Fungal microbiomes are determined by host phylogeny and exhibit widespread associations with the bacterial microbiome
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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 that fungi form critical components of putative microbial interaction networks, where the strength and frequency of interactions varies with host taxonomy. Host phylogeny drives differences in overall richness of bacterial and fungal communities, but the effect of diet on richness was only evident in mammals and for the bacterial microbiome. 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.
SIGNIFICANCE STATEMENT
Microbes perform vital metabolic functions that shape the physiology of their hosts. However, almost all research to date in wild animals has focused exclusively on the bacterial microbiota, to the exclusion of other microbial groups. Although likely to be critical components of the host microbiome, we have limited knowledge of the drivers of fungal composition across host species. Here we show that fungal community composition is determined by host species identity and phylogeny, and that fungi form extensive interaction networks with bacteria in the microbiome of a diverse range of animal species. This highlights the importance of microbial interactions as mediators of microbiome-health relationships in the wild.
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Reviewer #2:
In this work, the authors analyze fungal and bacterial communities in 49 host species and find evidence of phylosymbiosis, a correlation between these microbiomes and host that suggests host recruitment of specific microbial communities. They further carry out a network analysis that suggests co-occurrence of fungal and bacterial communities across hosts. While host recruitment has been shown previously for bacteria, the authors here include a broad survey of mycobiomes and based on their analysis conclude that fungal communities are also critical to interactions and host health.
This descriptive study provides important insight regarding the general characteristics of the mycobiome and its relationship to the bacterial communities and the host. The work is in agreement with these fungal communities being important for host …
Reviewer #2:
In this work, the authors analyze fungal and bacterial communities in 49 host species and find evidence of phylosymbiosis, a correlation between these microbiomes and host that suggests host recruitment of specific microbial communities. They further carry out a network analysis that suggests co-occurrence of fungal and bacterial communities across hosts. While host recruitment has been shown previously for bacteria, the authors here include a broad survey of mycobiomes and based on their analysis conclude that fungal communities are also critical to interactions and host health.
This descriptive study provides important insight regarding the general characteristics of the mycobiome and its relationship to the bacterial communities and the host. The work is in agreement with these fungal communities being important for host function and health, the work does not provide direct information on these communities, their interactions or possible effects on the host.
The overall presentation of the results are geared towards a focused readership.
The authors could be more explicit regarding the value behind the modularity of networks for a given host (in mammals) and what exactly is the significance of this finding in the broad context of microbiomes.
Some groups of samples are obtained from very varied sources (amphibia) but others are not. Beyond sample type being important, what other effects could these sampling differences have on the final conclusions, for example in their network analysis?
What is the significance of having some species with more negative interactions? Are there any ideas how a negative interaction can be sustained over time?
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Reviewer #1:
The importance of host associated microbiomes for health and disease of their hosts cannot be overstated. Fungi tend to feature more prominently in microbiome studies of soil or plants, but microbiome work in animals has mostly focused on bacteria, with fungi having received comparatively less attention. The current study addresses the question whether there is evidence for co-evolution or consistent ecological filtering of fungal communities in the animal gut, similar to what has been reported for bacteria. Such patterns have been termed "phylosymbiosis", even though the ecological interactions that underlie such patterns are largely unknown.
The strength of the study is the wide range of animals investigated, 49 species from eight different classes of vertebrates and invertebrates. However, this wide sampling also is a …
Reviewer #1:
The importance of host associated microbiomes for health and disease of their hosts cannot be overstated. Fungi tend to feature more prominently in microbiome studies of soil or plants, but microbiome work in animals has mostly focused on bacteria, with fungi having received comparatively less attention. The current study addresses the question whether there is evidence for co-evolution or consistent ecological filtering of fungal communities in the animal gut, similar to what has been reported for bacteria. Such patterns have been termed "phylosymbiosis", even though the ecological interactions that underlie such patterns are largely unknown.
The strength of the study is the wide range of animals investigated, 49 species from eight different classes of vertebrates and invertebrates. However, this wide sampling also is a weakness, as few groups are well sampled. Members of the same species are found to have relatively similar bacterial and fungal microbiota, and fungal microbiota are found to be somewhat correlated with phylogenetic distance. There is also correlation between bacterial and fungal communities, but whether this is driven by independent effects of the host on both groups, or primarily by interactions between the two microbial groups remains unknown. Some of the other observations, such as the tendency of bacterial diversity to be higher than fungal diversity, are more difficult to parse, since it is not clear what the proper yardstick for diversity comparisons is (i.e., whether functional differences between fungal ASVs are comparable to functional differences between bacterial ASVs). This study provides interesting insight regarding the general characteristics of the fungal microbiome and its relationship to the bacterial communities and the host. It does not directly reveal how these communities might affect the host. As the authors themselves state, "The drivers of phylosymbiosis remain unclear".
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