Strong influence of vertebrate host phylogeny on gut archaeal diversity

Abstract

Commonly used 16S rRNA gene primers miss much of the archaeal diversity present in the vertebrate gut, leaving open the question of which archaea are host associated, the specificities of such associations, and the major factors influencing archaeal diversity. We applied 16S rRNA amplicon sequencing with Archaea-targeting primers to a dataset of 311 fecal/gut samples spanning 5 taxonomic classes (Mammalia, Aves, Reptilia, Amphibia, and Actinopterygii) and obtained from mainly wild individuals (76% were wild). We obtained sufficient archaeal sequence data from 185 samples comprising 110 species that span all 5 classes. We provide evidence for novel Archaea-host associations, including Bathyarchaeia and Methanothermobacter — the latter of which was prevalent among Aves and enriched in higher body temperatures. Host phylogeny more strongly explained archaeal diversity than diet, while specific taxa were associated with each factor. Co-phylogeny was significant and strongest for mammalian herbivores. Methanobacteria was the only class predicted to be present in the last command ancestors of mammals and all host species. Archaea-Bacteria interactions seem to have a limited effect on archaeal diversity. These findings substantially expand on the paradigm of Archaea-vertebrate associations and the factors that explain those associations.SignificanceArchaea play key roles in the vertebrate gut such as promoting bacterial fermentation via consumption of waste products. Moreover, gut-inhabiting methanogenic Archaea in livestock are a substantial source of greenhouse gas production. Still, much is not known of the archaeal diversity in most vertebrates, especially since 16S rRNA sequence surveys often miss much of the archaeal diversity that is present. By applying Archaea-targeted gut microbiome sequencing to a large collection of diverse vertebrates, we reveal new Archaea-host associations such as a high prevalence of Methanothermobacter in birds. We also show that host evolutionary history explains archaeal diversity better than diet, and certain genera in one particular class of Archaea (Methanobacteria) were likely pervasive in the ancestral vertebrate gut.

Blowing Hot and Cold: Body Temperature and the Microbiome

“…This association may be driven by various host factors shared by flighted animals ( 65 ); however, body temperature is one such factor that has not yet been explored. Recently, our lab reported a positive correlation between abundance of the thermophilic archaeon Methanothermobacter and host body temperature across a range of mammalian and avian hosts ( 68 ). Although this correlation was inseparable from host phylogeny and might therefore be confounded by other host properties, it supports the hypothesis that host body temperatures can play a role in shaping gut microbiota composition.…”

Codiversification of gut microbiota with humans

“…Coevolution, an evolutionary process involving reciprocal selection between two or more species, is more likely to occur when the partners share a parallel evolutionary history, a pattern termed codiversification (1). Codiversification between members of the gut microbiota and their mammalian hosts has been suggested for specific gut bacteria, based on host phylogenies matching bacterial single-gene phylogenies (2)(3)(4). Using this approach in wild apes, Moeller et al (2016) demonstrated that several gut bacterial families codiversified with hominids over the last 15 million years (5).…”

A comprehensive analysis of the global human gut archaeome from a thousand genome catalogue

“…Overall this work contributes substantially to the understanding of the microbiome as a complex multi-domain microbial network of the human gastrointestinal tract (Taffner et al 2018; Nayfach, Roux, et al 2020; Youngblut, Reischer, et al 2020; Youngblut, Cuesta-Zuluaga, et al 2020). We showed that despite the availability of more than 1,000 genomes, the human archaeome still remains undersampled.…”