Diversity in growth patterns among strains of the lethal fungal pathogen Batrachochytrium dendrobatidis across extended thermal optima

Abstract

The thermal sensitivities of organisms regulate a wide range of ecological interactions, including host-parasite dynamics. The effect of temperature on disease ecology can be remarkably complex in disease systems where the hosts are ectothermic and where thermal conditions constrain pathogen reproductive rates. Amphibian chytridiomycosis, caused by the pathogen Batrachochytrium dendrobatidis (Bd), is a lethal fungal disease that is influenced by temperature. However, recent temperature studies have produced contradictory findings, suggesting that our current understanding of thermal effects on Bd may be incomplete. We investigated how temperature affects three different Bd strains to evaluate diversity in thermal responses. We quantified growth across the entire thermal range of Bd, and beyond the known thermal limits (T _max and T _min). Our results show that all Bd strains remained viable and grew following 24 h freeze (-12 °C) and heat shock (28 °C) treatments. Additionally, we found that two Bd strains had higher logistic growth rates (r) and carrying capacities (K) at the upper and lower extremities of the temperature range, and especially in low temperature conditions (2-3 °C). In contrast, a third strain exhibited relatively lower growth rates and carrying capacities at these same thermal extremes. Overall, our results suggest that there is considerable variation among Bd strains in thermal tolerance, and they establish a new thermal sensitivity profile for Bd. More generally, our findings point toward important questions concerning the mechanisms that dictate fungal thermal tolerances and temperature-dependent pathogenesis in other fungal disease systems.

Keywords: Amphibian chytridiomycosis; Batrachochytrium dendrobatidis; Disease ecology; Psychrophilic fungi; Temperature.

Fig. 1

A model of the classical phases of microbial growth (lag phase, exponential phase and stationary phase) for the fungal pathogen Batrachochytrium dendrobatidis (Bd). Curves represent the growth, measured by optical density (OD), of Bd in two temperatures: 21 °C (dashed line) and 4 °C (solid line)

Fig. 2

A model of the relationship between temperature and exponential growth rate (r) of the lethal fungal pathogen Batrachochytrium dendrobatidis (Bd). The lines represent an example of r for Bd in two temperatures: 21 °C (dashed line) and 4 °C (solid line)

Fig. 3

Growth of three strains of Batrachochytrium dendrobatidis (Bd) representing different phylogenetic clades: CJB5-2 or “Temperate” (a), LFT or “Tropical” (b) and UM-142 or “Bullfrog” (c). Growth was measured by optical density (OD) following either a 12 h freeze shock treatment (solid shapes, solid lines) or maintained at 21 °C (open shapes, dashed lines)

Fig. 4

Growth of three strains of Batrachochytrium dendrobatidis (Bd) representing different phylogenetic clades: CJB5-2 or “Temperate’’ (a), LFT or “Tropical” (b) and UM-142 or “Bullfrog” (c). Growth was measured by optical density (OD) following either a 12 h heat shock treatment at 28 °C (solid shapes) or maintained at 21 °C (control; open shapes). Note that for the Bullfrog strain the control and heat shock treatments behave in the same way (i.e., a model with both fit as one curve is preferred by DIC)

Fig. 5

Thermal breadth expressed in terms of a Logistic growth rate (r) and b area under the curve (AUC) for three strains of Batrachochytrium dendrobatidis (Bd) representing different phylogenetic clades. CJB5-2 or “Temperate” (solid line, open circles), LFT or “Tropical” (dashed line, open triangles) and UM-142 or “Bullfrog” (dotted lines and open diamonds) across temperatures (2–28 °C). Asterisks (*) indicate the optima for each strain