1887

Abstract

A total of 218 actinobacteria strains were isolated from wild perennial liquorice plants L. and BAT. Based on morphological characteristics, 45 and 32 strains from and , respectively, were selected for further analyses. According to 16S rRNA sequence analysis, most of the strains belonged to genus and a few strains represented the rare actinobacteria and . A total of 39 strains from and 27 strains from showed antimicrobial activity against at least one indicator organism. The range of the antimicrobial activity of the strains isolated from and was similar. A total of 34 strains from and 29 strains from carried at least one of the genes encoding polyketide synthases, non-ribosomal peptide synthetase and FADH-dependent halogenase. In the type II polyketide synthase KSα gene phylogenetic analysis, the strains were divided into two major clades: one included known spore pigment production-linked KSα sequences and other sequences were linked to the production of different types of aromatic polyketide antibiotics. Based on the antimicrobial range, the isolates that carried different KSα types were not separated from each other or from the isolates that did not carry KSα. The incongruent phylogenies of 16S rRNA and KSα genes indicated that the KSα genes were possibly horizontally transferred. In all, the liquorice plants were a rich source of biocontrol agents that may produce novel bioactive compounds.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000301
2016-07-01
2020-04-07
Loading full text...

Full text loading...

/deliver/fulltext/micro/162/7/1135.html?itemId=/content/journal/micro/10.1099/mic.0.000301&mimeType=html&fmt=ahah

References

  1. Asl M. N., Hosseinzadeh H.. 2008; Review of pharmacological effects of Glycyrrhiza sp. and its bioactive compounds. Phytother Res22:709–724 [CrossRef][PubMed]
    [Google Scholar]
  2. Ayuso-Sacido A., Genilloud O.. 2005; New PCR primers for the screening of NRPS and PKS-I systems in actinomycetes: detection and distribution of these biosynthetic gene sequences in major taxonomic groups. Microb Ecol49:10–24 [CrossRef][PubMed]
    [Google Scholar]
  3. Baba M. S., Zin N. M., Hassan Z. A., Latip J., Pethick F., Hunter I. S., Edrada-Ebel R., Herron P. R.. 2015; In vivo antimalarial activity of the endophytic actinobacteria, Streptomyces SUK 10. J Microbiol53:847–855 [CrossRef][PubMed]
    [Google Scholar]
  4. Barka E. A., Vatsa P., Sanchez L., Gaveau-Vaillant N., Jacquard C., Klenk H. P., Clément C., Ouhdouch Y., van Wezel G. P.. 2016; Taxonomy, physiology, and natural products of actinobacteria. Microbiol Mol Biol Rev80:1–43 [CrossRef][PubMed]
    [Google Scholar]
  5. Bascom-Slack C. A., Ma C., Moore E., Babbs B., Fenn K., Greene J. S., Hann B. D., Keehner J., Kelley-Swift E. G. et al. 2009; Multiple, novel biologically active endophytic actinomycetes isolated from upper Amazonian rainforests. Microb Ecol58:374–383 [CrossRef][PubMed]
    [Google Scholar]
  6. Castillo U. F., Browne L., Strobel G., Hess W. M., Ezra S., Pacheco G., Ezra D.. 2007; Biologically active endophytic streptomycetes from Nothofagus spp. and other plants in Patagonia. Microb Ecol53:12–19 [CrossRef][PubMed]
    [Google Scholar]
  7. Castillo U., Harper J. K., Strobel G. A., Sears J., Alesi K., Ford E., Lin J., Hunter M., Maranta M. et al. 2003; Kakadumycins, novel antibiotics from Streptomyces sp NRRL 30566, an endophyte of Grevillea pteridifolia. FEMS Microbiol Lett224:183–190 [CrossRef][PubMed]
    [Google Scholar]
  8. Cinatl J., Morgenstern B., Bauer G., Chandra P., Rabenau H., Doerr H. W.. 2003; Glycyrrhizin, an active component of liquorice roots, and replication of SARS-associated coronavirus. Lancet361:2045–2046 [CrossRef]
    [Google Scholar]
  9. Cui X. L., Mao P. H., Zeng M., Li W. J., Zhang L. P., Xu L. H., Jiang C. L.. 2001; Streptimonospora salina gen. nov., sp. nov., a new member of the family Nocardiopsaceae. Int J Syst Evol Microbiol51:357–363 [CrossRef][PubMed]
    [Google Scholar]
  10. Donadio S., Monciardini P., Sosio M.. 2007; Polyketide synthases and nonribosomal peptide synthetases: the emerging view from bacterial genomics. Nat Prod Rep24:1073–1109 [CrossRef][PubMed]
    [Google Scholar]
  11. Engelhardt K., Degnes K. F., Kemmler M., Bredholt H., Fjaervik E., Klinkenberg G., Sletta H., Ellingsen T. E., Zotchev S. B.. 2010; Production of a new thiopeptide antibiotic, TP-1161, by a marine Nocardiopsis species. Appl Environ Microbiol76:4969–4976 [CrossRef][PubMed]
    [Google Scholar]
  12. Ezra D., Castillo U. F., Strobel G. A., Hess W. M., Porter H., Jensen J. B., Condron M. A., Teplow D. B., Sears J. et al. 2004; Coronamycins, peptide antibiotics produced by a verticillate Streptomyces sp. (MSU-2110) endophytic on Monstera sp. Microbiology150:785–793 [CrossRef][PubMed]
    [Google Scholar]
  13. Fernández-Moreno M. A., Martínez E., Boto L., Hopwood D. A., Malpartida F.. 1992; Nucleotide sequence and deduced functions of a set of cotranscribed genes of Streptomyces coelicolor A3(2) including the polyketide synthase for the antibiotic actinorhodin. J Biol Chem267:19278–19290[PubMed]
    [Google Scholar]
  14. Fukai T., Marumo A., Kaitou K., Kanda T., Terada S., Nomura T.. 2002; Antimicrobial activity of licorice flavonoids against methicillin-resistant Staphylococcus aureus. Fitoterapia73:536–539 [CrossRef][PubMed]
    [Google Scholar]
  15. Gao P., Huang Y.. 2009; Detection, distribution, and organohalogen compound discovery implications of the reduced flavin adenine dinucleotide-dependent halogenase gene in major filamentous actinomycete taxonomic groups. Appl Environ Microbiol75:4813–4820 [CrossRef][PubMed]
    [Google Scholar]
  16. Ginolhac A., Jarrin C., Robe P., Perrière G., Vogel T. M., Simonet P., Nalin R.. 2005; Type I polyketide synthases may have evolved through horizontal gene transfer. J Mol Evol60:716–725 [CrossRef][PubMed]
    [Google Scholar]
  17. Gontang E. A., Gaudêncio S. P., Fenical W., Jensen P. R.. 2010; Sequence-based analysis of secondary-metabolite biosynthesis in marine actinobacteria. Appl Environ Microbiol76:2487–2499 [CrossRef][PubMed]
    [Google Scholar]
  18. Goudjal Y., Toumatia O., Yekkour A., Sabaou N., Mathieu F., Zitouni A.. 2014; Biocontrol of Rhizoctonia solani damping-off and promotion of tomato plant growth by endophytic actinomycetes isolated from native plants of Algerian Sahara. Microbiol Res169:59–65 [CrossRef][PubMed]
    [Google Scholar]
  19. Han L., Yang K., Ramalingam E., Mosher R. H., Vining L. C.. 1994; Cloning and characterization of polyketide synthase genes for jadomycin B biosynthesis in Streptomyces venezuelae ISP5230. Microbiol140:3379–3389 [CrossRef]
    [Google Scholar]
  20. Harris C. M., Kannan R., Kopecka H., Harris T. M.. 1985; The role of the chlorine substituents in the antibiotic vancomycin: preparation and characterization of mono- and didechlorovancomycin. J Am Chem Soc107:6652–6658 [CrossRef]
    [Google Scholar]
  21. Hertweck C., Luzhetskyy A., Rebets Y., Bechthold A.. 2007; Type II polyketide synthases: gaining a deeper insight into enzymatic teamwork. Nat Prod Rep24:162–190 [CrossRef][PubMed]
    [Google Scholar]
  22. Hornung A., Bertazzo M., Dziarnowski A., Schneider K., Welzel K., Wohlert S. E., Holzenkämpfer M., Nicholson G. J., Bechthold A. et al. 2007; A genomic screening approach to the structure-guided identification of drug candidates from natural sources. Chembiochem8:757–766 [CrossRef][PubMed]
    [Google Scholar]
  23. Hotta K., Okami Y.. 1996; Diversity in aminoglycoside antibiotic resistance of actinomycetes and its exploitation in the search for novel antibiotics. J Ind Microbiol17:352–358 [CrossRef]
    [Google Scholar]
  24. Hwang B. K., Lim S. W., Kim B. S., Lee J. Y., Moon S. S.. 2001; Isolation and in vivo and in vitro antifungal activity of phenylacetic acid and sodium phenylacetate from Streptomyces humidus. Appl Environ Microbiol67:3739–3745 [CrossRef][PubMed]
    [Google Scholar]
  25. Ito M., Sato A., Hirabayashi K., Tanabe F., Shigeta S., Baba M., De Clercq E., Nakashima H., Yamamoto N.. 1988; Mechanism of inhibitory effect of glycyrrhizin on replication of human immunodeficiency virus (HIV). Antiviral Res10:289–298 [CrossRef][PubMed]
    [Google Scholar]
  26. Jiang S., Sun W., Chen M., Dai S., Zhang L., Liu Y., Lee K. J., Li X.. 2007; Diversity of culturable actinobacteria isolated from marine sponge Haliclona sp. Antonie Van Leeuwenhoek92:405–416 [CrossRef][PubMed]
    [Google Scholar]
  27. Kim H. K., Park Y., Kim H. N., Choi B. H., Jeong H. G., Lee D. G., Hahm K.-S.. 2002; Antimicrobial mechanism of β-glycyrrhetinic acid isolated from licorice, Glycyrrhiza glabra. Biotechnol Lett24:1899–1902[CrossRef]
    [Google Scholar]
  28. Kim T. U., Cho S. H., Han J. H., Shin Y. M., Lee H. B., Kim S. B., Min S. Y.. 2012; Diversity and physiological properties of root endophytic actinobacteria in native herbaceous plants of Korea. J Microbiol50:50–57 [CrossRef][PubMed]
    [Google Scholar]
  29. Komaki H., Harayama S.. 2006; Sequence diversity of type-II polyketide synthase genes in Streptomyces. Actinomycetologica20:42–48 [CrossRef]
    [Google Scholar]
  30. Kominek L. A.. 1972; Biosynthesis of novobiocin by Streptomyces niveus. Antimicrob Agents Chemother1:123–134 [CrossRef][PubMed]
    [Google Scholar]
  31. Kondo K., Shiba M., Nakamura R., Morota T., Shoyama Y.. 2007; Constituent properties of licorices derived from Glycyrrhiza uralensis, G . glabra, or G. inflata identified by genetic information. Biol Pharm Bull30:1271–1277[PubMed][CrossRef]
    [Google Scholar]
  32. Li J., Zhao G. Z., Huang H. Y., Qin S., Zhu W. Y., Zhao L. X., Xu L. H., Zhang S., Li W. J. et al. 2012; Isolation and characterization of culturable endophytic actinobacteria associated with Artemisia annua L. Antonie Van Leeuwenhoek101:515–527 [CrossRef][PubMed]
    [Google Scholar]
  33. Li W., Asada Y., Yoshikawa T, Li W. A. Y.. 2000; Flavonoid constituents from Glycyrrhiza glabra hairy root cultures. Phytochemistry55:447–456 [CrossRef]
    [Google Scholar]
  34. Liu M., Abdel-Mageed W. M., Ren B., He W., Huang P., Li X., Bolla K., Guo H., Chen C. et al. 2014; Endophytic Streptomyces sp. Y3111 from traditional Chinese medicine produced antitubercular pluramycins. Appl Microbiol Biotechnol98:1077–1085 [CrossRef][PubMed]
    [Google Scholar]
  35. Lombó F., Blanco G., Fernández E., Méndez C., Salas J. A.. 1996; Characterization of Streptomyces argillaceus genes encoding a polyketide synthase involved in the biosynthesis of the antitumor mithramycin. Gene172:87–91 [CrossRef][PubMed]
    [Google Scholar]
  36. Maldonado L. A., Fragoso-Yáñez D., Pérez-García A., Rosellón-Druker J., Quintana E. T.. 2009; Actinobacterial diversity from marine sediments collected in Mexico. Antonie Van Leeuwenhoek95:111–120 [CrossRef][PubMed]
    [Google Scholar]
  37. Mesbah N. M., Abou-El-Ela S. H., Wiegel J.. 2007; Novel and unexpected prokaryotic diversity in water and sediments of the alkaline, hypersaline lakes of the Wadi An Natrun, Egypt. Microb Ecol54:598–617 [CrossRef][PubMed]
    [Google Scholar]
  38. Metsä-Ketelä M., Halo L., Munukka E., Hakala J., Mäntsälä P., Ylihonko K.. 2002; Molecular evolution of aromatic polyketides and comparative sequence analysis of polyketide ketosynthase and 16S ribosomal DNA genes from various streptomyces species. Appl Environ Microbiol68:4472–4479 [CrossRef][PubMed]
    [Google Scholar]
  39. Metsä-Ketelä M., Salo V., Halo L., Hautala A., Hakala J., Mäntsälä P., Ylihonko K.. 1999; An efficient approach for screening minimal PKS genes from Streptomyces. FEMS Microbiol Lett180:1–6 [CrossRef][PubMed]
    [Google Scholar]
  40. Metsä-Ketelä M., Ylihonko K., Mäntsälä P.. 2004; Partial activation of a silent angucycline-type gene cluster from a rubromycin beta producing Streptomyces sp. PGA64. J Antibiot57:502–510[PubMed][CrossRef]
    [Google Scholar]
  41. Nelson M. L., Levy S. B.. 2011; The history of the tetracyclines. Ann N Y Acad Sci1241:17–32 [CrossRef][PubMed]
    [Google Scholar]
  42. Newman D. J., Cragg G. M.. 2007; Natural products as sources of new drugs over the last 25 years. J Nat Prod70:461–477 [CrossRef][PubMed]
    [Google Scholar]
  43. Oksanen J., Blanchet F. G., Kindt R., Legendre P., Minchin P. R., O'Hara R., Simpson G. L., Solymos P., Stevens M. H. H. et al. 2015; Package ‘vegan’. Community Ecology Package version 2.3-5
    [Google Scholar]
  44. Qin S., Li J., Chen H. H., Zhao G. Z., Zhu W. Y., Jiang C. L., Xu L. H., Li W. J.. 2009; Isolation, diversity, and antimicrobial activity of rare actinobacteria from medicinal plants of tropical rain forests in Xishuangbanna, China. Appl Environ Microbiol75:6176–6186 [CrossRef][PubMed]
    [Google Scholar]
  45. Raja A., Prabakaran P.. 2011; Actinomycetes and drug-an overview. Am J Drug Discovery Dev1:75–84 [CrossRef]
    [Google Scholar]
  46. Räty K., Kantola J., Hautala A., Hakala J., Ylihonko K., Mäntsälä P.. 2002; Cloning and characterization of Streptomyces galilaeus aclacinomycins polyketide synthase (PKS) cluster. Gene293:115–122 [CrossRef][PubMed]
    [Google Scholar]
  47. Schirmer A., Gadkari R., Reeves C. D., Ibrahim F., DeLong E. F., Hutchinson C. R.. 2005; Metagenomic analysis reveals diverse polyketide synthase gene clusters in microorganisms associated with the marine sponge Discodermia dissoluta. Appl Environ Microbiol71:4840–4849 [CrossRef][PubMed]
    [Google Scholar]
  48. Sheil D.. 1999; Tropical forest diversity, environmental change and species augmentation: after the intermediate disturbance hypothesis. J Veg Sci10:851–860 [CrossRef]
    [Google Scholar]
  49. Stierle A., Strobel G., Stierle D.. 1993; Taxol and taxane production by Taxomyces andreanae, an endophytic fungus of Pacific yew. Science260:214–216 [CrossRef][PubMed]
    [Google Scholar]
  50. Stone J. K., Bacon C. W., White J.. 2000; An overview of endophytic microbes: endophytism defined. Microb Endophytes3:29–33
    [Google Scholar]
  51. Strobel G., Daisy B.. 2003; Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev67:491–502[PubMed][CrossRef]
    [Google Scholar]
  52. Strobel G., Daisy B., Castillo U., Harper J.. 2004; Natural products from endophytic microorganisms. J Nat Prod67:257–268 [CrossRef][PubMed]
    [Google Scholar]
  53. Sun W., Peng C., Zhao Y., Li Z.. 2012; Functional gene-guided discovery of type II polyketides from culturable actinomycetes associated with soft coral Scleronephthya sp. PLoS One7:e42847 [CrossRef][PubMed]
    [Google Scholar]
  54. Taechowisan T., Lu C., Shen Y., Lumyong S.. 2005; Secondary metabolites from endophytic Streptomyces aureofaciens CMUAc130 and their antifungal activity. Microbiology151:1691–1695 [CrossRef][PubMed]
    [Google Scholar]
  55. Tamura K., Dudley J., Nei M., Kumar S.. 2007; MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol24:1596–1599[CrossRef]
    [Google Scholar]
  56. Thaker M. N., Wang W., Spanogiannopoulos P., Waglechner N., King A. M., Medina R., Wright G. D.. 2013; Identifying producers of antibacterial compounds by screening for antibiotic resistance. Nat Biotechnol31:922–927 [CrossRef][PubMed]
    [Google Scholar]
  57. Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G.. 1997; The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res25:4876–4882 [CrossRef][PubMed]
    [Google Scholar]
  58. Tsukiyama R., Katsura H., Tokuriki N., Kobayashi M.. 2002; Antibacterial activity of licochalcone A against spore-forming bacteria. Antimicrob Agents Chemother46:1226–1230 [CrossRef][PubMed]
    [Google Scholar]
  59. Xie J., Zhang Y., Wang W.. 2010; HPLC analysis of glycyrrhizin and licochalcone a in Glycyrrhiza inflata from Xinjiang (China). Chem Nat Compd46:148–151[CrossRef]
    [Google Scholar]
  60. Xu J.. 2011; Biomolecules produced by mangrove-associated microbes. Curr Med Chem18:5224–5266[PubMed][CrossRef]
    [Google Scholar]
  61. Yan X. C.. 1992; Isolation and Identification of Actinomycetes Beijing: China Sci Press;
    [Google Scholar]
  62. Zhang Y., Chen Y., Pan B.. 2005; Distribution and floristics of desert plant communities in the lower reaches of Tarim River, southern Xinjiang, People's Republic of China. J Arid Environ63:772–784[CrossRef]
    [Google Scholar]
  63. Zhao K., Penttinen P., Chen Q., Guan T., Lindström K., Ao X., Zhang L., Zhang X.. 2012; The rhizospheres of traditional medicinal plants in Panxi, China, host a diverse selection of actinobacteria with antimicrobial properties. Appl Microbiol Biotechnol94:1321–1335 [CrossRef][PubMed]
    [Google Scholar]
  64. Zhao K., Penttinen P., Guan T., Xiao J., Chen Q., Xu J., Lindström K., Zhang L., Zhang X. et al. 2011; The diversity and anti-microbial activity of endophytic actinomycetes isolated from medicinal plants in Panxi plateau, China. Curr Microbiol62:182–190 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000301
Loading
/content/journal/micro/10.1099/mic.0.000301
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Most cited this month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error