Assessing fungal contributions to cellulose degradation in soil by using high-throughput stable isotope probing
Abstract
Soils represent one of the largest and most active pools of C in the biosphere, and soil respiration represents a major component of global C flux. Fungi are essential to soil carbon cycling due to their propensity for decomposing organic polymers such as cellulose. We performed high throughput sequencing enabled stable isotope probing (HTS-SIP) with 13C-cellulose to characterize the dynamics of fungi and bacteria during cellulose degradation in an agricultural soil. Here, a total of 1900 fungal taxa were observed and 190 of these assimilated 13C-cellulose during a 30-day incubation. A majority of 13C-labeled fungi belonged to Ascomycota, Basidiomycota, and Mucoromycota. However, most 13C-labeled fungi could not be annotated at the species (71%, n = 134), or genus (49%, n = 93) level. Mucoromycota were 13C-labeled early, and by day 3 the most abundant 13C-labeled organism belonged to Mortierella. In contrast, 13C-labeled Ascomycota increased in diversity through day 14 and their relative abundance comprised more than 40% of fungal ITS sequences by day 30. These results show that: i) the majority of fungal taxa that assimilated 13C from 13C-cellulose are uncultivated and poorly characterized, ii) the beta-diversity of 13C-labeled fungi changed significantly over time during cellulose degradation, iii) a relativelymore »
- Authors:
-
- Cornell Univ., Ithaca, NY (United States)
- Publication Date:
- Research Org.:
- Cornell Univ., Ithaca, NY (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
- OSTI Identifier:
- 1864319
- Grant/Contract Number:
- SC0016364; SC0004486; SC0010558
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Soil Biology and Biochemistry
- Additional Journal Information:
- Journal Volume: 130; Journal ID: ISSN 0038-0717
- Publisher:
- Elsevier
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Carbon cycling; Stable isotope probing; Fungi; Cellulose; Decomposition
Citation Formats
Koechli, Chantal, Campbell, Ashley N., Pepe-Ranney, Charles, and Buckley, Daniel H. Assessing fungal contributions to cellulose degradation in soil by using high-throughput stable isotope probing. United States: N. p., 2018.
Web. doi:10.1016/j.soilbio.2018.12.013.
Koechli, Chantal, Campbell, Ashley N., Pepe-Ranney, Charles, & Buckley, Daniel H. Assessing fungal contributions to cellulose degradation in soil by using high-throughput stable isotope probing. United States. https://doi.org/10.1016/j.soilbio.2018.12.013
Koechli, Chantal, Campbell, Ashley N., Pepe-Ranney, Charles, and Buckley, Daniel H. Mon .
"Assessing fungal contributions to cellulose degradation in soil by using high-throughput stable isotope probing". United States. https://doi.org/10.1016/j.soilbio.2018.12.013. https://www.osti.gov/servlets/purl/1864319.
@article{osti_1864319,
title = {Assessing fungal contributions to cellulose degradation in soil by using high-throughput stable isotope probing},
author = {Koechli, Chantal and Campbell, Ashley N. and Pepe-Ranney, Charles and Buckley, Daniel H.},
abstractNote = {Soils represent one of the largest and most active pools of C in the biosphere, and soil respiration represents a major component of global C flux. Fungi are essential to soil carbon cycling due to their propensity for decomposing organic polymers such as cellulose. We performed high throughput sequencing enabled stable isotope probing (HTS-SIP) with 13C-cellulose to characterize the dynamics of fungi and bacteria during cellulose degradation in an agricultural soil. Here, a total of 1900 fungal taxa were observed and 190 of these assimilated 13C-cellulose during a 30-day incubation. A majority of 13C-labeled fungi belonged to Ascomycota, Basidiomycota, and Mucoromycota. However, most 13C-labeled fungi could not be annotated at the species (71%, n = 134), or genus (49%, n = 93) level. Mucoromycota were 13C-labeled early, and by day 3 the most abundant 13C-labeled organism belonged to Mortierella. In contrast, 13C-labeled Ascomycota increased in diversity through day 14 and their relative abundance comprised more than 40% of fungal ITS sequences by day 30. These results show that: i) the majority of fungal taxa that assimilated 13C from 13C-cellulose are uncultivated and poorly characterized, ii) the beta-diversity of 13C-labeled fungi changed significantly over time during cellulose degradation, iii) a relatively small number of the 13C-labeled taxa dominated the community response to cellulose, and iv) fungi incorporated cellulose into DNA more rapidly and in greater numbers than did bacteria. Furthermore, these results show that fungi in a tilled agricultural field respond rapidly to new cellulose inputs, exhibiting complex temporal dynamics that likely drive carbon flow into diverse taxa within the soil community.},
doi = {10.1016/j.soilbio.2018.12.013},
journal = {Soil Biology and Biochemistry},
number = ,
volume = 130,
place = {United States},
year = {Mon Dec 17 00:00:00 EST 2018},
month = {Mon Dec 17 00:00:00 EST 2018}
}
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Works referenced in this record:
Microbial carbon recycling: an underestimated process controlling soil carbon dynamics – Part 2: A C3-C4 vegetation change field labelling experiment
journal, January 2015
- Basler, A.; Dippold, M.; Helfrich, M.
- Biogeosciences, Vol. 12, Issue 21
Linking molecular size, composition and carbon turnover of extractable soil microbial compounds
journal, September 2016
- Malik, Ashish A.; Roth, Vanessa-Nina; Hébert, Mathieu
- Soil Biology and Biochemistry, Vol. 100
Energetics of bacterial growth: balance of anabolic and catabolic reactions.
journal, January 1995
- Russell, J. B.; Cook, G. M.
- Microbiological reviews, Vol. 59, Issue 1
Carbon flow into microbial and fungal biomass as a basis for the belowground food web of agroecosystems
journal, March 2012
- Kramer, Susanne; Marhan, Sven; Ruess, Liliane
- Pedobiologia, Vol. 55, Issue 2
Sequencing and functional analysis of the genome of a nematode egg-parasitic fungus, Pochonia chlamydosporia
journal, April 2014
- Larriba, Eduardo; Jaime, María D. L. A.; Carbonell-Caballero, José
- Fungal Genetics and Biology, Vol. 65
Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review
journal, October 2008
- Blagodatskaya, Е.; Kuzyakov, Y.
- Biology and Fertility of Soils, Vol. 45, Issue 2
Bacterial and Fungal Contributions to Carbon Sequestration in Agroecosystems
journal, January 2006
- Six, J.; Frey, S. D.; Thiet, R. K.
- Soil Science Society of America Journal, Vol. 70, Issue 2
An Ordination of the Upland Forest Communities of Southern Wisconsin
journal, February 1957
- Bray, J. Roger; Curtis, J. T.
- Ecological Monographs, Vol. 27, Issue 4
Soil carbon and nitrogen mineralization: Theory and models across scales
journal, July 2009
- Manzoni, Stefano; Porporato, Amilcare
- Soil Biology and Biochemistry, Vol. 41, Issue 7
Development of a Dual-Index Sequencing Strategy and Curation Pipeline for Analyzing Amplicon Sequence Data on the MiSeq Illumina Sequencing Platform
journal, June 2013
- Kozich, James J.; Westcott, Sarah L.; Baxter, Nielson T.
- Applied and Environmental Microbiology, Vol. 79, Issue 17
Differential expression analysis for sequence count data
journal, October 2010
- Anders, Simon; Huber, Wolfgang
- Genome Biology, Vol. 11, Issue 10
Agricultural Management and Labile Carbon Additions Affect Soil Microbial Community Structure and Interact with Carbon and Nitrogen Cycling
journal, April 2013
- Berthrong, Sean T.; Buckley, Daniel H.; Drinkwater, Laurie E.
- Microbial Ecology, Vol. 66, Issue 1
Waste Not, Want Not: Why Rarefying Microbiome Data Is Inadmissible
journal, April 2014
- McMurdie, Paul J.; Holmes, Susan
- PLoS Computational Biology, Vol. 10, Issue 4
Carbon transfer from maize roots and litter into bacteria and fungi depends on soil depth and time
journal, February 2016
- Müller, Karolin; Kramer, Susanne; Haslwimmer, Heike
- Soil Biology and Biochemistry, Vol. 93
Meeting Report: Fungal ITS Workshop (October 2012)
journal, April 2013
- Bates, Scott T.; Ahrendt, Steven; Bik, Holly M.
- Standards in Genomic Sciences, Vol. 8, Issue 1
Rapid Method for Coextraction of DNA and RNA from Natural Environments for Analysis of Ribosomal DNA- and rRNA-Based Microbial Community Composition
journal, December 2000
- Griffiths, R. I.; Whiteley, A. S.; O'Donnell, A. G.
- Applied and Environmental Microbiology, Vol. 66, Issue 12
The use of stable isotope probing techniques in bioreactor and field studies on bioremediation
journal, February 2006
- Madsen, Eugene L.
- Current Opinion in Biotechnology, Vol. 17, Issue 1
Molecular Biology of Cellulose Degradation
journal, October 1990
- Beguin, Pierre
- Annual Review of Microbiology, Vol. 44, Issue 1
HTSSIP: An R package for analysis of high throughput sequencing data from nucleic acid stable isotope probing (SIP) experiments
journal, January 2018
- Youngblut, Nicholas D.; Barnett, Samuel E.; Buckley, Daniel H.
- PLOS ONE, Vol. 13, Issue 1
Biochemistry of hexose and pentose transformations in soil analyzed by position-specific labeling and 13C-PLFA
journal, January 2015
- Apostel, Carolin; Dippold, Michaela; Kuzyakov, Yakov
- Soil Biology and Biochemistry, Vol. 80
Dynamics and identification of soil microbial populations actively assimilating carbon from 13 C-labelled wheat residue as estimated by DNA- and RNA-SIP techniques
journal, March 2007
- Bernard, Laetitia; Mougel, Christophe; Maron, Pierre-Alain
- Environmental Microbiology, Vol. 9, Issue 3
SIPSim: A Modeling Toolkit to Predict Accuracy and Aid Design of DNA-SIP Experiments
journal, March 2018
- Youngblut, Nicholas D.; Barnett, Samuel E.; Buckley, Daniel H.
- Frontiers in Microbiology, Vol. 9
Arthrobotrys oligospora : a model organism for understanding the interaction between fungi and nematodes
journal, March 2011
- Niu, Xue-Mei; Zhang, Ke-Qin
- Mycology, Vol. 2, Issue 2
A first comprehensive census of fungi in soil reveals both hyperdiversity and fine-scale niche partitioning
journal, February 2014
- Taylor, D. Lee; Hollingsworth, Teresa N.; McFarland, Jack W.
- Ecological Monographs, Vol. 84, Issue 1
The biological degradation of cellulose
journal, January 1994
- Beguin, Pierre; Aubert, Jean-Paul
- FEMS Microbiology Reviews, Vol. 13, Issue 1, p. 25-58
Bacterial populations assimilating carbon from 13C-labeled plant residue in soil: Analysis by a DNA-SIP approach
journal, April 2011
- Lee, Chol Gyu; Watanabe, Takeshi; Sato, Yutaka
- Soil Biology and Biochemistry, Vol. 43, Issue 4
Development of a new management strategy for the control of root-knot nematodes (Meloidogyne spp) in organic vegetable production
journal, January 2003
- Atkins, Simon D.; Hidalgo-Diaz, Leopoldo; Kalisz, Helen
- Pest Management Science, Vol. 59, Issue 2
Size and functional diversity of microbe populations control plant persistence and long-term soil carbon accumulation: Modelling long-term SOM dynamics
journal, August 2005
- Fontaine, Sébastien; Barot, Sébastien
- Ecology Letters, Vol. 8, Issue 10
Search and clustering orders of magnitude faster than BLAST
journal, August 2010
- Edgar, Robert C.
- Bioinformatics, Vol. 26, Issue 19, p. 2460-2461
An overview of the systematics of the Sordariomycetes based on a four-gene phylogeny
journal, November 2006
- Zhang, Ning; Castlebury, Lisa A.; Miller, Andrew N.
- Mycologia, Vol. 98, Issue 6
Cellulose-decomposing fungi in polder soils and their possible influence on pathogenic fungi
journal, September 1969
- Pugh, G. J. F.; Emden, J. H.
- Netherlands Journal of Plant Pathology, Vol. 75, Issue 5
Living in a fungal world: impact of fungi on soil bacterial niche development
journal, September 2005
- Boer, Wietse de; Folman, Larissa B.; Summerbell, Richard C.
- FEMS Microbiology Reviews, Vol. 29, Issue 4
Microbial utilization and mineralization of [14C]glucose added in six orders of concentration to soil
journal, August 2008
- Schneckenberger, Katja; Demin, Dmitry; Stahr, Karl
- Soil Biology and Biochemistry, Vol. 40, Issue 8
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data
journal, April 2013
- McMurdie, Paul J.; Holmes, Susan
- PLoS ONE, Vol. 8, Issue 4
Applications and impacts of stable isotope probing for analysis of microbial interactions
journal, April 2014
- Abraham, Wolf-Rainer
- Applied Microbiology and Biotechnology, Vol. 98, Issue 11
UPARSE: highly accurate OTU sequences from microbial amplicon reads
journal, August 2013
- Edgar, Robert C.
- Nature Methods, Vol. 10, Issue 10
Towards a unified paradigm for sequence-based identification of fungi
journal, September 2013
- Kõljalg, Urmas; Nilsson, R. Henrik; Abarenkov, Kessy
- Molecular Ecology, Vol. 22, Issue 21
Spore Density Determines Infection Strategy by the Plant Pathogenic Fungus Plectosphaerella cucumerina
journal, February 2016
- Pétriacq, Pierre; Stassen, Joost H. M.; Ton, Jurriaan
- Plant Physiology, Vol. 170, Issue 4
Molecular phylogeny of Acremonium and its taxonomic implications
journal, May 1996
- Glenn, Anthony E.; Bacon, Charles W.; Price, Robert
- Mycologia, Vol. 88, Issue 3
Soil organic matter dynamics: a biological perspective derived from the use of compound-specific isotopes studies
journal, February 2013
- Gleixner, Gerd
- Ecological Research, Vol. 28, Issue 5
Cellulose utilization in forest litter and soil: identification of bacterial and fungal decomposers
journal, March 2012
- Štursová, Martina; Žifčáková, Lucia; Leigh, Mary Beth
- FEMS Microbiology Ecology, Vol. 80, Issue 3
Studies on Morphological forms of Staphylotrichum Coccosporum
journal, March 1963
- Maciejowska, Zofia; Williams, E. B.
- Mycologia, Vol. 55, Issue 2
Global diversity and geography of soil fungi
journal, November 2014
- Tedersoo, Leho; Bahram, Mohammad; Põlme, Sergei
- Science, Vol. 346, Issue 6213
Microbial diversity of cellulose hydrolysis
journal, June 2011
- Wilson, David B.
- Current Opinion in Microbiology, Vol. 14, Issue 3
Stable isotope probing — linking microbial identity to function
journal, May 2005
- Dumont, Marc G.; Murrell, J. Colin
- Nature Reviews Microbiology, Vol. 3, Issue 6
Independent filtering increases detection power for high-throughput experiments
journal, May 2010
- Bourgon, R.; Gentleman, R.; Huber, W.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 21
Resource Partitioning between Bacteria, Fungi, and Protists in the Detritusphere of an Agricultural Soil
journal, September 2016
- Kramer, Susanne; Dibbern, Dörte; Moll, Julia
- Frontiers in Microbiology, Vol. 7
The Status of YATP and Maintenance Energy as Biologically Interpretable Phenomena
journal, October 1984
- Tempest, D. W.; Neijssel, O. M.
- Annual Review of Microbiology, Vol. 38, Issue 1
Influence of repeated prescribed burning on incorporation of 13C from cellulose by forest soil fungi as determined by RNA stable isotope probing
journal, March 2009
- Bastias, Brigitte A.; Anderson, Ian C.; Rangel-Castro, J. Ignacio
- Soil Biology and Biochemistry, Vol. 41, Issue 3
Microbial communities and their relevance for ecosystem models: Decomposition as a case study
journal, April 2010
- McGuire, Krista L.; Treseder, Kathleen K.
- Soil Biology and Biochemistry, Vol. 42, Issue 4
Protozoa and plant growth: the microbial loop in soil revisited
journal, June 2004
- Bonkowski, Michael
- New Phytologist, Vol. 162, Issue 3
QIIME allows analysis of high-throughput community sequencing data
journal, April 2010
- Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse
- Nature Methods, Vol. 7, Issue 5
PEAR: a fast and accurate Illumina Paired-End reAd mergeR
journal, October 2013
- Zhang, J.; Kobert, K.; Flouri, T.
- Bioinformatics, Vol. 30, Issue 5
Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi
journal, March 2012
- Schoch, C. L.; Seifert, K. A.; Huhndorf, S.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 16
Metabolic responses of novel cellulolytic and saccharolytic agricultural soil Bacteria to oxygen: Metabolic response of soil cellulose degraders
journal, December 2009
- Schellenberger, Stefanie; Kolb, Steffen; Drake, Harold L.
- Environmental Microbiology, Vol. 12, Issue 4
RNA Stable Isotope Probing, a Novel Means of Linking Microbial Community Function to Phylogeny
journal, November 2002
- Manefield, M.; Whiteley, A. S.; Griffiths, R. I.
- Applied and Environmental Microbiology, Vol. 68, Issue 11
Labile and recalcitrant plant fractions are utilised by distinct microbial communities in soil: Independent of the presence of roots and mycorrhizal fungi
journal, May 2008
- Paterson, Eric; Osler, Graham; Dawson, Lorna A.
- Soil Biology and Biochemistry, Vol. 40, Issue 5
Identification of Cellulose-Responsive Bacterial and Fungal Communities in Geographically and Edaphically Different Soils by Using Stable Isotope Probing
journal, January 2012
- Eichorst, Stephanie A.; Kuske, Cheryl R.
- Applied and Environmental Microbiology, Vol. 78, Issue 7
Taxonomic Reliability of DNA Sequences in Public Sequence Databases: A Fungal Perspective
journal, December 2006
- Nilsson, R. Henrik; Ryberg, Martin; Kristiansson, Erik
- PLoS ONE, Vol. 1, Issue 1
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing
journal, January 1995
- Benjamini, Yoav; Hochberg, Yosef
- Journal of the Royal Statistical Society: Series B (Methodological), Vol. 57, Issue 1
Carbon use efficiency of microbial communities: stoichiometry, methodology and modelling
journal, April 2013
- Sinsabaugh, Robert L.; Manzoni, Stefano; Moorhead, Daryl L.
- Ecology Letters, Vol. 16, Issue 7
The microbial loop concept as used in terrestrial soil ecology studies
journal, September 1994
- Coleman, D. C.
- Microbial Ecology, Vol. 28, Issue 2
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
Use of Field-Based Stable Isotope Probing To Identify Adapted Populations and Track Carbon Flow through a Phenol-Degrading Soil Microbial Community
journal, December 2005
- DeRito, C. M.; Pumphrey, G. M.; Madsen, E. L.
- Applied and Environmental Microbiology, Vol. 71, Issue 12
Global patterns in belowground communities
journal, November 2009
- Fierer, Noah; Strickland, Michael S.; Liptzin, Daniel
- Ecology Letters, Vol. 12, Issue 11
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Ontogenic succession of thermokarst thaw ponds is linked to dissolved organic matter quality and microbial degradation potential
journal, January 2020
- Peura, Sari; Wauthy, Maxime; Simone, Domenico
- Limnology and Oceanography, Vol. 65, Issue S1