The amphibian microbiome exhibits poor resilience following pathogen-induced disturbance

Andrea J Jani,Cédric G Arisdakessian,Daniel M Boiano,Cathy Brown,Mahdi Belcaid,Roland A Knapp,Jessie Bushell

doi:10.1038/s41396-020-00875-w

Abstract

Infectious pathogens can disrupt the microbiome in addition to directly affecting the host. Impacts of disease may be dependent on the ability of the microbiome to recover from such disturbance, yet remarkably little is known about microbiome recovery after disease, particularly in nonhuman animals. We assessed the resilience of the amphibian skin microbial community after disturbance by the pathogen, Batrachochytrium dendrobatidis (Bd). Skin microbial communities of laboratory-reared mountain yellow-legged frogs were tracked through three experimental phases: prior to Bd infection, after Bd infection (disturbance), and after clearing Bd infection (recovery period). Bd infection disturbed microbiome composition and altered the relative abundances of several dominant bacterial taxa. After Bd infection, frogs were treated with an antifungal drug that cleared Bd infection, but this did not lead to recovery of microbiome composition (measured as Unifrac distance) or relative abundances of dominant bacterial groups. These results indicate that Bd infection can lead to an alternate stable state in the microbiome of sensitive amphibians, or that microbiome recovery is extremely slow—in either case resilience is low. Furthermore, antifungal treatment and clearance of Bd infection had the additional effect of reducing microbial community variability, which we hypothesize results from similarity across frogs in the taxa that colonize community vacancies resulting from the removal of Bd. Our results indicate that the skin microbiota of mountain yellow-legged frogs has low resilience following Bd-induced disturbance and is further altered by the process of clearing Bd infection, which may have implications for the conservation of this endangered amphibian.

Highlights

Ecological communities exist in dynamic environmental landscapes, and experience changes ranging from regular incremental shifts such as light and nutrient gradients to large scale disturbances such as disease outbreaks or storm events
Batrachochytrium dendrobatidis (Bd) infection altered microbiome composition on frogs: post-infection, the microbiota of Bd+ and Bd− frogs differed in composition (PERMANOVA, P < 0.001, Fig. 1B, Table S6) but not alpha diversity (P > 0.05 for all metrics, Table S7) or dispersion (BETADISPER P = 0.880, Fig. 1B, Table S4)
We found that Bd infection altered the microbiota as expected, but clearing infection did not lead to recovery of the original bacterial community structure

Summary

Introduction

Ecological communities exist in dynamic environmental landscapes, and experience changes ranging from regular incremental shifts such as light and nutrient gradients to large scale disturbances such as disease outbreaks or storm events. Disturbance can alter the structure of ecological communities: it can maintain long term community diversity [1], but can degrade community or ecosystem function [2,3,4]. Understanding what enables a community to maintain stable structure or function in the face of disturbances is a fundamental aim of ecology, and has increasing practical importance as human activities alter the frequency and intensity of disturbances such as fire, storms, drought, and disease outbreaks [5]. A growing number of studies has examined resistance (or its converse, sensitivity) to disturbance, but far fewer studies have explicitly tested resilience [6]. Soil communities often fail to return to baseline structure [7], while lake microbial communities showed complete recovery [8, 9]. Studies of microbiome resilience in nonhuman animals are rare [6], but see [14, 15]

Methods

Results

Conclusion