Host and Aquatic Environment Shape the Amphibian Skin Microbiome but Effects on Downstream Resistance to the Pathogen Batrachochytrium dendrobatidis Are Variable

Abstract

Symbiotic microbial communities play key roles in the health and development of their multicellular hosts. Understanding why microbial communities vary among different host species or individuals is an important step toward understanding the diversity and function of the microbiome. The amphibian skin microbiome may affect resistance to the fungal pathogen Batrachochytrium dendrobatidis (Bd). Still, the factors that determine the diversity and composition of the amphibian skin microbiome, and therefore may ultimately contribute to disease resistance, are not well understood. We conducted a two-phase experiment to first test how host and environment shape the amphibian skin microbiome, and then test if the microbiome affects or is affected by Bd infection. Most lab experiments testing assembly of the amphibian skin microbiome so far have compared sterile to non-sterile environments or heavily augmented to non-augmented frogs. A goal of this study was to evaluate, in an experimental setting, realistic potential drivers of microbiome assembly that would be relevant to patterns observed in nature. We tested effects of frog genetic background (2 source populations) and 6 natural lake water sources in shaping the microbiome of the frog Rana sierrae. Water in which frogs were housed affected the microbiome in a manner that partially mimicked patterns observed in natural populations. In particular, frogs housed in water from disease-resistant populations had greater bacterial richness than frogs housed in water from populations that died out due to Bd. However, in the experiment this difference in microbiomes did not lead to differences in host mortality or rates of pathogen load increase. Frog source population also affected the microbiome and, although none of the frogs in this study showed true resistance to infection, host source population had a small effect on the rate of pathogen load increase. This difference in infection trajectories could be due to the observed differences in the microbiome, but could also be due to other traits that differ between frogs from the two populations. In addition to examining effects of the microbiome on Bd, we tested the effect of Bd infection severity on the microbiome. Specifically, we studied a time series of the microbiome over the course of infection to test if the effects of Bd on the microbiome are dependent on Bd infection severity. Although limited to a small subset of frogs, time series analysis suggested that relative abundances of several bacterial phylotypes changed as Bd loads increased through time, indicating that Bd-induced disturbance of the R. sierrae microbiome is not a binary effect but instead is dependent on infection severity. We conclude that both host and aquatic environment help shape the R. sierrae skin microbiome, with links to small changes in disease resistance in some cases, but in this study the effect of Bd on the microbiome was greater than the effect of the microbiome on Bd. Assessment of the microbiome differences between more distantly related ...

Microbial associations and spatial proximity predict North American moose (Alces alces) gastrointestinal community composition

“…Jani & Briggs, ; Mshelia et al, ). Host characteristics such as sex, body condition and the presence or absence of pathogens are recognized as important for shaping microbial communities (Britton & Young, ; Cheng et al, ; Ganz et al, ; Hooper, Littman, & Macpherson, ; Jani & Briggs, , ; McKenney et al, ; Mshelia et al, ; Näpflin & Schmid‐Hempel, ). For example, horses in poor body condition have greater microbial diversity and a different suite of microbial species present compared to horses in good body condition (Mshelia et al, ).…”

“…For example, horses in poor body condition have greater microbial diversity and a different suite of microbial species present compared to horses in good body condition (Mshelia et al, ). High loads of the pathogen Batrachochytrium dendrobatidis can not only increase amphibian skin microbial diversity but also alter microbial composition (Jani & Briggs, , ). Microbial community structure is also likely to be shaped by dispersal or transmission as physical distance between hosts can produce barriers to gut microbe transmission that accelerate compositional divergence (Moeller et al, ).…”

Population dynamics ofRana sierraeat Dusy Basin: influence of non‐native predators, drought, and restoration potential

“…Important to reintroduction efforts is the observation that different frog species show varying degrees of susceptibility to chytridiomycosis (Fisher et al 2009). Sierra Nevada yellow-legged frogs are one of the most well-studied systems to give insight into chytridiomycosis progression and the role of the host microbiome on disease outcome in the wild (Jani and Briggs 2018). This variation has recently also been shown to exist across populations of R. sierrae (Joseph and Knapp 2018).…”

“…Eventually, this detrimental Bd strain made its way into one of the most remote environments of North America, the Dusy Basin within Kings Canyon National Park (Olson et al 2013). The population decline due to Bd spanned two full years before all adult individuals disappeared with relatively high infection intensity and load (Jani 2014, Jani andBriggs 2018). One such local extirpation occurred within Dusy Basin where we had been monitoring R. sierrae populations since 1997.…”

Fungal infection alters the selection, dispersal and drift processes structuring the amphibian skin microbiome

“…The amphibian skin microbiome has been proposed as a potential protective factor against chytridiomycosis (Harris et al, ; Becker & Harris, ). While studies have found a clear association between the composition of the amphibian microbiome and population‐level outcomes of Bd invasion (Jani et al, ; Bates et al, ), the demonstrable effect of the amphibian skin microbiome as a protective mechanism against Bd infection has been variable (Harris et al, ; Woodhams et al, ; Jani & Briggs, ). Field and laboratory results suggest that the magnitude of the Bd effect on microbiome can be greater than the magnitude of the microbiome effect on Bd (if any) (Jani & Briggs, ,, ).…”