Role of Phylogenetic Structure in the Dynamics of Coastal Viral Assemblages

Abstract

Marine microbes, including viruses, are an essential part of the marine ecosystem, forming the base of the foodweb and driving biogeochemical cycles. Within this system, the composition of viral assemblages changes markedly with time, with some of these changes being repeatable through time; however, the extent to which these dynamics are reflected within versus among evolutionarily-related groups of viruses is largely unexplored. To examine these dynamics, changes in the composition of two groups of ecologically important viruses and communities of their potential hosts were sampled every two weeks for 13 months at a coastal site in British Columbia, Canada. We sequenced two marker genes for viruses, the major capsid protein (gp23) of T4-like phages and their relatives, and the RNA-dependent RNA polymerase (RdRp) of marnavirus-like RNA viruses, as well as their bacterial and eukaryotic host communities, the genes encoding 16S and 18S ribosomal RNA (rRNA). There were strong lagged correlations between viral diversity and community similarity of putative hosts implying that the viruses influenced the composition of the host communities. The results showed that for both viral assemblages, the dominant clusters of phylogenetically-related viruses shifted over time and this was correlated with environmental changes. Viral clusters contained many ephemeral taxa and few persistent taxa, but within a viral assemblage the ephemeral and persistent taxa were closely related implying ecological dynamics within these clusters. Furthermore, these dynamics occurred in both the RNA and DNA viral assemblages surveyed, implying that this structure is common in natural viral assemblages. Importance Viruses are major agents of microbial mortality in marine systems; yet, little is known about changes in the composition of viral assemblages in relation to that of the microbial communities that they infect. Here, we sampled coastal seawater every two weeks for one year and used high-throughput sequencing of marker genes to follow changes in the composition of two groups of ecologically important viruses, as well as the communities of bacteria and protists that serve as their respective hosts. Different subsets of genetically related viruses dominated at different times. These results demonstrate that although the genetic composition of viral genotypes is highly dynamic temporally, for the most part the shuffling of genotypes occurs within a few clusters of phylogenetically related viruses. Thus, it appears that even in temperate coastal waters with large seasonal changes the highly dynamic shuffling of viral genotypes largely occurs within a few subsets of related individuals.

vAMPirus: A versatile amplicon processing and analysis program for studying viruses

“…Targeted gene sequencing is increasingly being applied to explore spatiotemporal patterns of viral diversity (Adriaenssens & Cowan, 2014;Finke & Suttle, 2019;Frantzen & Holo, 2019;Gustavsen & Suttle, 2021;Howe-Kerr et al, 2022;Y. Li et al, 2018;Montalvo-Proaño et al, 2017;Prodinger et al, 2020;Short et al, 2010;Tong et al, 2016).…”

“…Amplicon sequencing is a targeted, polymerase chain reaction (PCR)-based HTS approach that allows deep characterization of genetic variants within virus populations (Short et al 2010). The targeted nature of amplicon sequencing reduces the economic and computational investment required for spatiotemporal investigations of virus communities at ecologically relevant scales (see Finke & Suttle, 2019;Frantzen & Holo, 2019;Gustavsen & Suttle, 2021;Howe-Kerr et al, 2022;Montalvo-Proaño et al, 2017). The number of studies leveraging virus amplicon sequencing has increased rapidly over the last two decades (e.g., 16 peer-reviewed publications in 1998 compared to 127 in 2021 based on a Web of Science search of 'virus amplicon sequencing', November 2022).…”

Over two decades of research on the marine RNA virosphere

“…Four monophyletic clades of picorna‐like viruses probably representing at least two new viral families were identified using sequence analysis, showing the potential of a single‐gene survey for RNA viral discovery in marine environments [ 107 ]. In addition to viral discovery, more recent studies based on RdRp‐targeted RT‐PCR also revealed the temporal and spatial variation of picorna‐like ssRNA viruses in the coastal areas of British Columbia by combining location and time‐series sampling [ 108 ], the predominant role of picornavirads in the pool of RNA viruses in tropical coastal seawater samples through additional metagenomic methods [ 109 ], and the impact of RNA viruses on the community composition of the potential host with extra amplicon sequencing of marker genes [ 108 , 110 ]. Notably, these data gave an initial glimpse into the diversity, richness, and ecology of a particular RNA virus group in the ocean, but this method provided little information about genetic diversity (i.e., other viral genes) and is inapplicable to the global and comprehensive assessment of RNA viruses, especially at the genome and function levels, because of underrepresentation of all viral groups and the lack of complete genetic materials.…”

World Society for Virology first international conference: Tackling global virus epidemics

“…Globally 91.4% of all sequences from ocean microbes are unidentifiable organisms, thus our knowledge is miniscule. Viruses are key players in oceans – they catalyze the cycling of nutrients, and are critical to global biogeochemical cycles ( Gao et al, 2021 ; Gustavsen and Suttle, 2021 ).…”