Spindle-shaped viruses infect marine ammonia-oxidizing thaumarchaea

Abstract

Ammonia-oxidizing archaea (AOA) from the phylum Thaumarchaeota are ubiquitous in marine ecosystems and play a prominent role in carbon and nitrogen cycling. Previous studies have suggested that, like all microbes, thaumarchaea are infected by viruses and that viral predation has a profound impact on thaumarchaeal functioning and mortality, thereby regulating global biogeochemical cycles. However, not a single virus capable of infecting thaumarchaea has been reported thus far. Here we describe the isolation and characterization of three Nitrosopumilus spindle-shaped viruses (NSVs) that infect AOA and are distinct from other known marine viruses. Although NSVs have a narrow host range, they efficiently infect autochthonous Nitrosopumilus strains and display high rates of adsorption to their host cells. The NSVs have linear double-stranded DNA genomes of ∼28 kb that do not display appreciable sequence similarity to genomes of other known archaeal or bacterial viruses and could be considered as representatives of a new virus family, the “Thaspiviridae.” Upon infection, NSV replication leads to inhibition of AOA growth, accompanied by severe reduction in the rate of ammonia oxidation and nitrite reduction. Nevertheless, unlike in the case of lytic bacteriophages, NSV propagation is not associated with detectable degradation of the host chromosome or a decrease in cell counts. The broad distribution of NSVs in AOA-dominated marine environments suggests that NSV predation might regulate the diversity and dynamics of AOA communities. Collectively, our results shed light on the diversity, evolution, and potential impact of the virosphere associated with ecologically important mesophilic archaea.

Extraordinary diversity of viruses in deep‐sea sediments as revealed by metagenomics without prior virion separation

“…Interestingly, three complete genomes from archaeal viruses, including two thaumarchaeal viruses, were identified. However, these thaumarchaeal virus genomes are different from those reported previously (Ahlgren et al ., 2017; 2019; Kim et al ., 2019; Lopez‐Perez et al ., 2019).…”

Taxonomy of prokaryotic viruses: 2018-2019 update from the ICTV Bacterial and Archaeal Viruses Subcommittee

“…The virions of Nitrosopumilus spindle-shaped virus 1 (NSV1) measure 64 ± 3 nm in diameter and 112 ± 6 nm in length, with a short tail at one pole [20]. This morphology is similar to that of fuselloviruses and the halspivirus His1 [13].…”

“…NSV1 encodes 48 predicted proteins, only one of which (protein-primed family B DNA polymerase) displays significant sequence similarity to the proteins of other known archaeal or bacterial viruses. NSV1 is the first and, thus far, the only virus isolated on ammonia-oxidising archaea of the phylum Thaumarchaeota [20]. NSV1 has been classified into the species Nitmarvirus NSV1 within the genus Nitmarvirus (for Nitrosopumilus maritimus virus) and the new family Thaspiviridae (Tha-for thaumarchaeal, spi-for spindle-shaped viruses).…”

Diverse viruses carrying genes for microbial extremotolerance in the Atacama Desert hyperarid soil

“…Notably, we also identified a putative thaumarchaeal virus matched to eight thaumarchaeal MAGs found across all three sampling sites. While recent studies have isolated a novel family of viruses infecting marine Thaumarchaeota(52), and a provirus in order Caudovirales in mesophilic soil Nitrososphaera viennensis(53,54), very little is known about lytic viruses infecting soil Thaumarchaeota, despite their ubiquity and abundance in many terrestrial ecosystems(55,56).The abundance and diversity of the viruses in the Atacama Desert soils are surprising considering that the microorganisms that inhabit these soils are low in both biodiversity and biomass. Typically, groups of viruses infecting the same host exchange genetic materials, forming genotypic clusters.…”