diastereomers in cell walls of Gram-positive bacteria. Lett Appl Microbiol 2000; 30:178–182 [View Article]
    [Google Scholar]
  36. Lechevalier MP, Lechevalier HA. The chemotaxonomy of actinomycetes. Dietz A, Thayer D. eds In Actinomycete Taxonomy Special Publication Vol 6 Arlington: 1980 pp 227–291
    [Google Scholar]
  37. Minnikin DE, O’Donnell AG, Goodfellow M, Alderson G, Athalye M et al. An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 1984; 2:233–241 [View Article]
    [Google Scholar]
  38. Collins MD. Isoprenoid quinone analyses in bacterial classification and identification. Goodfellow M, Minnikin D. eds In Chemical Methods in Bacterial Systematics London: Academic Press; 1985 pp 267–284
    [Google Scholar]
  39. Qu Z, Ruan JS, Hong K. Application of high-performance liquid chromatography and gas chromatography in the identification of actinomyces. BioBulletin 2009; s1:79–82
    [Google Scholar]
  40. Song J, Qiu SW, Zhao JW, Han CY, Wang Y et al. Pseudonocardia tritici sp. nov., a novel actinomycete isolated from rhizosphere soil of wheat (Triticum aestivum L. Antonie van Leeuwenhoek 2019; 112:765–773 [View Article]
    [Google Scholar]
  41. Xiang WS, Liu CX, Wang XJ, Du J, Xi LJ et al. Actinoalloteichus nanshanensis sp. nov., isolated from the rhizosphere of a fig tree (Ficus religiosa. Int J Syst Evol Microbiol 2011; 61:1165–1169 [View Article]
    [Google Scholar]
  42. Kim SB, Brown R, Oldfield C, Gilbert SC, Iliarionov S et al. Gordonia amicalis sp. nov., a novel dibenzothiophene-desulphurizing actinomycete. Int J Syst Evol Microbiol 2000; 50:2031–2036 [View Article]
    [Google Scholar]
  43. Yoon SH, Ha SM, Kwon S, Lim J, Kim Y et al. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 2017; 67:1613–1617 [View Article]
    [Google Scholar]
  44. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406–425 [View Article]
    [Google Scholar]
  45. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 1981; 17:368–376 [View Article]
    [Google Scholar]
  46. Kumar S, Stecher G, Tamura K. Mega7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article]
    [Google Scholar]
  47. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:83–791 [View Article]
    [Google Scholar]
  48. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 1980; 16:111–120 [View Article]
    [Google Scholar]
  49. Blin K, Wolf T, Chevrette MG, Lu X, Schwalen CJ et al. AntiSMASH 4.0-Improvements in chemistry prediction and gene cluster boundary identification. Nucleic Acids Res 2017; 45:W36–W41 [View Article]
    [Google Scholar]
  50. Li RQ, Zhu HM, Ruan J, Qian WB, Fang XD et al. De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 2010; 20:265–272 [View Article]
    [Google Scholar]
  51. Li R, Li Y, Kristiansen K, Wang J. SOAP: Short Oligonucleotide Alignment Program. Bioinformatics 2008; 24:713–714 [View Article]
    [Google Scholar]
  52. De Ley J, Cattoir H, Reynaerts A. The quantitative measurement of DNA hybridization from renaturation rates. Eur J Biochem 1970; 12:133–142 [View Article]
    [Google Scholar]
  53. Huss VAR, Festl H, Schleifer KH. Studies on the spectrometric determination of DNA hybridisation from renaturation rates. Syst Appl Microbiol 1983; 4:184–192 [View Article]
    [Google Scholar]
  54. Yoon SH, Ha SM, Lim J, Kwon S, Chun J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie van Leeuwenhoek 2017; 110:1281–1286 [View Article]
    [Google Scholar]
  55. Meier-Kolthoff JP, Auch AF, Klenk HP, Goker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article]
    [Google Scholar]
  56. Wang C, Zhang Y, Zhang W, Yuan S, Ng T et al. Purification of an antifungal peptide from seeds of Brassica oleracea var. gongylodes and investigation of its antifungal activity and mechanism of action. Molecules 2019; 24:1337 [View Article]
    [Google Scholar]
  57. Barra-Bucarei L, France Iglesias A, Gerding González M, Silva Aguayo G, Carrasco-Fernández J et al. Antifungal activity of Beauveria bassiana endophyte against Botrytis cinerea in two Solanaceae crops. Microorganisms 2019; 8:65 [View Article]
    [Google Scholar]
  58. Cao P, Li CX, Wang H, Yu ZY, Xu X et al. Community structures and antifungal activity of root-associated endophytic actinobacteria in healthy and diseased cucumber plants and Streptomyces sp. HAAG3-15 as a promising biocontrol agent. Microorganisms 2020; 8:236 [View Article]
    [Google Scholar]
  59. Toral L, Rodríguez M, Béjar V, Sampedro I. Antifungal activity of lipopeptides from Bacillus XT1 CECT 8661 against Botrytis cinerea. Front Microbiol 2018; 9:1315 [View Article]
    [Google Scholar]
  60. Fu YS, Yan R, Liu DL, Zhao JW, Song J et al. Characterization of Sinomonas gamaensis sp. nov., a novel soil bacterium with antifungal activity against Exserohilum turcicum. Microorganisms 2019; 7:170 [View Article]
    [Google Scholar]
  61. Magaldi S, Mata-Essayag S, de Capriles CH, Perez C, Colella MT et al. Well diffusion for antifungal susceptibility. Int J Infect Dis 2004; 8:39–45 [View Article]
    [Google Scholar]
  62. Rong X, Huang Y. 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 2012; 35:7–18 [View Article]
    [Google Scholar]
  63. Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O et al. International Committee on Systematic Bacteriology. Report of the ad hoc Committee on Reconciliation of Approaches to Bacterial Systematics. Int J Syst Bacteriol 1987; 37:463–464 [View Article]
    [Google Scholar]
  64. Richter M, Rossello-Mora R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 2009; 106:19126–19131 [View Article]
    [Google Scholar]
  65. Chun J, Rainey FA. Integrating genomics into the taxonomy and systematics of the Bacteria and Archaea. Int J Syst Evol Microbiol 2014; 64:316–324 [View Article]
    [Google Scholar]
  66. Getha K, Vikineswary S. Antagonistic effects of Streptomyces violaceusniger strain G10 on Fusarium oxysporum f.sp. cubense race 4: indirect evidence for the role of antibiosis in the antagonistic process. J Ind Microbiol Biotechnol 2002; 28:303–310 [View Article]
    [Google Scholar]
  67. Jing T, Zhou DB, Zhang MY, Yun TY, Qi DF et al. Newly isolated Streptomyces sp. JBS5-6 as a potential biocontrol agent to control banana fusarium wilt: genome sequencing and secondary metabolite cluster profiles. Front Microbiol 2020; 11:602591 [View Article]
    [Google Scholar]
  68. Marian M, Ohno T, Suzuki H, Kitamura H, Kuroda K et al. A novel strain of endophytic Streptomyces for the biocontrol of strawberry anthracnose caused by Glomerella cingulata. Microbiol Res 2020; 234:126428 [View Article]
    [Google Scholar]
  69. Sarwar A, Latif Z, Zhang S, Hao J, Bechthold A. A potential biocontrol agent Streptomyces violaceusniger AC12AB for managing potato common scab. Front Microbiol 2019; 10:202 [View Article]
    [Google Scholar]
  70. Shakeel Q, Lyu A, Zhang J, Wu MD, Li GQ et al. Biocontrol of Aspergillus flavus on peanut kernels using Streptomyces yanglinensis 3-10. Front Microbiol 2018; 9:1049 [View Article]
    [Google Scholar]
  71. El-Shatoury SA, Ameen F, Moussa H, Abdul Wahid O, Dewedar A et al. Biocontrol of chocolate spot disease (Botrytis cinerea) in faba bean using endophytic actinomycetes Streptomyces: a field study to compare application techniques. PeerJ 2020; 8:e8582 [View Article]
    [Google Scholar]
  72. Chaiharn M, Theantana T, Pathom-Aree W. Evaluation of biocontrol activities of Streptomyces spp. against rice blast disease fungi. Pathogens 2020; 9:126 [View Article]
    [Google Scholar]
  73. Colombo EM, Kunova A, Pizzatti C, Saracchi M, Cortesi P et al. Selection of an endophytic Streptomyces sp. strain DEF09 from wheat roots as a biocontrol agent against Fusarium graminearum. Front Microbiol 2019; 10:2356 [View Article]
    [Google Scholar]
  74. Hassan N, Nakasuji S, Elsharkawy MM, Naznin HA, Kubota M et al. Biocontrol potential of an endophytic Streptomyces sp. strain MBCN152-1 against Alternaria brassicicola on cabbage plug seedlings. Microbes Environ 2017; 32:133–141 [View Article]
    [Google Scholar]
  75. Lian QG, Zhang J, Gan L, Ma Q, Zong ZF et al. The biocontrol efficacy of Streptomyces pratensis LMM15 on Botrytis cinerea in tomato. Biomed Res Int 2017; 9486794: [View Article]
    [Google Scholar]
  76. Wang XY, Zhou XA, Cai ZB, Guo L, Chen XL et al. A biocontrol strain of Pseudomonas aeruginosa CQ-40 promote growth and control Botrytis cinerea in tomato. Pathogens 2020; 10:E22 [View Article]
    [Google Scholar]
  77. Wang H, Shi YY, Wang DD, Yao ZT, Wang YM et al. A biocontrol strain of Bacillus subtilis WXCDD105 used to control tomato Botrytis cinerea and Cladosporium fulvum Cooke and promote the growth of seedlings. Int J Mol Sci 2018; 19:1371 [View Article]
    [Google Scholar]
  78. Saito N, Kitame F, Kikuchi M, Ishida N. Studies on a new antiviral antibiotic, 9-methylstreptimidone. I. Physicochemical and biological properties. J Antibiot 1974; 27:206–214 [View Article]
    [Google Scholar]
  79. Allen MS, Becker AM, Rickards RW. The glutarimide antibiotic 9-methylstreptimidone: Structure, biogenesis and biological activity. Aust J Chem 1976; 29:673–679 [View Article]
    [Google Scholar]
  80. Wang B, Song YX, Luo MH, Chen Q, Ma JY et al. Biosynthesis of 9-methylstreptimidone involves a new decarboxylative step for polyketide terminal diene formation. Org Lett 2013; 15:1278–1281 [View Article]
    [Google Scholar]
  81. Zhou ZY, Liu JK. Pigments of fungi (macromycetes. Nat Prod Rep 2010; 27:1531–1570 [View Article] [PubMed]
    [Google Scholar]
  82. Zhu J, Chen W, Li YY, Deng JJ, Zhu DY et al. Identification and catalytic characterization of a nonribosomal peptide synthetase-like (NRPS-like) enzyme involved in the biosynthesis of echosides from Streptomyces sp. LZ35. Gene 2014; 546:352–358 [View Article]
    [Google Scholar]
  83. Sobin BA, Tanner FW. Anisomycin, a new anti-protozoan antibiotic. J Am Chem Soc 1954; 76:4053 [View Article]
    [Google Scholar]
  84. Wang X, Ren Q, Tong Z, Gu H, Zhang Z. Studies on the effective components of agricultural antibiotic 120. Zhongguo Shengwu Fangzhi Xuebao 1994; 10:131–134 [View Article]
    [Google Scholar]
  85. Grollman AP. Inhibitors of protein biosynthesis. II. Mode of action of anisomycin. J Biol Chem 1967; 242:3226–3233 [View Article]
    [Google Scholar]
  86. Zheng XQ, Cheng QX, Yao F, Wang XZ, Kong LX et al. Biosynthesis of the pyrrolidine protein synthesis inhibitor anisomycin involves novel gene ensemble and cryptic biosynthetic steps. Proc Natl Acad Sci 2017; 114:4135–4140 [View Article]
    [Google Scholar]
  87. Challis GL, Ravel J. Coelichelin, a new peptide siderophore encoded by the Streptomyces coelicolor genome: structure prediction from the sequence of its non-ribosomal peptide synthetase. FEMS Microbiol Lett 2000; 187:111–114 [View Article]
    [Google Scholar]
  88. Neilands JB. Siderophores. Arch Biochem Biophys 1993; 302:1–3 [View Article]
    [Google Scholar]
  89. Barona-Gómez F, Wong U, Giannakopulos AE, Derrick PJ, Challis GL. Identification of a cluster of genes that directs desferrioxamine biosynthesis in Streptomyces coelicolor M145. J Am Chem Soc 2004; 126:16282–16283 [View Article]
    [Google Scholar]
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