Simulated nitrogen deposition and precipitation events alter microbial carbon cycling during early stages of litter decomposition

Kroeger, Marie Elizabeth; Wang, Renée Z.; Suazo, Dennis Daniel; Yoshida, Thomas M.; Albright, Michaeline Burr Nelson; Dunbar, John Martin

doi:10.1093/sumbio/qvae031

Simulated nitrogen deposition and precipitation events alter microbial carbon cycling during early stages of litter decomposition

Journal Article · Wed Nov 13 23:00:00 EST 2024 · Sustainable Microbiology

DOI:https://doi.org/10.1093/sumbio/qvae031· OSTI ID:2478640

^[1]; Wang, Renée Z. ^[2]; ^[3]; ^[4]; ^[5]; ^[4]

Los Alamos National Laboratory (LANL), Los Alamos, NM (United States); In-Pipe Technology, LLC, Wood Dale, IL (United States)
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States); California Institute of Technology (CalTech), Pasadena, CA (United States); University of California, Berkeley, CA (United States)
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States); University of California, Berkeley, CA (United States)
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States); Allonnia, LLC, Boston, MA (United States)

Plant litter decomposition is a major nutrient input to terrestrial ecosystems that is primarily driven by microorganisms. Litter quality is considered a key drive of decomposition; however, human-induced global disturbance like nitrogen deposition and increasing extreme precipitation events will shift nutrient availability during litter decomposition. Little is known about how shifting nutrient availability will impact dissolved organic matter concentrations and microbially driven carbon cycling that are critical to soil organic matter formation. This study investigated the effect of simulated nitrogen deposition and repeated precipitation events on microbially driven carbon flow during short-term litter decomposition using a ‘common garden’ experiment with microcosms containing sand and blue grama grass litter inoculated with different microbial communities. Overall, nitrogen deposition decoupled respiration and dissolved organic carbon (DOC) by increasing respiration and not affecting DOC concentrations. Moreover, nitrogen deposition had no effect on microbial carbon use efficiency (CUE). Repeated simulated precipitation events significantly increased DOC concentrations, decreased microbial CUE, increased the microbial metabolic quotient (qCO2), and altered microbial composition and diversity. These findings highlight the complex interactions and responses of surface litter decomposers to shifting nutrient availability and contradicts previous findings that nitrogen deposition will increase soil carbon sequestration from a larger supply of DOC and reduced respiration.

View Accepted Manuscript (DOE)

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

Sponsoring Organization:: USDOE National Nuclear Security Administration (NNSA); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: 89233218CNA000001

OSTI ID:: 2478640

Report Number(s):: LA-UR--22-30063

Journal Information:: Sustainable Microbiology, Journal Name: Sustainable Microbiology Journal Issue: 1 Vol. 1; ISSN 2755-1970

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

References (67)

ggplot2 Wickham, Hadley Use R! https://doi.org/10.1007/978-3-319-24277-4	book	January 2016
Influence of inorganic and organic fertilization on soil microbial biomass, metabolic quotient and heavy metal bioavailability Leita, L.; De Nobili, M.; Mondini, C. Biology and Fertility of Soils, Vol. 28, Issue 4 https://doi.org/10.1007/s003740050506	journal	February 1999
Effects of Long-Term Nitrogen Addition on Microbial Enzyme Activity in Eight Forested and Grassland Sites: Implications for Litter and Soil Organic Matter Decomposition Keeler, Bonnie L.; Hobbie, Sarah E.; Kellogg, Laurie E. Ecosystems, Vol. 12, Issue 1 https://doi.org/10.1007/s10021-008-9199-z	journal	October 2008
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
The partitioning of litter carbon fates during decomposition under different rainfall patterns: a laboratory study Yang, Xu; Szlavecz, Katalin; Pitz, Scott L. Biogeochemistry, Vol. 148, Issue 2 https://doi.org/10.1007/s10533-020-00651-0	journal	March 2020
Soil microorganisms regulate extracellular enzyme production to maximize their growth rate Calabrese, Salvatore; Mohanty, Binayak P.; Malik, Ashish A. Biogeochemistry, Vol. 158, Issue 3 https://doi.org/10.1007/s10533-022-00899-8	journal	February 2022
Enzymatic removal of inhibitory compounds from lignocellulosic hydrolysates for biomass to bioproducts applications Tramontina, Robson; Brenelli, Lívia Beatriz; Sodré, Victoria World Journal of Microbiology and Biotechnology, Vol. 36, Issue 11 https://doi.org/10.1007/s11274-020-02942-y	journal	October 2020
Effects of nitrogen addition on litter decomposition, soil microbial biomass, and enzyme activities between leguminous and non‐leguminous forests Lv, Yanna; Wang, Congyan; Wang, Fangyuan Ecological Research, Vol. 28, Issue 5 https://doi.org/10.1007/s11284-013-1060-y	journal	June 2013
Soil Microbial Metabolic Quotient in Inner Mongolian Grasslands: Patterns and Influence Factors Cao, Yingqiu; Xu, Li; Zhang, Zhen Chinese Geographical Science, Vol. 29, Issue 6 https://doi.org/10.1007/s11769-019-1084-5	journal	December 2019
Litter decomposition in forest ecosystems: a review Krishna, M. P.; Mohan, Mahesh Energy, Ecology and Environment, Vol. 2, Issue 4 https://doi.org/10.1007/s40974-017-0064-9	journal	July 2017
Resource control on the production of dissolved organic carbon and nitrogen in a deciduous forest floor Park, Ji-Hyung; Kalbitz, Karsten; Matzner, Egbert Soil Biology and Biochemistry, Vol. 34, Issue 6 https://doi.org/10.1016/S0038-0717(02)00011-1	journal	June 2002
Interactive effects of pH and substrate quality on the fungal-to-bacterial ratio and qCO2 of microbial communities in forest soils Blagodatskaya, Evgenia V.; Anderson, Traute-Heidi Soil Biology and Biochemistry, Vol. 30, Issue 10-11 https://doi.org/10.1016/S0038-0717(98)00050-9	journal	September 1998
Dissolved organic carbon and nitrogen relationships in forest litter as affected by nitrogen deposition Magill, Alison H.; Aber, John D. Soil Biology and Biochemistry, Vol. 32, Issue 5 https://doi.org/10.1016/S0038-0717(99)00187-X	journal	May 2000
Effects of nitrogen addition and litter properties on litter decomposition and enzyme activities of individual fungi Jiang, Xinyu; Cao, Lixiang; Zhang, Renduo Applied Soil Ecology, Vol. 80 https://doi.org/10.1016/j.apsoil.2014.04.002	journal	August 2014
Experimental nitrogen deposition alters the quantity and quality of soil dissolved organic carbon in an alpine meadow on the Qinghai-Tibetan Plateau Fang, Huajun; Cheng, Shulan; Yu, Guirui Applied Soil Ecology, Vol. 81 https://doi.org/10.1016/j.apsoil.2014.04.007	journal	September 2014
Pretreatment of lignocellulose: Formation of inhibitory by-products and strategies for minimizing their effects Jönsson, Leif J.; Martín, Carlos Bioresource Technology, Vol. 199 https://doi.org/10.1016/j.biortech.2015.10.009	journal	January 2016
Effect of litter substrate quality and soil nutrients on forest litter decomposition: A review Ge, Xiaogai; Zeng, Lixiong; Xiao, Wenfa Acta Ecologica Sinica, Vol. 33, Issue 2 https://doi.org/10.1016/j.chnaes.2013.01.006	journal	April 2013
Atmospheric nitrogen deposition: A review of quantification methods and its spatial pattern derived from the global monitoring networks Zhang, Qi; Li, Yanan; Wang, Mengru Ecotoxicology and Environmental Safety, Vol. 216 https://doi.org/10.1016/j.ecoenv.2021.112180	journal	June 2021
Nitrogen deposition and dissolved organic carbon production in northern temperate forests Sinsabaugh, R. L.; Zak, D. R.; Gallo, M. Soil Biology and Biochemistry, Vol. 36, Issue 9 https://doi.org/10.1016/j.soilbio.2004.04.026	journal	September 2004
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
Contribution of sorption, DOC transport and microbial interactions to the 14C age of a soil organic carbon profile: Insights from a calibrated process model Ahrens, Bernhard; Braakhekke, Maarten C.; Guggenberger, Georg Soil Biology and Biochemistry, Vol. 88 https://doi.org/10.1016/j.soilbio.2015.06.008	journal	September 2015
Mechanisms driving the soil organic matter decomposition response to nitrogen enrichment in grassland soils Riggs, Charlotte E.; Hobbie, Sarah E. Soil Biology and Biochemistry, Vol. 99 https://doi.org/10.1016/j.soilbio.2016.04.023	journal	August 2016
Changing rainfall frequency rather than drought rapidly alters annual soil respiration in a tropical forest Deng, Qi; Zhang, Deqiang; Han, Xi Soil Biology and Biochemistry, Vol. 121 https://doi.org/10.1016/j.soilbio.2018.02.023	journal	June 2018
Characteristics of Dissolved Organic Matter and Dissolved Lignin Phenols in Tropical Forest Soil Solutions during Rainy Seasons and Their Responses to Nitrogen Deposition Wang, Mengke; Zhang, Ziting; Wang, Yinghui ACS Earth and Space Chemistry, Vol. 5, Issue 11 https://doi.org/10.1021/acsearthspacechem.1c00243	journal	October 2021
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
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
Bacterial competition: surviving and thriving in the microbial jungle Hibbing, Michael E.; Fuqua, Clay; Parsek, Matthew R. Nature Reviews Microbiology, Vol. 8, Issue 1 https://doi.org/10.1038/nrmicro2259	journal	November 2009
Discovery of lignin-transforming bacteria and enzymes in thermophilic environments using stable isotope probing Levy-Booth, David J.; Navas, Laura E.; Fetherolf, Morgan M. The ISME Journal, Vol. 16, Issue 8 https://doi.org/10.1038/s41396-022-01241-8	journal	May 2022
Universal microbial reworking of dissolved organic matter along environmental gradients Freeman, Erika C.; Emilson, Erik J. S.; Dittmar, Thorsten Nature Communications, Vol. 15, Issue 1 https://doi.org/10.1038/s41467-023-44431-4	journal	January 2024
Scientists’ warning to humanity: microorganisms and climate change Cavicchioli, Ricardo; Ripple, William J.; Timmis, Kenneth N. Nature Reviews Microbiology, Vol. 17, Issue 9 https://doi.org/10.1038/s41579-019-0222-5	journal	June 2019
Rain-induced changes in soil CO2 flux and microbial community composition in a tropical forest of China Deng, Qi; Hui, Dafeng; Chu, Guowei Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-06345-2	journal	July 2017
Global variation of soil microbial carbon-use efficiency in relation to growth temperature and substrate supply Qiao, Yang; Wang, Jing; Liang, Guopeng Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-42145-6	journal	April 2019
Climate change impact on flood and extreme precipitation increases with water availability Tabari, Hossein Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-70816-2	journal	August 2020
Experimental evidence for the impact of soil viruses on carbon cycling during surface plant litter decomposition Albright, Michaeline B. N.; Gallegos-Graves, La Verne; Feeser, Kelli L. ISME Communications, Vol. 2, Issue 1 https://doi.org/10.1038/s43705-022-00109-4	journal	March 2022
Nutrient availability shapes the microbial community structure in sugarcane bagasse compost-derived consortia Mello, Bruno L.; Alessi, Anna M.; McQueen-Mason, Simon Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep38781	journal	December 2016
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
A new fungal large subunit ribosomal RNA primer for high throughput sequencing surveys Mueller, Rebecca C.; Gallegos-Graves, La Verne; Kuske, Cheryl R. FEMS Microbiology Ecology https://doi.org/10.1093/femsec/fiv153	journal	December 2015
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
Litter decomposition and nutrient release from monospecific and mixed litters: Comparisons of litter quality, fauna and decomposition site effects Yang, Kai; Zhu, Jiaojun; Zhang, Weiwei Journal of Ecology, Vol. 110, Issue 7 https://doi.org/10.1111/1365-2745.13902	journal	May 2022
Microbial community composition controls carbon flux across litter types in early phase of litter decomposition Kroeger, Marie E.; Rae DeVan, M.; Thompson, Jaron Environmental Microbiology, Vol. 23, Issue 11 https://doi.org/10.1111/1462-2920.15705	journal	August 2021
Temporal dynamics of biotic and abiotic drivers of litter decomposition García-Palacios, Pablo; Shaw, E. Ashley; Wall, Diana H. Ecology Letters, Vol. 19, Issue 5 https://doi.org/10.1111/ele.12590	journal	March 2016
The Microbial Efficiency-Matrix Stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter? Cotrufo, M. Francesca; Wallenstein, Matthew D.; Boot, Claudia M. Global Change Biology, Vol. 19, Issue 4 https://doi.org/10.1111/gcb.12113	journal	February 2013
Long‐term nitrogen addition modifies microbial composition and functions for slow carbon cycling and increased sequestration in tropical forest soil Tian, Jing; Dungait, Jennifer A. J.; Lu, Xiankai Global Change Biology, Vol. 25, Issue 10 https://doi.org/10.1111/gcb.14750	journal	August 2019
Leaching of dissolved organic carbon from mineral soils plays a significant role in the terrestrial carbon balance Nakhavali, Mahdi; Lauerwald, Ronny; Regnier, Pierre Global Change Biology, Vol. 27, Issue 5 https://doi.org/10.1111/gcb.15460	journal	December 2020
Microbial activity and soil respiration under nitrogen addition in Alaskan boreal forest Allison, Steven D.; Czimczik, Claudia I.; Treseder, Kathleen K. Global Change Biology, Vol. 14, Issue 5 https://doi.org/10.1111/j.1365-2486.2008.01549.x	journal	May 2008
Improving indicator species analysis by combining groups of sites De Cáceres, Miquel; Legendre, Pierre; Moretti, Marco Oikos, Vol. 119, Issue 10 https://doi.org/10.1111/j.1600-0706.2010.18334.x	journal	September 2010
Life in leaf litter: novel insights into community dynamics of bacteria and fungi during litter decomposition Purahong, Witoon; Wubet, Tesfaye; Lentendu, Guillaume Molecular Ecology, Vol. 25, Issue 16 https://doi.org/10.1111/mec.13739	journal	August 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
Competitive Exclusion and Metabolic Dependency among Microorganisms Structure the Cellulose Economy of an Agricultural Soil Wilhelm, Roland C.; Pepe-Ranney, Charles; Weisenhorn, Pamela mBio, Vol. 12, Issue 1 https://doi.org/10.1128/mBio.03099-20	journal	February 2021
Current knowledge and perspectives of Paenibacillus: a review Grady, Elliot Nicholas; MacDonald, Jacqueline; Liu, Linda Microbial Cell Factories, Vol. 15, Issue 1 https://doi.org/10.1186/s12934-016-0603-7	journal	December 2016
Characterization of Trapped Lignin-Degrading Microbes in Tropical Forest Soil DeAngelis, Kristen M.; Allgaier, Martin; Chavarria, Yaucin PLoS ONE, Vol. 6, Issue 4 https://doi.org/10.1371/journal.pone.0019306	journal	April 2011
Differential Nutrient Limitation of Soil Microbial Biomass and Metabolic Quotients (qCO2): Is There a Biological Stoichiometry of Soil Microbes? Hartman, Wyatt H.; Richardson, Curtis J. PLoS ONE, Vol. 8, Issue 3 https://doi.org/10.1371/journal.pone.0057127	journal	March 2013
Influence of Litter Diversity on Dissolved Organic Matter Release and Soil Carbon Formation in a Mixed Beech Forest Scheibe, Andrea; Gleixner, Gerd PLoS ONE, Vol. 9, Issue 12 https://doi.org/10.1371/journal.pone.0114040	journal	December 2014
The responses of extracellular enzyme activities and microbial community composition under nitrogen addition in an upland soil Ullah, Sami; Ai, Chao; Huang, Shaohui PLOS ONE, Vol. 14, Issue 9 https://doi.org/10.1371/journal.pone.0223026	journal	September 2019
A Theoretical Model of Litter Decay and Microbial Interaction Moorhead, Daryl L.; Sinsabaugh, Robert L. Ecological Monographs, Vol. 76, Issue 2 https://doi.org/10.1890/0012-9615(2006)076%5b0151:ATMOLD%5d2.0.CO;2	journal	May 2006
Microbial Nitrogen Limitation Increases Decomposition Craine, Joseph M.; Morrow, Carl; Fierer, Noah Ecology, Vol. 88, Issue 8 https://doi.org/10.1890/06-1847.1	journal	August 2007
Associations between species and groups of sites: indices and statistical inference Cáceres, Miquel De; Legendre, Pierre Ecology, Vol. 90, Issue 12 https://doi.org/10.1890/08-1823.1	journal	December 2009
Nutritive Quality of Nitrogen Fertilized and Unfertilized Blue Grama Pieper, Rex D.; Kelsey, R. Joe; Nelson, Arnold B. Journal of Range Management, Vol. 27, Issue 6 https://doi.org/10.2307/3896725	journal	November 1974
Acidotolerant Bacteria and Fungi as a Sink of Methanol-Derived Carbon in a Deciduous Forest Soil Morawe, Mareen; Hoeke, Henrike; Wissenbach, Dirk K. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01361	journal	July 2017
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
Microbial Communities Influence Soil Dissolved Organic Carbon Concentration by Altering Metabolite Composition Campbell, Tayte P.; Ulrich, Danielle E. M.; Toyoda, Jason Frontiers in Microbiology, Vol. 12 https://doi.org/10.3389/fmicb.2021.799014	journal	January 2022
Identification of bacteria and fungi responsible for litter decomposition in desert steppes via combined DNA stable isotope probing Ye, He; Tu, Nare; Wu, Zhendan Frontiers in Microbiology, Vol. 15 https://doi.org/10.3389/fmicb.2024.1353629	journal	March 2024
Long-term nitrogen addition decreases carbon leaching in a nitrogen-rich forest ecosystem Lu, X.; Gilliam, F. S.; Yu, G. Biogeosciences, Vol. 10, Issue 6 https://doi.org/10.5194/bg-10-3931-2013	journal	June 2013
Patterns of dissolved organic carbon and nitrogen fluxes in deciduous and coniferous forests under historic high nitrogen deposition Sleutel, S.; Vandenbruwane, J.; De Schrijver, A. Biogeosciences, Vol. 6, Issue 12 https://doi.org/10.5194/bg-6-2743-2009	journal	December 2009
Nutrient levels and trade-offs control diversity in a serial dilution ecosystem Erez, Amir; Lopez, Jaime G.; Weiner, Benjamin G. eLife, Vol. 9 https://doi.org/10.7554/eLife.57790	journal	September 2020

Similar Records

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 · OSTI ID:1826519

Reparameterizing Litter Decomposition Using a Simplified Monte Carlo Method Improves Litter Decay Simulated by a Microbial Model and Alters Bioenergy Soil Carbon Estimates

Journal Article · Thu Mar 07 23:00:00 EST 2024 · Journal of Geophysical Research. Biogeosciences · OSTI ID:2324058

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
biological Sciences
dissolved organic carbon
microbial community
nitrogen deposition
nutrient availability
precipitation effect

Simulated nitrogen deposition and precipitation events alter microbial carbon cycling during early stages of litter decomposition

Citation Formats

References (67)

Similar Records

Related Subjects