Fungal ecological strategies reflected in gene transcription - a case study of two litter decomposers
Abstract
Microbial communities interplay with their environment through their functional traits that can be a response or an effect on the environment. Here, we explore how a functional trait-the decomposition of organic matter, can be addressed based on genetic markers and how the expression of these markers reflect ecological strategies of two fungal litter decomposer Gymnopus androsaceus and Chalara longipes. We sequenced the genomes of these two fungi, as well as their transcriptomes at different steps of Pinus sylvestris needles decomposition in microcosms. Our results highlighted that if the gene content of the two species could indicate similar potential decomposition abilities, the expression levels of specific gene families belonging to the glycoside hydrolase category reflected contrasting ecological strategies. Actually, C. longipes, the weaker decomposer in this experiment, turned out to have a high content of genes involved in cell wall polysaccharides decomposition but low expression levels, reflecting a versatile ecology compare to the more competitive G. androsaceus with high expression levels of keystone functional genes. Finally, we established that sequential expression of genes coding for different components of the decomposer machinery indicated adaptation to chemical changes in the substrate as decomposition progressed.
- Authors:
-
[1];
- Swedish Univ. of Agricultural Sciences, Uppsala (Sweden)
- Univ. de Lorraine, Champenoux (France)
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States)
- Aix‐Marseille Univ., Marseille (France); INRA, Marseille (France); King Abdulaziz Univ., Jeddah (Saudi Arabia)
- Department of Soil and EnvironmentSwedish University of Agricultural Sciences Box 7014, SE‐750 07 Uppsala Sweden
- Univ. de Lorraine, Champenoux (France); Beijing Forestry Univ. (China)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC); Swedish Research Council (SRC)
- OSTI Identifier:
- 1619166
- Alternate Identifier(s):
- OSTI ID: 1577420
- Grant/Contract Number:
- AC02-05CH11231; 2011-1747; ANR-11-LABX-0002_ARBRE
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Environmental Microbiology
- Additional Journal Information:
- Journal Volume: 22; Journal Issue: 3; Journal ID: ISSN 1462-2912
- Publisher:
- Wiley
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Barbi, Florian, Kohler, Annegret, Barry, Kerrie, Baskaran, Preetisri, Daum, Chris, Fauchery, Laure, Ihrmark, Katarina, Kuo, Alan, LaButti, Kurt, Lipzen, Anna, Morin, Emmanuelle, Grigoriev, Igor V., Henrissat, Bernard, Lindahl, Björn D., and Martin, Francis. Fungal ecological strategies reflected in gene transcription - a case study of two litter decomposers. United States: N. p., 2019.
Web. doi:10.1111/1462-2920.14873.
Barbi, Florian, Kohler, Annegret, Barry, Kerrie, Baskaran, Preetisri, Daum, Chris, Fauchery, Laure, Ihrmark, Katarina, Kuo, Alan, LaButti, Kurt, Lipzen, Anna, Morin, Emmanuelle, Grigoriev, Igor V., Henrissat, Bernard, Lindahl, Björn D., & Martin, Francis. Fungal ecological strategies reflected in gene transcription - a case study of two litter decomposers. United States. https://doi.org/10.1111/1462-2920.14873
Barbi, Florian, Kohler, Annegret, Barry, Kerrie, Baskaran, Preetisri, Daum, Chris, Fauchery, Laure, Ihrmark, Katarina, Kuo, Alan, LaButti, Kurt, Lipzen, Anna, Morin, Emmanuelle, Grigoriev, Igor V., Henrissat, Bernard, Lindahl, Björn D., and Martin, Francis. Sun .
"Fungal ecological strategies reflected in gene transcription - a case study of two litter decomposers". United States. https://doi.org/10.1111/1462-2920.14873. https://www.osti.gov/servlets/purl/1619166.
@article{osti_1619166,
title = {Fungal ecological strategies reflected in gene transcription - a case study of two litter decomposers},
author = {Barbi, Florian and Kohler, Annegret and Barry, Kerrie and Baskaran, Preetisri and Daum, Chris and Fauchery, Laure and Ihrmark, Katarina and Kuo, Alan and LaButti, Kurt and Lipzen, Anna and Morin, Emmanuelle and Grigoriev, Igor V. and Henrissat, Bernard and Lindahl, Björn D. and Martin, Francis},
abstractNote = {Microbial communities interplay with their environment through their functional traits that can be a response or an effect on the environment. Here, we explore how a functional trait-the decomposition of organic matter, can be addressed based on genetic markers and how the expression of these markers reflect ecological strategies of two fungal litter decomposer Gymnopus androsaceus and Chalara longipes. We sequenced the genomes of these two fungi, as well as their transcriptomes at different steps of Pinus sylvestris needles decomposition in microcosms. Our results highlighted that if the gene content of the two species could indicate similar potential decomposition abilities, the expression levels of specific gene families belonging to the glycoside hydrolase category reflected contrasting ecological strategies. Actually, C. longipes, the weaker decomposer in this experiment, turned out to have a high content of genes involved in cell wall polysaccharides decomposition but low expression levels, reflecting a versatile ecology compare to the more competitive G. androsaceus with high expression levels of keystone functional genes. Finally, we established that sequential expression of genes coding for different components of the decomposer machinery indicated adaptation to chemical changes in the substrate as decomposition progressed.},
doi = {10.1111/1462-2920.14873},
journal = {Environmental Microbiology},
number = 3,
volume = 22,
place = {United States},
year = {2019},
month = {11}
}
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Works referenced in this record:
Vegetation classification by reference to strategies
journal, July 1974
- Grime, J. P.
- Nature, Vol. 250, Issue 5461
Manganese availability is negatively associated with carbon storage in northern coniferous forest humus layers
journal, November 2017
- Stendahl, Johan; Berg, Björn; Lindahl, Björn D.
- Scientific Reports, Vol. 7, Issue 1
Fungal community on decomposing leaf litter undergoes rapid successional changes
journal, October 2012
- Voříšková, Jana; Baldrian, Petr
- The ISME Journal, Vol. 7, Issue 3
Fungal Cellulases
journal, January 2015
- Payne, Christina M.; Knott, Brandon C.; Mayes, Heather B.
- Chemical Reviews, Vol. 115, Issue 3
A Theoretical Model of Litter Decay and Microbial Interaction
journal, May 2006
- Moorhead, Daryl L.; Sinsabaugh, Robert L.
- Ecological Monographs, Vol. 76, Issue 2
The Paleozoic Origin of Enzymatic Lignin Decomposition Reconstructed from 31 Fungal Genomes
journal, June 2012
- Floudas, Dimitrios; Binder, Manfred; Riley, Robert
- Science, Vol. 336, Issue 6089
Widespread Occurrence of Expressed Fungal Secretory Peroxidases in Forest Soils
journal, April 2014
- Kellner, Harald; Luis, Patricia; Pecyna, Marek J.
- PLoS ONE, Vol. 9, Issue 4
Nitrogen dynamics of decomposing Scots pine needle litter depends on colonizing fungal species
journal, April 2019
- Baskaran, Preetisri; Ekblad, Alf; Soucémarianadin, Laure N.
- FEMS Microbiology Ecology, Vol. 95, Issue 6
Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists
journal, February 2015
- Kohler, Annegret; Kuo, Alan; Nagy, Laszlo G.
- Nature Genetics, Vol. 47, Issue 4
Stimulation of Lignocellulosic Biomass Hydrolysis by Proteins of Glycoside Hydrolase Family 61 Structure and Function of a Large, Enigmatic Family
journal, April 2010
- Harris, Paul; Welner, Ditte; McFarland, K.
- Biochemistry, Vol. 49, Issue 15, p. 3305-3316
Covalent Cross-Links in the Cell Wall
journal, February 1994
- Iiyama, K.; Lam, Tbt.; Stone, B. A.
- Plant Physiology, Vol. 104, Issue 2
Comparative genomics and transcriptomics depict ericoid mycorrhizal fungi as versatile saprotrophs and plant mutualists
journal, January 2018
- Martino, Elena; Morin, Emmanuelle; Grelet, Gwen-Aëlle
- New Phytologist, Vol. 217, Issue 3
The carbohydrate-active enzymes database (CAZy) in 2013
journal, November 2013
- Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie
- Nucleic Acids Research, Vol. 42, Issue D1
Coupling Secretomics with Enzyme Activities To Compare the Temporal Processes of Wood Metabolism among White and Brown Rot Fungi
journal, June 2018
- Presley, Gerald N.; Panisko, Ellen; Purvine, Samuel O.
- Applied and Environmental Microbiology, Vol. 84, Issue 16
Untangling the fungal niche: the trait-based approach
journal, October 2014
- Crowther, Thomas W.; Maynard, Daniel S.; Crowther, Terence R.
- Frontiers in Microbiology, Vol. 5
Below-ground organic matter accumulation along a boreal forest fertility gradient relates to guild interaction within fungal communities
journal, October 2017
- Kyaschenko, Julia; Clemmensen, Karina E.; Karltun, Erik
- Ecology Letters, Vol. 20, Issue 12
Carbon-13 nuclear magnetic resonance of polymers spinning at the magic angle
journal, February 1976
- Schaefer, Jacob; Stejskal, E. O.
- Journal of the American Chemical Society, Vol. 98, Issue 4
Multi-omic Analyses of Extensively Decayed Pinus contorta Reveal Expression of a Diverse Array of Lignocellulose-Degrading Enzymes
journal, August 2018
- Hori, Chiaki; Gaskell, Jill; Cullen, Dan
- Applied and Environmental Microbiology, Vol. 84, Issue 20
The structure and synthesis of the fungal cell wall
journal, January 2006
- Bowman, Shaun M.; Free, Stephen J.
- BioEssays, Vol. 28, Issue 8
New species of Chalara occupying coniferous needles
journal, April 2011
- Koukol, Ondřej
- Fungal Diversity, Vol. 49, Issue 1
Substrate factors that influence the synergistic interaction of AA9 and cellulases during the enzymatic hydrolysis of biomass
journal, January 2014
- Hu, Jinguang; Arantes, Valdeir; Pribowo, Amadeus
- Energy Environ. Sci., Vol. 7, Issue 7
Prospects and challenges for fungal metatranscriptomics of complex communities
journal, April 2015
- Kuske, Cheryl R.; Hesse, Cedar N.; Challacombe, Jean F.
- Fungal Ecology, Vol. 14
Plant cell walls throughout evolution: towards a molecular understanding of their design principles
journal, August 2009
- Sarkar, P.; Bosneaga, E.; Auer, M.
- Journal of Experimental Botany, Vol. 60, Issue 13
Decomposing capacity of fungi commonly detected in Pinus sylvestris needle litter
journal, February 2011
- Boberg, Johanna B.; Ihrmark, Katarina; Lindahl, Björn D.
- Fungal Ecology, Vol. 4, Issue 1
Effects of Cellulose Crystallinity, Hemicellulose, and Lignin on the Enzymatic Hydrolysis of Miscanthus sinensis to Monosaccharides
journal, March 2008
- Yoshida, Makoto; Liu, Yuan; Uchida, Satoshi
- Bioscience, Biotechnology, and Biochemistry, Vol. 72, Issue 3
Litter chemistry influences decomposition through activity of specific microbial functional guilds
journal, May 2018
- Bhatnagar, Jennifer M.; Peay, Kabir G.; Treseder, Kathleen K.
- Ecological Monographs, Vol. 88, Issue 3
Functional guild classification predicts the enzymatic role of fungi in litter and soil biogeochemistry
journal, September 2015
- Talbot, Jennifer M.; Martin, Francis; Kohler, Annegret
- Soil Biology and Biochemistry, Vol. 88
Enhanced degradation of softwood versus hardwood by the white-rot fungus Pycnoporus coccineus
journal, December 2015
- Couturier, Marie; Navarro, David; Chevret, Didier
- Biotechnology for Biofuels, Vol. 8, Issue 1
Determining place and process: functional traits of ectomycorrhizal fungi that affect both community structure and ecosystem function
journal, October 2013
- Koide, Roger T.; Fernandez, Christopher; Malcolm, Glenna
- New Phytologist, Vol. 201, Issue 2
Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion
journal, February 2009
- Martinez, Diego; Challacombe, Jean; Morgenstern, Ingo
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 6
Transformation of Quercus petraea litter: successive changes in litter chemistry are reflected in differential enzyme activity and changes in the microbial community composition: Transformation of Quercus petraea litter
journal, November 2010
- Šnajdr, Jaroslav; Cajthaml, Tomáš; Valášková, Vendula
- FEMS Microbiology Ecology, Vol. 75, Issue 2
Changes in fungal communities along a boreal forest soil fertility gradient
journal, May 2015
- Sterkenburg, Erica; Bahr, Adam; Brandström Durling, Mikael
- New Phytologist, Vol. 207, Issue 4
Microbial genomics, transcriptomics and proteomics: new discoveries in decomposition research using complementary methods
journal, January 2014
- Baldrian, Petr; López-Mondéjar, Rubén
- Applied Microbiology and Biotechnology, Vol. 98, Issue 4
Fungal Traits That Drive Ecosystem Dynamics on Land
journal, May 2015
- Treseder, Kathleen K.; Lennon, Jay T.
- Microbiology and Molecular Biology Reviews, Vol. 79, Issue 2
The Plant Cell Wall-Decomposing Machinery Underlies the Functional Diversity of Forest Fungi
journal, July 2011
- Eastwood, D. C.; Floudas, D.; Binder, M.
- Science, Vol. 333, Issue 6043, p. 762-765
PeroxiBase: a database for large-scale evolutionary analysis of peroxidases
journal, November 2012
- Fawal, Nizar; Li, Qiang; Savelli, Bruno
- Nucleic Acids Research, Vol. 41, Issue D1
New and classic families of secreted fungal heme peroxidases
journal, May 2010
- Hofrichter, Martin; Ullrich, René; Pecyna, Marek J.
- Applied Microbiology and Biotechnology, Vol. 87, Issue 3
Quantification and monosaccharide composition of hemicelluloses from different plant functional types
journal, January 2010
- Schädel, Christina; Blöchl, Andreas; Richter, Andreas
- Plant Physiology and Biochemistry, Vol. 48, Issue 1
MycoCosm portal: gearing up for 1000 fungal genomes
journal, December 2013
- Grigoriev, Igor V.; Nikitin, Roman; Haridas, Sajeet
- Nucleic Acids Research, Vol. 42, Issue D1
Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi
journal, June 2014
- Riley, Robert; Salamov, Asaf A.; Brown, Daren W.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 27
Reviews and syntheses: Carbon use efficiency from organisms to ecosystems – definitions, theories, and empirical evidence
journal, January 2018
- Manzoni, Stefano; Čapek, Petr; Porada, Philipp
- Biogeosciences, Vol. 15, Issue 19
PCR Primers to Study the Diversity of Expressed Fungal Genes Encoding Lignocellulolytic Enzymes in Soils Using High-Throughput Sequencing
journal, December 2014
- Barbi, Florian; Bragalini, Claudia; Vallon, Laurent
- PLoS ONE, Vol. 9, Issue 12
Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes
journal, January 2013
- Levasseur, Anthony; Drula, Elodie; Lombard, Vincent
- Biotechnology for Biofuels, Vol. 6, Issue 1, Article No. 41
Comparative mitochondrial genome analysis reveals intron dynamics and gene rearrangements in two Trametes species
journal, January 2021
- Chen, Cheng; Li, Qiang; Fu, Rongtao
- Scientific Reports, Vol. 11, Issue 1
Fungal cellulases
journal, February 1992
- Wood, Thomas M.
- Biochemical Society Transactions, Vol. 20, Issue 1
Genome-scale model reconstruction of the methylotrophic yeast Ogataea polymorpha
text, January 2021
- Liebal, Ulf Winfried; Fabry, Brigida A.; Ravikrishnan, Aarthi
- RWTH Aachen University