Fungal microbiomes are determined by host phylogeny and exhibit widespread associations with the bacterial microbiome

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.

The interplay of fungal and bacterial microbiomes on rainforest frogs following a disease outbreak

“…This is consistent with studies on humans and ruminants (Kittelmann et al, 2012; Qin et al, 2010). Similarly, a study looking at a wide range of animal hosts found that Shannon diversity was higher for bacteria than for fungi in 47 out of 49 species (Harrison et al, 2021).…”

“…Thus, a frog that is suitable for hosting a rich assemblage of bacteria may also be suitable for hosting a rich assemblage of fungi. Indeed, Harrison et al (2021) found evidence of co‐occurrence between fungi and bacteria and associations between host phylogeny and microbiomes across a range of species, suggesting that aspects of the hosts were simultaneously selecting specific fungi and bacteria. This explanation is reasonable given that, on a particular frog, both communities will be exposed to the same antimicrobial peptides and experience the same environments and climate.…”

“…Within vertebrates, fungal microbiome studies are largely restricted to humans (Findley et al, 2013;Hoffmann et al, 2013;Huffnagle & Noverr, 2013;Wargo & Hogan, 2006), domesticated animals (Chermprapai et al, 2019;Kittelmann et al, 2013), and laboratory rodents (Scupham et al, 2006). Relatively few studies have examined fungal microbiomes of vertebrate wildlife (Allender et al, 2018;Chen et al, 2018;Harrison et al, 2021;Kearns et al, 2017;Kueneman et al, 2016Kueneman et al, , 2017Medina et al, 2019). Further, while these studies provide valuable starting points, they have often had limitations, in that they were either conducted in captivity (Chen et al, 2018;Kearns et al, 2017), which alters microbiomes (Becker et al, 2014;Loudon, Woodhams, et al, 2014), or used 18S primers (Kueneman et al, 2016(Kueneman et al, , 2017, which provide less information about fungal microbiomes than do internal transcribe sequences (ITS) primers (Schoch et al, 2012).…”

Houseflies harbor less diverse microbiota under laboratory conditions but maintain a consistent set of host-associated bacteria

“…Nevertheless, bacterial and fungal communities co-varied within all samples and both within and between housefly strains. Co-variation of the bacterial and the fungal microbiota has been reported in the case of many species 47 . A major gap in our knowledge is the extent to which this phenomenon can be attributed to selection by the host or to interactions within the microbiome.…”

Bowel Movement: Integrating Host Mobility and Microbial Transmission Across Host Taxa

“…A transfer of microbes across predator-prey networks has been suggested for insectivorous birds and predatory insects ( Tiede et al, 2017 ; Suenami et al, 2019 ; Dion-Phénix et al, 2021 ). The mammalian microbiota is strongly influenced by species identity and type of diet, but an increase of invertebrate prey (i.e., insects) within the diet correlates with a decrease in bacterial alpha diversity compared to mammals with a primarily herbivorous lifestyle ( Knowles et al, 2019 ; Harrison et al, 2021 ). Tough “insectivory” includes the consumption of non-flying insects (i.e., ants or termites) as well as other invertebrates, such a dietary preference seems to result in a convergent adaptation in the microbiota of phylogenetically distant mammalian clades (Pilosa, Cingulata, Tubulidentata, and Carnivora) ( Delsuc et al, 2014 ).…”