Viral dark matter and virus-host interactions resolved from publicly available microbial genomes

  1. Simon Roux
  2. Steven J Hallam
  3. Tanja Woyke
  4. Matthew B Sullivan  Is a corresponding author
  1. The Ohio State University, United States
  2. University of British Columbia, Canada
  3. U.S Department of Energy Joint Genome Institute, United States

Abstract

The ecological importance of viruses is now widely recognized, yet our limited knowledge of viral sequence space and virus-host interactions precludes accurate prediction of their roles and impacts. Here we mined publicly available bacterial and archaeal genomic datasets to identify 12,498 high‑confidence viral genomes linked to their microbial hosts. These data augment public datasets 10-fold, provide first viral sequences for 13 new bacterial phyla including ecologically abundant phyla, and help taxonomically identify 7-38% of 'unknown' sequence space in viromes. Genome- and network-based classification was largely consistent with accepted viral taxonomy and suggested that (i) 264 new viral genera were identified (doubling known genera) and (ii) cross-taxon genomic recombination is limited. Further analyses provided empirical data on extrachromosomal prophages and co‑infection prevalences, as well as evaluation of in silico virus-host linkage predictions. Together these findings illustrate the value of mining viral signal from microbial genomes.

Article and author information

Author details

  1. Simon Roux

    Department of Microbiology, The Ohio State University, Columbus, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Steven J Hallam

    Department of Microbiology and Immunology, University of British Columbia, Vancouver, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. Tanja Woyke

    U.S Department of Energy Joint Genome Institute, Walnut Creek, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Matthew B Sullivan

    Department of Microbiology, The Ohio State University, Columbus, United States
    For correspondence
    mbsulli@email.arizona.edu
    Competing interests
    The authors declare that no competing interests exist.

Copyright

© 2015, Roux et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 11,668
    views
  • 2,366
    downloads
  • 405
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Simon Roux
  2. Steven J Hallam
  3. Tanja Woyke
  4. Matthew B Sullivan
(2015)
Viral dark matter and virus-host interactions resolved from publicly available microbial genomes
eLife 4:e08490.
https://doi.org/10.7554/eLife.08490

Share this article

https://doi.org/10.7554/eLife.08490

Further reading

    1. Ecology
    2. Evolutionary Biology
    Justine Boutry, Océane Rieu ... Fréderic Thomas
    Research Article

    While host phenotypic manipulation by parasites is a widespread phenomenon, whether tumors, which can be likened to parasite entities, can also manipulate their hosts is not known. Theory predicts that this should nevertheless be the case, especially when tumors (neoplasms) are transmissible. We explored this hypothesis in a cnidarian Hydra model system, in which spontaneous tumors can occur in the lab, and lineages in which such neoplastic cells are vertically transmitted (through host budding) have been maintained for over 15 years. Remarkably, the hydras with long-term transmissible tumors show an unexpected increase in the number of their tentacles, allowing for the possibility that these neoplastic cells can manipulate the host. By experimentally transplanting healthy as well as neoplastic tissues derived from both recent and long-term transmissible tumors, we found that only the long-term transmissible tumors were able to trigger the growth of additional tentacles. Also, supernumerary tentacles, by permitting higher foraging efficiency for the host, were associated with an increased budding rate, thereby favoring the vertical transmission of tumors. To our knowledge, this is the first evidence that, like true parasites, transmissible tumors can evolve strategies to manipulate the phenotype of their host.

    1. Ecology
    Ming-Qiang Wang, Shi-Kun Guo ... Chao-Dong Zhu
    Research Article

    Environmental factors can influence ecological networks, but these effects are poorly understood in the realm of the phylogeny of host-parasitoid interactions. Especially, we lack a comprehensive understanding of the ways that biotic factors, including plant species richness, overall community phylogenetic and functional composition of consumers, and abiotic factors such as microclimate, determine host-parasitoid network structure and host-parasitoid community dynamics. To address this, we leveraged a 5-year dataset of trap-nesting bees and wasps and their parasitoids collected in a highly controlled, large-scale subtropical tree biodiversity experiment. We tested for effects of tree species richness, tree phylogenetic, and functional diversity, and species and phylogenetic composition on species and phylogenetic diversity of both host and parasitoid communities and the composition of their interaction networks. We show that multiple components of tree diversity and canopy cover impacted both, species and phylogenetic composition of hosts and parasitoids. Generally, phylogenetic associations between hosts and parasitoids reflected nonrandomly structured interactions between phylogenetic trees of hosts and parasitoids. Further, host-parasitoid network structure was influenced by tree species richness, tree phylogenetic diversity, and canopy cover. Our study indicates that the composition of higher trophic levels and corresponding interaction networks are determined by plant diversity and canopy cover, especially via trophic links in species-rich ecosystems.