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The production of myco-diesel hydrocarbons and their derivatives by the endophytic fungus Gliocladium roseum (NRRL 50072)

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Gary A Strobel
Gary A Strobel
Gary A Strobel
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W. Berk Knighton at Montana State University
W. Berk Knighton
Katreena Kluck
Katreena Kluck
Katreena Kluck
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Yuhao Ren
Yuhao Ren
Yuhao Ren
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Abstract

An endophytic fungus, Gliocladium roseum (NRRL 50072), produced a series of volatile hydrocarbons and hydrocarbon derivatives on an oatmeal-based agar under microaerophilic conditions as analysed by solid-phase micro-extraction (SPME)-GC/MS. As an example, this organism produced an extensive series of the acetic acid esters of straight-chained alkanes including those of pentyl, hexyl, heptyl, octyl, sec-octyl and decyl alcohols. Other hydrocarbons were also produced by this organism, including undecane, 2,6-dimethyl; decane, 3,3,5-trimethyl; cyclohexene, 4-methyl; decane, 3,3,6-trimethyl; and undecane, 4,4-dimethyl. Volatile hydrocarbons were also produced on a cellulose-based medium, including heptane, octane, benzene, and some branched hydrocarbons. An extract of the host plant, Eucryphia cordifolia (ulmo), supported the growth and hydrocarbon production of this fungus. Quantification of volatile organic compounds, as measured by proton transfer mass spectrometry (PTR-MS), indicated a level of organic substances in the order of 80 p.p.m.v. (parts per million by volume) in the air space above the oatmeal agar medium in an 18 day old culture. Scaling the PTR-MS profile the acetic acid heptyl ester was quantified (at 500 p.p.b.v.) and subsequently the amount of each compound in the GC/MS profile could be estimated; all yielded a total value of about 4.0 p.p.m.v. The hydrocarbon profile of G. roseum contains a number of compounds normally associated with diesel fuel and so the volatiles of this fungus have been dubbed 'myco-diesel'. Extraction of liquid cultures of the fungus revealed the presence of numerous fatty acids and other lipids. All of these findings have implications in energy production and utilization.
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Corrigendum The production of myco-diesel hydrocarbons and
their derivatives by the endophytic fungus
Gliocladium roseum (NRRL 50072)
Gary A. Strobel, Berk Knighton, Katreena Kluck, Yuhao Ren,
Tom Livinghouse, Meghan Griffin, Daniel Spakowicz and Joe Sears
Microbiology (2008), 154, part 11, 3319–3328.
The authors would like to note that technical errors occurred in the above report.
In the report, in order to determine which volatile compounds were produced by the
fungus, the volatile organic compounds (VOCs) found in the GC-MS analyses of controls
were removed from the list of VOCs appearing in the flask supporting fungal growth as
done previously (Strobel et al., 2001). However, an examination of this approach has
revealed that it was inaccurate for the study. The automated library search results generated
from the NIST 2005 database spectral search were used as the only means of compound
comparison between fungal products and those of the control. Due to the similarity of
many alkane fragmentation patterns the automated search is not always reliable (Schulz &
Dickschat, 2007). This difficulty in alkane identification was further complicated by a
complex mixture of gases produced by NRRL 50072 that resulted in overlapping
chromatographic peaks. The incomplete separation resulted in the automated library
search algorithm (Agilent Chem Station Version C.0.0) returning different VOC assign-
ments. This led to the incorrect conclusion that some compounds were in the fungal
fermentation VOCs but not present in the controls. In addition to the automated library
database search comparisons, manual inspection of retention times and fragmentation
profiles for each chromatographic peak is necessary to accurately account for the media-
derived VOCs. The data reported in the revised tables (below) reflect changes made after
these additional aspects of the GC-MS data analyses were considered and these represent the
most conservative estimates of the fungal VOC production. The temperature programme
used for GC was as follows: 40 uC for 2 min, 10 uC min
21
ramp to 230 uC final temperature
and a 5 min hold at 230 uC.
Therefore, as a result of these analytical difficulties, the VOCs in the tables in this
Corrigendum primarily differ from those in the original paper by the absence of the
branched- and long-chained alkanes. Since many of the VOCs made by this organism can
serve as fuels or fuel additives, the term myco-diesel still applies, especially as it relates to the
ability of this organism to produce a series of alkyl acetates, alcohols and acids representing
some of the major straight-chained alkanes of diesel. Furthermore, the ability of the
organism to digest cellulose and subsequently produce VOCs with fuel potential, while
qualitatively different in the tables, is still notable. A more detailed and comprehensive
study on the VOCs of this organism and a number of its close relatives is in this issue of
Microbiology (Griffin et al., 2010). The overall conclusion is that the products of this
organism following growth on a number of substrates have potential as fuels.
The authors would like to make the following corrections to the paper listed above.
1. Table 1, page 3322–3323
Table 1 is now replaced with a new Table 1, as shown below. Please also note that the
relative peak areas presented in this table are corrected values.
2. Table 2, page 3325
Table 2 is now replaced with a new Table 2, as shown below.
3. Table 3, page 3326
Table 3 is now replaced with a new Table 3, as shown below.
Microbiology (2010), 156, 3830–3833 DOI 10.1099/mic.0.2010/30824-0
3830 30824 G2010 SGM Printed in Great Britain
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Table 1. A GC-MS air space analysis of the volatile compounds produced by NRRL 50072 after an 18 day incubation under
microaerophilic conditions at 23 6C on oatmeal agar
Compounds found in the control oatmeal agar bottle are not included in this table. Comparative GC-MS data with standard compounds are
indicated in the footnotes under ‘Stds’. The total dry weight of the mycelial mat under these conditions was 38.9 mg.
Time Relative area Stds Possible compound Molecular mass (kDa)
4.598 7.132 * EthanolD46.04
7.232 0.601 * 1-Propanol, 2-methyl- 74.07
7.648 1.807 * 1-Butanol, 3-methyl-, acetate 130.10
8.303 0.335 * Pentane, 1-iodo- 197.99
8.364 1.379 * 2-Hexanol 102.10
8.735 1.228 * Hexanoic acid, methyl ester 130.10
9.066 7.956 * 1-Butanol, 3-methyl- 88.09
9.302 0.134 Phenol, 4-ethyl- 122.07
9.817 0.710 * 3-Octanone 128.12
10.054 1.780 * Acetic acid, hexyl ester 144.12
10.708 0.143 * 2-Heptanol 116.12
10.985 0.574 7-Octen-2-one 126.10
11.329 0.550 * Acetic acid, sec-octyl ester 172.15
11.545 11.294 * Acetic acid, heptyl ester 158.13
11.938 0.485 3,5-Octadiene (Z, Z) 110.11
12.127 0.604 * 2-Octanol 130.14
12.878 11.533 * Acetic acid 60.02
12.931 12.008 * Acetic acid, octyl ester 172.15
13.584 0.176 Sesquiterpene 1 204.19
14.651 0.651 Unknown 124.13
14.926 0.254 Unknown 122.11
15.673 0.465 Pentanoic acid, 3-methyl- 116.08
17.653 1.657 * Hexanoic acid 116.08
18.360 1.073 * Phenylethyl alcohol 122.07
19.588 0.355 * Phenol, 4-ethyl-2-methoxy- 152.08
*The retention time and MS spectrum closely matched or were identical to an authentic standard compound. Those compounds without a footnote
symbol have an MS spectrum that most closely matched the appropriate compound in the NIST database.
DTraces of the substance were also found in the control and the amount of the substance in the fungal flask was many fold greater in relative
concentration.
Corrigendum
http://mic.sgmjournals.org 3831
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Table 2. A GC-MS air space analysis of the volatile compounds produced by NRRL 50072 after an 18 day incubation under
microaerophilic conditions at 23 6C on a cellulose-based medium
Compounds found in the control bottle are not included in this table. Comparative GC-MS data with standard compounds are indicated in the
footnotes under ‘Stds’. The total dry weight of the mycelial mat under these conditions was 4.7 mg.
Time (min) Relative area Stds* Possible compound Molecular mass (kDa)
2.608 1.830 * Octane 114.14
4.562 50.710 * EthanolD46.04
5.248 0.473 * 2-Pentanone 86.07
5.747 397.632 * Pentanone, 4-methyl-D100.09
5.820 40.064 * Unknown 100.05
6.492 1.577 * 3-Hexanone 100.09
6.853 4.860 3-Hexanone, 4-methyl- 114.10
8.333 28.715 * 2-Hexanol 102.10
9.013 47.600 * 1-Butanol, 3-methyl- 88.09
10.437 6.675 3-Heptanone, 5-ethyl-4-methyl-d156.15
11.775 0.858 * 2-Nonanone 142.13
12.809 26.776 * Acetic acid 60.02
13.556 4.539 Sesquiterpene 1 204.19
14.213 7.333 Sesquiterpene 2 204.19
14.598 4.076 Sesquiterpene 3 204.19
14.648 1.223 Sesquiterpene 4 204.19
14.902 24.840 * Benzonitrile 103.04
14.957 3.169 Sesquiterpene 5 204.19
15.522 3.996 Sesquiterpene 6 204.19
15.961 1.625 * Sesquiterpene 7 204.19
16.037 1.478 Unknown 136.12
16.104 3.081 * Benzene, 1,4-dibromo- 233.87
17.281 6.366 Benzene, 1,3,5-trichloro-2-methoxy- 209.94
17.840 0.430 6-Methoxy-1-acetonaphthone 200.08
17.905 0.570 * Benzenemethanol 108.06
18.596 2.401 * Benzeneethanol 122.07
*The retention time and MS spectrum closely matched or were identical to an authentic standard compound. Those compounds without a footnote
symbol have an MS spectrum that most closely matched the appropriate compound in the NIST database.
DTraces of the substance were also found in the control and the amount of the substance in the fungal flask was many fold greater in relative
concentration.
dSome questions remain as to the identity of this compound.
G.A. Strobel and others
3832 Microbiology 156
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References
Griffin, M. A., Spakowicz, D. J., Gianoulis, T. A. & Strobel, S. A.
(2010). Volatile organic compound production by organisms in the
genus Ascocoryne and a re-evaluation of myco-diesel production by
NRRL 50072. Microbiology 156, 3814–3829.
Schulz, S. & Dickschat, J. S. (2007). Bacterial volatiles: the smell of
small organisms. Nat Prod Rep 24, 814–842.
Strobel, G. A., Dirksie, E., Sears, J. & Markworth, C. (2001). Volatile
antimicrobials from Muscodor albus, a novel endophytic fungus.
Microbiology 147, 2943–2950.
Table 3. A GC-MS air space analysis of the volatile compounds produced by NRRL 50072 after an 18 day incubation under
microaerophilic conditions at 23 6C on host medium
Compounds found in the control bottle are not included in this table. Comparative GC-MS data/notes with standard compounds are indicated in
the footnotes under ‘Stds’. The total dry weight of the mycelial mat under these conditions was 5.3 mg.
Time (min) Relative area Stds* Possible compound Molecular mass (kDa)
1.552 14.136 * 1-Butene, 2-methyl- 70.08
2.806 2.304 * 1-Octene 112.12
8.407 2.114 * 1-Butanol, 2-methyl- 88.09
11.591 11.384 * Benzene, 1-methoxy-2-methyl- 122.07
12.075 1.046 * Benzene, 1-methoxy-3-methyl- 122.07
12.847 2.816 Unknown 136.12
14.292 4.192 Phenol, 3-ethyl- 122.07
14.770 2.669 Pinocarveol 152.12
14.927 0.900 Sesquiterpene 1 204.19
15.367 0.871 Sesquiterpene 2 204.19
16.324 2.829 * Myrtenol 152.12
16.691 1.006 Unknown 209.94
20.292 0.817 Unknown 122.07
*The retention time and MS spectrum closely matched or were identical to an authentic standard compound. Those compounds without a
designated footnote have an MS spectrum that most closely matched the appropriate compound in the NIST database at a high quality level.
Corrigendum
http://mic.sgmjournals.org 3833

Supplementary resource (1)

Fungal endophyte MSU-2259 28S ribosomal RNA gene, partial sequence; internal transcribed spacer 2, 5.8S ribosomal RNA gene and internal transcribed spacer 1, complete sequence; and 18S ribosomal RNA gene, partial sequence
Nucleotide Sequence
January 2003
M. Stinson · David Ezra · G. Strobel
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... The concept of mycodiesel was first reported by Gary Strobel and his research team, who observed the production of mycodiesel in an endophytic fungus called Gliocladium roseum. This fungus was isolated from the leaves of the ulmo tree (Eucryphia cordifolia) in the Andes mountain region of Patagonia (Strobel et al. 2008). 206 S. Sen et al. ...
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Article
  • Oct 2003
  • PLANT SCI
An endophytic isolate of Gliocladium sp. was obtained from the Patagonian Eucryphiacean tree—Eucryphia cordifolia, known locally as “ulmo”. The fungus was identified on the basis of its morphology and aspects of its molecular biology. This fungus produces a mixture of volatile organic compounds (VOC's) lethal to such plant pathogenic fungi as Pythium ultimum and Verticillum dahliae, while other pathogens were only inhibited by its volatiles. Some of the same volatile bioactive compounds exuded by Gliocladium sp. such as 1-butanol, 3-methyl-, phenylethyl alcohol and acetic acid, 2-phenylethyl ester, as well as various propanoic acid esters, are also produced by Muscodor albus, a well known volatile antimicrobial producer. In fact, M. albus was used as a selection tool to effectively isolate Gliocladium sp. since it is resistant to VOC's produced by M. albus. However, the primary volatile compound produced by Gliocladium sp. is 1,3,5,7-cyclooctatetraene or [8]annulene, which by itself, was an effective inhibitor of fungal growth. The authenticated VOC's of Gliocladium sp. were inhibitory to all, and lethal to some test fungi in a manner that nearly mimicked the gases of Gliocladium sp. itself. This report shows that the production of selective volatile antibiotics by endophytic fungi is not exclusively confined to the Muscodor spp.
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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
Article
  • Feb 1998
  • Int J Mass Spectrom Ion Process
A proton transfer reaction mass spectrometer (PTR-MS) system has been developed which allows for on-line measurements of trace components with concentrations as low as a few pptv. The method is based on reactions of H3O+ ions, which perform non-dissociative proton transfer to most of the common volatile organic compounds (VOCs) but do not react with any of the components present in clean air. Medical applications by means of breath analysis allow for monitoring of metabolic processes in the human body, and examples of food research are discussed on the basis of VOC emissions from fruit, coffee and meat. Environmental applications include investigations of VOC emissions from decaying biomatter which have been found to be an important source for tropospheric acetone, methanol and ethanol. On-line monitoring of the diurnal variations of VOCs in the troposphere yield data demonstrating the present sensitivity of PTR-MS to be in the range of a few pptv. Finally, PTR-MS has proven to be an ideal tool to measure Henry's law constants and their dependencies on temperature as well as on the salt content of water.
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