Soil habitat and drought shape microbial traits associated with mineral-associated soil carbon formation

Soil microorganisms are frontline managers of the terrestrial carbon cycle. To better understand and model their effects under a changing climate, it is critical to determine which microbial ecophysiological traits are associated with soil organic matter formation – particularly mineral-associated organic matter (MAOM). Yet major uncertainty surrounds the traits that regulate this process, and how environmental context (e.g. spatial habitat, moisture conditions) shapes the manifestation of these traits. Microbial carbon-use efficiency (CUE) is posited to be a particularly key microbial trait, yet direct evidence for this relationship is sparse, and few other microbial traits have been directly tested as predictors of MAOM formation.

To investigate the relationship between different microbial traits and MAOM, we 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 droughted (8 ± 2%) conditions. Using a continuous ¹³CO₂-labeling growth chamber system, we 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. We also measured active microbial community composition (via ¹³C-quantiative stable isotope probing; qSIP) and a suite of microbial traits that may be important in soil carbon formation, including community-level 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).

We found that different microbial traits were associated with MAOM formation in the rhizosphere versus the detritusphere, and their effect was influenced by soil moisture. In the rhizosphere, fast growth and turnover were positively associated with MAOM, as were total ¹³C-MBC and ¹³C-EPS production. In contrast, growth rate was negatively associated with MAOM formation in the detritusphere, as were CUE, ¹³C-MBC, and ¹³C-EPS. However, extracellular enzyme activity was positively associated with MAOM in the detritusphere. These results, paired with data on the chemical composition of MAOM (via STXM-NEXAFS) suggest that traits associated with fast growth and death rates, as well as high necromass yield, generate microbial-derived MAOM in the rhizosphere, whereas traits associated with resource acquisition generate plant-derived MAOM in the detritusphere. We also present ¹³C-qSIP data demonstrating that fungal taxa are more active in the detritusphere, whereas certain bacterial phyla (e.g., Firmicutes) are more active in the rhizosphere. Together, our results show that distinct traits, communities, and pathways of MAOM formation predominate in the rhizosphere versus the detritusphere. New research should focus on a broader suite of microbial traits – including but not limited to CUE – to model the role of microbes in MAOM formation in distinct habitats and moisture conditions of the soil.