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Endogenous viral elements found in a marine protozoan have a function in defence against infection by giant viruses. Mavirus provirophages defend host protists Matthias Fischer and Thomas Hackl show here that endogenous viral elements found in a marine protozoan have a function in defence against infection by giant viruses. Virophages are a recently discovered group of DNA viruses that are obligate parasites of protist-infecting giant DNA viruses such as mimivirus. Fischer and Hackl find mavirus, a virophage sharing an evolutionary origin with a class of self-synthesizing DNA transposons called Maverick/Polinton elements, integrates into the genome of the marine protozoan Cafeteria roenbergensis . Superinfection of the protozoan in vitro with the giant virus Cafeteria roenbergensis virus (CroV) induces the production of infectious mavirus particles, which are released upon host cell lysis and can then suppress CroV replication in other CroV-infected flagellate populations. Endogenous viral elements are increasingly found in eukaryotic genomes 1 , yet little is known about their origins, dynamics, or function. Here we provide a compelling example of a DNA virus that readily integrates into a eukaryotic genome where it acts as an inducible antiviral defence system. We found that the virophage mavirus 2 , a parasite of the giant Cafeteria roenbergensis virus (CroV) 3 , integrates at multiple sites within the nuclear genome of the marine protozoan Cafeteria roenbergensis 4 . The endogenous mavirus is structurally and genetically similar to eukaryotic DNA transposons and endogenous viruses of the Maverick/Polinton family 5 , 6 , 7 . Provirophage genes are not constitutively expressed, but are specifically activated by superinfection with CroV, which induces the production of infectious mavirus particles. Virophages can inhibit the replication of mimivirus-like giant viruses and an anti-viral protective effect of provirophages on their hosts has been hypothesized 2 , 8 . We find that provirophage-carrying cells are not directly protected from CroV; however, lysis of these cells releases infectious mavirus particles that are then able to suppress CroV replication and enhance host survival during subsequent rounds of infection. The microbial host–parasite interaction described here involves an altruistic aspect and suggests that giant-virus-induced activation of provirophages might be ecologically relevant in natural protist populations.

Giant viruses ( Nucleocytoviricota ) are significant lethality agents of various eukaryotic hosts. Although metagenomics indicates their ubiquitous distribution, available giant virus isolates are restricted to a very small number of protist and algal hosts. Here we report on the first viral isolate that replicates in the amoeboflagellate Naegleria . This genus comprises the notorious human pathogen Naegleria fowleri , the causative agent of the rare but fatal primary amoebic meningoencephalitis. We have elucidated the structure and infection cycle of this giant virus, Catovirus naegleriensis (a.k.a. Naegleriavirus, NiV), and show its unique adaptations to its Naegleria host using fluorescence in situ hybridization, electron microscopy, genomics, and proteomics. Naegleriavirus is only the fourth isolate of the highly diverse subfamily Klosneuvirinae , and like its relatives the NiV genome contains a large number of translation genes, but lacks transfer RNAs (tRNAs). NiV has acquired genes from its Naegleria host, which code for heat shock proteins and apoptosis inhibiting factors, presumably for host interactions. Notably, NiV infection was lethal to all Naegleria species tested, including the human pathogen N. fowleri . This study expands our experimental framework for investigating giant viruses and may help to better understand the basic biology of the human pathogen N. fowleri . This is the first report on a virus infecting the amoeboflagellate Naegleria , including the lethal human pathogen N. fowleri . The new virus isolate, Catovirus naegleriensis (Naegleriavirus, NiV), shows hallmarks of giant viruses (Nucleocytoviricota) and unique adaptations to its protist host.

In this paper, the characteristics of 40 so far described virophages—parasites of giant viruses—are given, and the similarities and differences between virophages and satellite viruses, which also, like virophages, require helper viruses for replication, are described. The replication of virophages taking place at a specific site—the viral particle factory of giant viruses—and its consequences are presented, and the defence mechanisms of virophages for giant virus hosts, as a protective action for giant virus hosts—protozoa and algae—are approximated. The defence systems of giant viruses against virophages were also presented, which are similar to the CRISPR/Cas defence system found in bacteria and in Archea. These facts, and related to the very specific biological features of virophages (specific site of replication, specific mechanisms of their defensive effects for giant virus hosts, defence systems in giant viruses against virophages), indicate that virophages, and their host giant viruses, are biological objects, forming a ‘novelty’ in biology.

Giant viruses have remarkable genomic repertoires—blurring the line with cellular life—and act as top–down controls of eukaryotic plankton. However, to date only six cultured giant virus genomes are available from the pelagic ocean. We used at-sea flow cytometry with staining and sorting designed to target wild predatory eukaryotes, followed by DNA sequencing and assembly, to recover novel giant viruses from the Pacific Ocean. We retrieved four ‘PacV’ partial genomes that range from 421 to 1605 Kb, with 13 contigs on average, including the largest marine viral genomic assembly reported to date. Phylogenetic analyses indicate that three of the new viruses span a clade with deep-branching members of giant Mimiviridae , incorporating the Cafeteria roenbergensis virus, the uncultivated terrestrial Faunusvirus, one PacV from a choanoflagellate and two PacV with unclear hosts. The fourth virus, oPacV-421, is phylogenetically related to viruses that infect haptophyte algae. About half the predicted proteins in each PacV have no matches in NCBI nr ( e -value < 10 −5 ), totalling 1735 previously unknown proteins; the closest affiliations of the other proteins were evenly distributed across eukaryotes, prokaryotes and viruses of eukaryotes. The PacVs encode many translational proteins and two encode eukaryotic-like proteins from the Rh family of the ammonium transporter superfamily, likely influencing the uptake of nitrogen during infection. cPacV-1605 encodes a microbial viral rhodopsin (VirR) and the biosynthesis pathway for the required chromophore, the second finding of a choanoflagellate-associated virus that encodes these genes. In co-collected metatranscriptomes, 85% of cPacV-1605 genes were expressed, with capsids, heat shock proteins and proteases among the most highly expressed. Based on orthologue presence–absence patterns across the PacVs and other eukaryotic viruses, we posit the observed viral groupings are connected to host lifestyles as heterotrophs or phototrophs. This article is part of a discussion meeting issue ‘Single cell ecology’.

Giant viruses can control their eukaryotic host populations, shaping the ecology and evolution of aquatic microbial communities. Understanding the impact of the viruses’ own parasites, the virophages, on the control of microbial communities remains a challenge. Most virophages have two modes of infection. They can exist as free particles coinfecting host cells together with the virus, where they replicate while inhibiting viral replication. Virophages can also integrate into the host genome, replicate through host cell division and remain dormant until the host is infected with a virus, leading to virophage reactivation and replication without inhibiting viral replication. Both infection modes (reactivation vs. coinfection) occur within host-virus-virophage communities, and their relative contributions are expected to be dynamic and context dependent. The consequences of this dynamic regime for ecological and evolutionary dynamics remain unexplored. Here, we test whether and how the relative contribution of virophage infection modes influences the ecological dynamics of an experimental host-virus-virophage system and the evolutionary responses of the virophage. We indirectly manipulated the level of virophage (Mavirus) integration into the host (Cafeteria burkhardae) in the presence of the giant Cafeteria roenbergensis virus. Communities with higher virophage integration were characterized by lower population densities and reduced fluctuations in host and virus populations, whereas virophage fluctuations were increased. The virophage evolved toward lower inhibition and higher replication, but the evolution of these traits was weaker with higher virophage integration. Our study shows that differences in the virophage infection modes contributes to the complex interplay between virophages, viruses and hosts.

Background Endogenized giant viruses are emerging as major contributors to the genome evolution of microbial eukaryotes, with both degraded and fully functional latent viruses being found integrated in diverse lineages. The mechanisms that determine the fate of viral integrants are poorly understood, however. Acanthamoeba is a unicellular eukaryote known for undergoing lateral gene transfer (LGT) with viruses. Here we have leveraged chromosome-scale assemblies of two strains of Acanthamoeba , Neff and C3, to investigate the genomic mechanisms that mediate the fate of viral integrations in eukaryotic genomes. Results Viral integrations in the C3 and Neff genomes are largely non-overlapping and disproportionately found in sub-telomeric regions. Multiple partial copies of these insertions are found throughout the Neff genome, but they are not expressed, do not obviously encode functions associated with their own mobility, and are colonized by host mobile elements. Viral regions are hypermethylated and highly condensed, suggesting that the expression of recently acquired viral DNA is suppressed in heterochromatic regions. Conclusions We propose a model for the trajectory of viral sequences in Acanthamoeba : (i) integration of DNA from giant viruses, (ii) epigenetic suppression of the viral DNAs, allowing them to persist in the genome, and (iii) deterioration of viral genomes by point mutation, mobile element colonization, and intra- and inter-chromosomal recombination. Viral integrations in Acanthamoeba spp. are transient and may not have long-lasting effects on the fitness of the amoeba. Our work highlights the importance of host genome dynamics and epigenetic silencing for understanding the evolution of endogenized viral elements.

Giant viruses of protists are a diverse and likely ubiquitous group of organisms. Here, we describe Jyvaskylavirus, the first giant virus isolated from Finland. This clade B marseillevirus was found in Acanthamoeba castellanii from a composting soil sample in Jyväskylä, Central Finland. Its genome shares similarities with other marseilleviruses. Helium ion microscopy and electron microscopy of infected cells unraveled stages of the Jyvaskylavirus life cycle. We reconstructed the Jyvaskylavirus particle to 6.3 Å resolution using cryo-electron microscopy. The ~2500 Å diameter virion displays structural similarities to other Marseilleviridae giant viruses. The capsid comprises of 9240 copies of the major capsid protein, encoded by open reading frame (ORF) 184, which possesses a double jellyroll fold arranged in trimers forming pseudo-hexameric capsomers. Below the capsid shell, the internal membrane vesicle encloses the genome. Through cross-structural and -sequence comparisons with other Marseilleviridae using AI-based software in model building and prediction, we elucidated ORF142 as the penton protein, which plugs the 12 vertices of the capsid. Five additional ORFs were identified, with models predicted and fitted into densities that either cap the capsomers externally or stabilize them internally. The isolation of Jyvaskylavirus suggests that these viruses may be widespread in the boreal environment and provide structural insights extendable to other marseilleviruses. Viruses are everywhere. Some viruses can cause illness in humans, which has led to people often viewing them as threats. But most viruses are harmless to humans. Many viruses target microbes instead of humans. These viruses likely play essential roles in maintaining a healthy balance in ecosystems by preventing overpopulation of their target microbes. Yet, scientists know very little about most viruses and their role in ecosystems. Scientists have recently discovered a special group of giant viruses that target microscopic creatures called amoebas. The giant viruses that target them are much larger than most viruses and have some other unique features, such as having large genomes. A tough outer coating provides the structural reinforcement necessary to support their large size. Most of the giant viruses identified so far have been discovered in Europe and South America. A few have been found in North Africa, India, Japan and Siberia. But scientists still do not know how many giant viruses there are and where else they exist around the world. They are also still learning about the structures that allow these giant viruses to be so large. Almeida et al. describe the first giant virus ever discovered in Finland. In the experiments, the researchers mixed a type of amoeba called Acanthamoeba castellanii with environmental samples and monitored the amoebas for infection. The experiments revealed a giant amoeba-infecting virus in a compost sample. Almeida et al. named it Jyvaskylavirus after the city from which the compost sample came. The investigators then sequenced the virus’ DNA and used a cutting-edge imaging tool called cryogenic electron microscopy and artificial intelligence to determine details of the viral structure. This detailed structure of Jyvaskylavirus provided information about the structure of giant viruses and key structural proteins, which may also benefit scientists studying other kinds of viruses. The experiments confirm that giant viruses are a part of Finland’s boreal forest ecosystem, extending the known range of these unusual viruses. More studies are needed to identify the full range of giant viruses worldwide and to understand their role in ecosystems.

Giant viruses are a group of eukaryotic double-stranded DNA viruses with large virion and genome size that challenged the traditional view of virus. Newly isolated strains and sequenced genomes in the last two decades have substantially advanced our knowledge of their host diversity, gene functions, and evolutionary history. Giant viruses are now known to infect hosts from all major supergroups in the eukaryotic tree of life, which predominantly comprises microbial organisms. The seven well-recognized viral clades (taxonomic families) have drastically different host range. Mimiviridae and Phycodnaviridae, both with notable intrafamilial genome variation and high abundance in environmental samples, have members that infect the most diverse eukaryotic lineages. Laboratory experiments and comparative genomics have shed light on the unprecedented functional potential of giant viruses, encoding proteins for genetic information flow, energy metabolism, synthesis of biomolecules, membrane transport, and sensing that allow for sophisticated control of intracellular conditions and cell-environment interactions. Evolutionary genomics can illuminate how current and past hosts shape viral gene repertoires, although it becomes more obscure with divergent sequences and deep phylogenies. Continued works to characterize giant viruses from marine and other environments will further contribute to our understanding of their host range, coding potential, and virus-host coevolution.

Since the discovery of mimivirus, numerous giant viruses associated with free-living amoebae have been described. The genome of giant viruses can be more than 2.5 megabases, and virus particles can exceed the size of many bacteria. The unexpected characteristics of these viruses have made them intriguing research targets and, as a result, studies focusing on their interactions with their amoeba host have gained increased attention. Studies have shown that giant viruses can establish host–pathogen interactions, which have not been previously demonstrated, including the unprecedented interaction with a new group of small viruses, called virophages, that parasitize their viral factories. In this brief review, we present recent advances in virophage–giant virus–host interactions and highlight selected studies involving interactions between giant viruses and amoebae. These unprecedented interactions involve the giant viruses mimivirus, marseillevirus, tupanviruses and faustovirus, all of which modulate the amoeba environment, affecting both their replication and their spread to new hosts.

The last decade has been marked by two eminent discoveries that have changed our perception of the virology field: The discovery of giant viruses and a distinct new class of viral agents that parasitize their viral factories, the virophages. Coculture and metagenomics have actively contributed to the expansion of the virophage family by isolating dozens of new members. This increase in the body of data on virophage not only revealed the diversity of the virophage group, but also the relevant ecological impact of these small viruses and their potential role in the dynamics of the microbial network. In addition, the isolation of virophages has led us to discover previously unknown features displayed by their host viruses and cells. In this review, we present an update of all the knowledge on the isolation, biology, genomics, and morphological features of the virophages, a decade after the discovery of their first member, the Sputnik virophage. We discuss their parasitic lifestyle as bona fide viruses of the giant virus factories, genetic parasites of their genomes, and then their role as a key component or target for some host defense mechanisms during the tripartite virophage–giant virus–host cell interaction. We also present the latest advances regarding their origin, classification, and definition that have been widely discussed.