The role of ectomycorrhizal functional diversity in mediating soil carbon cycling under global change

Instead of expecting a consistent response of ectomycorrhizal-mediated soil C input and output processes to global change, we are likely to be confronted with a set of diverging responses of a functionally diverse ectomycorrhizal fungal community... High functional diversity is rooted in the evolutionary history of ECM fungi. ECM fungi independently evolved from > 80 lineages of saprotrophic ancestors (Tedersoo & Smith, 2017). As a result, ECM fungi are highly diverse with respect to traits influencing both soil C inputs and outputs. ECM fungal traits relevant for soil C inputs include their influence on plant growth and belowground C allocation (Bunn et al., 2024; Anthony, 2025), which may be affected by physiological processes as well as the extension, hydrophobicity, and chemistry of extraradical mycelium (Agerer, 2001). These same mycelium traits are relevant for soil C loss. Rates of growth, respiration, and turnover influence necromass production, while mycelium features, like rhizomorph and melanin production, add to the chemical recalcitrance of soil organic matter (Certano et al., 2018). The genomic capacity of ECM fungi to produce enzymes that decompose plant and microbial cell wall proteins, and take up and transport nitrogen and phosphorus, is exceptionally divergent across ECM fungi (Fig. 2), and differential expression of these genes can influence plant–ECM fungal resource exchange (Plett et al., 2024). Building upon a body of earlier research comparing differences among Pisolithus species, Carrillo et al. demonstrate that we must be careful to consider the functional differences of ECM fungal species when evaluating soil C cycling responses to elevated CO2. Carrillo et al. compared two closely related species, Pisolithus albus and Pisolithus microcarpus, associated with eucalypt host trees. Despite being genetically closely related, the two ECM fungal species are known to differ in their symbiotic behaviour, N and C metabolism, enzymatic capabilities to degrade SOM, and responses to N and CO2 conditions (e.g. Plett et al., 2022, 2024). The present study went beyond earlier characterisations of the two species and demonstrates that they also differentially mediate soil C turnover. While both fungi decreased plant-derived soil C (likely a consequence of these ECM fungi also decreasing plant growth), only P. albus decreased soil-derived C and, in turn, total soil C. The contrasting effects of the two fungi on soil-derived C were even more pronounced under elevated CO2. This indicates that P. albus accelerated the loss of native soil C while P. microcarpus did not and that elevated CO2 amplified this difference. Interestingly, it was only P. albus which increased plant-derived dissolved organic C in the soil under elevated CO2. These findings could allow us to speculate that the negative effect of P. albus on soil C stock was mediated by some kind of priming effect, which was not the case for P. microcarpus. The involvement of ECM in priming effects is one of the least well-understood functional traits of ECM fungi. While there has been a large focus on the capacities of ectomycorrhizal fungi in slowing soil C cycling through negative interactions with saprotrophs (i.e. the Gadgill effect), more recent work suggests that ectomycorrhizal fungi generally stimulate soil C loss via priming (Choreño-Parra & Treseder, 2024). Even further, it has been shown that ECM fungi select for a specific bacterial community at the species level (Dietrich et al., 2022). Such a preference/selection could facilitate a fungal species-specific activation of a specific cohort of saprotrophs. This emphasises that we not only need to understand the more obvious functional traits of individual ECM fungi (as listed above; see also Fig. 2) but also the more difficult-to-measure traits involved in mediating interactions between ECM fungi and other members of the soil microbiome. The net effect of global change on soil C storage depends on the balance of C inputs and outputs. Does elevated CO2 and other global change factors increase C inputs more than it increases potential ECM-fungi mediated effects on C outputs? This likely depends on various concurrent drivers of global change (temperature, eCO2, and moisture) as well as the ecosystem type and local soil properties (i.e. N availability). While models strive to find a simplification to incorporate ECM fungi to better predict future C budgets (e.g. Sulman et al., 2019), the study by Carrillo et al. provides a first glimpse into a potentially more complicated reality. Combining these findings with known functional variation among ECM fungi, described using microbiological and genomic tools such as whole genome comparisons and metatranscriptomics, we can expect a considerable variation of functional effect and response types to global change across ECM fungal species. That means that not only ECM fungi but also ECM fungal community composition and species identity likely play a role in soil C responses to elevated CO2. Instead of expecting a consistent response of ectomycorrhizal-mediated soil C input and output processes to global change, we are likely to be confronted with a set of diverging responses of a functionally diverse ECM fungal community, each with unknown directions and unknown potential for synergistic and antagonistic interactions among them (Fig. 1b). The question will then be: can we see a general trend of a stronger effect on one or the other, input or output processes? And also, which ECM fungi are favoured by future climate conditions, and how would a potential community shift among ECM fungi shape ecosystem C balance? One key to understanding general and species-specific ECM impacts on soil C turnover is to distinguish among different soil C processes, such as the addition and cycling of plant-derived C or losses of the native soil C pool. Carrillo et al. addressed this using a continuous 13CO2 labelling technique, which allowed them to detect effects of ECM fungal isolates on the native soil C pool after 4 months of plant growth. Their prior genomic and microbiological investigations to characterise fine-scale differences between ECM fungal species enabled this newest discovery, and it suggests we may be able to do similar for other ECM fungi. While their work did not aim to evaluate long-term dynamics and potential ecosystem feedbacks, these can be addressed by Free-Air Carbon Dioxide Enrichment (FACE) experiments, which are long-term and deliver valuable insights into whole ecosystem C level responses to elevated CO2 (Terrer et al., 2018). Combining such experiments with close monitoring of ECM fungal community composition over time could shed new light on the role of ECM fungi functional composition and diversity. Measuring the specific responses of ECM fungal species from ambient and elevated CO2 plots, under different conditions, and using similar methodologies as Carrillo et al. would offer a more comprehensive understanding of the possible responses and mechanisms driving divergent soil C cycling outcomes under elevated CO2. In the end, it is the net effect on soil C stocks that matters, but this will be orchestrated by a functionally highly diverse community of ectomycorrhizal fungi. Genome data was produced by the U.S. Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, supported by the Office of Science of the U.S. Department of Energy under Contract No. DE-AC02-05CH11231. This work was supported by the Austrian Science Fund (FWF) (doi: 10.55776/COE7). The New Phytologist Foundation remains neutral with regard to jurisdictional claims in maps and in any institutional affiliations.