Trait-based assembly of arbuscular mycorrhizal fungal communities determines soil carbon formation and retention.

Fungi are crucial for soil organic carbon (SOC) formation, especially for the more persistent mineral-associated organic C (MAOC) pool. Yet, evidence for this often overlooks arbuscular mycorrhizal fungi (AMF) communities and how their composition and traits impact SOC accumulation. We grew sudangrass with AMF communities representing different traits conserved at the family level: competitors, from the Gigasporaceae family; ruderals, from the Glomeraceae family; or both families combined. We labeled sudangrass with 13 C-CO2 to assess AMF contributions to SOC, impacts on SOC priming, and fungal biomass persistence in MAOC. Single-family AMF communities decreased total SOC by 13.8%, likely due to fungal priming. Despite net SOC losses, all AMF communities contributed fungal C to soil but only the Glomeraceae community initially contributed to MAOC. After a month of decomposition, both the Glomeraceae and mixed-family communities contributed to MAOC formation. Plant phosphorus uptake, but not hyphal chemistry, was positively related to AMF soil C and MAOC accumulation. Arbuscular mycorrhizal fungi contribution to MAOC is dependent on the specific traits of the AMF community and related to phosphorus uptake. These findings provide insight into how variations in AMF community composition and traits, and thus processes like environmental filtering of AMF, may impact SOC accumulation.

Arbuscular mycorrhizal fungal communities with contrasting life-history traits influence host nutrient acquisition.

Life-history traits differ substantially among arbuscular mycorrhizal (AM) fungal families, potentially affecting hyphal nutrient acquisition efficiency, host nutrition, and thereby plant health and ecosystem function. Despite these implications, AM fungal community life-history strategies and community trait diversity effects on host nutrient acquisition are poorly understood. To address this knowledge gap, we grew sudangrass with AM fungal communities representing contrasting life-history traits and diversity: either (1) five species in the AM family Gigasporaceae, representing competitor traits, (2) five Glomerales species, representing ruderal traits, or (3) a mixed-trait community combining all ten AM fungal species. After 12 weeks, we measured above and belowground plant biomass and aboveground nutrient uptake and concentration. Overall, AM fungal colonization increased host nutrition, biomass, and foliar δ5nitrogen enrichment compared to the uncolonized control. Between the single-trait communities, the Glomeraceae community generally outperformed the Gigasporaceae community in host nutrition and plant growth, increasing plant phosphorus (P) uptake 1.5 times more than the Gigasporaceae community. We saw weak evidence for a synergistic effect of the mixed community, which was only higher for plant P concentration (1.26 times higher) and root colonization (1.26 times higher) compared to the single-trait communities. However, this higher P concentration did not translate to more P uptake or the highest plant biomass for the mixed community. These findings demonstrate that the AM symbiosis is affected by community differences at high taxonomic levels and provide insight into how different AM fungal communities and their associated traits affect host nutrition for fast-growing plant species.

A holistic framework integrating plant-microbe-mineral regulation of soil bioavailable nitrogen.

Soil organic nitrogen (N) is a critical resource for plants and microbes, but the processes that govern its cycle are not well-described. To promote a holistic understanding of soil N dynamics, we need an integrated model that links soil organic matter (SOM) cycling to bioavailable N in both unmanaged and managed landscapes, including agroecosystems. We present a framework that unifies recent conceptual advances in our understanding of three critical steps in bioavailable N cycling: organic N (ON) depolymerization and solubilization; bioavailable N sorption and desorption on mineral surfaces; and microbial ON turnover including assimilation, mineralization, and the recycling of microbial products. Consideration of the balance between these processes provides insight into the sources, sinks, and flux rates of bioavailable N. By accounting for interactions among the biological, physical, and chemical controls over ON and its availability to plants and microbes, our conceptual model unifies complex mechanisms of ON transformation in a concrete conceptual framework that is amenable to experimental testing and translates into ideas for new management practices. This framework will allow researchers and practitioners to use common measurements of particulate organic matter (POM) and mineral-associated organic matter (MAOM) to design strategic organic N-cycle interventions that optimize ecosystem productivity and minimize environmental N loss. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s10533-021-00793-9.

Managing Agroecosystems for Soil Microbial Carbon Use Efficiency: Ecological Unknowns, Potential Outcomes, and a Path Forward.

Agricultural systems are increasingly managed for improving soil carbon (C) accumulation. However, there are limits to C returns in agricultural systems that constrain soil C accumulation capacity. Increasing the efficiency of how soil microbes process C is gaining interest as an important management strategy for increasing soil C and is a key feature of soil C dynamics in many new microbial-explicit models. A higher microbial C use efficiency (CUE) may increase C storage while reducing C system losses and is a fundamental trait affecting community assembly dynamics and nutrient cycling. However, the numerous ecological unknowns influencing CUE limit our ability to effectively manage CUE in agricultural soils for greater soil C storage. In this perspective, we consider three complex drivers of agroecosystem CUE that need to be resolved to develop effective C sequestration management practices in the future: (1) the environment as an individual trait moderator versus a filter, (2) microbial community competitive and faciliatory interactions, and (3) spatiotemporal dynamics through the soil profile and across the microbial lifecycle. We highlight ways that amendments, crop rotations, and tillage practices might affect microbial CUE conditions and the variable outcomes of these practices. We argue that to resolve some of the unknowns of CUE dynamics, we need to include more mechanistic, trait-based approaches that capitalize on advanced methods and innovative field research designs within an agroecosystem-specific context. By identifying the management-level determinants of CUE expression, we will be better positioned to optimize CUE to increase soil C storage in agricultural systems.

Author Correction: Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls.

In the originally published version of this Article, financial support was not fully acknowledged. The PDF and HTML versions of the Article have now been corrected to include support from the NSF Long-term Ecological Research Program (DEB 1637653) at the Kellogg Biological Station and from Michigan State University AgBioResearch.

Root traits and root biomass allocation impact how wheat genotypes respond to organic amendments and earthworms.

Plant-soil biological interactions are increasingly recognized as a key feature of agroecosystems, promoting both crop and soil health. However, the effectiveness of plant-soil synergies is likely modulated by both root system characteristics and soil management impacts on soil biological communities. To successfully manage for plant-soil interactions, we need to better understand how crops respond to changes in soil management, especially in terms of belowground investment. Specifically, crop genotypes that exhibit reduced plasticity in root growth and investment may not be able to take full advantage of changes in soil biological activity associated with soil health promoting practices. We hypothesized that genotypes with greater belowground investment respond more, in terms of plant growth and crop nitrogen (N) uptake, to compost and earthworm additions, agronomic factors commonly associated with soil health. We evaluated four spring wheat (Triticum aestivum) genotypes with distinct breeding and environmental histories, and one progenitor of wheat (Aegilops tauschii) under low soil fertility conditions in the greenhouse for differences in belowground root biomass and architecture. We then determined how these belowground traits influenced genotype response to additions of compost and earthworms. Measurements included plant growth, biomass, grain yield, root characteristics, plant N uptake, and soil N. Overall, in unamended soils, genotypes differed in above and belowground phenotypic traits. In general, Ae. tauschii had three times greater root: shoot (R:S) ratio, root length, and root biomass relative to wheat genotypes. We found that genotypes with higher R:S ratios responded more positively to compost additions compared to those with lower R:S ratios, particularly in terms of plant aboveground biomass, N uptake and soil N-cycling, and also exhibited greater plasticity in root morphology. Consequently, while higher R:S genotypes had relatively poorer yields in unamended soils, they outperformed lower R:S genotypes in total seed weight under compost treatments. Our findings suggest that genotypes with greater belowground investment may be better able to take advantage of soil health promoting practices, such as the use of organic amendments. These results highlight the need to consider soil management practices (and associated biological communities) in parallel with root phenotypic plasticity when evaluating wheat lines for improvements in plant-soil synergies.

Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls.

Soil organic matter (SOM) and the carbon and nutrients therein drive fundamental submicron- to global-scale biogeochemical processes and influence carbon-climate feedbacks. Consensus is emerging that microbial materials are an important constituent of stable SOM, and new conceptual and quantitative SOM models are rapidly incorporating this view. However, direct evidence demonstrating that microbial residues account for the chemistry, stability and abundance of SOM is still lacking. Further, emerging models emphasize the stabilization of microbial-derived SOM by abiotic mechanisms, while the effects of microbial physiology on microbial residue production remain unclear. Here we provide the first direct evidence that soil microbes produce chemically diverse, stable SOM. We show that SOM accumulation is driven by distinct microbial communities more so than clay mineralogy, where microbial-derived SOM accumulation is greatest in soils with higher fungal abundances and more efficient microbial biomass production.