Genomic Science Program
U.S. Department of Energy | Office of Science | Biological and Environmental Research Program

Drought Influences Microbial Activity and the Accrual and Composition of Soil Organic Carbon

Authors:

Linea Honecker1* (honeker1@llnl.gov), Noah W. Sokol1, Megan Foley2, Gianna Marschmann3, Nicole DiDonato4, Chaevien S. Clendinen4, Kent J. Bloodsworth4, Jeffrey Kimbrel1, G. Michael Allen1, Michaela Hayer2, Eoin Brodie3, Bruce Hungate2, Ljiljana Paša-Tolić4, Katerina Estera-Molina1, Steven Blazewicz1, Jennifer Pett-Ridge1,5

Institutions:

1Physical and Life Science Directorate, Lawrence Livermore National Laboratory; 2Center for Ecosystem Science and Society, Northern Arizona University; 3Earth and Environmental Sciences, Lawrence Berkeley National Laboratory; 4Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory; 5Life and Environmental Sciences Department, University of California–Merced

URLs:

Goals

Microorganisms play key roles in soil carbon turnover and stabilization of persistent organic matter via their metabolic activities, cellular biochemistry, and extracellular products. Microbial residues are the primary ingredients in soil organic matter (SOM), a pool critical to Earth’s soil health and climate. Researchers hypothesize that microbial cellular-chemistry, functional potential, and ecophysiology fundamentally shape soil carbon persistence, and are characterizing this via stable isotope probing (SIP) of genome-resolved metagenomes and viromes. Researchers focus on soil moisture as a master controller of microbial activity and mortality, since altered precipitation regimes are predicted across the temperate U.S. The Science Focus Area’s (SFA) ultimate goal is to determine how microbial soil ecophysiology, population dynamics, and microbe-mineral-organic matter interactions regulate the persistence of microbial residues under changing moisture regimes.

Abstract

Soil microorganisms shape the global carbon balance by transforming plant rhizodeposits and root detritus into soil organic matter (SOM). It remains unclear how drought influences transformations of these distinct root sources, particularly into the largest and slowest-cycling SOM pool mineral-associated organic matter (MAOM), and how researchers might predict these transformations with changing climate. Since living and decaying roots often exist in close proximity, researchers need to understand how their interaction affects the accrual of MAOM, e.g., through priming effects induced by enhanced microbial activity or the effects of specific microbial taxa. To investigate relationships between drought, microbial ecophysiology, and SOM accrual in a Mediterranean grassland soil, the team conducted a 12-week continuous 13CO2 tracer study with the annual grass Avena barbata, tracking movement of rhizodeposits and root detritus into microbial communities and SOM pools under moisture replete (15 ± 4.2%) or water-limited (8 ± 2%) conditions. Upon harvest, the team measured formation of 13C-MAOM from either 13C-enriched rhizodeposition alone, decomposing 13C-enriched root detritus alone, or the two together. The team measured active microbial community composition (via 18O- and 13C-quantiative stable isotope probing; qSIP), microbial community-level growth rate and carbon-use efficiency, and the chemical composition of SOM using mass spectrometry. These data inform the modeling, which integrates dynamic plant growth models, microhabitats, and a trait-based dynamic energy budget model (DEBmicroTrait) to simulate how precipitation patterns impact both, the timing and magnitude of belowground carbon allocation in Avena barbata, rhizosphere community dynamics and ultimately MAOM accrual.

Overall, drought significantly reduced the accrual of 13C-MAOM, with contrasting interactions between habitat and time. In droughted rhizosphere soil, there was significantly less 13C-MAOM relative to moisture replete soil at week 12. But at that time, moisture replete rhizosphere soils had the greatest aboveground plant biomass, microbial community-level growth rate and carbon use efficiency. In the detritusphere, droughted soils had the greatest difference in 13C-MAOM at week 4–during early stages of root litter decomposition. At this same point, detritusphere microbial community-level growth rate and carbon-use efficiency was greatest under normal moisture conditions. The chemical composition of SOM was also significantly different between rhizosphere and detritusphere habitats, with greater abundance of diacylglycerophosphocholine lipids in the detritusphere, and triacylglycerol lipids in the rhizosphere. Metabolomics suggested more short chain saturated and hydroxy fatty acids in the rhizosphere and more di- and tri-saccharides, C-8 amino sugars and some nucleobases (thymine and cytosine) in the detritusphere.

When living and dead roots co-existed, the presence of living roots decreased the accrual of 13C-MAOM formed from detritus. However, the inverse was not true: root detritus did not affect 13C-MAOM derived from rhizodeposition. In the detritusphere, the effect of living roots on microbial growth rates depended on soil moisture. Under drought, living roots increased relative growth rates of fungal and bacterial taxa. When soils were moisture replete, living roots increased relative growth rates of detritusphere fungal taxa, with no effect on bacteria. In comparison, the presence of detritus increased relative growth rates of fungal and bacterial rhizosphere taxa regardless of soil moisture.

Funding Information

This research is based upon work of the LLNL Microbes Persist Soil Microbiome SFA, supported by the U.S. DOE Office of Science, BER Program GSP under Award Number SCW1632 to the Lawrence Livermore National Laboratory, and subcontracts to the Northern Arizona University, Lawrence Berkeley National Laboratory, and the Pacific Northwest National Laboratory. Work at Lawrence Livermore National Laboratory was performed under U.S. DOE Contract DE-AC52-07NA27344. A portion of this research was performed at the Environmental Molecular Sciences Laboratory, a DOE Office of Science User Facility sponsored by the BER program under Contract No. DE-AC05-76RL01830.