Biomass-degrading enzymes are catabolite repressed in anaerobic gut fungi
Abstract
Anaerobic fungi are among the most active plant‐degrading microbes in nature. Increased insight into the mechanisms and environmental cues that regulate fungal hydrolysis would better inform bioprocessing strategies to depolymerize lignocellulose. Here, we compare the response of three strains of anaerobic fungi ( Piromyces finnis , Anaeromyces robustus , and Neocallimastix californiae ) to catabolite regulation by simple carbohydrates. Anaerobic fungi exhibited high enzymatic activity against crystalline cellulose, which was repressed upon incubation with free sugars. Cellulolytic degradation was also inhibited when fungi were exposed to sugars they did not metabolize, suggesting a general mode of catabolite repression. RNA‐Seq experiments in the presence of excess glucose confirmed repression of carbohydrate active enzymes during sugar uptake, and offer a path towards unmasking the function of co‐regulated genes that could be involved in biomass degradation. Overall, these results suggest that sugar‐rich hydrolysates tune the behavior of anaerobic fungi by dampening production of their biomass‐degrading enzymes. © 2018 American Institute of Chemical Engineers AIChE J , 64: 4263–4270, 2018
- Authors:
-
- Univ. of California, Santa Barbara, CA (United States). Dept. of Chemical Engineering
- Publication Date:
- Research Org.:
- Univ. of California, Santa Barbara, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
- OSTI Identifier:
- 1485151
- Alternate Identifier(s):
- OSTI ID: 1475228
- Grant/Contract Number:
- SC0010352; AC02-05CH11231; AC05-76RL01830
- Resource Type:
- Accepted Manuscript
- Journal Name:
- AIChE Journal
- Additional Journal Information:
- Journal Volume: 64; Journal Issue: 12; Journal ID: ISSN 0001-1541
- Publisher:
- American Institute of Chemical Engineers
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 09 BIOMASS FUELS; anaerobic fungi; cellulases; biofuel; regulation; Neocallimastigales
Citation Formats
Henske, John K., Gilmore, Sean P., Haitjema, Charles H., Solomon, Kevin V., and O'Malley, Michelle A. Biomass-degrading enzymes are catabolite repressed in anaerobic gut fungi. United States: N. p., 2018.
Web. doi:10.1002/aic.16395.
Henske, John K., Gilmore, Sean P., Haitjema, Charles H., Solomon, Kevin V., & O'Malley, Michelle A. Biomass-degrading enzymes are catabolite repressed in anaerobic gut fungi. United States. https://doi.org/10.1002/aic.16395
Henske, John K., Gilmore, Sean P., Haitjema, Charles H., Solomon, Kevin V., and O'Malley, Michelle A. Thu .
"Biomass-degrading enzymes are catabolite repressed in anaerobic gut fungi". United States. https://doi.org/10.1002/aic.16395. https://www.osti.gov/servlets/purl/1485151.
@article{osti_1485151,
title = {Biomass-degrading enzymes are catabolite repressed in anaerobic gut fungi},
author = {Henske, John K. and Gilmore, Sean P. and Haitjema, Charles H. and Solomon, Kevin V. and O'Malley, Michelle A.},
abstractNote = {Anaerobic fungi are among the most active plant‐degrading microbes in nature. Increased insight into the mechanisms and environmental cues that regulate fungal hydrolysis would better inform bioprocessing strategies to depolymerize lignocellulose. Here, we compare the response of three strains of anaerobic fungi ( Piromyces finnis , Anaeromyces robustus , and Neocallimastix californiae ) to catabolite regulation by simple carbohydrates. Anaerobic fungi exhibited high enzymatic activity against crystalline cellulose, which was repressed upon incubation with free sugars. Cellulolytic degradation was also inhibited when fungi were exposed to sugars they did not metabolize, suggesting a general mode of catabolite repression. RNA‐Seq experiments in the presence of excess glucose confirmed repression of carbohydrate active enzymes during sugar uptake, and offer a path towards unmasking the function of co‐regulated genes that could be involved in biomass degradation. Overall, these results suggest that sugar‐rich hydrolysates tune the behavior of anaerobic fungi by dampening production of their biomass‐degrading enzymes. © 2018 American Institute of Chemical Engineers AIChE J , 64: 4263–4270, 2018},
doi = {10.1002/aic.16395},
journal = {AIChE Journal},
number = 12,
volume = 64,
place = {United States},
year = {Thu Aug 30 00:00:00 EDT 2018},
month = {Thu Aug 30 00:00:00 EDT 2018}
}
Web of Science
Works referenced in this record:
Driving biomass breakdown through engineered cellulosomes
journal, February 2015
- Gilmore, Sean P.; Henske, John K.; O'Malley, Michelle A.
- Bioengineered, Vol. 6, Issue 4
Yeast Carbon Catabolite Repression
journal, June 1998
- Gancedo, Juana M.
- Microbiology and Molecular Biology Reviews, Vol. 62, Issue 2
Primary sequence and enzymic properties of two modular endoglucanases, Cel5A and Cel45A, from the anaerobic fungus Piromyces equi
journal, August 2000
- Hazlewood, Geoffrey P.; Gilbert, Harry J.; Eberhardt, Ruth Y.
- Microbiology, Vol. 146, Issue 8
Diversity of anaerobic fungal populations in cattle revealed by selective enrichment culture using different carbon sources
journal, May 2009
- Griffith, G. W.; Ozkose, E.; Theodorou, M. K.
- Fungal Ecology, Vol. 2, Issue 2
Regulation of Expression of Cellulosomal Cellulase and Hemicellulase Genes in Clostridium cellulovorans
journal, October 2003
- Han, S. O.; Yukawa, H.; Inui, M.
- Journal of Bacteriology, Vol. 185, Issue 20
Comparison of growth characteristics of anaerobic fungi isolated from ruminant and non-ruminant herbivores during cultivation in a defined medium
journal, June 1991
- Teunissen, M. J.; Op den Camp, H. J. M.; Orpin, C. G.
- Journal of General Microbiology, Vol. 137, Issue 6
Anaerobic fungi (phylum Neocallimastigomycota ): advances in understanding their taxonomy, life cycle, ecology, role and biotechnological potential
journal, August 2014
- Gruninger, Robert J.; Puniya, Anil K.; Callaghan, Tony M.
- FEMS Microbiology Ecology, Vol. 90, Issue 1
Anaerobic fungi in herbivorous animals
journal, February 1994
- Trinci, Anthony P. J.; Davies, David R.; Gull, Keith
- Mycological Research, Vol. 98, Issue 2
The importance of sourcing enzymes from non-conventional fungi for metabolic engineering and biomass breakdown
journal, November 2017
- Seppälä, Susanna; Wilken, St. Elmo; Knop, Doriv
- Metabolic Engineering, Vol. 44
Production of cellulolytic and xylanolytic enzymes during growth of the anaerobic fungus Piromyces sp. on different substrates
journal, August 1992
- Teunissen, M. J.; De Kort, G. V. M.; Op Den Camp, H. J. M.
- Journal of General Microbiology, Vol. 138, Issue 8
Molecular analysis of the anaerobic rumen fungus Orpinomyces - insights into an AT-rich genome
journal, January 2005
- Nicholson, M. J.
- Microbiology, Vol. 151, Issue 1
Transcriptomic characterization of Caecomyces churrovis: a novel, non-rhizoid-forming lignocellulolytic anaerobic fungus
journal, December 2017
- Henske, John K.; Gilmore, Sean P.; Knop, Doriv
- Biotechnology for Biofuels, Vol. 10, Issue 1
featureCounts: an efficient general purpose program for assigning sequence reads to genomic features
journal, November 2013
- Liao, Y.; Smyth, G. K.; Shi, W.
- Bioinformatics, Vol. 30, Issue 7
Substrate-based differential expression analysis reveals control of biomass degrading enzymes in Pycnoporus cinnabarinus
journal, February 2018
- Henske, John K.; Springer, Stephen D.; O'Malley, Michelle A.
- Biochemical Engineering Journal, Vol. 130
In Silico Identification of Microbial Partners to Form Consortia with Anaerobic Fungi
journal, January 2018
- Wilken, St.; Saxena, Mohan; Petzold, Linda
- Processes, Vol. 6, Issue 1
Transcriptional Regulation of Biomass-degrading Enzymes in the Filamentous Fungus Trichoderma reesei
journal, June 2003
- Foreman, Pamela K.; Brown, Doug; Dankmeyer, Lydia
- Journal of Biological Chemistry, Vol. 278, Issue 34, p. 31988-31997
Mapping the membrane proteome of anaerobic gut fungi identifies a wealth of carbohydrate binding proteins and transporters
journal, December 2016
- Seppälä, Susanna; Solomon, Kevin V.; Gilmore, Sean P.
- Microbial Cell Factories, Vol. 15, Issue 1
Biomass as feedstock for a bioenergy and bioproducts industry: The technical feasibility of a billion-ton annual supply
report, April 2005
- Perlack, Robert D.; Wright, Lynn L.; Turhollow, Anthony F.
Cellulases and hemicellulases of the anaerobic fungus Piromyces constitute a multiprotein cellulose-binding complex and are encoded by multigene families
journal, January 1995
- Ali, Bassam R. S.; Zhou, Liqing; Graves, Fiona M.
- FEMS Microbiology Letters, Vol. 125, Issue 1
Mutualistic Fermentative Digestion in the Gastrointestinal Tract: Diversity and Evolution
journal, April 2002
- Mackie, R. I.
- Integrative and Comparative Biology, Vol. 42, Issue 2
Anaerobic fungi and their cellulolytic and xylanolytic enzymes
journal, January 1993
- Teunissen, Marcel J.; Op den Camp, Huub J. M.
- Antonie van Leeuwenhoek, Vol. 63, Issue 1
Early-branching gut fungi possess a large, comprehensive array of biomass-degrading enzymes
journal, February 2016
- Solomon, Kevin V.; Haitjema, Charles H.; Henske, John K.
- Science, Vol. 351, Issue 6278
Metabolic characterization of anaerobic fungi provides a path forward for bioprocessing of crude lignocellulose
journal, January 2018
- Henske, John K.; Wilken, St. Elmo; Solomon, Kevin V.
- Biotechnology and Bioengineering, Vol. 115, Issue 4
Degradation of structural polysaccharides by the plant cell-wall degrading enzyme system from anaerobic fungi: An application study
journal, August 1997
- Dijkerman, Rembrandt; Bhansing, Diana C. P.; Op den Camp, Huub J. M.
- Enzyme and Microbial Technology, Vol. 21, Issue 2
Microbial Ecology and Activities in the Rumen: Part I
journal, January 1982
- Hobson, P. N.; Wallace, R. J.; Bryant, Marvin P.
- CRC Critical Reviews in Microbiology, Vol. 9, Issue 3
Regulation of Cellulase and Hemicellulase Gene Expression in Fungi
journal, June 2013
- Amore, Antonella; Giacobbe, Simona; Faraco, Vincenza
- Current Genomics, Vol. 14, Issue 4
Opportunities to improve fiber degradation in the rumen: microbiology, ecology, and genomics
journal, December 2003
- Krause, Denis O.; Denman, Stuart E.; Mackie, Roderick I.
- FEMS Microbiology Reviews, Vol. 27, Issue 5
Anaerobic gut fungi: Advances in isolation, culture, and cellulolytic enzyme discovery for biofuel production: Anaerobic Gut Fungi
journal, May 2014
- Haitjema, Charles H.; Solomon, Kevin V.; Henske, John K.
- Biotechnology and Bioengineering, Vol. 111, Issue 8
Genetic Modification of Carbon Catabolite Repression in Trichoderma reesei for Improved Protein Production
journal, May 2009
- Nakari-Setala, T.; Paloheimo, M.; Kallio, J.
- Applied and Environmental Microbiology, Vol. 75, Issue 14
Microbial Cellulose Utilization: Fundamentals and Biotechnology
journal, December 2002
- Lynd, L. R.; Weimer, P. J.; van Zyl, W. H.
- Microbiology and Molecular Biology Reviews, Vol. 66, Issue 4, p. 739-739
Finding a robust strain for biomethanation: Anaerobic fungi (Neocallimastigomycota) from the Alpine ibex (Capra ibex) and their associated methanogens
journal, October 2014
- Leis, Stefanie; Dresch, Philipp; Peintner, Ursula
- Anaerobe, Vol. 29
Carbon catabolite repression in bacteria: many ways to make the most out of nutrients
journal, August 2008
- Görke, Boris; Stülke, Jörg
- Nature Reviews Microbiology, Vol. 6, Issue 8, p. 613-624
The Genome of the Anaerobic Fungus Orpinomyces sp. Strain C1A Reveals the Unique Evolutionary History of a Remarkable Plant Biomass Degrader
journal, May 2013
- Youssef, Noha H.; Couger, M. B.; Struchtemeyer, Christopher G.
- Applied and Environmental Microbiology, Vol. 79, Issue 15
Outlook for cellulase improvement: Screening and selection strategies
journal, September 2006
- Percival Zhang, Y.-H.; Himmel, Michael E.; Mielenz, Jonathan R.
- Biotechnology Advances, Vol. 24, Issue 5, p. 452-481
RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome
journal, August 2011
- Li, Bo; Dewey, Colin N.
- BMC Bioinformatics, Vol. 12, Issue 1
A parts list for fungal cellulosomes revealed by comparative genomics
journal, May 2017
- Haitjema, Charles H.; Gilmore, Sean P.; Henske, John K.
- Nature Microbiology, Vol. 2, Issue 8
Metagenomic Discovery of Biomass-Degrading Genes and Genomes from Cow Rumen
journal, January 2011
- Hess, M.; Sczyrba, A.; Egan, R.
- Science, Vol. 331, Issue 6016
Microbial communities for bioprocessing: lessons learned from nature
journal, November 2016
- Peng, Xuefeng “Nick”; Gilmore, Sean P.; O’Malley, Michelle A.
- Current Opinion in Chemical Engineering, Vol. 14
Tracking the roots of cellulase hyperproduction by the fungus Trichoderma reesei using massively parallel DNA sequencing
journal, September 2009
- Le Crom, S.; Schackwitz, W.; Pennacchio, L.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 38
HISAT: a fast spliced aligner with low memory requirements
journal, March 2015
- Kim, Daehwan; Langmead, Ben; Salzberg, Steven L.
- Nature Methods, Vol. 12, 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
Cellulase adsorption on lignin: A roadblock for economic hydrolysis of biomass
journal, December 2016
- Saini, Jitendra Kumar; Patel, Anil Kumar; Adsul, Mukund
- Renewable Energy, Vol. 98
Extracting data from the muck: deriving biological insight from complex microbial communities and non-model organisms with next generation sequencing
journal, August 2014
- Solomon, Kevin V.; Haitjema, Charles H.; Thompson, Dawn A.
- Current Opinion in Biotechnology, Vol. 28
Genomic DNA analysis of genes encoding (hemi-)cellulolytic enzymes of the anaerobic fungus Piromyces sp. E2
journal, September 2003
- Harhangi, Harry R.; Akhmanova, Anna; Steenbakkers, Peter J. M.
- Gene, Vol. 314
Spatio-temporal characterization of polyhydroxybutyrate accumulation in sugarcane
journal, January 2007
- Purnell, Matthew P.; Petrasovits, Lars A.; Nielsen, Lars K.
- Plant Biotechnology Journal, Vol. 5, Issue 1
Enumeration of Anaerobic Chytridiomycetes as Thallus-Forming Units: Novel Method for Quantification of Fibrolytic Fungal Populations from the Digestive Tract Ecosystem
journal, January 1990
- Theodorou, Michael K.; Gill, Margaret; King-Spooner, Catherine
- Applied and Environmental Microbiology, Vol. 56, Issue 4
Anaerobic fungi
book, January 2006
- Theodorou, Michael K.; Brookman, Jayne; Trinci, Anthony P. J.
- Methods in Gut Microbial Ecology for Ruminants
Role of catabolite regulatory mechanisms in control of carbohydrate utilization by the rumen anaerobic fungus Neocallimastix frontalis.
journal, January 1983
- Mountfort, D. O.; Asher, R. A.
- Applied and Environmental Microbiology, Vol. 46, Issue 6
Production and regulation of cellulase by two strains of the rumen anaerobic fungus Neocallimastix frontalis.
journal, January 1985
- Mountfort, D. O.; Asher, R. A.
- Applied and Environmental Microbiology, Vol. 49, Issue 5
Production of α-Amylase by the Ruminal Anaerobic Fungus Neocallimastix frontalis
journal, January 1988
- Mountfort, Douglas O.; Asher, Rodney A.
- Applied and Environmental Microbiology, Vol. 54, Issue 9
ARS2/MAGL signaling in glioblastoma stem cells promotes self-renewal and M2-like polarization of tumor-associated macrophages
journal, June 2020
- Yin, Jinlong; Kim, Sung Soo; Choi, Eunji
- Nature Communications, Vol. 11, Issue 1
Crotonylation of key metabolic enzymes regulates carbon catabolite repression in Streptomyces roseosporus
journal, April 2020
- Sun, Chen-Fan; Xu, Wei-Feng; Zhao, Qing-Wei
- Communications Biology, Vol. 3, Issue 1
Datura genome reveals duplications of psychoactive alkaloid biosynthetic genes and high mutation rate following tissue culture
journal, March 2021
- Rajewski, Alex; Carter-House, Derreck; Stajich, Jason
- BMC Genomics, Vol. 22, Issue 1
featureCounts: An efficient general-purpose program for assigning sequence reads to genomic features
text, January 2013
- Liao, Yang; Smyth, Gordon K.; Shi, Wei
- arXiv
Works referencing / citing this record:
Co-cultivation of the anaerobic fungus Anaeromyces robustus with Methanobacterium bryantii enhances transcription of carbohydrate active enzymes
journal, May 2019
- Swift, Candice L.; Brown, Jennifer L.; Seppälä, Susanna
- Journal of Industrial Microbiology & Biotechnology, Vol. 46, Issue 9-10
Proteome specialization of anaerobic fungi during ruminal degradation of recalcitrant plant fiber
journal, September 2020
- Hagen, Live H.; Brooke, Charles G.; Shaw, Claire A.
- The ISME Journal, Vol. 15, Issue 2