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Strong influence of vertebrate host phylogeny on gut archaeal diversity

View ORCID ProfileNicholas D. Youngblut, Georg H. Reischer, Silke Dauser, Chris Walzer, Gabrielle Stalder, Andreas H. Farnleitner, View ORCID ProfileRuth E. Ley
doi: https://doi.org/10.1101/2020.11.10.376293
Nicholas D. Youngblut
1Department of Microbiome Science, Max Planck Institute for Developmental Biology, Max Planck Ring 5, 72076 Tübingen, Germany
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  • ORCID record for Nicholas D. Youngblut
  • For correspondence: rley@tuebingen.mpg.de nyoungblut@tuebingen.mpg.de
Georg H. Reischer
2TU Wien, Institute of Chemical, Environmental and Bioscience Engineering, Research Group for Environmental Microbiology and Molecular Diagnostics 166/5/3, Gumpendorfer Straße 1a, A-1060 Vienna, Austria
3ICC Interuniversity Cooperation Centre Water & Health, 1160 Vienna, Austria
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Silke Dauser
1Department of Microbiome Science, Max Planck Institute for Developmental Biology, Max Planck Ring 5, 72076 Tübingen, Germany
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Chris Walzer
4Wildlife Conservation Society, 2300 Southern Blvd. 10460 Bronx, NY, USA
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Gabrielle Stalder
5Research Institute of Wildlife Ecology, University of Veterinary Medicine, Vienna, Austria
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Andreas H. Farnleitner
2TU Wien, Institute of Chemical, Environmental and Bioscience Engineering, Research Group for Environmental Microbiology and Molecular Diagnostics 166/5/3, Gumpendorfer Straße 1a, A-1060 Vienna, Austria
3ICC Interuniversity Cooperation Centre Water & Health, 1160 Vienna, Austria
6Research Division Water Quality and Health, Karl Landsteiner University for Health Sciences, 3500 Krems an der Donau, Austria
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Ruth E. Ley
1Department of Microbiome Science, Max Planck Institute for Developmental Biology, Max Planck Ring 5, 72076 Tübingen, Germany
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  • For correspondence: rley@tuebingen.mpg.de nyoungblut@tuebingen.mpg.de
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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.

Significance Archaea 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.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Posted November 10, 2020.
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Strong influence of vertebrate host phylogeny on gut archaeal diversity
Nicholas D. Youngblut, Georg H. Reischer, Silke Dauser, Chris Walzer, Gabrielle Stalder, Andreas H. Farnleitner, Ruth E. Ley
bioRxiv 2020.11.10.376293; doi: https://doi.org/10.1101/2020.11.10.376293
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Strong influence of vertebrate host phylogeny on gut archaeal diversity
Nicholas D. Youngblut, Georg H. Reischer, Silke Dauser, Chris Walzer, Gabrielle Stalder, Andreas H. Farnleitner, Ruth E. Ley
bioRxiv 2020.11.10.376293; doi: https://doi.org/10.1101/2020.11.10.376293

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