Large-scale invasion of unicellular eukaryotic genomes by integrating DNA viruses

Proceedings of the National Academy of Sciences, Journal Year: 2023, Volume and Issue: 120(16)

Published: April 10, 2023

Eukaryotic genomes contain a variety of endogenous viral elements (EVEs), which are mostly derived from RNA and ssDNA viruses that no longer functional considered to be "genomic fossils." Genomic surveys EVEs, however, strongly biased toward animals plants, whereas protists, represent the majority eukaryotic diversity, remain poorly represented. Here, we show protist harbor tens thousands diverse, ~14 40 kbp long dsDNA viruses. These composed virophages, Polinton-like viruses, related entities, have remained hitherto hidden owing poor sequence conservation between virus groups their repetitive nature precluded accurate short-read assembly. We long-read sequencing technology is ideal for resolving insertions. Many EVEs appear intact, most encode integrases, suggests they actively colonized hosts across tree eukaryotes. also found evidence gene expression in host transcriptomes closely virophage abundant metagenomes, indicating many probably

Language: Английский

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Giant Starship Elements Mobilize Accessory Genes in Fungal Genomes

Molecular Biology and Evolution, Journal Year: 2022, Volume and Issue: 39(5)

Published: May 1, 2022

Accessory genes are variably present among members of a species and reservoir adaptive functions. In bacteria, differences in gene distributions individuals largely result from mobile elements that acquire disperse accessory as cargo. contrast, the impact cargo-carrying on eukaryotic evolution remains unknown. Here, we show variation genome content within multiple fungal is facilitated by Starships, newly discovered group massive 110 kb long average, share conserved components, carry diverse arrays genes. We identified hundreds Starship-like regions across every major class filamentous Ascomycetes, including 28 distinct Starships range 27 to 393 last shared common ancestor ca. 400 Ma. Using new long-read assemblies plant pathogen Macrophomina phaseolina, characterize four additional whose activities contribute standing structure content. One these elements, Voyager, inserts into 5S rDNA contains candidate virulence factor increasing copy number has contrasting associations with pathogenic saprophytic growth, suggesting Voyager's activity underlies an ecological trade-off. propose analogs bacterial integrative conjugative based parallels between their components may therefore represent first dedicated agents active transfer eukaryotes. Our results suggest have shaped genomes for millions years reveal concerted route throughout entire phylum.

Language: Английский

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Virologs, viral mimicry, and virocell metabolism: the expanding scale of cellular functions encoded in the complex genomes of giant viruses

FEMS Microbiology Reviews, Journal Year: 2023, Volume and Issue: 47(5)

Published: Sept. 1, 2023

The phylum Nucleocytoviricota includes the largest and most complex viruses known. These "giant viruses" have a long evolutionary history that dates back to early diversification of eukaryotes, over time they evolved elaborate strategies for manipulating physiology their hosts during infection. One captivating these mechanisms involves use genes acquired from host-referred here as viral homologs or "virologs"-as means promoting propagation. best-known examples are involved in mimicry, which machinery "imitates" immunomodulatory elements vertebrate defense system. But recent findings highlighted vast rapidly expanding array other virologs include many not typically found viruses, such those translation, central carbon metabolism, cytoskeletal structure, nutrient transport, vesicular trafficking, light harvesting. Unraveling roles infection well pathways through functional repertoires by important frontiers at forefront giant virus research.

Language: Английский

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Systematic identification of cargo-mobilizing genetic elements reveals new dimensions of eukaryotic diversity

Nucleic Acids Research, Journal Year: 2024, Volume and Issue: 52(10), P. 5496 - 5513

Published: April 15, 2024

Abstract Cargo-mobilizing mobile elements (CMEs) are genetic entities that faithfully transpose diverse protein coding sequences. Although common in bacteria, we know little about eukaryotic CMEs because no appropriate tools exist for their annotation. For example, Starships giant fungal whose functions largely unknown they require time-intensive manual curation. To address this knowledge gap, developed starfish, a computational workflow high-throughput CME We applied starfish to 2 899 genomes of 1 649 species and found recovers known with 95% combined precision recall while expanding the number annotated ten-fold. Extant Starship diversity is partitioned into 11 families differ enrichment patterns across classes. cargo changes rapidly such from same family substantially functional repertoires, which predicted contribute biological processes as metabolism. Many have convergently evolved insert 5S rDNA AT-rich sequence others integrate random locations, revealing both specialist generalist strategies persistence. Our work establishes framework advancing element biology provides means investigate an emerging dimension diversity, within genomes.

Language: Английский

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DNA methylation enables recurrent endogenization of giant viruses in an animal relative

Science Advances, Journal Year: 2024, Volume and Issue: 10(28)

Published: July 12, 2024

5-Methylcytosine (5mC) is a widespread silencing mechanism that controls genomic parasites. In eukaryotes, 5mC has gained complex roles in gene regulation beyond parasite control, yet also been lost many lineages. The causes for retention and its consequences are still poorly understood. Here, we show the protist closely related to animals Amoebidium appalachense features both transposon body methylation, pattern reminiscent of invertebrates plants. Unexpectedly, hypermethylated regions derive from viral insertions, including hundreds endogenized giant viruses, contributing 14% proteome. Using combination inhibitors assays, demonstrate silences these virus insertions. Moreover, alternative isolates polymorphic highlighting dynamic process infection, endogenization, purging. Our results indicate critical controlled coexistence newly acquired DNA into eukaryotic genomes, making unique model understand hybrid origins DNA.

Language: Английский

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Evolutionary genomics of the emergence of brown algae as key components of coastal ecosystems

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2024, Volume and Issue: unknown

Published: Feb. 20, 2024

SUMMARY Brown seaweeds are keystone species of coastal ecosystems, often forming extensive underwater forests, that under considerable threat from climate change. Despite their ecological and evolutionary importance, this phylogenetic group, which is very distantly related to animals land plants, still poorly characterised at the genome level. Here we analyse 60 new genomes include all major brown algal orders. Comparative analysis these indicated occurrence several events coinciding approximately with emergence lineage. These included marked gain orthologous gene families, enhanced protein domain rearrangement, horizontal transfer acquisition novel signalling molecules metabolic pathways. The latter enzymes implicated in processes emblematic algae such as biosynthesis alginate-based extracellular matrix, halogen phlorotannin biosynthesis. early genomic innovations enabled adaptation intertidal habitats. subsequent diversification orders tended involve loss features were identified correlated differences life cycle strategy, flagellar structure metabolism. Analysis microevolutionary patterns within genus Ectocarpus deep flow between may be an important factor evolution on more recent timescales. Finally, show integration large viral has had a significant impact content propose process persisted throughout history

Language: Английский

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Giant viral signatures on the Greenland ice sheet

Microbiome, Journal Year: 2024, Volume and Issue: 12(1)

Published: May 17, 2024

Abstract Background Dark pigmented snow and glacier ice algae on glaciers sheets contribute to accelerating melt. The biological controls these algae, particularly the role of viruses, remain poorly understood. Giant classified under nucleocytoplasmic large DNA viruses (NCLDV) supergroup (phylum Nucleocytoviricota), are diverse globally distributed. NCLDVs known infect eukaryotic cells in marine freshwater environments, providing a control algal population ecosystems. However, there is very limited information diversity ecosystem function terrestrial icy habitats. Results In this study, we investigate for first time giant their host connections habitats, such as cryoconite, dark ice, core, red green snow, genomic assemblies five cultivated Chlorophyta algae. virus marker genes were present almost all samples; highest abundances recovered from assemblies, followed by ice. variety active protists GrIS habitats containing NCLDV suggests that infection can occur range hosts. Metagenomic data contained evidence metagenome-assembled genomes orders Imitervirales, Asfuvirales, Algavirales. Conclusion Our study highlights family signatures samples Greenland sheet. (GVMAGs) found samples, related identified culture assemblies; implying relationship between Metatranscriptomic viral also aligned with metagenomic sequences, suggesting an component microbial community potential “top-down” protistan members. This reveals unprecedented presence glacial dominated

Language: Английский

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Evolutionary genomics of the emergence of brown algae as key components of coastal ecosystems

Cell, Journal Year: 2024, Volume and Issue: 187(24), P. 6943 - 6965.e39

Published: Nov. 1, 2024

Brown seaweeds are keystone species of coastal ecosystems, often forming extensive underwater forests, and under considerable threat from climate change. In this study, analysis multiple genomes has provided insights across the entire evolutionary history lineage, initial emergence, through later diversification brown algal orders, down to microevolutionary events at genus level. Emergence lineage was associated with a marked gain new orthologous gene families, enhanced protein domain rearrangement, increased horizontal transfer events, acquisition novel signaling molecules key metabolic pathways, latter notably related biosynthesis alginate-based extracellular matrix, halogen phlorotannin biosynthesis. We show that genome is tightly linked phenotypic divergence, including changes in life cycle strategy zoid flagellar structure. The study also showed integration large viral had significant impact on content throughout emergence lineage.

Language: Английский

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DNA methylation enables recurrent endogenization of giant viruses in an animal relative

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2024, Volume and Issue: unknown

Published: Jan. 8, 2024

Abstract 5-methylcytosine (5mC) is a widespread silencing mechanism that controls genomic parasites. However, in many eukaryotes 5mC has gained complex roles gene regulation beyond parasite control. Animals are quintessential case for evolution, as they show variability across lineages, ranging from and transposable element control to loss of this base modification. Here we the protist closely related animals Amoebidium appalachense features both transposon body methylation, pattern reminiscent invertebrates plants. Unexpectedly, large hypermethylated regions genome derive viral insertions, including hundreds endogenized giant viruses contributing 14% encoded genes, an extent never reported before any eukaryotic genome. Using combination inhibitors functional assays, demonstrate silences these virus insertions. Moreover, alternative isolates polymorphic highlighting dynamic process infection, endogenization purging. Our results indicate critical controlled co-existence newly acquired DNA into genomes, making unique model understand hybrid origins genomes.

Language: Английский

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Eukaryotic genomic data uncover an extensive host range of mirusviruses

Current Biology, Journal Year: 2024, Volume and Issue: 34(12), P. 2633 - 2643.e3

Published: May 27, 2024

Language: Английский

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