Temporal dynamics of uncultured viruses: a new dimension in viral diversity

Abstract

Recent work has vastly expanded the known viral genomic sequence space, but the seasonal dynamics of viral populations at the genome level remain unexplored. Here we followed the viral community in a freshwater lake for 1 year using genome-resolved viral metagenomics, combined with detailed analyses of the viral community structure, associated bacterial populations and environmental variables. We reconstructed 8950 complete and partial viral genomes, the majority of which were not persistent in the lake throughout the year, but instead continuously succeeded each other. Temporal analysis of 732 viral genus-level clusters demonstrated that one-fifth were undetectable at specific periods of the year. Based on host predictions for a subset of reconstructed viral genomes, we for the first time reveal three distinct patterns of host–pathogen dynamics, where the viruses may peak before, during or after the peak in their host’s abundance, providing new possibilities for modelling of their interactions. Time series metagenomics opens up a new dimension in viral profiling, which is essential to understand the full scale of viral diversity and evolution, and the ecological roles of these important factors in the global ecosystem.

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

“…Relative abundance of LBVGs and LBVCs was determined based on metagenomic read coverage, shown as fragments per kilobase per mapped million reads (FPKM) (Nishimura et al, 2017a;Yoshida and 5). The rapid succession of the viral community in the epilimnion was in line with previous studies (Rodriguez-Brito et al, 2010;Arkhipova et al, 2018). By contrast, in the hypolimnion, many viral lineages persistently dominated for more than a month ( Fig.…”

“…In addition, we have previously unveiled the vertical stratification of bacterioplankton communities in deep freshwater lakes, where the oxygenated hypolimnion i.e., the deep aerobic water layer below the thermocline, which generally constitutes a volumetrically significant part of deep temperate, oligo-mesotrophic lakes was dominated by specific lineages that are uncommon in the epilimnion, including members of Chloroflexi (Okazaki et al, 2013, Planctomycetes, Nitrospira and Thaumarchaeota (Okazaki and Nakano, 2016;Okazaki et al, 2017). These lineages are likely responsible for important biogeochemical processes in the oxygenated hypolimnion, such as remineralization or conversion of semi-labile organic matter (Maki et al, 2010;Thottathil et al, 2013), nitrification (Small et al, 2013; However, despite a growing number of viromic studies in freshwater systems (Skvortsov et al, 2016;Moon et al, 2017;Silva et al, 2017;Arkhipova et al, 2018), viruses infecting other typical freshwater bacterioplankton lineages, such as LD12 (Ca. Fonsibacter) (Henson et al, 2018) and Limnohabitans (Kasalický et al, 2013) have yet to be characterized.…”

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

“…and ). The rapid succession of the viral community in the epilimnion was in line with previous studies (Rodriguez‐Brito et al ., ; Arkhipova et al ., ). By contrast, in the hypolimnion, many viral lineages persistently dominated for more than a month (Fig.…”

“…The RVG was prepared by extracting 2621 genomes of isolated dsDNA prokaryotic viruses from the Virus‐Host Database (as of 6 February 2018) (Mihara et al ., ). The EVG was built based on 1811 genomes compiled for the previous study (Nishimura et al ., ) and augmented with the following datasets: (i) 125 842 mVCs (metagenomic Viral Contigs), which were generated from metagenomes deposited in the IMG/M database (Paez‐Espino et al ., ); (ii) 28 complete viral genomes retrieved from a Mediterranean deep‐ocean virome (Mizuno et al ., ); (iii) contigs assembled from six viromes collected seasonally from Lake Soyang (PRJEB15535) (Moon et al ., ); (iv) 488 contigs previously compiled from published freshwater viromes (Arkhipova et al ., ); and (v) 313 complete viral genomes recovered from Lake Neagh (Arkhipova et al ., ). In addition, the genomes of recently reported freshwater viruses, including the Synechococcus virus S‐EIV1 (Chénard et al ., ), eight actinoviruses (Ghai et al ., ), a LD28 virus (Moon et al ., ), two Comamonadaceae viruses (Moon et al ., ) and a Polynucleobacter virus (Cabello‐Yeves et al ., ) were compiled.…”

“…Elucidating such predominant virus-host interactions is key to characterizing viruses playing central roles in the microbial ecosystem and biogeochemical cycling. However, despite a growing number of viromic studies in freshwater systems (Skvortsov et al, 2016;Moon et al, 2017;Silva et al, 2017;Arkhipova et al, 2018), viruses infecting other typical freshwater bacterioplankton lineages, such as LD12 (Ca. Fonsibacter) (Henson et al, 2018) and Limnohabitans (Kasalický et al, 2013) have yet to be characterized.…”