Virus genomes from deep sea sediments expand the ocean megavirome and support independent origins of viral gigantism

AbstractThe Nucleocytoplasmic Large DNA Viruses (NCLDV) of eukaryotes (proposed order ”Megavirales”) include the families Poxviridae, Asfarviridae, Iridoviridae, Ascoviridae, Phycodnaviridae, Marseilleviridae, and Mimiviridae, as well as still unclassified Pithoviruses, Pandoraviruses, Molliviruses and Faustoviruses. Several of these virus groups include giant viruses, with genome and particle sizes exceeding those of many bacterial and archaeal cells. We explored the diversity of the NCLDV in deep-sea sediments from the Loki’s Castle hydrothermal vent area. Using metagenomics, we reconstructed 23 high quality genomic bins of novel NCLDV, 15 of which are closest related to Pithoviruses, 5 to Marseilleviruses, 1 to Iridoviruses, and 2 to Klosneuviruses. Some of the identified Pitho-like and Marseille-like genomes belong to deep branches in the phylogenetic tree of core NCLDV genes, substantially expanding the diversity and phylogenetic depth of the respective groups. The discovered viruses have a broad range of apparent genome sizes including putative giant members of the family Marseilleviridae, in agreement with multiple, independent origins of gigantism in different branches of the NCLDV. Phylogenomic analysis reaffirms the monophyly of the Pitho-Irido-Marseille branch of NCLDV. Similarly to other giant viruses, the Pitho-like viruses from Loki’s Castle encode translation systems components. Phylogenetic analysis of these genes indicates a greater bacterial contribution than detected previously. Genome comparison suggests extensive gene exchange between members of the Pitho-like viruses and Mimiviridae. Further exploration of the genomic diversity of “Megavirales” in additional sediment samples is expected to yield new insights into the evolution of giant viruses and the composition of the ocean megavirome.ImportanceGenomics and evolution of giant viruses is one of the most vigorously developing areas of virus research. Lately, metagenomics has become the main source of new virus genomes. Here we describe a metagenomic analysis of the genomes of large and giant viruses from deep sea sediments. The assembled new virus genomes substantially expand the known diveristy of the Nucleo-Cytoplasmic Large DNA Viruses of eukaryotes. The results support the concept of independent evolution of giant viruses from smaller ancestors in different virus branches.

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Virus Genomes from Deep Sea Sediments Expand the Ocean Megavirome and Support Independent Origins of Viral Gigantism

mBio ◽

10.1128/mbio.02497-18 ◽

2019 ◽

Vol 10 (2) ◽

Cited By ~ 23

Author(s):

Disa Bäckström ◽

Natalya Yutin ◽

Steffen L. Jørgensen ◽

Jennah Dharamshi ◽

Felix Homa ◽

...

Keyword(s):

Deep Sea ◽

Genomic Diversity ◽

Genome Comparison ◽

Phylogenomic Analysis ◽

Dna Viruses ◽

Deep Sea Sediments ◽

Giant Viruses ◽

Nucleocytoplasmic Large Dna Viruses ◽

Loki’S Castle ◽

Virus Genomes

ABSTRACT The nucleocytoplasmic large DNA viruses (NCLDV) of eukaryotes (proposed order, “Megavirales”) include the families Poxviridae, Asfarviridae, Iridoviridae, Ascoviridae, Phycodnaviridae, Marseilleviridae, and Mimiviridae, as well as still unclassified pithoviruses, pandoraviruses, molliviruses, and faustoviruses. Several of these virus groups include giant viruses, with genome and particle sizes exceeding those of many bacterial and archaeal cells. We explored the diversity of the NCLDV in deep sea sediments from the Loki’s Castle hydrothermal vent area. Using metagenomics, we reconstructed 23 high-quality genomic bins of novel NCLDV, 15 of which are related to pithoviruses, 5 to marseilleviruses, 1 to iridoviruses, and 2 to klosneuviruses. Some of the identified pithovirus-like and marseillevirus-like genomes belong to deep branches in the phylogenetic tree of core NCLDV genes, substantially expanding the diversity and phylogenetic depth of the respective groups. The discovered viruses, including putative giant members of the family Marseilleviridae, have a broad range of apparent genome sizes, in agreement with the multiple, independent origins of gigantism in different branches of the NCLDV. Phylogenomic analysis reaffirms the monophyly of the pithovirus-iridovirus-marseillevirus branch of the NCLDV. Similarly to other giant viruses, the pithovirus-like viruses from Loki’s Castle encode translation systems components. Phylogenetic analysis of these genes indicates a greater bacterial contribution than had been detected previously. Genome comparison suggests extensive gene exchange between members of the pithovirus-like viruses and Mimiviridae. Further exploration of the genomic diversity of Megavirales in additional sediment samples is expected to yield new insights into the evolution of giant viruses and the composition of the ocean megavirome. IMPORTANCE Genomics and evolution of giant viruses are two of the most vigorously developing areas of virus research. Lately, metagenomics has become the main source of new virus genomes. Here we describe a metagenomic analysis of the genomes of large and giant viruses from deep sea sediments. The assembled new virus genomes substantially expand the known diversity of the nucleocytoplasmic large DNA viruses of eukaryotes. The results support the concept of independent evolution of giant viruses from smaller ancestors in different virus branches.

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Advantages and Limits of Metagenomic Assembly and Binning of a Giant Virus

mSystems ◽

10.1128/msystems.00048-20 ◽

2020 ◽

Vol 5 (3) ◽

Author(s):

Frederik Schulz ◽

Julien Andreani ◽

Rania Francis ◽

Hadjer Boudjemaa ◽

Jacques Yaacoub Bou Khalil ◽

...

Keyword(s):

Sequence Data ◽

Giant Virus ◽

Dna Viruses ◽

Successful Recovery ◽

Metagenome Assembly ◽

Giant Viruses ◽

Nucleocytoplasmic Large Dna Viruses ◽

Metagenomic Assembly ◽

Virus Genomes ◽

Coding Potential

ABSTRACT Giant viruses have large genomes, often within the size range of cellular organisms. This distinguishes them from most other viruses and demands additional effort for the successful recovery of their genomes from environmental sequence data. Here, we tested the performance of genome-resolved metagenomics on a recently isolated giant virus, Fadolivirus, by spiking it into an environmental sample from which two other giant viruses were isolated. At high spike-in levels, metagenome assembly and binning led to the successful genomic recovery of Fadolivirus from the sample. A complementary survey of the major capsid protein indicated the presence of other giant viruses in the sample matrix but did not detect the two isolated from this sample. Our results indicate that genome-resolved metagenomics is a valid approach for the recovery of near-complete giant virus genomes given that sufficient clonal particles are present. However, our data also underline that a vast majority of giant viruses remain currently undetected, even in an era of terabase-scale metagenomics. IMPORTANCE The discovery of large and giant nucleocytoplasmic large DNA viruses (NCLDV) with genomes in the megabase range and equipped with a wide variety of features typically associated with cellular organisms was one of the most unexpected, intriguing, and spectacular breakthroughs in virology. Recent studies suggest that these viruses are highly abundant in the oceans, freshwater, and soil, impact the biology and ecology of their eukaryotic hosts, and ultimately affect global nutrient cycles. Genome-resolved metagenomics is becoming an increasingly popular tool to assess the diversity and coding potential of giant viruses, but this approach is currently lacking validation.

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Unique viruses that infect Archaea related to eukaryotes

10.1101/2021.07.29.454249 ◽

2021 ◽

Author(s):

Ian M Rambo ◽

Valerie De Anda ◽

Marguerite V Langwig ◽

Brett J Baker

Keyword(s):

Transcriptional Regulation ◽

Deep Sea ◽

Structural Proteins ◽

Genome Replication ◽

Dna Viruses ◽

Viral Genomes ◽

Archaeal Viruses ◽

Hydrothermal Sediments ◽

Nucleocytoplasmic Large Dna Viruses ◽

Globally Distributed

Asgard archaea are newly described microbes that are related to eukaryotes. Asgards are diverse and globally distributed, however, their viruses have not been described. Here we characterize seven viral genomes that infected Lokiarchaeota, Helarchaeota, and Thorarchaeota in deep-sea hydrothermal sediments. These viruses code for structural proteins similar to those in Caudovirales, as well as proteins distinct from those described in archaeal viruses. They also have genes common in eukaryotic nucleocytoplasmic large DNA viruses (NCLDVs), and are predicted to be capable of semi-autonomous genome replication, repair, epigenetic modifications, and transcriptional regulation. Moreover, Helarchaeota viruses may hijack host ubiquitin systems similar to eukaryotic viruses. This first glimpse of Asgard viruses reveals they have features of both prokaryotic and eukaryotic viruses, and provides insights into their roles in the ecology and evolution of these globally distributed microbes.

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Multiple evolutionary origins of giant viruses

F1000Research ◽

10.12688/f1000research.16248.1 ◽

2018 ◽

Vol 7 ◽

pp. 1840 ◽

Cited By ~ 28

Author(s):

Eugene V. Koonin ◽

Natalya Yutin

Keyword(s):

Life Forms ◽

Translation System ◽

Dna Viruses ◽

Evolutionary Forces ◽

Evolutionary Origins ◽

Cellular Life ◽

Giant Viruses ◽

Nucleocytoplasmic Large Dna Viruses ◽

Phylogenomic Analyses ◽

Definition Of

The nucleocytoplasmic large DNA viruses (NCLDVs) are a monophyletic group of diverse eukaryotic viruses that reproduce primarily in the cytoplasm of the infected cells and include the largest viruses currently known: the giant mimiviruses, pandoraviruses, and pithoviruses. With virions measuring up to 1.5 μm and genomes of up to 2.5 Mb, the giant viruses break the now-outdated definition of a virus and extend deep into the genome size range typical of bacteria and archaea. Additionally, giant viruses encode multiple proteins that are universal among cellular life forms, particularly components of the translation system, the signature cellular molecular machinery. These findings triggered hypotheses on the origin of giant viruses from cells, likely of an extinct fourth domain of cellular life, via reductive evolution. However, phylogenomic analyses reveal a different picture, namely multiple origins of giant viruses from smaller NCLDVs via acquisition of multiple genes from the eukaryotic hosts and bacteria, along with gene duplication. Thus, with regard to their origin, the giant viruses do not appear to qualitatively differ from the rest of the virosphere. However, the evolutionary forces that led to the emergence of virus gigantism remain enigmatic.

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A New Family of DNA Viruses Causing Disease in Crustaceans from Diverse Aquatic Biomes

mBio ◽

10.1128/mbio.02938-19 ◽

2020 ◽

Vol 11 (1) ◽

Cited By ~ 10

Author(s):

Kuttichantran Subramaniam ◽

Donald C. Behringer ◽

Jamie Bojko ◽

Natalya Yutin ◽

Abigail S. Clark ◽

...

Keyword(s):

Spiny Lobster ◽

Carcinus Maenas ◽

Shore Crab ◽

Phylogenomic Analysis ◽

Dna Viruses ◽

Content Type ◽

Complete Genomes ◽

The Caribbean ◽

Nucleocytoplasmic Large Dna Viruses ◽

Dikerogammarus Haemobaphes

ABSTRACT Panulirus argus virus 1 (PaV1) is the only known virus infecting the Caribbean spiny lobster (Panulirus argus) from the Caribbean Sea. Recently, related viruses, Dikerogammarus haemobaphes virus 1 (DhV1) and Carcinus maenas virus 1 (CmV1), have been detected in the demon shrimp (Dikerogammarus haemobaphes) and the European shore crab (Carcinus maenas), respectively, from sites in the United Kingdom. The virion morphology of these crustacean viruses is similar to that of iridoviruses. However, unlike iridoviruses and other nucleocytoplasmic large DNA viruses (NCLDVs), these viruses complete their morphogenesis in the host cell nucleus rather than in the cytoplasm. To date, these crustacean viruses have remained unclassified due to a lack of genomic data. Using an Illumina MiSeq sequencer, we sequenced the complete genomes of PaV1, CmV1, and DhV1. Comparative genome analysis shows that these crustacean virus genomes encode the 10 hallmark proteins previously described for the NCLDVs of eukaryotes, strongly suggesting that they are members of this group. With a size range of 70 to 74 kb, these are the smallest NCLDV genomes identified to date. Extensive gene loss, divergence of gene sequences, and the accumulation of low-complexity sequences reflect the extreme degradation of the genomes of these “minimal” NCLDVs rather than any direct relationship with the NCLDV ancestor. Phylogenomic analysis supports the classification of these crustacean viruses as a distinct family, “Mininucleoviridae,” within the pitho-irido-Marseille branch of the NCLDVs. IMPORTANCE Recent genomic and metagenomic studies have led to a dramatic expansion of the known diversity of nucleocytoplasmic large DNA viruses (NCLDVs) of eukaryotes, which include giant viruses of protists and important pathogens of vertebrates, such as poxviruses. However, the characterization of viruses from nonmodel hosts still lags behind. We sequenced the complete genomes of three viruses infecting crustaceans, the Caribbean spiny lobster, demon shrimp, and European shore crab. These viruses have the smallest genomes among the known NCLDVs, with losses of many core genes, some of which are shared with iridoviruses. The deterioration of the transcription apparatus is compatible with microscopic and ultrastructural observations indicating that these viruses replicate in the nucleus of infected cells rather than in the cytoplasm. Phylogenomic analysis indicates that these viruses are sufficiently distinct from all other NCLDVs to justify the creation of a separate family, for which we propose the name “Mininucleoviridae” (i.e., small viruses reproducing in the cell nucleus).

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Provirophages in the Bigelowiella genome bear testimony to past encounters with giant viruses

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1506469112 ◽

2015 ◽

Vol 112 (38) ◽

pp. E5318-E5326 ◽

Cited By ~ 47

Author(s):

Guillaume Blanc ◽

Lucie Gallot-Lavallée ◽

Florian Maumus

Keyword(s):

Host Cell ◽

Nuclear Genome ◽

Eukaryotic Cell ◽

Dna Viruses ◽

Unicellular Eukaryotes ◽

Indirect Control ◽

Double Stranded Dna ◽

Cell Mortality ◽

Giant Viruses ◽

Nucleocytoplasmic Large Dna Viruses

Virophages are recently discovered double-stranded DNA virus satellites that prey on giant viruses (nucleocytoplasmic large DNA viruses; NCLDVs), which are themselves parasites of unicellular eukaryotes. This coupled parasitism can result in the indirect control of eukaryotic cell mortality by virophages. However, the details of such tripartite relationships remain largely unexplored. We have discovered ∼300 predicted genes of putative virophage origin in the nuclear genome of the unicellular alga Bigelowiella natans. Physical clustering of these genes indicates that virophage genomes are integrated into the B. natans genome. Virophage inserts show high levels of similarity and synteny between each other, indicating that they are closely related. Virophage genes are transcribed not only in the sequenced B. natans strain but also in other Bigelowiella isolates, suggesting that transcriptionally active virophage inserts are widespread in Bigelowiella populations. Evidence that B. natans is also a host to NCLDV members is provided by the identification of NCLDV inserts in its genome. These putative large DNA viruses may be infected by B. natans virophages. We also identify four repeated elements sharing structural and genetic similarities with transpovirons—a class of mobile elements first discovered in giant viruses—that were probably independently inserted in the B. natans genome. We argue that endogenized provirophages may be beneficial to both the virophage and B. natans by (i) increasing the chances for the virophage to coinfect the host cell with an NCLDV prey and (ii) defending the host cell against fatal NCLDV infections.

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Comparative Analysis of Transcriptional Regulation Patterns: Understanding the Gene Expression Profile in Nucleocytoviricota

Pathogens ◽

10.3390/pathogens10080935 ◽

2021 ◽

Vol 10 (8) ◽

pp. 935

Author(s):

Fernanda Gil de Souza ◽

Jônatas Santos Abrahão ◽

Rodrigo Araújo Lima Rodrigues

Keyword(s):

Gene Expression ◽

Transcriptional Regulation ◽

Evolutionary History ◽

Dna Viruses ◽

Lack Of Information ◽

Multiplication Cycle ◽

Giant Viruses ◽

Nucleocytoplasmic Large Dna Viruses ◽

Transcriptional Process ◽

Evolutionary Aspects

The nucleocytoplasmic large DNA viruses (NCLDV) possess unique characteristics that have drawn the attention of the scientific community, and they are now classified in the phylum Nucleocytoviricota. They are characterized by sharing many genes and have their own transcriptional apparatus, which provides certain independence from their host’s machinery. Thus, the presence of a robust transcriptional apparatus has raised much discussion about the evolutionary aspects of these viruses and their genomes. Understanding the transcriptional process in NCLDV would provide information regarding their evolutionary history and a better comprehension of the biology of these viruses and their interaction with hosts. In this work, we reviewed NCLDV transcription and performed a comparative functional analysis of the groups of genes expressed at different times of infection of representatives of six different viral families of giant viruses. With this analysis, it was possible to observe a temporal profile of their gene expression and set of genes activated in specific phases throughout the multiplication cycle as a common characteristic of this group. Due to the lack of information regarding the transcriptional regulation process of this group of pathogens, we sought to provide information that contributes to and opens up the field for transcriptional studies of other viruses belonging to Nucleocytoviricota.

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Unique viruses that infect Archaea related to eukaryotes

10.21203/rs.3.rs-960995/v1 ◽

2021 ◽

Author(s):

Ian Rambo ◽

Valerie De Anda ◽

Marguerite Langwig ◽

Brett Baker

Keyword(s):

Deep Sea ◽

Structural Proteins ◽

Genome Replication ◽

Dna Viruses ◽

Viral Genomes ◽

Double Stranded Dna ◽

Archaeal Viruses ◽

Hydrothermal Sediments ◽

Nucleocytoplasmic Large Dna Viruses ◽

Globally Distributed

Abstract Asgard archaea are globally distributed, newly described microbes related to eukaryotes. Despite their importance, Asgard viruses have not been described. Here we characterize seven double-stranded DNA (dsDNA) viral genomes that infected Lokiarchaeota, Helarchaeota, and Thorarchaeota in deep-sea hydrothermal sediments. These viruses code for Caudovirales-like structural proteins, as well as proteins distinct from those described in archaeal viruses. They contain genes common in eukaryotic nucleocytoplasmic large DNA viruses (NCLDVs), and appear to be capable of semi-autonomous genome replication, repair, epigenetic modifications, and transcriptional regulation. Moreover, Helarchaeota viruses may hijack host ubiquitin systems similar to eukaryotic viruses. Recovery of these Asgard viral genomes reveals they contain features of both prokaryotic and eukaryotic viruses, and provides insights into their roles in the ecology and evolution of their hosts.

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A phylogenomic framework for charting the diversity and evolution of giant viruses

PLoS Biology ◽

10.1371/journal.pbio.3001430 ◽

2021 ◽

Vol 19 (10) ◽

pp. e3001430

Author(s):

Frank O. Aylward ◽

Mohammad Moniruzzaman ◽

Anh D. Ha ◽

Eugene V. Koonin

Keyword(s):

Giant Virus ◽

Phylogenomic Analysis ◽

Environmental Distribution ◽

Dna Viruses ◽

Giant Viruses ◽

Taxonomic Framework

Large DNA viruses of the phylum Nucleocytoviricota have recently emerged as important members of ecosystems around the globe that challenge traditional views of viral complexity. Numerous members of this phylum that cannot be classified within established families have recently been reported, and there is presently a strong need for a robust phylogenomic and taxonomic framework for these viruses. Here, we report a comprehensive phylogenomic analysis of the Nucleocytoviricota, present a set of giant virus orthologous groups (GVOGs) together with a benchmarked reference phylogeny, and delineate a hierarchical taxonomy within this phylum. We show that the majority of Nucleocytoviricota diversity can be partitioned into 6 orders, 32 families, and 344 genera, substantially expanding the number of currently recognized taxonomic ranks for these viruses. We integrate our results within a taxonomy that has been adopted for all viruses to establish a unifying framework for the study of Nucleocytoviricota diversity, evolution, and environmental distribution.

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