Assessing the viral content of uncultured picoeukaryotes in the global‐ocean by single cell genomics

Abstract

Viruses are the most abundant biological entities on Earth and have fundamental ecological roles in controlling microbial communities. Yet, although their diversity is being increasingly explored, little is known about the extent of viral interactions with their protist hosts as most studies are limited to a few cultivated species. Here, we exploit the potential of single‐cell genomics to unveil viral associations in 65 individual cells of 11 essentially uncultured stramenopiles lineages sampled during the Tara Oceans expedition. We identified viral signals in 57% of the cells, covering nearly every lineage and with narrow host specificity signal. Only seven out of the 64 detected viruses displayed homologies to known viral sequences. A search for our viral sequences in global ocean metagenomes showed that they were preferentially found at the DCM and within the 0.2–3 µm size fraction. Some of the viral signals were widely distributed, while others geographically constrained. Among the viral signals we detected an endogenous mavirus virophage potentially integrated within the nuclear genome of two distant uncultured stramenopiles. Virophages have been previously reported as a cell's defence mechanism against other viruses, and may therefore play an important ecological role in regulating protist populations. Our results point to single‐cell genomics as a powerful tool to investigate viral associations in uncultured protists, suggesting a wide distribution of these relationships, and providing new insights into the global viral diversity.

Virophages and retrotransposons colonize the genomes of a heterotrophic flagellate

“…In the resulting phylogenetic trees, EMALE core proteins formed monophyletic clades with mavirus and related sequences from environmental samples, thus significantly expanding the known diversity of the genus Mavirus . The environmental sequences that clustered with EMALE core proteins include a single amplified genome (SAG) from an uncultured chrysophyte ( Castillo et al, 2019 ), the metagenomic Ace Lake Mavirus (ALM) ( Zhou et al, 2013 ), and four additional metagenomes that were identified in a global survey of virophage sequences ( Paez-Espino et al, 2019 ). The chrysophyte SAG is nearly identical to mavirus strain Spezl and indicates that the host range of mavirus extends beyond bicosoecids.…”

Single Cell Genomics Reveals Viruses Consumed by Marine Protists

“…The sharing of nearly identical viral sequences across multiple eukaryote phyla within the GoM protists (Figure 3) also makes it unlikely that these viruses are integrated into protistan genomes. Earlier single cell genomics studies of protists in marine environments have reported the presence of bacteriophage, ssDNA and other virus sequences in individuals such as Picozoa (Yoon et al, 2011), Cercozoa (Bhattacharya et al, 2012), and Stramenopiles (Roy et al, 2014;Castillo et al, 2019). In these cases, identified viruses were hypothesized to be either infecting the protist (Yoon et al, 2011), bacterial viruses originating from infected bacterial prey or epibionts (Yoon et al, 2011;Bhattacharya et al, 2012), or simply removed from analysis without further consideration (Roy et al, 2014).…”

Virophages and retrotransposons colonize the genomes of a heterotrophic flagellate

“…In the resulting phylogenetic trees, EMALE proteins formed monophyletic clades with mavirus and related sequences from environmental samples, thus significantly expanding the known diversity of the genus Mavirus. The environmental sequences that clustered with EMALE proteins include a single amplified genome (SAG) from an uncultured chrysophyte 29 , the metagenomic Ace Lake Mavirus (ALM) 30 , and four additional metagenomes that were identified in a global survey of virophage sequences 23 . The chrysophyte SAG is nearly identical to mavirus strain Spezl and shows that the host range of mavirus is broader than previously assumed.…”