Plasticity and constraint in growth and protein mineralization of ectomycorrhizal fungi under simulated nitrogen deposition

Abstract

Ectomycorrhizal fungi allow their host plants access to organic forms of N through enzymatic mineralization of the substrate and enhanced absorption of amino acids and mineral N. The cost to the plant is carbohydrates that support fungal growth and metabolism. Enrichment of soils with mineral N, as through atmospheric deposition, may affect the growth and function of these fungi by direct effects of increased N availability on fungi and indirect effects through reduced plant C allocation to roots. We tested the potential of N enrichment and altered carbohydrate supply to affect the growth and protein mineralization activity of 10 ectomycorrhizal fungi in sterile liquid media. Nitrogen treatments consisted of organic N only vs organic plus mineral N. Carbon treatments consisted of 5 g per liter glucose vs. no glucose added. Fungi differed widely in their growth and mineralization responses to these variables. Seven of 10 fungi had at least 20% reduced growth with reduced carbohydrates. Only 2 of 10 increased growth by 20% or more with increased mineral N. Carbohydrates affected growth more in a purely organic N environment suggesting an energy limitation to mineralization. Protein mineralization activity tended to be depressed by reductions in carbohydrates and increased by increased mineral N. The high sensitivity of fungal growth to carbohydrates suggests important indirect effects of N enrichment via altered C allocation in host trees. Principal Components analysis separated most fungal species along an axis representing a gradient from high protein mineralization efficiency to high intrinsic growth rate. Those fungi with slow growth and efficient mineralization activity corresponded closely to fungi often cited as late successional species, while fungi with high growth rates and low mineralization efficiency are often categorized as early successional. One fungus, Cenococcum geophillum, separated from others on an axis representing strong N dependence in growth. Nitrogen enrichment has the potential to alter the composition and function of the ectomycorrhizal fungus community. Physiological differences among species provide a starting point for predicting community responses and anticipating ecosystem consequences.

Forests trapped in nitrogen limitation – an ecological market perspective on ectomycorrhizal symbiosis

“…A plant's strategy in the model is defined by its C allocation to EMF ( C f ), which in effect regulates the trade‐off between C investments in N uptake (via EMF) and C use for growth. A fungus strategy is defined by its ratio ( u ) of C allocation to reproductive growth versus N uptake components, in line with the observed trade‐off between intrinsic growth rate and potential N uptake capacity (measured as efficiency of protein mineralization) among EMF species (Eaton & Ayres, ). Changes in u may reflect both phenotypic plasticity and changes in active EMF community (species) composition.…”

Diversity and Enzyme Activity of Ectomycorrhizal Fungal Communities Following Nitrogen Fertilization in an Urban-Adjacent Pine Plantation

“…Most ECM fungal taxa produce a diversity of extracellular and cell wall-bound hydrolytic and oxidative enzymes that mobilize the release of smaller organic molecules (potential C, N, or P sources) from soil organic matter (SOM) [17], including polyphenol-protein complexes. Studies have revealed substantial interspecific differences in ECM enzymatic activities [18][19][20][21][22][23][24][25][26][27][28]. Such differences can be predicted in part by ECM life history strategies.…”

“…Ectomycorrhizal fungi may respond to shortages in host C allocation by up-regulating the activity of enzymes used to obtain labile carbohydrates [13], while changes in the relative availabilities of N and P are known to modify the activity of extracellular N-and P-mobilizing enzymes. For example, N fertilization could accelerate the degradation of easily decomposable litter and reduce the activity of extracellular ECM enzymes targeting recalcitrant litter with high levels of lignin and complex organic forms of N [24][25][26][27][28]. Both outcomes may reflect the stimulation or repression of different sets of enzymes.…”

Long‐term increase in nitrogen supply alters above‐ and below‐ground ectomycorrhizal communities and increases the dominance ofRussulaspp. in a temperate oak savanna

“…N is an essential nutrient for EMF (Smith & Read, 1997) but is spatially, temporally and chemically heterogeneous in soil (Robertson et al ., 1988; Cain et al ., 1999). This may have selected EMF to evolve diverse N extraction and utilization traits and is consistent with culture experiments showing that different species of EMF have different growth responses to different forms and levels of N (Dickie et al ., 1998; Eaton & Ayers, 2002; Lilleskov et al ., 2002b). Soils at Cedar Creek are N impoverished and, as in many terrestrial ecosystems, plant growth is limited by N supply (Tilman, 1987).…”