Abstract
Variation among animals in their host-associated microbial communities is increasingly recognized as a key determinant of important life history traits including growth, metabolism, and resistance to disease. Quantitative estimates of the factors shaping the stability of host microbiomes over time at the individual level in non-model organisms are scarce. Addressing this gap in our knowledge is important, as variation among individuals in microbiome stability may represent temporal gain or loss of key microbial species and functions linked to host health and/or fitness. Here we use controlled experiments to investigate how both heterogeneity in microbial species richness of the environment and exposure to the emerging pathogen Ranavirus influence the structure and temporal dynamics of the skin microbiome in a vertebrate host, the European common frog (Rana temporaria). Our evidence suggests that altering the bacterial species richness of the environment drives divergent temporal microbiome dynamics of the amphibian skin. Exposure to ranavirus effects changes in skin microbiome structure irrespective of total microbial diversity, but individuals with higher pre-exposure skin microbiome diversity appeared to exhibit higher survival. Higher diversity skin microbiomes also appear less stable over time compared to lower diversity microbiomes, but stability of the 100 most abundant (“core”) community members was similar irrespective of microbiome richness. Our study highlights the importance of extrinsic factors in determining the stability of host microbiomes over time, which may in turn have important consequences for the stability of host-microbe interactions and microbiome-fitness correlations.
Highlights
Animals are host to diverse communities of microbes, collectively referred to as the microbiome
There was no evidence of an effect of the interaction between time, habitat and pathogen exposure, or a main effect of ranavirus exposure on overall species richness of the microbiome (Supplementary Table S1)
As for species richness, these results indicated that community evenness was lower in Simple Habitats prior to ranavirus exposure (Supplementary Table S2b)
Summary
Animals are host to diverse communities of microbes, collectively referred to as the microbiome. Amphibian Skin Microbiomes and Ranavirus can have deleterious effects on host physiology, an understanding of the drivers of individual microbiome dynamics over time, and resistance to perturbation, remain relatively scarce in non-model organisms (Loudon et al, 2014b, 2016; Videvall et al, 2019). Addressing this shortfall in our knowledge is of fundamental importance to understanding the adaptive value of microbiomes for host health and fitness, as microbiome-health correlations may not be stable over time if microbiome flux represents loss of key microbial species and/or genes critical for optimal host physiology. Though several studies have sought to measure the influence of pathogenic infection on host microbiome structure (Jani and Briggs, 2014; Longo et al, 2015; Longo and Zamudio, 2017), investigations of whether the magnitude of microbiome disruption for infected hosts is modulated by initial microbiome state remains relatively scarce (see Jani et al, 2017; Jani and Briggs, 2018)
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