Abstract
Interactions between hosts and their resident microbial communities are a fundamental component of fitness for both agents. Though recent research has highlighted the importance of interactions between animals and their bacterial communities, comparative evidence for fungi is lacking, especially in natural populations. Using data from 49 species, we present novel evidence of strong covariation between fungal and bacterial communities across the host phylogeny, indicative of recruitment by hosts for specific suites of microbes. Using co-occurrence networks, we demonstrate marked variation across host taxonomy in patterns of covariation between bacterial and fungal abundances. Host phylogeny drives differences in the overall richness of bacterial and fungal communities, but the effect of diet on richness was only evident in the mammalian gut microbiome. Sample type, tissue storage and DNA extraction method also affected bacterial and fungal community composition, and future studies would benefit from standardized approaches to sample processing. Collectively these data indicate fungal microbiomes may play a key role in host fitness and suggest an urgent need to study multiple agents of the animal microbiome to accurately determine the strength and ecological significance of host–microbe interactions.
Highlights
Multicellular organisms support diverse microbial communities critical for physiological functioning, immunity, development, evolution and behaviour [1,2,3]
PERMANOVA analyses on centred-log ratio (CLR) transformed amplicon sequence variants (ASVs) abundances revealed significant phylogenetic effects of host class, order and species, as well as effects of sample storage and library preparation protocol for both microbial groups. For both bacteria and fungi, host species identity explained more variation than host class or order, and this pattern remained when re-running the models without sample preparation protocol effects, though this inflated the estimate of R2 for all taxonomic groupings
Consistent with previous studies, we find evidence of phylosymbiosis in the bacterial microbiome [29], but crucially, we demonstrate strong and consistent covariation between fungal and bacterial communities across host phylogeny, especially at higher microbial taxonomic levels
Summary
Multicellular organisms support diverse microbial communities critical for physiological functioning, immunity, development, evolution and behaviour [1,2,3]. Evidence of phylosymbiosis, and its drivers, in other microbial kingdoms or domains is lacking Addressing this major gap in our knowledge is crucial as we likely underestimate the strength and importance of coevolution between animal hosts and their resident communities, in the context of cross-kingdom interactions within the microbiome [28]. We used ITS and 16S rRNA gene amplicon sequencing to characterize fungal and bacterial communities of primarily gut and faecal samples from 49 host species across eight classes, including both vertebrates and invertebrates (electronic supplementary material, table S1). We predicted that both fungal and bacterial microbiomes would demonstrate strong signals of phylosymbiosis across the broad host taxonomic range tested. We tested the prediction that cross-kingdom phylosymbiosis may be partially driven by similarity in host dietary niche across the 32 bird and mammal species sampled
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