Pyrolyzed Substrates Induce Aromatic Compound Metabolism in the Post-fire Fungus, Pyronema domesticum
Abstract
Wildfires represent a fundamental and profound disturbance in many ecosystems, and their frequency and severity are increasing in many regions of the world. Fire affects soil by removing carbon in the form of CO2 and transforming remaining surface carbon into pyrolyzed organic matter (PyOM). Fires also generate substantial necromass at depths where the heat kills soil organisms but does not catalyze the formation of PyOM. Pyronema species strongly dominate soil fungal communities within weeks to months after fire. However, the carbon pool (i.e., necromass or PyOM) that fuels their rise in abundance is unknown. We used a Pyronema domesticum isolate from the catastrophic 2013 Rim Fire (CA, United States) to ask whether P. domesticum is capable of metabolizing PyOM. Pyronema domesticum grew readily on agar media where the sole carbon source was PyOM (specifically, pine wood PyOM produced at 750°C). Using RNAseq, we investigated the response of P. domesticum to PyOM and observed a comprehensive induction of genes involved in the metabolism and mineralization of aromatic compounds, typical of those found in PyOM. Lastly, we used 13C-labeled 750°C PyOM to demonstrate that P. domesticum is capable of mineralizing PyOM to CO2. Collectively, our results indicate a robust potential for P.more »
- Authors:
-
- Univ. of California, Berkeley, CA (United States)
- Univ. of Wisconsin, Madison, WI (United States)
- Publication Date:
- Research Org.:
- Univ. of California, Berkeley, CA (United States); Univ. of Wisconsin, Madison, WI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1829221
- Grant/Contract Number:
- SC0020351
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Frontiers in Microbiology
- Additional Journal Information:
- Journal Volume: 12; Journal ID: ISSN 1664-302X
- Publisher:
- Frontiers Research Foundation
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; aromatic hydorcarbons; RNAseq; fire; carbon metabolic activity; PyOM; filamentous fungi
Citation Formats
Fischer, Monika S., Stark, Frances Grace, Berry, Timothy D., Zeba, Nayela, Whitman, Thea, and Traxler, Matthew F. Pyrolyzed Substrates Induce Aromatic Compound Metabolism in the Post-fire Fungus, Pyronema domesticum. United States: N. p., 2021.
Web. doi:10.3389/fmicb.2021.729289.
Fischer, Monika S., Stark, Frances Grace, Berry, Timothy D., Zeba, Nayela, Whitman, Thea, & Traxler, Matthew F. Pyrolyzed Substrates Induce Aromatic Compound Metabolism in the Post-fire Fungus, Pyronema domesticum. United States. https://doi.org/10.3389/fmicb.2021.729289
Fischer, Monika S., Stark, Frances Grace, Berry, Timothy D., Zeba, Nayela, Whitman, Thea, and Traxler, Matthew F. Wed .
"Pyrolyzed Substrates Induce Aromatic Compound Metabolism in the Post-fire Fungus, Pyronema domesticum". United States. https://doi.org/10.3389/fmicb.2021.729289. https://www.osti.gov/servlets/purl/1829221.
@article{osti_1829221,
title = {Pyrolyzed Substrates Induce Aromatic Compound Metabolism in the Post-fire Fungus, Pyronema domesticum},
author = {Fischer, Monika S. and Stark, Frances Grace and Berry, Timothy D. and Zeba, Nayela and Whitman, Thea and Traxler, Matthew F.},
abstractNote = {Wildfires represent a fundamental and profound disturbance in many ecosystems, and their frequency and severity are increasing in many regions of the world. Fire affects soil by removing carbon in the form of CO2 and transforming remaining surface carbon into pyrolyzed organic matter (PyOM). Fires also generate substantial necromass at depths where the heat kills soil organisms but does not catalyze the formation of PyOM. Pyronema species strongly dominate soil fungal communities within weeks to months after fire. However, the carbon pool (i.e., necromass or PyOM) that fuels their rise in abundance is unknown. We used a Pyronema domesticum isolate from the catastrophic 2013 Rim Fire (CA, United States) to ask whether P. domesticum is capable of metabolizing PyOM. Pyronema domesticum grew readily on agar media where the sole carbon source was PyOM (specifically, pine wood PyOM produced at 750°C). Using RNAseq, we investigated the response of P. domesticum to PyOM and observed a comprehensive induction of genes involved in the metabolism and mineralization of aromatic compounds, typical of those found in PyOM. Lastly, we used 13C-labeled 750°C PyOM to demonstrate that P. domesticum is capable of mineralizing PyOM to CO2. Collectively, our results indicate a robust potential for P. domesticum to liberate carbon from PyOM in post-fire ecosystems and return it to the bioavailable carbon pool.},
doi = {10.3389/fmicb.2021.729289},
journal = {Frontiers in Microbiology},
number = ,
volume = 12,
place = {United States},
year = {2021},
month = {10}
}
Works referenced in this record:
The Pyrogenic Carbon Cycle
journal, May 2015
- Bird, Michael I.; Wynn, Jonathan G.; Saiz, Gustavo
- Annual Review of Earth and Planetary Sciences, Vol. 43, Issue 1
Fire Effects on Nitrogen Pools and Dynamics in Terrestrial Ecosystems: a Meta-Analysis
journal, October 2001
- Wan, Shiqiang; Hui, Dafeng; Luo, Yiqi
- Ecological Applications, Vol. 11, Issue 5
Fire-derived organic carbon in soil turns over on a centennial scale
journal, January 2012
- Singh, N.; Abiven, S.; Torn, M. S.
- Biogeosciences, Vol. 9, Issue 8
The old 3-oxoadipate pathway revisited: New insights in the catabolism of aromatics in the saprophytic fungus Aspergillus nidulans
journal, January 2015
- Martins, Tiago M.; Hartmann, Diego O.; Planchon, Sébastien
- Fungal Genetics and Biology, Vol. 74
The versatility of the fungal cytochrome P450 monooxygenase system is instrumental in xenobiotic detoxification: Fungal P450 systems in xenobiotic detoxification
journal, August 2011
- Lah, Ljerka; Podobnik, Barbara; Novak, Metka
- Molecular Microbiology, Vol. 81, Issue 5
Fungal degradation of benzoic acid and related compounds
journal, January 1993
- Wright, J. D.
- World Journal of Microbiology & Biotechnology, Vol. 9, Issue 1
Fire as a fundamental ecological process: Research advances and frontiers
journal, June 2020
- McLauchlan, Kendra K.; Higuera, Philip E.; Miesel, Jessica
- Journal of Ecology, Vol. 108, Issue 5
Degradation of polycyclic aromatic hydrocarbons (2–7 rings) under microaerobic and very-low-oxygen conditions by soil fungi
journal, March 2009
- Silva, Isis S.; Grossman, Matthew; Durrant, Lucia R.
- International Biodeterioration & Biodegradation, Vol. 63, Issue 2
Vegetation change during 40 years of repeated managed wildfires in the Sierra Nevada, California
journal, October 2017
- Boisramé, Gabrielle F. S.; Thompson, Sally E.; Kelly, Maggi
- Forest Ecology and Management, Vol. 402
Genetic Bases of Fungal White Rot Wood Decay Predicted by Phylogenomic Analysis of Correlated Gene-Phenotype Evolution
journal, November 2016
- Nagy, László G.; Riley, Robert; Bergmann, Philip J.
- Molecular Biology and Evolution, Vol. 34, Issue 1
The metabolism of aromatic acids by micro-organisms. Metabolic pathways in the fungi
journal, August 1968
- Cain, R. B.; Bilton, R. F.; Darrah, Josephine A.
- Biochemical Journal, Vol. 108, Issue 5
Trimmomatic: a flexible trimmer for Illumina sequence data
journal, April 2014
- Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern
- Bioinformatics, Vol. 30, Issue 15
The carbon starvation response of Aspergillus niger during submerged cultivation: Insights from the transcriptome and secretome
journal, January 2012
- Nitsche, Benjamin M.; Jørgensen, Thomas R.; Akeroyd, Michiel
- BMC Genomics, Vol. 13, Issue 1
The Inducible Quinate-Shikimate Catabolic Pathway in Neurospora crassa: Genetic Organization
journal, February 2000
- Chaleff, R. S.
- Microbiology, Vol. 81, Issue 2
Studies on pyrophilous discomycetes
journal, September 1968
- El-Abyad, M. S. H.; Webster, J.
- Transactions of the British Mycological Society, Vol. 51, Issue 3-4
Synthesis of Aromatic Compounds by Neurospora
journal, May 1954
- Tatum, E. L.; Gross, S. R.; Ehrensvard, G.
- Proceedings of the National Academy of Sciences, Vol. 40, Issue 5
Effects of fire on properties of forest soils: a review
journal, February 2005
- Certini, Giacomo
- Oecologia, Vol. 143, Issue 1
Induction of aryl hydrocarbon hydroxylase inNeurospora crassa by benzo (α) pyrene
journal, May 1979
- Lin, W. S.; Kapoor, M.
- Current Microbiology, Vol. 3, Issue 3
The carbon starvation response of the ectomycorrhizal fungus Paxillus involutus
journal, March 2015
- Ellström, Magnus; Shah, Firoz; Johansson, Tomas
- FEMS Microbiology Ecology, Vol. 91, Issue 4
Extracellular DNA in soil and sediment: fate and ecological relevance
journal, December 2008
- Pietramellara, G.; Ascher, J.; Borgogni, F.
- Biology and Fertility of Soils, Vol. 45, Issue 3
Fire as a global ‘herbivore’: the ecology and evolution of flammable ecosystems
journal, July 2005
- Bond, W.; Keeley, J.
- Trends in Ecology & Evolution, Vol. 20, Issue 7
Soil Temperatures During Forest Fires and Their Effect on the Survival of Vegetation
journal, February 1940
- Beadle, N. C. W.
- The Journal of Ecology, Vol. 28, Issue 1
Dynamic Molecular Structure of Plant Biomass-Derived Black Carbon (Biochar)
journal, February 2010
- Keiluweit, Marco; Nico, Peter S.; Johnson, Mark G.
- Environmental Science & Technology, Vol. 44, Issue 4
The TamA Protein Fused to a DNA-Binding Domain Can Recruit AreA, the Major Nitrogen Regulatory Protein, to Activate Gene Expression in Aspergillus nidulans
journal, September 1999
- Small, Anna J.; Hynes, Michael J.; Davis, Meryl A.
- Genetics, Vol. 153, Issue 1
Belowground community responses to fire: meta-analysis reveals contrasting responses of soil microorganisms and mesofauna
journal, October 2018
- Pressler, Yamina; Moore, John C.; Cotrufo, M. Francesca
- Oikos, Vol. 128, Issue 3
A simple pyrocosm for studying soil microbial response to fire reveals a rapid, massive response by Pyronema species
journal, March 2020
- Bruns, Thomas D.; Chung, Judy A.; Carver, Akiko A.
- PLOS ONE, Vol. 15, Issue 3
Cycling of extracellular DNA in the soil environment
journal, December 2007
- Levy-Booth, David J.; Campbell, Rachel G.; Gulden, Robert H.
- Soil Biology and Biochemistry, Vol. 39, Issue 12
Partitioning the contributions of biochar properties to enhanced biological nitrogen fixation in common bean (Phaseolus vulgaris)
journal, January 2015
- Güereña, David T.; Lehmann, Johannes; Thies, Janice E.
- Biology and Fertility of Soils, Vol. 51, Issue 4
Where are they hiding? Testing the body snatchers hypothesis in pyrophilous fungi
journal, February 2020
- Raudabaugh, Daniel B.; Matheny, P. Brandon; Hughes, Karen W.
- Fungal Ecology, Vol. 43
An open-source, automated, gas sampling peripheral for laboratory incubation experiments using cavity ring-down spectroscopy
journal, October 2021
- Berry, Timothy D.; Creelman, Chance; Nickerson, Nick
- HardwareX, Vol. 10
HTSeq--a Python framework to work with high-throughput sequencing data
journal, September 2014
- Anders, S.; Pyl, P. T.; Huber, W.
- Bioinformatics, Vol. 31, Issue 2
Forest floor chemical transformations in a boreal forest fire and their correlations with temperature and heating duration
journal, February 2016
- Santín, Cristina; Doerr, Stefan H.; Merino, Agustín
- Geoderma, Vol. 264
Fire effects on temperate forest soil C and N storage
journal, June 2011
- Nave, Lucas E.; Vance, Eric D.; Swanston, Christopher W.
- Ecological Applications, Vol. 21, Issue 4
Cytochrome P450 Monooxygenase-Mediated Metabolic Utilization of Benzo[ a ]Pyrene by Aspergillus Species
journal, June 2019
- Ostrem Loss, Erin M.; Lee, Mi-Kyung; Wu, Ming-Yueh
- mBio, Vol. 10, Issue 3
Current State of Knowledge in Microbial Degradation of Polycyclic Aromatic Hydrocarbons (PAHs): A Review
journal, August 2016
- Ghosal, Debajyoti; Ghosh, Shreya; Dutta, Tapan K.
- Frontiers in Microbiology, Vol. 7
Relic DNA is abundant in soil and obscures estimates of soil microbial diversity
journal, December 2016
- Carini, Paul; Marsden, Patrick J.; Leff, Jonathan W.
- Nature Microbiology, Vol. 2, Issue 3
Two-Component FAD-Dependent Monooxygenases: Current Knowledge and Biotechnological Opportunities
journal, August 2018
- Heine, Thomas; van Berkel, Willem; Gassner, George
- Biology, Vol. 7, Issue 3
Conversion of furfural to furoic acid and furfuryl alcohol by Neurospora ascospores
journal, January 1970
- Eilers, Frederick I.; Sussman, Alfred S.
- Planta, Vol. 94, Issue 4
Studies on pyrophilous discomycetes
journal, September 1968
- El-Abyad, M. S. H.; Webster, J.
- Transactions of the British Mycological Society, Vol. 51, Issue 3-4
The Inducible Quinate-Shikimate Catabolic Pathway in Neurospora crassa: Induction and Regulation of Enzyme Synthesis
journal, February 2000
- Chaleff, R. S.
- Microbiology, Vol. 81, Issue 2
Implications of changing climate for global wildland fire
journal, January 2009
- Flannigan, Mike D.; Krawchuk, Meg A.; de Groot, William J.
- International Journal of Wildland Fire, Vol. 18, Issue 5
Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype
journal, August 2019
- Kim, Daehwan; Paggi, Joseph M.; Park, Chanhee
- Nature Biotechnology, Vol. 37, Issue 8
Biotechnology Potential of Marine Fungi Degrading Plant and Algae Polymeric Substrates
journal, July 2018
- Balabanova, Larissa; Slepchenko, Lubov; Son, Oksana
- Frontiers in Microbiology, Vol. 9
Studies in Pyrophilous Fungi: I. The Occurrence and Cultivation of Pyronema
journal, July 1909
- Seaver, Fred J.
- Mycologia, Vol. 1, Issue 4
Fire-induced transformation of C- and N- forms in different organic soil fractions from a Dystric Cambisol under a Mediterranean pine forest ()
journal, April 2005
- Knicker, H.; Gonzalezvila, F.; Polvillo, O.
- Soil Biology and Biochemistry, Vol. 37, Issue 4
The genome portal of the Department of Energy Joint Genome Institute: 2014 updates
journal, November 2013
- Nordberg, Henrik; Cantor, Michael; Dusheyko, Serge
- Nucleic Acids Research, Vol. 42, Issue D1
Lignin degradation: microorganisms, enzymes involved, genomes analysis and evolution
journal, October 2017
- Janusz, Grzegorz; Pawlik, Anna; Sulej, Justyna
- FEMS Microbiology Reviews, Vol. 41, Issue 6
Population genomics and local adaptation in wild isolates of a model microbial eukaryote
journal, January 2011
- Ellison, C. E.; Hall, C.; Kowbel, D.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 7
Controls on black carbon storage in soils: BLACK CARBON IN SOILS
journal, July 2007
- Czimczik, Claudia I.; Masiello, Caroline A.
- Global Biogeochemical Cycles, Vol. 21, Issue 3
Factors shaping communities of pyrophilous macrofungi in microhabitats destroyed by illegal campfires
journal, September 2012
- Adamczyk, Jolanta J.; Kruk, Andrzej; Penczak, Tadeusz
- Fungal Biology, Vol. 116, Issue 9
A Universally Applicable and Rapid Method for Measuring the Growth of Streptomyces and Other Filamentous Microorganisms by Methylene Blue Adsorption-Desorption
journal, July 2013
- Fischer, Marco; Sawers, R. Gary
- Applied and Environmental Microbiology, Vol. 79, Issue 14
The Structure of Neurospora crassa 3-Carboxy-cis,cis-Muconate Lactonizing Enzyme, a β Propeller Cycloisomerase
journal, April 2002
- Kajander, Tommi; Merckel, Michael C.; Thompson, Andrew
- Structure, Vol. 10, Issue 4
Identification and manipulation of Neurospora crassa genes involved in sensitivity to furfural
journal, September 2019
- Feldman, Daria; Kowbel, David J.; Cohen, Adi
- Biotechnology for Biofuels, Vol. 12, Issue 1
Pyrogenic organic matter production from wildfires: a missing sink in the global carbon cycle
journal, January 2015
- Santín, Cristina; Doerr, Stefan H.; Preston, Caroline M.
- Global Change Biology, Vol. 21, Issue 4
Thermal alteration of soil organic matter properties: a systematic study to infer response of Sierra Nevada climosequence soils to forest fires
journal, January 2017
- Araya, Samuel N.; Fogel, Marilyn L.; Berhe, Asmeret Asefaw
- SOIL, Vol. 3, Issue 1
Pyrophilous fungi detected after wildfires in the Great Smoky Mountains National Park expand known species ranges and biodiversity estimates
journal, June 2020
- Hughes, Karen W.; Matheny, P. Brandon; Miller, Andrew N.
- Mycologia, Vol. 112, Issue 4
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014
- Love, Michael I.; Huber, Wolfgang; Anders, Simon
- Genome Biology, Vol. 15, Issue 12