Journal Article

Phylogeny and disease associations of a widespread and ancient intestinal bacteriophage lineage

Zwinderman, Aeilko H., Nieuwdorp, Max, de Jonge, Patrick A., Dutilh, Bas E., Herrema, Hilde, van den Born, Bert-Jan H.

2024

Overview

Viruses are core components of the human microbiome, impacting health through interactions with gut bacteria and the immune system. Most human microbiome viruses are bacteriophages, which exclusively infect bacteria. Until recently, most gut virome studies focused on low taxonomic resolution (e.g., viral operational taxonomic units), hampering population-level analyses. We previously identified an expansive and widespread bacteriophage lineage in inhabitants of Amsterdam, the Netherlands. Here, we study their biodiversity and evolution in various human populations. Based on a phylogeny using sequences from six viral genome databases, we propose the Candidatus order Heliusvirales . We identify heliusviruses in 82% of 5441 individuals across 39 studies, and in nine metagenomes from humans that lived in Europe and North America between 1000 and 5000 years ago. We show that a large lineage started to diversify when Homo sapiens first appeared some 300,000 years ago. Ancient peoples and modern hunter-gatherers have distinct Ca. Heliusvirales populations with lower richness than modern urbanized people. Urbanized people suffering from type 1 and type 2 diabetes, as well as inflammatory bowel disease, have higher Ca. Heliusvirales richness than healthy controls. We thus conclude that these ancient core members of the human gut virome have thrived with increasingly westernized lifestyles. Here, based on phylogeny analyses using sequences from six viral genome databases, the authors study the biodiversity and evolution of a new bacteriophage lineage, Candidatus order Heliusvirales , and identify heliusviruses in 82% of 5,441 individuals across 39 studies, and in nine metagenomes from humans that lived in Europe and North America between 1,000 and 5,000 years ago, revealing associations with human diseases.

• Publisher: Nature Publishing Group UK,Nature Publishing Group,Nature Portfolio
• Subject: 45/22 / 49 / 49/23 / 631/326/1321 / 631/326/2565/2134 / Adult / Bacteria / Bacteriophages - classification / Bacteriophages - genetics / Bacteriophages - isolation & purification / Biodiversity / Candidatus Heliusviridae / Diabetes mellitus (insulin dependent) / Diabetes mellitus (non-insulin dependent) / Diabetes Mellitus, Type 2 - virology / Digestive system / Disease control / Europe / Evolution / Female / Gastrointestinal Microbiome - genetics / Gastrointestinal tract / Gene sequencing / Genome, Viral - genetics / Genomes / Human populations / Humanities and Social Sciences / Humans / Immune system / Inflammatory bowel diseases / Inflammatory Bowel Diseases - virology / Male / Metagenome - genetics / Microbiomes / multidisciplinary / Netherlands / Phages / Phylogeny / Population studies / Populations / Science / Science (multidisciplinary) / Taxonomy / Virome - genetics / Viruses