Species-Specific Viromes in the Ancestral Holobiont Hydra

Abstract

Recent evidence showing host specificity of colonizing bacteria supports the view that multicellular organisms are holobionts comprised of the macroscopic host in synergistic interdependence with a heterogeneous and host-specific microbial community. Whereas host-bacteria interactions have been extensively investigated, comparatively little is known about host-virus interactions and viral contribution to the holobiont. We sought to determine the viral communities associating with different Hydra species, whether these viral communities were altered with environmental stress, and whether these viruses affect the Hydra-associated holobiont. Here we show that each species of Hydra harbors a diverse host-associated virome. Primary viral families associated with Hydra are Myoviridae, Siphoviridae, Inoviridae, and Herpesviridae. Most Hydra-associated viruses are bacteriophages, a reflection of their involvement in the holobiont. Changes in environmental conditions alter the associated virome, increase viral diversity, and affect the metabolism of the holobiont. The specificity and dynamics of the virome point to potential viral involvement in regulating microbial associations in the Hydra holobiont. While viruses are generally regarded as pathogenic agents, our study suggests an evolutionary conserved ability of viruses to function as holobiont regulators and, therefore, constitutes an emerging paradigm shift in host-microbe interactions.

Sequence analysis of malacoherpesvirus proteins: Pan-herpesvirus capsid module and replication enzymes with an ancient connection to “Megavirales”

“…This, as well as the earlier discovery of a nearlycomplete virus-like DNA scaffold co-deposited with the genome of amphioxus B. floridae (Savin et al, 2010), suggest that herpesviruses may be consorting with diverse marine invertebrates. Putative herpesvirus-like isolated from other aquatic Metazoa, such as two species of stony corals and wild-caught Hydra sp., have been reported (Vega Thurber et al, 2008;Grasis et al, 2014;Correa et al, 2016). Caution has been advised in interpreting these results (Houldcroft and Breuer, 2015;Wood-Charlson et al, 2015;Sweet and Bythell, 2016), and our reanalysis of the three publicly available short sequences from these studies annotated as fragments of anthozoan herpesvirus DNA suggests that they are in fact of bacterial and fungal provenance (Additional File 6).…”

No genome is an island: toward a 21st century agenda for evolution

“…A more general role for lysogeny and lysogenic conversion has been described for the bacterial microbiome that attaches to the mucus layers covering aquatic metazoa, such as Hydra in fresh water and environmentally threatened reef corals in oceans . According to the Piggyback‐the‐Winner (PtW) model of marine holobionts, lysogeny for toxin production in mucus‐associated bacteria provides protection both to the bacteria (from phage superinfection and protist grazing) and to the underlying metazoan host, by blocking infections of bacterial pathogens and parasitic protists.…”

Functions of the Microbiota for the Physiology of Animal Metaorganisms

“…However, metaorganisms are constantly reinfected with low-virulent viruses that can function as mutualistic symbionts, provide fitness advantages for their hosts [6], and even build a stable and species-specific virome [34]. There is evidence that eukaryotic virus infections can alter and enhance host immunity and make the host more resistant to pathogens and diseases.…”