Resource Legacies of Organic and Conventional Management Differentiate Soil Microbial Carbon Use

Abstract

Long-term contrasts in agricultural management can shift soil resource availability with potential consequences to microbial carbon (C) use efficiency (CUE) and the fate of C in soils. Isothermal calorimetry was combined with 13C-labeled glucose stable isotope probing (SIP) of 16S rRNA genes to test the hypothesis that organically managed soils would support microbial communities with greater thermodynamic efficiency compared to conventional soils due to a legacy of lower resource availability and a resultant shift toward communities supportive of more oligotrophic taxa. Resource availability was greater in conventionally managed soils, with 3.5 times higher available phosphorus, 5% more nitrate, and 36% more dissolved organic C. The two management systems harbored distinct glucose-utilizing populations of Proteobacteria and Actinobacteria, with a higher Proteobacteria:Actinobacteria ratio (2.4 vs. 0.7) in conventional soils. Organically managed soils also harbored notable activity of Firmicutes. Thermodynamic efficiency indices were similar between soils, indicating that glucose was metabolized at similar energetic cost. However, differentially abundant glucose utilizers in organically managed soils were positively correlated with soil organic matter (SOM) priming and negatively correlated to soil nutrient and carbon availability, respiration, and heat production. These correlation patterns were strongly reversed in the conventionally managed soils indicating clear differentiation of microbial functioning related to soil resource availability. Fresh C addition caused proportionally more priming of SOM decomposition (57 vs. 51%) in organically managed soils likely due to mineralization of organic nutrients to satisfy microbial demands during glucose utilization in these more resource deprived soils. The additional heat released from SOM oxidation may explain the similar community level thermodynamic efficiencies between management systems. Restoring fertility to soils with a legacy of nutrient limitation requires a balanced supply of both nutrients and energy to protect stable SOM from microbial degradation. These results highlight the need to consider managing C for the energy it provides to ıcritical biological processes that underpin soil health.

Analysis of microbial utilization of rice straw in paddy soil using a DNA‐SIP approach

“…The proportion of 13 C derived from labeled rice straw in the soil was calculated using Equation (Arcand et al., ): …”

“…The proportion of 13 C derived from labeled rice straw in the soil was calculated using Equation (1) (Arcand et al, 2017):…”

“…However, phylogenetic resolution based on PLFA analyses is not sufficient to characterize all species and their individual contributions to C utilization (Dumont and Murrell, ). To obtained more information at better resolution, DNA/RNA‐SIP has been combined with high‐throughput sequencing to track the fate of simple C substrates including CO 2 (Hou, Ai, Zhou, Liang, & He, ), CH 4 (Morris, Radajewski, Willison, & Murrel, ), glucose (Arcand, Levy‐Booth, & Helgason, ), methanol (Ginige et al., ), cellulose/xylose (Pepe‐Ranney et al., ) and rice callus (Lee et al., ) at higher resolution. However, the results of such studies on simple substrates could not fully reflect the complex situation of crop straw decomposition in agricultural soils.…”

Nutrient Cycling in Organic Field Crops in Canada and the United States

“…Nutrient availability and SOM formation are affected by C use efficiency (CUE; Arcand et al, 2017; Hagerty et al, 2018; Silva‐Sanchez et al, 2019; Soares and Rousk, 2019). In turn, CUE can be impacted by microbial community structure and activity, resource availability, SOM quality, stoichiometry, environmental factors, and priming effects (Arcand et al, 2017; Di Lonardo et al, 2019; Soares and Rousk 2019). Priming refers to short‐term changes in SOM turnover caused by additions of readily degradable organic matter.…”

“…Priming refers to short‐term changes in SOM turnover caused by additions of readily degradable organic matter. Carbon additions can have a greater priming effect on SOM decomposition in organic than conventional systems since the former oftentimes are more nutrient deprived (Arcand et al, 2017), but its magnitude can be impacted by the ratio of added C to biomass, pH, and nutrient availability (Di Lonardo et al, 2019; Silva‐Sanchez et al, 2019). Microbes may be better adapted at receiving organic matter inputs in organic than conventional systems (Bowles et al, 2014; Di Lonardo et al, 2019), but more research is needed to elucidate the underlying relationships and mechanistic drivers, particularly in organic systems.…”