Detection of an archaeal-specific viral family, previously thought to infect exclusively hyperthermophiles, in human gut metaviromes
Résumé
Viruses of archaea have an exceptional diversity [1]. Several of their families are shared with
bacteria, typically those from the cosmopolitan Caudovirales order. However, the majority of
them are archaea-specific; they have very diverse genomic contents and morphotypes, such
as two-tailed (Bicaudaviridae), spindle (Fuselloviridae, Salterprovirus), rod (Rudiviridae), or
filamentous (Lipothrixviridae) shapes. Most of the known archaea-specific viruses infect
hyperthermophiles and halophiles. Nevertheless, the viruses of many archaeal phylogenetic
groups remain poorly explored, such as those of methanogens. Six of the seven known
methanogen-infecting viruses belong to the Caudovirales order [1]. Interestingly, a spherical
virus infecting Methanosarcina strains has recently been isolated [2]. Named MetSV, it
probably represents a new family [1]. The smacoviruses have moreover been suggested to
infect methanogens rather than human, based on metavirome analysis [3]. Finally, unusual
morphotypes have been detected in metaviromes from anaerobic digestion plants, as well
as contigs of unknown hosts from various archaea-specific viral families: Salterprovirus,
Bicaudaviridae, Fuselloviridae, Lipothrixviridae, and Rudiviridae [4].
To identify putative viruses of methanogens in metaviromes from anaerobic ecosystems, we
developed a bioinformatics pipe-line based on metaSPADES [5] for assembly and Kaiju [6] for
taxonomic assignation. As a first test, we applied our pipe-line to the raw reads of 4
previously published human gut metaviromes [7]. A total of 12 short contigs (~1 kb-3.5 kb)
were assigned by Kaiju to known families of archaeal viruses, corresponding to Rudiviridae
exclusively; this assignation was confirmed by blast analyses. Using WiSH [8], we predicted
their possible hosts among archaea. Nine of them had best predictions for Sulfolobales
members, their presently known acidothermophilic hosts, while the remaining 3 were
predicted to infect methanogens (genera Methanosarcina, Methanosphaera and
Methanobrevibacter). It suggests that some of these contigs could originate from viruses of
methanogens, consistent with methanogens being the dominant archaea in the human gut.
In the future, we plan to include a CRISPR-spacer matching tool to our pipe-line, to predict
the hosts by a complementary method. Using a state-of-the art assembler [9] yielded only
short Rudiviridae contigs, likely because ruvidiruses have a low abundance in the human gut.
It advocates for the use of enrichment approaches to study them more specifically. Our
results reinforce the notion that archaea-specific viruses may not be mostly restricted to
extremophiles and could be more widespread in the biosphere than previously thought.
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