Diverse genotypes of the amphibian‐killing fungus produce distinct phenotypes through plastic responses to temperature

Abstract

Phenotypes are the target of selection and affect the ability of organisms to persist in variable environments. Phenotypes can be influenced directly by genes and/or by phenotypic plasticity. The amphibian‐killing fungus Batrachochytrium dendrobatidis (Bd) has a global distribution, unusually broad host range, and high genetic diversity. Phenotypic plasticity may be an important process that allows this pathogen to infect hundreds of species in diverse environments. We quantified phenotypic variation of nine Bd genotypes from two Bd lineages (Global Pandemic Lineage [GPL] and Brazil) and a hybrid (GPL‐Brazil) grown at three temperatures (12, 18 and 24°C). We measured five functional traits including two morphological traits (zoospore and zoosporangium sizes) and three life history traits (carrying capacity, time to fastest growth and exponential growth rate) in a phylogenetic framework. Temperature caused highly plastic responses within each genotype, with all Bd genotypes showing phenotypic plasticity in at least three traits. Among genotypes, Bd generally showed the same direction of plastic response to temperature: larger zoosporangia, higher carrying capacity, longer time to fastest growth and slower exponential growth at lower temperatures. The exception was zoospore size, which was highly variable. Our findings indicate that Bd genotypes have evolved novel phenotypes through plastic responses to temperature over very short timescales. High phenotypic variability likely extends to other traits and may facilitate the large host range and rapid spread of Bd.

Temperature‐mediated shifts in salamander transcriptomic responses to the amphibian‐killing fungus

“…Indeed, expression profiling of Xenopus tropicalis revealed differential activation of innate immune genes in response to infection at two temperatures (Ribas et al, ). However, despite evidence of temperature‐dependent survival in salamanders (Muletz‐Wolz, Barnett, et al, ; Muletz‐Wolz, Fleischer, et al, ; Vazquez et al, ), we do not yet have any study of temperature‐dependent gene expression responses of salamanders to Bd . More broadly, we have limited knowledge of how salamander immune expression responses to Bd infection — regardless of temperature—compare to those in anurans (Farrer et al, ).…”

“…In some species, underlying individual thermal preferences may be a predictor of infection susceptibility (Sauer et al, ), while in others ectotherm behavioural fever (active preference for warmer environments) appears to be important in enhancing survival during infections (Boltana et al, ). Widespread thermal‐dependence of parasite and pathogen life‐history traits (Bakke, Cable, & Harris, ; Muletz‐Wolz, Barnett, et al, ; Muletz‐Wolz, Fleischer, & Lips, ; Voyles et al, ) indicates that temperature is key to understanding infection processes and disease dynamics in ectotherm hosts.…”

“…Plethodon cinereus is well studied with respect to chytrid infections, typically exhibiting low Bd infection prevalence in the wild (Muletz et al, ), and capable of clearing moderate laboratory experimental infections (Muletz, Myers, Domangue, Herrick, & Harris, ). This species is a popular model for studying the protective role of commensal skin microbiota against Bd infection (e.g., Harris, Lauer, Simon, Banning, & Alford, ; Loudon et al, ; Muletz Wolz, Yarwood, Campbell Grant, Fleischer, & Lips, ; Muletz‐Wolz, Barnett, et al, ). However, we do not know their functional genetic responses to infection that control disease outcomes, especially under variable temperatures.…”

Fungal disease and temperature alter skin microbiome structure in an experimental salamander system

“…For instance, amphibian biodiversity is threatened by two deadly chytrid fungi, Batrachochytrium dendrobatidis (Bd) and its sister taxon B. salamandrivorans (Bsal), with differences in host responses that can depend on temperature (Berger et al, ; Blooi et al, ; Bustamante, Livo, & Carey, ; Murphy, St‐Hilaire, & Corn, ; Sauer et al, ). Temperature is an important environmental factor that directly affects Bd and Bsal growth and survival (Martel et al, ; Muletz‐Wolz et al, ). However, host properties may mediate the effects of temperature on Batrachochytrium growth and include: host skin shedding rate (Cramp, McPhee, Meyer, Ohmer, & Franklin, ), host immune response (Ribas et al, ) and host microbiome composition (Longo & Zamudio, ; Muletz‐Wolz, Almario, et al, ; Robak & Richards‐Zawacki, ).…”

Designing Probiotic Therapies With Broad-Spectrum Activity Against a Wildlife Pathogen

“…It would be particularly interesting to investigate whether clusters of inhibition-resistant genotypes cluster spatially and/or align with particular environmental conditions. Recent in vitro work has highlighted that abiotic conditions such as temperature can both affect the efficacy of bacterial probiotics against Bd (Muletz-Wolz et al, 2017) and virulence traits of the pathogen such as growth rate of zoosporangia (Muletz-Wolz et al, 2019). These studies suggest that although we have achieved relatively consistent inhibition across multiple pathogen genomic variants in this study under controlled laboratory conditions, the true emergent properties of probiotics in nature will instead be function of pathogen genome, probiotic genome(s), and environment interactions (GxGxE), which makes predicting FIGURE 5 | (A) Inhibition scores for single-genus probiotics of increasing complexity from single to three-isolate consortia, split by Bd isolate.…”