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An Endophytic Nodulisporium sp. from Central America Producing Volatile Organic Compounds with Both Biological and Fuel Potential

  • Syed, Riyaz-Ul-Hassan (Microbial Biotechnology Division, Indian Institute of Integrative Medicine (CSIR)) ;
  • Strobel, Gary (Department of Plant Sciences, Montana State University) ;
  • Geary, Brad (Department of Plant and Wildlife Sciences, Brigham Young University) ;
  • Sears, Joe (Center for Lab Services/RJ Lee Group)
  • Received : 2012.08.26
  • Accepted : 2012.09.08
  • Published : 2013.01.28

Abstract

A Nodulisporium sp. (Hypoxylon sp.) has been isolated as an endophyte of Thelypteris angustifolia (Broadleaf Leaf Maiden Fern) in a rainforest region of Central America. It has been identified both on the basis of its morphological characteristics and by scanning electron microscopy as well as ITS sequence analysis. The endophyte produces volatile organic compounds (VOCs) that have both fuel (mycodiesel) and use for biological control of plant disease. When grown on potato dextrose agar, the organism uniquely produces a series of ketones, including acetone; 2-pentanone; 3-hexanone, 4-methyl; 3-hexanone, 2,4-dimethyl; 2-hexanone, 4-methyl, and 5-hepten, 2-one and these account for about 25% of the total VOCs. The most abundant identified VOC was 1,8 cineole, which is commonly detected in this group of organisms. Other prominent VOCs produced by this endophyte include 1-butanol, 2-methyl, and phenylethanol alcohol. Moreover, of interest was the presence of cyclohexane, propyl, which is a common ingredient of diesel fuel. Furthermore, the VOCs of this isolate of Nodulisporium sp. were selectively active against a number of plant pathogens, and upon a 24 h exposure caused death to Phytophthora palmivora, Rhizoctonia solani, and Sclerotinia sclerotiorum and 100% inhibition to Phytophthora cinnamomi with only slight to no inhibition of the other pathogens that were tested. From this work, it is becoming increasingly apparent that each isolate of this endophytic Nodulisporium spp., including the Daldina sp. and Hypoxylon spp. teleomorphs, seems to produce its own unique set of VOCs.

Keywords

References

  1. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402. https://doi.org/10.1093/nar/25.17.3389
  2. Barton, A. and J. Tjandra. 1989. Eucalyptus oil as a cosolvent in water-ethanol-gasoline mixtures. Fuel 68: 11-17 https://doi.org/10.1016/0016-2361(89)90004-5
  3. Keller, N. P., G. Turner, and J. W. Bennett. 2005. Fungal secondary metabolism - from biochemistry to genomics. Nature Rev. Microbiol. 3: 937-947. https://doi.org/10.1038/nrmicro1286
  4. Kudalkar, P., G. Strobel, S. Riyaz-Ul-Hassan, B. Geary, and J. Sears. 2012. Muscodor sutura, a novel endophytic fungus with volatile antibiotic activities. Mycoscience DOI: 10.1007/s10267- 011-0165-9.
  5. Mends, M. T., E. Yu, S. Riyaz-Ul-Hassan, E. Booth, B. Geary, J. Sears, et al. 2012. An endophytic Nodulisporium sp. producing volatile organic compounds having bioactivity and fuel potential. J. Petrol. Environ. Biotechnol. 3: 3.
  6. Page, A., M. K. Tivey, D. S. Stakes, and A. L. Reysenbach. 2008. Temporal and spatial archaeal colonization of hydrothermal vent deposits. Environ. Microbiol. 10: 874-884. https://doi.org/10.1111/j.1462-2920.2007.01505.x
  7. Renniger, N. and D. McPhee. 2008. Fuel compositions comprising farnesane and farnesane derivatives and method of making and using same. U.S. Patent No. 7399323.
  8. Riyaz-Ul-Hassan, S., G. A. Strobel, E. Booth, B. Knighton, and J. Sears. 2012. Modulation of volatile organic compound formation in the mycodiesel producing endophyte Hypoxylon sp. CI-4. Microbiology 158: 465-473. https://doi.org/10.1099/mic.0.054643-0
  9. Romoli, R., M. C. Papaleo, D. de Pascale, M. L. Tutino, L. Michaud, A. LoGiudice, et al. 2011. Characterization of the volatile profile of Antarctic bacteria by using solid-phase microextraction-gas chromatography-mass spectrometry. J. Mass Spectrom. 46: 1051-1059. https://doi.org/10.1002/jms.1987
  10. Staley, J. T., R. W. Castenholz, R. R. Colwell, J. G. Holt, M. D. Kane, N. R. Pace, et al. 1997. The Microbial World: Foundation of the Biosphere. American Academy of Microbiology, Washington DC.
  11. Strobel, G. 2006. Harnessing endophytes for industrial microbiology. Curr. Opin. Microbiol. 9: 240-244. https://doi.org/10.1016/j.mib.2006.04.001
  12. Strobel, G., S. K. Singh, S. Riyaz-Ul-Hassan, A. M. Mitchel, B. Geary, and J. Sears. 2011. An endophytic/pathogenic Phoma sp. from creosote bush producing biologically active volatile compounds having fuel potential. FEMS Microbiol. Lett. 320: 87-94. https://doi.org/10.1111/j.1574-6968.2011.02297.x
  13. Strobel, G. A. and B. Daisy. 2003. Bioprospecting for microbial endophytes and their natural products. Microbiol. Mol. Biol. Rev. 67: 491-502. https://doi.org/10.1128/MMBR.67.4.491-502.2003
  14. Strobel, G. A., E. Dirksie, J. Sears, and C. Markworth. 2001. Volatile antimicrobials from Muscodor albus, a novel endophytic fungus. Microbiology 147: 2943-2950.
  15. Strobel, G. A., B. Knighton, K. Kluck, Y. Ren, T. Livinghouse, M. Griffen, et al. 2008. The production of myco-diesel hydrocarbons and their derivatives by the endophytic fungus Gliocladium roseum (NRRL 50072). Microbiology 154: 3319- 3328. https://doi.org/10.1099/mic.0.2008/022186-0
  16. Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Molec. Biol. Evol. 24: 1596-1599. https://doi.org/10.1093/molbev/msm092
  17. Tomsheck, A., G. A. Strobel, E. Booth, B. Geary, D. Spakowicz, and B. Knighton, et al. 2010. Hypoxylon sp., an endophyte of Perseaindica, producing 1,8-cineole and other bioactive volatiles with fuel potential. Microbial Ecol. 60: 903-914 https://doi.org/10.1007/s00248-010-9759-6
  18. Verma, V. C., R. N. Kharwar, and G. A. Strobel. 2009. Chemical and functional diversity of natural products from plant associated endophytic fungi. Nat. Prod. Commun. 4: 1511- 1532.
  19. Yu, X. D., J. Pickett, Y. Z. Ma, T. Bruce, J. Napier, H. D. Jones, and L. Q. Xia. 2012. Metabolic engineering of plant-derived (E)-$\beta$-farnesene synthase genes for a novel type of aphidresistant GM crop plants. J. Int. Plant Biol. 54: 282-299. https://doi.org/10.1111/j.1744-7909.2012.01107.x

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