The Path from Root Input to Mineral-Associated Soil Carbon is Dictated by Habitat-Specific Microbial Traits
Noah W. Sokol1, Megan M. Foley (email@example.com)2*, Amrita Battacharyya3,4, Nicole DiDonato5, Katerina Estera-Molina1,6, Alex Greenlon6, Jeffrey Kimbrel1, Jose Liquet1, Marissa Lafler1, Maxwell Marple1, Peter S. Nico3, Ljiljana Pasa-Tolic5, Eric Slessarev1, Mary Firestone6, Bruce A. Hungate2, Steven J. Blazewicz1, Jennifer Pett-Ridge1,7
1Lawrence Livermore National Laboratory; 2Northern Arizona University; 3Lawrence Berkeley National Laboratory; 4University of San Francisco; 5Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory; 6University of California–Berkeley; 7University of California–Merced
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. The team hypothesizes that microbial cellular-chemistry, functional potential, and ecophysiology fundamentally shape soil carbon persistence, and researchers are characterizing this via stable isotope probing (SIP) of genome-resolved metagenomes and viromes. The team is focusing on soil moisture as a master controller of microbial activity and mortality since altered precipitation regimes are predicted across the temperate United States. This science focus area’s 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.
Soil microorganisms influence the global carbon balance by transforming plant inputs into mineral-associated organic matter (MAOM), but which microbial traits control mineral-associated SOC storage is widely debated. While current theory and biogeochemical models have settled on microbial carbon-use efficiency and growth rate as positive predictors of mineral-associated SOC accrual, empirical tests are sparse and show contradictory observations. To investigate the relationship between different microbial traits and MAOM, researchers conducted a 12- week 13C tracer study to track the movement of rhizodeposits and root detritus into microbial communities and SOM pools under moisture-replete (15 ± 4.2%) or water-limited (8 ± 2%) conditions. Using a continuous 13CO2-labeling growth chamber system, researchers grew the annual grass Avena barbata for 12 weeks and measured formation of 13C-MAOM from either 13C-enriched rhizodeposition or decomposing 13C-enriched root detritus. The team also measured active microbial community composition (via 13C-quantiative stable isotope probing; qSIP) a suite of microbial traits including carbon-use efficiency, growth rate, and turnover (via the 18O-H2O method), extracellular enzyme activity, bulk 13C-extracellular polymeric substances (EPS), and total microbial biomass carbon (13C-MBC), as well as chemical composition of MAOM via 13C-nuclear magnetic resonance (NMR) and Fourier-transform ion cyclotron resonance mass spectrometry (FTICR-MS).
In the microbial habitat around living roots (rhizosphere), the activity of bacterial-dominated communities with fast growth, high biomass, and high production of extracellular polymeric substances were positively associated with the accrual of 13C-mineral–associated SOC under normal moisture conditions. However, under drought, the rhizosphere and the microbial habitat around decaying roots (detritusphere) had more fungal-dominated communities positively associated with 13C-mineral associated SOC with slower growth, lower carbon-use efficiency, and higher exoenzyme activity. 13C-qSIP revealed that bacterial taxa from the families Bacillaceae, Bradyrhizobiaceae, and Comamonadaceae were particularly active in the rhizosphere, whereas filamentous fungi (families Ceratostomataceae, Lasiosphaeriaceae, and Pleosporaceae) were dominant decomposers in the detritusphere. FTICR-MS and 13C-NMR indicated that rhizosphere MAOM has a higher O/C ratio than the detritusphere as well as having a greater amount of lipids and carbohydrates, whereas the detritusphere had a greater abundance of lignin-like compounds. Together, this suggests a more microbial-processed signature of MAOM in the rhizosphere and a more plant-derived signature in the detritusphere.
Overall, these findings emphasize that microbial traits linked with SOC storage vary with soil habitat and moisture conditions—a fact that emerging SOC models should explicitly reflect, since living versus decaying root ratios and moisture regimes will shift under a changing climate.
This research is based upon work of the LLNL Microbes Persist Soil Microbiome science focus area supported by the U.S. Department of Energy Office of Science, Office of Biological and Environmental Research Genomic Science program under Award Number SCW1632 to the Lawrence Livermore National Laboratory, and subcontracts to the Northern Arizona University and the Pacific Northwest National Laboratory. Work at Lawrence Livermore National Laboratory was performed under U.S. Department of Energy Contract DE-AC52-07NA27344.