Microbial community composition controls carbon flux across litter types in early phase of litter decomposition

Kroeger, Marie Elizabeth; DeVan, Megan Rae; Thompson, Jaron; Johansen, Renee; Gallegos-Graves, Laverne A.; Lopez, Deanna Lynn; Runde, Andreas; Yoshida, Thomas M.; Munsky, Brian; Sevanto, Sanna Annika; Albright, Michaeline Burr Nelson; Dunbar, John Martin

doi:10.1111/1462-2920.15705

Microbial community composition controls carbon flux across litter types in early phase of litter decomposition

Journal Article · Sat Aug 14 00:00:00 EDT 2021 · Environmental Microbiology

DOI:https://doi.org/10.1111/1462-2920.15705· OSTI ID:1826519

^[1]; DeVan, Megan Rae ^[1]; Thompson, Jaron ^[2]; Johansen, Renee ^[3]; Gallegos-Graves, Laverne A. ^[1]; Lopez, Deanna Lynn ^[1]; Runde, Andreas ^[1]; ^[1]; Munsky, Brian ^[2]; ^[1]; ^[1]; ^[1]

Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Colorado State Univ., Fort Collins, CO (United States)
Los Alamos National Lab. (LANL), Los Alamos, NM (United States); Landcare Research, Auckland (New Zealand)

Leaf litter decomposition is a major carbon input to soil, making it a target for increasing soil carbon storage through microbiome engineering. We expand upon previous findings to show with multiple leaf litter types that microbial composition can drive variation in carbon flow from litter decomposition and specific microbial community features are associated with synonymous patterns of carbon flow among litter types. Although plant litter type selects for different decomposer communities, within a litter type, microbial composition drives variation in the quantity of dissolved organic carbon (DOC) measured at the end of the decomposition period. Bacterial richness was negatively correlated with DOC quantity, supporting our hypothesis that across multiple litter types there are common microbial traits linked to carbon flow patterns. Variation in DOC abundance (i.e. high versus low DOC) driven by microbial composition is tentatively due to differences in bacterial metabolism of labile compounds, rather than catabolism of non-labile substrates such as lignin. The temporal asynchrony of metabolic processes across litter types may be a substantial impediment to discovering more microbial features common to synonymous patterns of carbon flow among litters. Overall, our findings support the concept that carbon flow may be programmed by manipulating microbial community composition.

View Accepted Manuscript (DOE)

Research Organization:: Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: USDOE Office of Science (SC). Biological and Environmental Research (BER)

Grant/Contract Number:: 89233218CNA000001

OSTI ID:: 1826519

Report Number(s):: LA-UR--21-24294

Journal Information:: Environmental Microbiology, Journal Name: Environmental Microbiology Journal Issue: 11 Vol. 23; ISSN 1462-2912

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (74)

ggplot2 Wickham, Hadley Use R! https://doi.org/10.1007/978-3-319-24277-4	book	January 2016
Soil carbon mineralisation responses to alterations of microbial diversity and soil structure Juarez, Sabrina; Nunan, Naoise; Duday, Anne-Claire Biology and Fertility of Soils, Vol. 49, Issue 7 https://doi.org/10.1007/s00374-013-0784-8	journal	March 2013
Litter quality versus soil microbial community controls over decomposition: a quantitative analysis Cleveland, Cory C.; Reed, Sasha C.; Keller, Adrienne B. Oecologia, Vol. 174, Issue 1 https://doi.org/10.1007/s00442-013-2758-9	journal	September 2013
Composition, Dynamics, and Fate of Leached Dissolved Organic Matter in Terrestrial Ecosystems: Results from a Decomposition Experiment Cleveland, Cory C.; Neff, Jason C.; Townsend, Alan R. Ecosystems, Vol. 7, Issue 3 https://doi.org/10.1007/s10021-003-0236-7	journal	April 2004
Control of climate and litter quality on leaf litter decomposition in different climatic zones Zhang, Xinyue; Wang, Wei Journal of Plant Research, Vol. 128, Issue 5 https://doi.org/10.1007/s10265-015-0743-6	journal	July 2015
Soil C and N models that integrate microbial diversity Louis, Benjamin P.; Maron, Pierre-Alain; Viaud, Valérie Environmental Chemistry Letters, Vol. 14, Issue 3 https://doi.org/10.1007/s10311-016-0571-5	journal	July 2016
Rothia marina sp. nov., isolated from an intertidal sediment of the South China Sea Liu, Zhu-Xiang; Yang, Ling-Ling; Huang, Ying Antonie van Leeuwenhoek, Vol. 104, Issue 3 https://doi.org/10.1007/s10482-013-9955-8	journal	June 2013
Litter decomposition: what controls it and how can we alter it to sequester more carbon in forest soils? Prescott, Cindy E. Biogeochemistry, Vol. 101, Issue 1-3 https://doi.org/10.1007/s10533-010-9439-0	journal	April 2010
Deep soil organic matter—a key but poorly understood component of terrestrial C cycle Rumpel, Cornelia; Kögel-Knabner, Ingrid Plant and Soil, Vol. 338, Issue 1-2 https://doi.org/10.1007/s11104-010-0391-5	journal	May 2010
Plant species effect on the decomposition and chemical changes of leaf litter in grassland and pine and oak forest soils Osono, Takashi; Azuma, Jun-ichi; Hirose, Dai Plant and Soil, Vol. 376, Issue 1-2 https://doi.org/10.1007/s11104-013-1993-5	journal	December 2013
Automated analysis for nitrate by hydrazine reduction Kamphake, L. J.; Hannah, S. A.; Cohen, J. M. Water Research, Vol. 1, Issue 3 https://doi.org/10.1016/0043-1354(67)90011-5	journal	March 1967
Molecular C dynamics downstream: The biochemical decomposition sequence and its impact on soil organic matter structure and function Grandy, A. Stuart; Neff, Jason C. Science of The Total Environment, Vol. 404, Issue 2-3 https://doi.org/10.1016/j.scitotenv.2007.11.013	journal	October 2008
Amounts and degradability of dissolved organic carbon from foliar litter at different decomposition stages Don, A.; Kalbitz, K. Soil Biology and Biochemistry, Vol. 37, Issue 12 https://doi.org/10.1016/j.soilbio.2005.03.019	journal	December 2005
Chemical composition of young and old carbon pools throughout Cambisol and Luvisol profiles under forests Schöning, Ingo; Kögel-Knabner, Ingrid Soil Biology and Biochemistry, Vol. 38, Issue 8 https://doi.org/10.1016/j.soilbio.2006.03.005	journal	August 2006
Temporal dynamics of microbial communities on decomposing leaf litter of 10 plant species in relation to decomposition rate Bray, Sarah R.; Kitajima, Kaoru; Mack, Michelle C. Soil Biology and Biochemistry, Vol. 49 https://doi.org/10.1016/j.soilbio.2012.02.009	journal	June 2012
Cycling downwards – dissolved organic matter in soils Kaiser, Klaus; Kalbitz, Karsten Soil Biology and Biochemistry, Vol. 52 https://doi.org/10.1016/j.soilbio.2012.04.002	journal	September 2012
Distributions of fungal melanin across species and soils Siletti, Cheta E.; Zeiner, Carolyn A.; Bhatnagar, Jennifer M. Soil Biology and Biochemistry, Vol. 113 https://doi.org/10.1016/j.soilbio.2017.05.030	journal	October 2017
Examining the global distribution of dominant archaeal populations in soil Bates, Scott T.; Berg-Lyons, Donna; Caporaso, J. Gregory The ISME Journal, Vol. 5, Issue 5 https://doi.org/10.1038/ismej.2010.171	journal	November 2010
Who is who in litter decomposition? Metaproteomics reveals major microbial players and their biogeochemical functions Schneider, Thomas; Keiblinger, Katharina M.; Schmid, Emanuel The ISME Journal, Vol. 6, Issue 9 https://doi.org/10.1038/ismej.2012.11	journal	March 2012
Persistence of soil organic matter as an ecosystem property Schmidt, Michael W. I.; Torn, Margaret S.; Abiven, Samuel Nature, Vol. 478, Issue 7367 https://doi.org/10.1038/nature10386	journal	October 2011
Climate fails to predict wood decomposition at regional scales Bradford, Mark A.; Warren II, Robert J.; Baldrian, Petr Nature Climate Change, Vol. 4, Issue 7 https://doi.org/10.1038/nclimate2251	journal	June 2014
Formation of soil organic matter via biochemical and physical pathways of litter mass loss Cotrufo, M. Francesca; Soong, Jennifer L.; Horton, Andrew J. Nature Geoscience, Vol. 8, Issue 10 https://doi.org/10.1038/ngeo2520	journal	September 2015
UPARSE: highly accurate OTU sequences from microbial amplicon reads Edgar, Robert C. Nature Methods, Vol. 10, Issue 10 https://doi.org/10.1038/nmeth.2604	journal	August 2013
Sequencing and beyond: integrating molecular 'omics' for microbial community profiling Franzosa, Eric A.; Hsu, Tiffany; Sirota-Madi, Alexandra Nature Reviews Microbiology, Vol. 13, Issue 6 https://doi.org/10.1038/nrmicro3451	journal	April 2015
Decomposer food web in a deciduous forest shows high share of generalist microorganisms and importance of microbial biomass recycling López-Mondéjar, Ruben; Brabcová, Vendula; Štursová, Martina The ISME Journal, Vol. 12, Issue 7 https://doi.org/10.1038/s41396-018-0084-2	journal	February 2018
Defining trait-based microbial strategies with consequences for soil carbon cycling under climate change Malik, Ashish A.; Martiny, Jennifer B. H.; Brodie, Eoin L. The ISME Journal, Vol. 14, Issue 1 https://doi.org/10.1038/s41396-019-0510-0	journal	September 2019
Developing a molecular picture of soil organic matter–mineral interactions by quantifying organo–mineral binding Newcomb, C. J.; Qafoku, N. P.; Grate, J. W. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-00407-9	journal	August 2017
Microbial carbon use efficiency predicted from genome-scale metabolic models Saifuddin, Mustafa; Bhatnagar, Jennifer M.; Segrè, Daniel Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-11488-z	journal	August 2019
Fungal-bacterial diversity and microbiome complexity predict ecosystem functioning Wagg, Cameron; Schlaeppi, Klaus; Banerjee, Samiran Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-12798-y	journal	October 2019
A test of the hierarchical model of litter decomposition Bradford, Mark A.; Veen, G. F.; Bonis, Anne Nature Ecology & Evolution, Vol. 1, Issue 12 https://doi.org/10.1038/s41559-017-0367-4	journal	November 2017
Spatial Heterogeneity of SOM Concentrations Associated with White-rot Versus Brown-rot Wood Decay Bai, Zhen; Ma, Qiang; Dai, Yucheng Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-14181-7	journal	October 2017
Modification of the NH ₄ HCO ₃ ‐DTPA soil test to omit carbon black Soltanpour, P. N.; Workman, S. Communications in Soil Science and Plant Analysis, Vol. 10, Issue 11 https://doi.org/10.1080/00103627909366996	journal	January 1979
Lignin and its effects on litter decomposition in forest ecosystems Rahman, Mohammed Mahabubur; Tsukamoto, Jiro; Rahman, Md. Motiur Chemistry and Ecology, Vol. 29, Issue 6 https://doi.org/10.1080/02757540.2013.790380	journal	August 2013
Differences in substrate use linked to divergent carbon flow during litter decomposition Albright, Michaeline B. N.; Thompson, Jaron; Kroeger, Marie E. FEMS Microbiology Ecology, Vol. 96, Issue 8 https://doi.org/10.1093/femsec/fiaa135	journal	July 2020
Lignin degradation: microorganisms, enzymes involved, genomes analysis and evolution Janusz, Grzegorz; Pawlik, Anna; Sulej, Justyna FEMS Microbiology Reviews, Vol. 41, Issue 6 https://doi.org/10.1093/femsre/fux049	journal	October 2017
KEGG as a reference resource for gene and protein annotation Kanehisa, Minoru; Sato, Yoko; Kawashima, Masayuki Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1070	journal	October 2015
Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation O'Leary, Nuala A.; Wright, Mathew W.; Brister, J. Rodney Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1189	journal	November 2015
An Examination of the Degtjareff Method for Determining soil Organic Matter, and a Proposed Modification of the Chromic acid Titration Method Walkley, A.; Black, I. Armstrong Soil Science, Vol. 37, Issue 1 https://doi.org/10.1097/00010694-193401000-00003	journal	January 1934
A Critical Examination of a Rapid Method for Determining Organic Carbon in Soils—Effect of Variations in Digestion Conditions and of Inorganic soil Constituents Walkley, Allan Soil Science, Vol. 63, Issue 4 https://doi.org/10.1097/00010694-194704000-00001	journal	January 1947
Phylogenetic and phenotypic evidence for the transfer of Eubacterium aerofaciens to the genus Collinsella as Collinsella aerofaciens gen. nov., comb. nov. Kageyama, A.; Benno, Y.; Nakase, T. International Journal of Systematic Bacteriology, Vol. 49, Issue 2 https://doi.org/10.1099/00207713-49-2-557	journal	April 1999
Understanding the dominant controls on litter decomposition Bradford, Mark A.; Berg, Björn; Maynard, Daniel S. Journal of Ecology, Vol. 104, Issue 1 https://doi.org/10.1111/1365-2745.12507	journal	November 2015
Differences in fungal and bacterial physiology alter soil carbon and nitrogen cycling: insights from meta-analysis and theoretical models Waring, Bonnie G.; Averill, Colin; Hawkes, Christine V. Ecology Letters, Vol. 16, Issue 7 https://doi.org/10.1111/ele.12125	journal	May 2013
Soil biodiversity and carbon cycling: a review and synthesis of studies examining diversity-function relationships Nielsen, U. N.; Ayres, E.; Wall, D. H. European Journal of Soil Science, Vol. 62, Issue 1 https://doi.org/10.1111/j.1365-2389.2010.01314.x	journal	November 2010
Multiple mechanisms for trait effects on litter decomposition: moving beyond home-field advantage with a new hypothesis Freschet, Grégoire T.; Aerts, Rien; Cornelissen, Johannes H. C. Journal of Ecology, Vol. 100, Issue 3 https://doi.org/10.1111/j.1365-2745.2011.01943.x	journal	January 2012
The origin of litter chemical complexity during decomposition Wickings, Kyle; Grandy, A. Stuart; Reed, Sasha C. Ecology Letters, Vol. 15, Issue 10 https://doi.org/10.1111/j.1461-0248.2012.01837.x	journal	August 2012
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 Šnajdr, Jaroslav; Cajthaml, Tomáš; Valášková, Vendula FEMS Microbiology Ecology, Vol. 75, Issue 2 https://doi.org/10.1111/j.1574-6941.2010.00999.x	journal	November 2010
The composition, localization and function of low-temperature-adapted microbial communities involved in methanogenic degradations of cellulose and chitin from Qinghai-Tibetan Plateau wetland soils Dai, Y.; Yan, Z.; Jia, L. Journal of Applied Microbiology, Vol. 121, Issue 1 https://doi.org/10.1111/jam.13164	journal	June 2016
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy Wang, Q.; Garrity, G. M.; Tiedje, J. M. Applied and Environmental Microbiology, Vol. 73, Issue 16 https://doi.org/10.1128/AEM.00062-07	journal	June 2007
Succession of Microbial Decomposers Is Determined by Litter Type, but Site Conditions Drive Decomposition Rates Buresova, A.; Kopecky, J.; Hrdinkova, V. Applied and Environmental Microbiology, Vol. 85, Issue 24 https://doi.org/10.1128/AEM.01760-19	journal	December 2019
High Microbial Diversity Promotes Soil Ecosystem Functioning Maron, Pierre-Alain; Sarr, Amadou; Kaisermann, Aurore Applied and Environmental Microbiology, Vol. 84, Issue 9 https://doi.org/10.1128/AEM.02738-17	journal	February 2018
Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Vilgalys, R.; Hester, M. Journal of Bacteriology, Vol. 172, Issue 8 https://doi.org/10.1128/JB.172.8.4238-4246.1990	journal	August 1990
Rothia Bacteremia: a 10-Year Experience at Mayo Clinic, Rochester, Minnesota Ramanan, Poornima; Barreto, Jason N.; Osmon, Douglas R. Journal of Clinical Microbiology, Vol. 52, Issue 9 https://doi.org/10.1128/JCM.01270-14	journal	June 2014
Oxidoreductases and Reactive Oxygen Species in Conversion of Lignocellulosic Biomass Bissaro, Bastien; Várnai, Anikó; Røhr, Åsmund K. Microbiology and Molecular Biology Reviews, Vol. 82, Issue 4 https://doi.org/10.1128/MMBR.00029-18	journal	September 2018
Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Vilgalys, R.; Hester, M. Journal of Bacteriology, Vol. 172, Issue 8 https://doi.org/10.1128/jb.172.8.4238-4246.1990	journal	August 1990
Substrate control of litter decomposition in four Rocky Mountain coniferous forests Taylor, B. R.; Prescott, C. E.; Parsons, W. J. F. Canadian Journal of Botany, Vol. 69, Issue 10 https://doi.org/10.1139/b91-281	journal	October 1991
The metagenomics RAST server – a public resource for the automatic phylogenetic and functional analysis of metagenomes Meyer, F.; Paarmann, D.; D'Souza, M. BMC Bioinformatics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2105-9-386	journal	September 2008
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Love, Michael I.; Huber, Wolfgang; Anders, Simon Genome Biology, Vol. 15, Issue 12 https://doi.org/10.1186/s13059-014-0550-8	journal	December 2014
Effects of Plant Litter Type and Additions of Nitrogen and Phosphorus on Bacterial Community-Level Physiological Profiles in a Brown Forest Soil Kunito, Takashi; Nagaoka, Kazunari Microbes and Environments, Vol. 24, Issue 1 https://doi.org/10.1264/jsme2.ME08546	journal	January 2009
Microbiome Profiling by Illumina Sequencing of Combinatorial Sequence-Tagged PCR Products Gloor, Gregory B.; Hummelen, Ruben; Macklaim, Jean M. PLoS ONE, Vol. 5, Issue 10 https://doi.org/10.1371/journal.pone.0015406	journal	October 2010
Machine learning to predict microbial community functions: An analysis of dissolved organic carbon from litter decomposition Thompson, Jaron; Johansen, Renee; Dunbar, John PLOS ONE, Vol. 14, Issue 7 https://doi.org/10.1371/journal.pone.0215502	journal	July 2019
Testing the functional significance of microbial community composition Strickland, Michael S.; Lauber, Christian; Fierer, Noah Ecology, Vol. 90, Issue 2 https://doi.org/10.1890/08-0296.1	journal	February 2009
Climate, Leaf Litter Chemistry and Leaf Litter Decomposition in Terrestrial Ecosystems: A Triangular Relationship Aerts, Rien Oikos, Vol. 79, Issue 3 https://doi.org/10.2307/3546886	journal	September 1997
Statsmodels: Econometric and Statistical Modeling with Python Seabold, Skipper; Perktold, Josef Proceedings of the Python in Science Conference https://doi.org/10.25080/Majora-92bf1922-011	conference	January 2010
Soil C Sequestration as a Biological Negative Emission Strategy Paustian, Keith; Larson, Eric; Kent, Jeffrey Frontiers in Climate, Vol. 1 https://doi.org/10.3389/fclim.2019.00008	journal	October 2019
Trait-based approaches for understanding microbial biodiversity and ecosystem functioning Krause, Sascha; Le Roux, Xavier; Niklaus, Pascal A. Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00251	journal	May 2014
Forest floor community metatranscriptomes identify fungal and bacterial responses to N deposition in two maple forests Hesse, Cedar N.; Mueller, Rebecca C.; Vuyisich, Momchilo Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00337	journal	April 2015
Soil bacterial and fungal community responses to nitrogen addition across soil depth and microhabitat in an arid shrubland Mueller, Rebecca C.; Belnap, Jayne; Kuske, Cheryl R. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00891	journal	September 2015
Microbes as Engines of Ecosystem Function: When Does Community Structure Enhance Predictions of Ecosystem Processes? Graham, Emily B.; Knelman, Joseph E.; Schindlbacher, Andreas Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00214	journal	February 2016
Soil Fungal:Bacterial Ratios Are Linked to Altered Carbon Cycling Malik, Ashish A.; Chowdhury, Somak; Schlager, Veronika Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01247	journal	August 2016
Land Use and Seasonal Effects on the Soil Microbiome of a Brazilian Dry Forest Lacerda-Júnior, Gileno V.; Noronha, Melline F.; Cabral, Lucélia Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00648	journal	April 2019
Managing Agroecosystems for Soil Microbial Carbon Use Efficiency: Ecological Unknowns, Potential Outcomes, and a Path Forward Kallenbach, Cynthia M.; Wallenstein, Matthew D.; Schipanksi, Meagan E. Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01146	journal	May 2019
Soil Bacterial and Fungal Richness Forecast Patterns of Early Pine Litter Decomposition Albright, Michaeline B. N.; Johansen, Renee; Thompson, Jaron Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.542220	journal	November 2020
Representing life in the Earth system with soil microbial functional traits in the MIMICS model Wieder, W. R.; Grandy, A. S.; Kallenbach, C. M. Geoscientific Model Development, Vol. 8, Issue 6 https://doi.org/10.5194/gmd-8-1789-2015	journal	January 2015
Degradation of Sawdust by Thermo Tolerant Microorganisms for Bio Fertilizer Synthesis Asadu, Christian; Aneke, Nebechukwu; Agulanna, Albert Asian Journal of Biotechnology and Bioresource Technology, Vol. 2, Issue 3 https://doi.org/10.9734/AJB2T/2017/38659	journal	January 2018

Similar Records

Differences in substrate use linked to divergent carbon flow during litter decomposition

Journal Article · Sun Jul 05 20:00:00 EDT 2020 · FEMS Microbiology Ecology (Online) · OSTI ID:1641872

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Biological Science

Microbial community composition controls carbon flux across litter types in early phase of litter decomposition

Citation Formats

References (74)

Similar Records

Related Subjects