Phosphorus deficiencies invoke optimal allocation of exoenzymes by ectomycorrhizas

Abstract

Ectomycorrhizal (EM) fungi can acquire phosphorus (P) through the production of extracellular hydrolytic enzymes (exoenzymes), but it is unclear as to the manner and extent native EM fungal communities respond to declining soil P availability. We examined the activity of six exoenzymes (xylosidase, N-acetyl glucosaminidase, β-glucosidase, acid phosphomonoesterase, acid phosphodiesterase [APD], laccase) from EM roots of Pseudotsuga menzesii across a soil podzolization gradient of coastal British Columbia. We found that APD activity increased fourfold in a curvilinear association with declining inorganic P. Exoenzyme activity was not related to organic P content, but at a finer resolution using 31P-NMR, there was a strong positive relationship between APD activity and the ratio of phosphodiesters to orthophosphate of surface organic horizons (forest floors). Substantial increases (two- to fivefold) in most exoenzymes were aligned with declining foliar P concentrations of P. menzesii, but responses were statistically better in relation to foliar nitrogen (N):P ratios. EM fungal species with consistently high production of key exoenzymes were exclusive to Podzol plots. Phosphorus deficiencies in relation to N limitations may provide the best predictor of exoenzyme investment, reflecting an optimal allocation strategy for EM fungi. Resource constraints contribute to species turnover and the assembly of distinct, well-adapted EM fungal communities.

Root phosphatase activity aligns with the collaboration gradient of the root economics space

“…S5), which differed from the findings of previous studies that pointed to soil P availability and leaf P stoichiometry as the major influences on phosphatase activity (Ushio et al ., 2015; Zemunik et al ., 2015; Cabugao et al ., 2017). At community level, it has been reported that RPA correlates negatively with soil available P content (Kitayama, 2013; Cabugao et al ., 2017; Meeds et al ., 2021). At species level, plants situated within a low‐P site generally exhibit higher RPA values than those situated within a high‐P site (Guilbeault‐Mayers et al ., 2020).…”

“…S8; Guo et al ., 2008; Kong et al ., 2014). The mycorrhizal partner enhances the ability of plants with thick roots to compete in P‐impoverished environments by forming an external mycelium and/or exuding carboxylates and exoenzymes to increase exploration, mobilization and absorption of inorganic P (Lambers et al ., 2008; Ding et al ., 2021; Meeds et al ., 2021). In line with our second hypothesis, the marked negative relationship between RPA and RMC suggested a trade‐off in P‐acquisition strategies across species, as reported by a recent study of just four tropical tree species (Nasto et al ., 2017).…”

Manganese limitations and the enhanced soil carbon sequestration of temperate rainforests

“…Mycorrhizal fungi provide an important source of C to forest soils (Frey 2019), but given the historic uniformity in stand composition these differential patterns in SOC are unlikely to re ect mycorrhizal type per se as described elsewhere (Taylor et al 2016;Craig et al 2018). It should be noted, however, that ectomycorrhizal fungal communities were equally distinct as saprotrophic communities between soil types, in part due to adaptations required for organic phosphorus (P) acquisition on Podzols (Meeds et al 2021). While select ectomycorrhizal species of Podzols displayed some capacity for laccase production (Meeds et al 2021), other ectomycorrhizal genera more common to Brunisols, such as Cortinarius and Piloderma, could potentially contribute alongside saprotrophic fungi to the differences in peroxidase activity of these substrates, thereby supplementing the long-term oxidation rates of SOC (Bödeker et al 2014;Sterkenburg et al 2018).…”

Ectomycorrhizal fungal decay traits along a soil nitrogen gradient

“…Ectomycorrhizal (ECM) fungi, in particular, dominate boreal and temperate forest soil microbial communities, providing plant hosts with the majority of their annual nitrogen (N) requirements (c. 70%) (Smith & Read, 2010). Despite being one of the most studied microbial groups, understanding of the distribution of ECM fungal traits remain poorly understood (Courty et al, 2016;van der Linde et al, 2018;Meeds et al, 2021). One prominent ECM fungal functional trait is the acquisition of N bound in soil organic matter (N-SOM), which constitutes the majority of soil N (Vitousek & Howarth, 1991).…”

“…Biological market perspectives provide insight into how N availability and fungal N acquisition traits may interact to structure these communities (Koide et al, 2014;Christian & Bever, 2018). Plants may partner with fungal mutualists that maximize N (or phosphorus) acquisition, while minimizing photosynthate expenditure (Hortal et al, 2017;Bogar et al, 2019;Meeds et al, 2021). Comparative genomic analyses suggest that ECM fungal decay potential varies widely across the c. 80 independent evolutionary originations of the ECM fungal lifestyle (Kohler et al, 2015;Shah et al, 2016;Pellitier & Zak, 2018).…”