Explore the vast range of titles available.

Giant viruses are remarkable for their large genomes, often rivaling those of small bacteria, and for having genes thought exclusive to cellular life. Most isolated to date infect nonmarine protists, leaving their strategies and prevalence in marine environments largely unknown. Using eukaryotic single-cell metagenomics in the Pacific, we discovered a Mimiviridae lineage of giant viruses, which infects choanoflagellates, widespread protistan predators related to metazoans. The ChoanoVirus genomes are the largest yet from pelagic ecosystems, with 442 of 862 predicted proteins lacking known homologs. They are enriched in enzymes formodifying organic compounds, including degradation of chitin, an abundant polysaccharide in oceans, and they encode 3 divergent type-1 rhodopsins (VirR) with distinct evolutionary histories from those that capture sunlight in cellular organisms. One (VirRDTS) is similar to the only other putative rhodopsin from a virus (PgV) with a known host (a marine alga). Unlike the algal virus, ChoanoViruses encode the entire pigment biosynthesis pathway and cleavage enzyme for producing the required chromophore, retinal. We demonstrate that the rhodopsin shared by ChoanoViruses and PgV binds retinal and pumps protons. Moreover, our 1.65-Å resolved VirRDTS crystal structure and mutational analyses exposed differences from previously characterized type-1 rhodopsins, all of which come from cellular organisms. Multiple VirR types are present in metagenomes from across surface oceans, where they are correlated with and nearly as abundant as a canonical marker gene from Mimiviridae . Our findings indicate that light-dependent energy transfer systems are likely common components of giant viruses of photosynthetic and phagotrophic unicellular marine eukaryotes.

Large dsDNA viruses are involved in the population control of many globally distributed species of eukaryotic phytoplankton and have a prominent role in bloom termination. The genus Phaeocystis (Haptophyta , Prymnesiophyceae) includes several high-biomass-forming phytoplankton species, such as Phaeocystis globosa , the blooms of which occur mostly in the coastal zone of the North Atlantic and the North Sea. Here, we report the 459,984-bp-long genome sequence of P. globosa virus strain PgV-16T, encoding 434 proteins and eight tRNAs and, thus, the largest fully sequenced genome to date among viruses infecting algae. Surprisingly, PgV-16T exhibits no phylogenetic affinity with other viruses infecting microalgae (e.g., phycodnaviruses), including those infecting Emiliania huxleyi , another ubiquitous bloom-forming haptophyte. Rather, PgV-16T belongs to an emerging clade (the Megaviridae) clustering the viruses endowed with the largest known genomes, including Megavirus, Mimivirus (both infecting acanthamoeba), and a virus infecting the marine microflagellate grazer Cafeteria roenbergensis . Seventy-five percent of the best matches of PgV-16T–predicted proteins correspond to two viruses [Organic Lake phycodnavirus (OLPV)1 and OLPV2] from a hypersaline lake in Antarctica (Organic Lake), the hosts of which are unknown. As for OLPVs and other Megaviridae, the PgV-16T sequence data revealed the presence of a virophage-like genome. However, no virophage particle was detected in infected P. globosa cultures. The presence of many genes found only in Megaviridae in its genome and the presence of an associated virophage strongly suggest that PgV-16T shares a common ancestry with the largest known dsDNA viruses, the host range of which already encompasses the earliest diverging branches of domain Eukarya.

Chrysochromulina parva ( C. parva ) is a eukaryotic freshwater haptophyte algae found in lakes and rivers worldwide. It is known to be infected by viruses, yet knowledge of the diversity and activity of these viruses is still very limited. Based on sequences of PCR-amplified DNA polymerase B ( polB) gene fragments, Chrysochromulina parva virus BQ1 (CpV-BQ1) was the first known lytic agent of C. parva , and was considered a member of the virus family Phycodnaviridae , order Algavirales . However, the genome of a different C. parva -infecting virus (CpV-BQ2, or Tethysvirus ontarioense ) from another virus family, the Mesomimiviridae , order Imitervirales , was the first sequenced. Here, we report the complete genome sequence of the putative phycodnavirus CpV-BQ1, accession PQ783904. The complete CpV-BQ1 genome sequence is 165,454 bp with a GC content of 32.32% and it encodes 193 open reading frames. Phylogenetic analyses of several virus hallmark genes including the polB , the late gene transcription factor (VLTF-3), and the putative A32-like virion packaging ATPase (Viral A32) all demonstrate that CpV-BQ1 is most closely related to other viruses in the phylum Megaviricetes within the order Algavirales , family Phycodnaviridae .

Viruses are abundant ubiquitous members of microbial communities and in the marine environment affect population structure and nutrient cycling by infecting and lysing primary producers. Antarctic lakes are microbially dominated ecosystems supporting truncated food webs in which viruses exert a major influence on the microbial loop. Here we report the discovery of a virophage (relative of the recently described Sputnik virophage) that preys on phycodnaviruses that infect prasinophytes (phototrophic algae). By performing metaproteogenomic analysis on samples from Organic Lake, a hypersaline meromictic lake in Antarctica, complete virophage and near-complete phycodnavirus genomes were obtained. By introducing the virophage as an additional predator of a predator-prey dynamic model we determined that the virophage stimulates secondary production through the microbial loop by reducing overall mortality of the host and increasing the frequency of blooms during polar summer light periods. Virophages remained abundant in the lake 2 y later and were represented by populations with a. high level of major capsid protein sequence variation (25-100% identity). Virophage signatures were also found in neighboring Ace Lake (in abundance) and in two tropical lakes (hypersaline and fresh), an estuary, and an ocean upwelling site. These findings indicate that virophages regulate host-virus interactions, influence overall carbon flux in Organic Lake, and play previously unrecognized roles in diverse aquatic ecosystems.

Nucleo-cytoplasmic large DNA viruses (NCLDVs) constitute a group of eukaryotic viruses that can have crucial ecological roles in the sea by accelerating the turnover of their unicellular hosts or by causing diseases in animals. To better characterize the diversity, abundance and biogeography of marine NCLDVs, we analyzed 17 metagenomes derived from microbial samples (0.2–1.6 μm size range) collected during the Tara Oceans Expedition. The sample set includes ecosystems under-represented in previous studies, such as the Arabian Sea oxygen minimum zone (OMZ) and Indian Ocean lagoons. By combining computationally derived relative abundance and direct prokaryote cell counts, the abundance of NCLDVs was found to be in the order of 10 4 –10 5 genomes ml −1 for the samples from the photic zone and 10 2 –10 3 genomes ml −1 for the OMZ. The Megaviridae and Phycodnaviridae dominated the NCLDV populations in the metagenomes, although most of the reads classified in these families showed large divergence from known viral genomes. Our taxon co-occurrence analysis revealed a potential association between viruses of the Megaviridae family and eukaryotes related to oomycetes. In support of this predicted association, we identified six cases of lateral gene transfer between Megaviridae and oomycetes. Our results suggest that marine NCLDVs probably outnumber eukaryotic organisms in the photic layer (per given water mass) and that metagenomic sequence analyses promise to shed new light on the biodiversity of marine viruses and their interactions with potential hosts.

Endogenous viral elements (EVEs)—viruses that have integrated their genomes into those of their hosts—are prevalent in eukaryotes and have an important role in genome evolution 1 , 2 . The vast majority of EVEs that have been identified to date are small genomic regions comprising a few genes 2 , but recent evidence suggests that some large double-stranded DNA viruses may also endogenize into the genome of the host 1 . Nucleocytoplasmic large DNA viruses (NCLDVs) have recently become of great interest owing to their large genomes and complex evolutionary origins 3 – 6 , but it is not yet known whether they are a prominent component of eukaryotic EVEs. Here we report the widespread endogenization of NCLDVs in diverse green algae; these giant EVEs reached sizes greater than 1 million base pairs and contained as many as around 10% of the total open reading frames in some genomes, substantially increasing the scale of known viral genes in eukaryotic genomes. These endogenized elements often shared genes with host genomic loci and contained numerous spliceosomal introns and large duplications, suggesting tight assimilation into host genomes. NCLDVs contain large and mosaic genomes with genes derived from multiple sources, and their endogenization represents an underappreciated conduit of new genetic material into eukaryotic lineages that can substantially impact genome composition. The authors show that large endogenous viral elements derived from giant viruses are prominent components of green algal genomes.

The virosphere is ubiquitous, but we have yet to characterize many environments where viruses exist. In an industrial polyculture of microalgae, a wealth of viruses persist, their diversity and dynamics changing over time and consequently give evidence of their evolution and ecological strategies. Several notable infectious agents of the culture’s algae appear, including giant viruses, polinton-like viruses, and a virophage. As our reliance and interest in algal compound-based cosmetics, pharmaceuticals, and bio-plastics increases, so must our understanding of these systems, including the unique viruses that appear there.

The majority of giant algal viruses belong to the family Phycodnaviridae, class Algavirales, phylum Nucleocytoviricota. Among them, the genus Chlorovirus is the most studied, with three recognized groups based on genomics and host range, although many fundamental questions remain to be elucidated, particularly regarding their diversity. In this study, we focus on betachloroviruses, a poorly explored subgroup that infects the alga Micractinium conductrix Pbi. Here, we describe the isolation and genomic analysis of 11 new betachloroviruses from water samples collected in Nebraska, USA. With 25 fully sequenced genomes now available, we assessed the genomic diversity of these viruses. They have double-stranded DNA genomes ranging from 295 to 374 kbp, encoding hundreds of ORFs, of which a large number (~40%) lack known function. Comparative genomics and phylogenetic analyses revealed three species of betachlorovirus, each with high intra-species genomic identity. Notably, some isolates with over 99.5% genomic identity display markedly different plaque phenotypes, which led us to propose the use of the term genomovar among giant algal viruses, a concept potentially applicable to other giant viral groups yet to be explored. Altogether, this work advances our understanding of betachloroviruses and highlights the importance of linking viral genotype to phenotype, opening new avenues for exploring the diversity of giant algal viruses.

Marine viruses constitute a major ecological and evolutionary driving force in the marine ecosystems. However, their dispersal mechanisms remain underexplored. Here we follow the dynamics of Emiliania huxleyi viruses ( Eh V) that infect the ubiquitous, bloom-forming phytoplankton E. huxleyi and show that Eh V are emitted to the atmosphere as primary marine aerosols. Using a laboratory-based setup, we showed that the dynamic of Eh V aerial emission is strongly coupled to the host–virus dynamic in the culture media. In addition, we recovered Eh V DNA from atmospheric samples collected over an E. huxleyi bloom in the North Atlantic, providing evidence for aerosolization of marine viruses in their natural environment. Decay rate analysis in the laboratory revealed that aerosolized viruses can remain infective under meteorological conditions prevailing during E. huxleyi blooms in the ocean, allowing potential dispersal and infectivity over hundreds of kilometers. Based on the combined laboratory and in situ findings, we propose that atmospheric transport of Eh V is an effective transmission mechanism for spreading viral infection over large areas in the ocean. This transmission mechanism may also have an important ecological impact on the large-scale host–virus “arms race” during bloom succession and consequently the turnover of carbon in the ocean. Significance Marine viruses constitute a major ecological and evolutionary driving force in marine ecosystems and are responsible for cycling of major nutrients; however, their dispersal mechanisms remain underexplored. By using one of the most established host–pathogen planktonic model systems we provide strong evidence that specific viruses of marine coccolithophores can be transmitted and stay infective as marine aerosols. Being transported by the wind, phytoplankton viruses can be conveyed long distances and transmit the infection to remote locations to which coccolithophore blooms can be extended. We show that this effective transmission mechanism that has been studied in human, animal, and plant diseases could play an important role in host–virus dynamics during phytoplankton blooms in the ocean.

The genus Micromonas comprises phytoplankton that show among the widest latitudinal distributions on Earth, and members of this genus are recurrently infected by prasinoviruses in contrasted thermal ecosystems. In this study, we assessed how temperature influences the interplay between the main genetic clades of this prominent microalga and their viruses. The growth of three Micromonas strains (Mic-A, Mic-B, Mic-C) and the stability of their respective lytic viruses (MicV-A, MicV-B, MicV-C) were measured over a thermal range of 4–32.5 °C. Similar growth temperature optima ( T opt ) were predicted for all three hosts but Mic-B exhibited a broader thermal tolerance than Mic-A and Mic-C, suggesting distinct thermoacclimation strategies. Similarly, the MicV-C virus displayed a remarkable thermal stability compared with MicV-A and MicV-B. Despite these divergences, infection dynamics showed that temperatures below T opt lengthened lytic cycle kinetics and reduced viral yield and, notably, that infection at temperatures above T opt did not usually result in cell lysis. Two mechanisms operated depending on the temperature and the biological system. Hosts either prevented the production of viral progeny or maintained their ability to produce virions with no apparent cell lysis, pointing to a possible switch in the viral life strategy. Hence, temperature changes critically affect the outcome of Micromonas infection and have implications for ocean biogeochemistry and evolution.