Genome‐resolved viral and cellular metagenomes revealed potential key virus‐host interactions in a deep freshwater lake

Abstract

Summary Metagenomics has dramatically expanded the known virosphere, but freshwater viral diversity and their ecological interaction with hosts remain poorly understood. Here, we conducted a metagenomic exploration of planktonic dsDNA prokaryotic viruses by sequencing both virion (<0.22 μm) and cellular (0.22–5.0 μm) fractions collected spatiotemporally from a deep freshwater lake (Lake Biwa, Japan). This simultaneously reconstructed 183 complete (i.e., circular) viral genomes and 57 bacterioplankton metagenome‐assembled genomes. Analysis of metagenomic read coverage revealed vertical partitioning of the viral community analogous to the vertically stratified bacterioplankton community. The hypolimnetic community was generally stable during stratification, but occasionally shifted abruptly, presumably due to lysogenic induction. Genes involved in assimilatory sulfate reduction were encoded in 20 (10.9%) viral genomes, including those of dominant viruses, and may aid viral propagation in sulfur‐limited freshwater systems. Hosts were predicted for 40 (21.9%) viral genomes, encompassing 10 phyla (or classes of Proteobacteria) including ubiquitous freshwater bacterioplankton lineages (e.g., Ca. Fonsibacter and Ca. Nitrosoarchaeum). Comparison with viral genomes derived from published metagenomes revealed viral phylogeographic connectivity in geographically isolated habitats. Notably, analogous to their hosts, actinobacterial viruses were among the most diverse, ubiquitous and abundant viral groups in freshwater systems, with potential high lytic activity in surface waters.

Deep sea sediments associated with cold seeps are a subsurface reservoir of viral diversity

“…Based on VIRBANT annotations (Supplementary Table 12 ), the most common AMG related to sulfur metabolism within the viral contigs was phosphoadenosine phosphosulfate reductase (PAPS reductase or CysH), which is predicted to participate in assimilatory sulfate reduction. Viral cysH has also been found in viral sequences obtained from oxygen-deficient water columns [ 83 ], rumen [ 84 ], a deep freshwater lake [ 16 ] and sulfidic mine tailings [ 85 ]. Here, we manually confirmed that three vOTUs from two distinct viral genera encoded PAPS reductase genes (Fig.…”

“…These methods have greatly advanced viral ecology from the identification of novel viruses to the global distribution of viruses. Studies from a variety of environments such as thawing permafrost [ 13 ], mangroves [ 14 ], arctic lakes [ 15 ], freshwater lakes [ 16 ], deep sea sediments [ 17 ], the terrestrial subsurface [ 18 , 19 ], and especially seawater [ 20 – 22 ] have suggested that prokaryotic viruses act as key agents in natural ecosystems via a range of interactions with their microbial hosts. Viruses can influence organic carbon and nutrient turnover by top-down control of microbial abundance via lysis of cells and subsequent release of cellular contents during lytic infection [ 23 ].…”

Extreme Viral Partitioning in a Marine-Derived High Arctic Lake

“…There are few studies that have compared levels of lake viral diversity over depth. A study from Lake Biwa (38) reported that Ͼ65% of viral genomes were unique to a particular depth. Similarly to Lake A data, a study of Lake Shunet, a sub-Arctic meromictic lake in Siberia (39), showed that very few viral taxa were present throughout the water column.…”

“…Studies investigating freshwater viromes have resulted in the observation of sharp differences in viral diversity driven by season (27,42,43) or by proximity to the shore or large water inputs or human perturbation (40,44). Several studies have identified salinity as the primary driver of viral diversity (38,45), where higher diversity corresponded with higher conductivity (45,46). Watkins et al (40) proposed that freshwater viral communities are likely to be more diverse than marine viral communities because freshwater environments are generally more heterogeneous.…”

Metagenome Mining Reveals Hidden Genomic Diversity of Pelagimyophages in Aquatic Environments

“…To assess the distribution and abundance patterns of the recovered PMP MAVGs, the genomes were recruited using BLASTN (96) against the Tara Oceans metagenomes (40,91), Geotraces cellular metagenomes (41), and the Mediterranean metagenomes described previously (14,39). PMP group PMP-D were also recruited against the virome data sets they were recovered from (97) and against samples from other freshwater environments (Lake Biwa [98], Lake Simoncouche [99], Lake Kivu [GOLD Study identifier {ID} Gs0127566], Baltic Sea [100]). Normalization was performed by calculating RPKG (reads recruited per kilobase of the genome per gigabase of the metagenome) so recruitment values could be compared across samples.…”