Toward understanding how cross-kingdom ecological strategies interactively influence soil carbon cycling

Abstract

Cultivating knowledge to enable accurate estimates of soil carbon fluxes has never been more critical as we contend with climate change. Nevertheless, the incredible diversity of soil communities and the environmental conditions that they experience obfuscates this understanding. Many of these environmental scenarios are influenced by the widespread, human-caused disturbance that has characterized recent history (e.g. deforestation). Environmental restoration practices hold promise to recover some ecosystem functions and aid in climate change mitigation (e.g. by capturing and storing carbon in soil), but many questions remain about the factors that determine the efficacy of these practices. Plants drive the influx of carbon to the soil through above- and belowground litter and root exudates, while the processing of this carbon by soil organisms determines whether carbon persists in soil or is respired to the atmosphere. An immensely diverse, microscopic community of bacteria, fungi, and animals (e.g. nematodes, protists) influences these soil carbon dynamics through their metabolic processes and interactions with one another. Despite this theoretical understanding, quantitative evidence of how inter-organismal interactions determine carbon flow in soil remains difficult to interpret in the context of soil carbon accrual since these interactions are immensely complex and dynamic. A recent publication by Zhang et al. (2024b; doi: 10.1111/nph.20166) in New Phytologist addresses this challenge in a compelling way by considering the ecological strategies of plants and nematodes interactively to explain soil carbon dynamics across a gradient of environmental conditions. Their approach is particularly novel and valuable because they not only consider the interactions between plants and nematodes across a gradient of environmental disturban but also connect this to microbial carbon cycling to explain soil carbon content.

‘…integrated plant and nematode ecological spectra explain more variation in soil carbon dynamics together, than either do alone.’

Viewing organisms through the lens of their ecological strategies allows us to understand how they function within ecosystems and, thus, conceptualize their interactions with other organisms. Plant ecologists have pioneered this effort, cultivating a historic body of knowledge regarding trade-offs between plant traits across environmental gradients. For example, the leaf economics spectrum defines leaf traits like mass per unit area and leaf tissue nitrogen as indicative of plant investment strategy, varying across environmental conditions (Wright et al., 2004). Such frameworks allow us to predict how plant communities may shift as ecosystems change, for instance following intense environmental disturbance. Soil ecologists have more recently sought to develop similar frameworks, identifying traits like body length and mass as important indicators of ecological trade-offs in nematodes (Zhang et al., 2024a). Still, an integrative understanding of cross-kingdom ecological strategies (i.e. how the ecological strategies of plants and soil organisms interact) is a pressing need since a long-standing body of knowledge supports strong interactions between plant and soil organisms. Without abundant quantitative links between these dynamics and soil carbon cycling parameters, our understanding of how interactions between plants and soil organisms govern soil carbon storage remains limited. The recent publication by Zhang et al. (2024b) is a significant contribution to this knowledge gap because it integrates nematode and plant ecological spectra across a gradient of environmental conditions and links this to microbial carbon use efficiency to explain soil carbon storage.

Among the most compelling results presented by Zhang et al. (2024b) is that integrated plant and nematode ecological spectra explain more variation in soil carbon dynamics together, than either do alone. They further identify that the integrated ecological strategies of plants and nematodes indirectly moderate soil carbon by controlling microbial carbon use efficiency (the amount of carbon incorporated into biomass vs respired to the atmosphere), while also directly contributing to soil carbon through, for example, litterfall. Microbial carbon use efficiency has been experimentally linked to plant traits (e.g. litter chemistry; Ridgeway et al., 2022), and to the interaction between microbial and nematode community composition (Kane et al., 2022). However, because these dynamics are co-occurring in soil environments, influencing soil carbon storage interactively, linking them to overall soil carbon storage remains a complex feat. Observations like those presented by Zhang et al. (2024b) are exciting because they could potentially be integrated into models to represent the influence of interactions between plants and soil organisms. Such data could further improve model predictions that seek to include microbial controls on soil organic matter pools (e.g. Sulman et al., 2014; Wieder et al., 2015). This would be a clear step forward in expanding models to include the influence of soil fauna like nematodes, an area of need that has been conceptually identified (Grandy et al., 2016; Fry et al., 2019). Additionally, the trait-based perspective presented by Zhang et al. (2024b) could be leveraged to facilitate quantitative soil organic carbon (SOC) estimation across scales by utilizing global trait databases (Kattge et al., 2011). Future work that expands these efforts across biomes could further implement the integrated fast–slow plant and nematode economics spectrum, aiding in larger scale predictions of soil carbon storage.

The recent manuscript by Zhang et al. (2024b) aids in filling key knowledge gaps, all while bringing to light exciting areas of future research. While this work eloquently argues that nematode traits like body mass, length, and diameter are strongly associated with plant traits to explain carbon cycling, it is important to note that nematode trophic habits also play a critical role in explaining soil nutrient fluxes and carbon dynamics (Bååth et al., 1981; Kane et al., 2022). For example, nematode trophic groups can influence the sequestration or degradation of SOC by regulating the composition and functionality of mycorrhizal and saprotrophic communities in the rhizosphere (Jiang et al., 2020). Considering the feeding habits of soil animals in the context of soil carbon accumulation poses interesting questions about how trophic interactions in the rhizosphere affect the formation and persistence of labile (particulate organic matter) and stabilized (mineral-associated organic matter) SOC pools. Classifying nematodes and other soil animals according to their trophic habits in similar experimental designs to the recent work by Zhang et al. (2024b) may bring additional explanatory power to soil carbon dynamics, especially when considered alongside plant and microbial traits.

The recent work by Zhang et al. (2024b) presents a strong study focusing on the ecological strategies of plants and nematodes as they relate to the community-wide carbon cycling of the microbial community and, therefore, soil carbon pools. While their approach was effective in explaining soil carbon dynamics, categorizing this community by their ecological strategies could be of great use as well. Soil microbial communities contain diverse communities of fungi, bacteria, and archaea. One gram of soil is thought to contain thousands of bacterial taxa comprising billions of bacterial cells, only a small fraction of which have been cultivated and studied in the laboratory (Roesch et al., 2007). The microscopic nature of these organisms and their vast phylogenetic and metabolic diversity make measuring and conceptualizing their traits challenging. Several recent frameworks have sought to do this with the goal of feasibly and accurately incorporating microbial carbon cycling into ecosystem models. For example, Malik et al. (2020) classify microbial taxa based on trade-offs between growth yield, nutrient acquisition, and stress tolerance, and Morrissey et al. (2023) categorize taxa based on their carbon source (plant material, dead microbial biomass, dissolved organic carbon, or live microbial biomass). These conceptual frameworks could potentially integrate with those like Zhang et al. (2024b) present in their recent article, together strengthening predictions of global carbon cycling. Connecting the fast–slow plant and nematode trait spectrum with the yield-resource acquisition-stress tolerance (Y-A-S) framework presented in Malik et al. (2020) with the restoration chronosequence presented in Zhang et al.'s (2024b) experiment could aid in resolving a mechanistic understanding SOC dynamics. For example, at the pioneer stage, high-quality litter input could fuel decomposition primarily by fast-growing microbial saprotrophs with high-growth yield traits. This could potentially promote the dominance of r-strategist nematodes (bacterivores and fungivores), which could increase SOC mineralization as CO₂. By contrast, at the climax stage, complex low-quality litter input might favor oligotrophic microbial communities that invest more in resource acquisition traits, leading to the dominance of k-strategist nematodes (e.g. omnivores and predators). This may result in slower SOC mineralization and an increase in SOC stocks.

All told, the new publication by Zhang et al. (2024b) showcases an elegant example of a pressing experimental need in the field of global change ecology – that is, to quantitatively relate interactions between plants and soil organisms to soil carbon storage. In the future, expanding upon this to also integrate bacterial, fungal, and archaeal life strategies may even further advance our understanding of the global carbon cycle and allow for increased accuracy when predicting future environmental scenarios.