Phenotypic plasticity of fungal traits in response to moisture and temperature

Abstract

Phenotypic plasticity of traits is commonly measured in plants to improve understanding of organismal and ecosystem responses to climate change but is far less studied for microbes. Specifically, decomposer fungi are thought to display high levels of phenotypic plasticity and their functions have important implications for ecosystem dynamics. Assessing the phenotypic plasticity of fungal traits may therefore be important for predicting fungal community response to climate change. Here, we assess the phenotypic plasticity of 15 fungal isolates (12 species) from a Southern California grassland. Fungi were incubated on litter at five moisture levels (ranging from 4-50% water holding capacity) and at five temperatures (ranging from 4-36 °C). After incubation, fungal biomass and activities of four extracellular enzymes (cellobiohydrolase (CBH), β-glucosidase (BG), β-xylosidase (BX), and N-acetyl-β-D-glucosaminidase (NAG)) were measured. We used response surface methodology to determine how fungal phenotypic plasticity differs across the moisture-temperature gradient. We hypothesized that fungal biomass and extracellular enzyme activities would vary with moisture and temperature and that the shape of the response surface would vary between fungal isolates. We further hypothesized that more closely related fungi would show more similar response surfaces across the moisture-temperature gradient. In support of our hypotheses, we found that plasticity differed between fungi along the temperature gradient for fungal biomass and for all the extracellular enzyme activities. Plasticity also differed between fungi along the moisture gradient for BG activity. These differences appear to be caused by variation mainly at the moisture and temperature extremes. We also found that more closely related fungi had more similar extracellular enzymes activities at the highest temperature. Altogether, this evidence suggests that with global warming, fungal biodiversity may become increasingly important as functional traits tend to diverge along phylogenetic lines at higher temperatures.

Fig. 1. Conceptual figure of hypotheses and example.

A Conceptual figure demonstrating traits as a function of both environmental (temperature and moisture) and genetic properties. Temperature and moisture are independent variables and the trait values are the dependent variables. Maximum trait values are in pink and minimum values are blue. We predicted that across fungal isolates, point values (i.e., enzyme activity or biomass at a given temperature and moisture level) should vary with temperature and moisture (Hypothesis 1). In addition, plasticity traits (i.e., enzyme responses or biomass across the temperature-moisture gradient) should vary between fungal isolates (Hypothesis 2). We also predicted that more similar fungi should exhibit more similar point values at specific points along with the moisture and temperature gradient (Hypothesis 3). B Examples of three response surfaces for N-acetyl-β-D-glucosaminidase (NAG). The numbers on the plot (panel B) represent the values of the contour lines (values are logged). In this example, the point values from the three different isolates are similar in the center of the response surface. However, moving to the edges of the temperature gradient, NAG activity for Coprinellus aff xanthotrhis (phylum Basidiomycota) diverges from Trichoderma koningii (phylum Ascomycota) and Sarocladium implicatum (phylum Ascomycota), the more phylogenetically similar species. The phylogeny for all of the fungi used in this experiment is in Figure S1.

Fig. 2. Response surface plots.

Contour plots of log-transformed data for the average activities of all of the isolates for (A) cellobiohydrolase (CBH), (B) β-glucosidase (BG), (C) β-xylosidase (BX), and (D) N-acetyl-β-D-glucosaminidase (NAG), and (E) fungal biomass across the moisture-temperature gradient (n = 18 for each response surface). Each response surface is on a separate scale, as indicated by the numbers on the lines on each contour plot. All maximum values are pink, and all minimum values are blue. The small black circles indicate incubation conditions. Response surfaces for each fungal isolate individually can be found in Figures S2–S6.

Fig. 3. Heat map representing the strength of the phylogenetic signal.

(A) cellobiohydrolase (CBH), (B) β-glucosidase (BG), (C) β-xylosidase (BX), and (D) N-acetyl-β-D-glucosaminidase (NAG), and (E) fungal biomass across the moisture-temperature gradient (n = 12 for each P-value). The color gradient signifies the P-value (unadjusted) associated with Blomberg’s K test at each specific point on the moisture-temperature gradient, with blue values indicating a significant phylogenetic signal (P < 0.05). The numbers in each colored box represent the P-value at that specific moisture × temperature combination.