Fast-decaying plant litter enhances soil carbon in temperate forests but not through microbial physiological traits

Abstract

Conceptual and empirical advances in soil biogeochemistry have challenged long-held assumptions about the role of soil micro-organisms in soil organic carbon (SOC) dynamics; yet, rigorous tests of emerging concepts remain sparse. Recent hypotheses suggest that microbial necromass production links plant inputs to SOC accumulation, with high-quality (i.e., rapidly decomposing) plant litter promoting microbial carbon use efficiency, growth, and turnover leading to more mineral stabilization of necromass. We test this hypothesis experimentally and with observations across six eastern US forests, using stable isotopes to measure microbial traits and SOC dynamics. Here we show, in both studies, that microbial growth, efficiency, and turnover are negatively (not positively) related to mineral-associated SOC. In the experiment, stimulation of microbial growth by high-quality litter enhances SOC decomposition, offsetting the positive effect of litter quality on SOC stabilization. We suggest that microbial necromass production is not the primary driver of SOC persistence in temperate forests. Factors such as microbial necromass origin, alternative SOC formation pathways, priming effects, and soil abiotic properties can strongly decouple microbial growth, efficiency, and turnover from mineral-associated SOC.

Divergent microbial traits influence the transformation of living versus dead root inputs to soil carbon

“…While we observed positive relationships between these traits and mineral-associated SOC in the rhizosphere, the lack of significant relationships in the detritusphere demonstrate that CUE and growth rate may be uncoupled from mineral-associated SOC formation in certain contexts, likely due to allocation of C to other compounds, such as extracellular enzymes 7,59 . These findings can help explain prior contrasting observations on the role of CUE and growth rate in mineral-associated SOC accrual 7,11 . Our results also emphasize that it is important to consider how soil microorganisms allocate their C under different resource environments and different climate stressors – whether to growth, resource acquisition, or to products like storage or stress compounds – in order to understand which microbial traits and taxa will be associated with the accrual of mineral-associated SOC 2,9,10 .…”

“…Decaying microbial residues -such as cell envelopes, DNA, and extracellular polymeric substances (collectively described as 'microbial necromass') -are increasingly recognized as key ingredients of mineral-associated SOC, and can comprise 50% or more of the total pool [4][5][6] . A dominant hypothesis is therefore that greater microbial carbon-use efficiency (CUE) and faster growth and turnover should lead to greater microbial necromass production, and greater accrual of mineral-associated SOC 7,8 . While this hypothesis has gained traction -and is represented in several 'microbial-explicit' biogeochemical models 9,10 -few empirical studies have directly tested it.…”

“…In ecosystems like croplands and grasslands, where a greater proportion of SOC appears to be 'microbial-derived' (i.e., plant C that is microbially assimilated and transformed to various microbial compounds, which then associate with soil minerals), greater microbial growth and CUE can lead to more mineral-associated SOC 11 . However, in ecosystems like temperate forests where a greater proportion of SOC appears to be 'plant-derived' (i.e., plant C that may be partially decomposed by microbial exoenzymes into simpler plant compounds, but does not pass through a microbial body before associating with soil minerals), these relationships can be neutral or negative 7 .…”

“…Growth rate and CUE therefore have contradictory effects on mineral-associated SOC formation, in part due to whether mineral-associated SOC is plant-derived or microbial-derived. However, the mechanisms underpinning these patterns remain elusive, impeding empirical understanding of how microbes control SOC cycling, and the subsequent development of accurate SOC models that predict SOC persistence and its responsiveness to climate change 2,7,12 . To understand contrasting effects of microbial traits on mineral-associated SOC, it is necessary to untangle their effects at the scale of the microbial habitat – the site where different sources of plant C input are transformed to SOC 12 .…”

Recarbonizing Global Soils for Sustainable Development

“…However, climate change, land use, and poor soil management practises-induced pressures might alter organo-mineral interactions, SOC dynamics, and the carbon source-sink relationships. Therefore, sustainable land-use practises and resource-efficient soil management initiatives are inevitable for offsetting carbon emissions while improving the residence time of carbon and stabilising the carbon in the soil (Luo et al 2019;Hong et al 2020;Craig et al 2022). Further, digital technology-based ecological restoration of degraded peatlands, wastelands, farmland, and contaminated lands could facilitate the options for improved agri-extensification, agroforestry, soil carbon sequestration, soil health and biodiversity, climate change adaptation and mitigation, food, nutritional, and livelihood security (Abhilash et al 2016;Mondejar et al 2021).…”