1887

Abstract

Volatile organic compound (VOC) production from an endophytic fungus was quantified at four oxygen concentrations (0, 1, 13 and 21 %) throughout culture growth phases. The filamentous fungus, a Nodulisporium sp. (designated TI-13), was grown in a solid-state reactor with an agricultural byproduct, beet pulp, as the solid substrate. The VOCs, with potential applications as biofuels, natural flavour compounds and bioactive mixtures, were measured with a recently introduced platinum catalyst and proton transfer reaction mass spectrometry quantification system. The highest-specific production rates of carbon number four and higher VOCs were observed under microaerophilic conditions, which is the expected environment within the plant host. Specific production rates of two ester compounds increased by at least 19 times under microaerophilic conditions compared with those under any other oxygen concentration studied. Total VOC production, including small molecules such as ethanol and acetaldehyde, increased by 23 times when compared between aerobic and anoxic conditions, predominately due to increased production of ethanol. Additionally, total specific production for all 21 compounds quantified was highest under reduced oxygen conditions.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000555
2017-11-07
2019-10-16
Loading full text...

Full text loading...

/deliver/fulltext/micro/163/12/1767.html?itemId=/content/journal/micro/10.1099/mic.0.000555&mimeType=html&fmt=ahah

References

  1. Wani ZA, Ashraf N, Mohiuddin T, Riyaz-Ul-Hassan S. Plant-endophyte symbiosis, an ecological perspective. Appl Microbiol Biotechnol 2015; 99: 2955– 2965 [CrossRef] [PubMed]
    [Google Scholar]
  2. Hardoim PR, van Overbeek LS, Berg G, Pirttilä AM, Compant S et al. The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 2015; 79: 293– 320 [CrossRef] [PubMed]
    [Google Scholar]
  3. Rodriguez RJ, White JF, Arnold AE, Redman RS. Fungal endophytes: diversity and functional roles. New Phytol 2009; 182: 314– 330 [CrossRef] [PubMed]
    [Google Scholar]
  4. Saikkonen K, Faeth SH, Helander M, Sullivan TJ. Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Syst 1998; 29: 319– 343 [CrossRef]
    [Google Scholar]
  5. Strobel GA, Knighton B, Kluck K, Ren Y, Livinghouse T et al. The production of myco-diesel hydrocarbons and their derivatives by the endophytic fungus Gliocladium roseum (NRRL 50072). Microbiology 2008; 154: 3319– 3328 [CrossRef]
    [Google Scholar]
  6. Guo M, Song W, Buhain J. Bioenergy and biofuels: history, status, and perspective. Renew Sustainable Energy Rev 2015; 42: 712– 725 [CrossRef]
    [Google Scholar]
  7. Atsumi S, Hanai T, Liao JC. Non-fermentative pathways for synthesis of branched-chain higher alcohols as biofuels. Nature 2008; 451: 86– 89 [CrossRef] [PubMed]
    [Google Scholar]
  8. Schwab W, Davidovich-Rikanati R, Lewinsohn E. Biosynthesis of plant-derived flavor compounds. Plant J 2008; 54: 712– 732 [CrossRef] [PubMed]
    [Google Scholar]
  9. Zhi-Lin Y, Yi-Cun C, Bai-Ge X, Chu-Long Z. Current perspectives on the volatile-producing fungal endophytes. Crit Rev Biotechnol 2012; 32: 363– 373 [CrossRef] [PubMed]
    [Google Scholar]
  10. Bunge M, Araghipour N, Mikoviny T, Dunkl J, Schnitzhofer R et al. On-line monitoring of microbial volatile metabolites by proton transfer reaction-mass spectrometry. Appl Environ Microbiol 2008; 74: 2179– 2186 [CrossRef] [PubMed]
    [Google Scholar]
  11. Kai M, Haustein M, Molina F, Petri A, Scholz B et al. Bacterial volatiles and their action potential. Appl Microbiol Biotechnol 2009; 81: 1001– 1012 [CrossRef] [PubMed]
    [Google Scholar]
  12. Strobel GA. Methods of discovery and techniques to study endophytic fungi producing fuel-related hydrocarbons. Nat Prod Rep 2014; 31: 259– 272 [CrossRef] [PubMed]
    [Google Scholar]
  13. Gianoulis TA, Griffin MA, Spakowicz DJ, Dunican BF, Alpha CJ, Sboner A et al. Genomic analysis of the hydrocarbon-producing, cellulolytic, endophytic fungus Ascocoryne sarcoides. PLoS Genet 2012; 8: e1002558 [CrossRef] [PubMed]
    [Google Scholar]
  14. Keller NP, Turner G, Bennett JW. Fungal secondary metabolism - from biochemistry to genomics. Nat Rev Microbiol 2005; 3: 937– 947 [CrossRef] [PubMed]
    [Google Scholar]
  15. Barker BM, Kroll K, Vödisch M, Mazurie A, Kniemeyer O et al. Transcriptomic and proteomic analyses of the Aspergillus fumigatus hypoxia response using an oxygen-controlled fermenter. BMC Genomics 2012; 13: 62– 25 [CrossRef] [PubMed]
    [Google Scholar]
  16. Brakhage AA. Regulation of fungal secondary metabolism. Nat Rev Microbiol 2013; 11: 21– 32 [CrossRef]
    [Google Scholar]
  17. Mallette N.D. Volatile fuel & organic compound production by Ascocoryne sarcoides. PhD Thesis Montana State University at Bozeman: 2013
    [Google Scholar]
  18. Mallette ND, Knighton WB, Strobel GA, Carlson RP, Peyton BM. Resolution of volatile fuel compound profiles from Ascocoryne sarcoides: a comparison by proton transfer reaction-mass spectrometry and solid phase microextraction gas chromatography-mass spectrometry. AMB Express 2012; 2: 23 [CrossRef] [PubMed]
    [Google Scholar]
  19. Nigg J, Strobel G, Knighton WB, Hilmer J, Geary B et al. Functionalized para-substituted benzenes as 1,8-cineole production modulators in an endophytic Nodulisporium species. Microbiology 2014; 160: 1772– 1782 [CrossRef]
    [Google Scholar]
  20. Ahamed A, Ahring BK. Production of hydrocarbon compounds by endophytic fungi Gliocladium species grown on cellulose. Bioresour Technol 2011; 102: 9718– 9722 [CrossRef] [PubMed]
    [Google Scholar]
  21. Li X-Y MZ-C, Y-x W, H-H H, Y-Q H. Comprehensive volatile organic compounds profiling of Bacillus species with biocontrol properties by head space solid phase microextraction with gas chromatography-mass spectrometry. Biocontrol Sci Technol 2015; 25: 132– 143 [Crossref]
    [Google Scholar]
  22. Lee S, Yap M, Behringer G, Hung R, Bennett JW. Volatile organic compounds emitted by Trichoderma species mediate plant growth. Fungal Biol Biotechnol 2016; 3: 7 [CrossRef] [PubMed]
    [Google Scholar]
  23. Zeng EY, Noblet JA. Theoretical considerations on the use of solid-phase microextraction with complex environmental samples. Environ Sci Technol 2002; 36: 3385– 3392 [CrossRef] [PubMed]
    [Google Scholar]
  24. Lindinger W, Hansel A, Jordan A. On-line monitoring of volatile organic compounds at pptv levels by means of proton-transfer-reaction mass spectrometry (PTR-MS) medical applications, food control and environmental research. Int J Mass Spectrom Ion Process 1998; 173: 191– 241 [CrossRef]
    [Google Scholar]
  25. Hung R, Lee S, Bennett JW. Fungal volatile organic compounds and their role in ecosystems. Appl Microbiol Biotechnol 2015; 99: 3395– 3405 [CrossRef] [PubMed]
    [Google Scholar]
  26. Ezra D, Hess WM, Strobel GA. New endophytic isolates of Muscodor albus, a volatile-antibiotic-producing fungus. Microbiology 2004; 150: 4023– 4031 [CrossRef] [PubMed]
    [Google Scholar]
  27. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72: 248– 254 [CrossRef] [PubMed]
    [Google Scholar]
  28. Schoen HR, Peyton BM, Knighton WB. Rapid total volatile organic carbon quantification from microbial fermentation using a platinum catalyst and proton transfer reaction-mass spectrometry. AMB Express 2016; 6: 90 [CrossRef] [PubMed]
    [Google Scholar]
  29. Couriol C, Amrane A, Prigent Y. A new model for the reconstruction of biomass history from carbon dioxide emission during batch cultivation of Geotrichum candidum. J Biosci Bioeng 2001; 91: 570– 575 [CrossRef] [PubMed]
    [Google Scholar]
  30. Luchner M, Gutmann R, Bayer K, Dunkl J, Hansel A et al. Implementation of proton transfer reaction-mass spectrometry (PTR-MS) for advanced bioprocess monitoring. Biotechnol Bioeng 2012; 109: 3059– 3069 [CrossRef] [PubMed]
    [Google Scholar]
  31. Steinbacher M, Dommen J, Ammann C, Spirig C, Neftel A et al. Performance characteristics of a proton-transfer-reaction mass spectrometer (PTR-MS) derived from laboratory and field measurements. Int J Mass Spectrom 2004; 239: 117– 128 [CrossRef]
    [Google Scholar]
  32. Knighton WB, Fortner EC, Herndon SC, Wood EC, Miake-Lye RC. Adaptation of a proton transfer reaction mass spectrometer instrument to employ NO+ as reagent ion for the detection of 1,3-butadiene in the ambient atmosphere. Rapid Commun Mass Spectrom 2009; 23: 3301– 3308 [CrossRef] [PubMed]
    [Google Scholar]
  33. Griffin MA, Spakowicz DJ, Gianoulis TA, Strobel SA. Volatile organic compound production by organisms in the genus Ascocoryne and a re-evaluation of myco-diesel production by NRRL 50072. Microbiology 2010; 156: 3814– 3829 [CrossRef]
    [Google Scholar]
  34. Garraway MO, Evans RC. Fungal Nutrition and Physiology New York, NY: Wiley; 1984
    [Google Scholar]
  35. Yoshioka K, Hashimoto N. Ester formation by alcohol acetyltransferase from Brewers’ yeast. Agric Biol Chem 1981; 45: 2183– 2190
    [Google Scholar]
  36. Verstrepen KJ, Derdelinckx G, Dufour JP, Winderickx J, Thevelein JM et al. Flavor-active esters: adding fruitiness to beer. J Biosci Bioeng 2003; 96: 110– 118 [CrossRef] [PubMed]
    [Google Scholar]
  37. Verstrepen KJ, van Laere SD, Vanderhaegen BM, Derdelinckx G, Dufour JP et al. Expression levels of the yeast alcohol acetyltransferase genes ATF1, Lg-ATF1, and ATF2 control the formation of a broad range of volatile esters. Appl Environ Microbiol 2003; 69: 5228– 5237 [CrossRef] [PubMed]
    [Google Scholar]
  38. Ezra D, Jasper J, Rogers T, Knighton B, Grimsrud E et al. Proton transfer reaction-mass spectrometry as a technique to measure volatile emissions of Muscodor albus. Plant Science 2004; 166: 1471– 1477 [CrossRef]
    [Google Scholar]
  39. Capozzi V, Makhoul S, Aprea E, Romano A, Cappellin L et al. PTR-MS characterization of VOCs associated with commercial aromatic bakery yeasts of wine and beer origin. Molecules 2016; 21: 483 [CrossRef] [PubMed]
    [Google Scholar]
  40. Plata C, Mauricio JC, Millán C, Ortega JM. Influence of glucose and oxygen on the production of ethyl acetate and isoamyl acetate by a Saccharomyces cerevisiae strain during alcoholic fermentation. World J Microbiol Biotechnol 2005; 21: 115– 121 [CrossRef]
    [Google Scholar]
  41. Alpha CJ, Campos M, Jacobs-Wagner C, Strobel SA. Mycofumigation by the volatile organic compound-producing Fungus Muscodor albus induces bacterial cell death through DNA damage. Appl Environ Microbiol 2015; 81: 1147– 1156 [CrossRef] [PubMed]
    [Google Scholar]
  42. Strobel GA, Dirkse E, Sears J, Markworth C. Volatile antimicrobials from Muscodor albus, a novel endophytic fungus. Microbiology 2001; 147: 2943– 2950 [CrossRef] [PubMed]
    [Google Scholar]
  43. Schoen HR, Hunt KA, Strobel GA, Peyton BM, Carlson RP. Carbon chain length of biofuel- and flavor-relevant volatile organic compounds produced by lignocellulolytic fungal endophytes changes with culture temperature. Mycoscience 2017; 58: 338– 343 [CrossRef]
    [Google Scholar]
  44. Chambergo FS, Bonaccorsi ED, Ferreira AJ, Ramos AS, Ferreira Júnior JR et al. Elucidation of the metabolic fate of glucose in the filamentous fungus Trichoderma reesei using expressed sequence tag (EST) analysis and cDNA microarrays. J Biol Chem 2002; 277: 13983– 13988 [CrossRef] [PubMed]
    [Google Scholar]
  45. Panagiotou G, Villas-Bôas SG, Christakopoulos P, Nielsen J, Olsson L. Intracellular metabolite profiling of Fusarium oxysporum converting glucose to ethanol. J Biotechnol 2005; 115: 425– 434 [CrossRef] [PubMed]
    [Google Scholar]
  46. Li S, Li G, Zhang L, Zhou Z, Han B et al. A demonstration study of ethanol production from sweet sorghum stems with advanced solid state fermentation technology. Appl Energy 2013; 102: 260– 265 [CrossRef]
    [Google Scholar]
  47. Lee SY, Lee DY, Kim TY. Systems biotechnology for strain improvement. Trends Biotechnol 2005; 23: 349– 358 [CrossRef] [PubMed]
    [Google Scholar]
  48. Stephanopoulos G, Aristidou AA, Nielsen J. Metabolic Engineering: Principles and Methodologies San Diego, CA: Academic Press; 1998
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000555
Loading
/content/journal/micro/10.1099/mic.0.000555
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF
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