Epigenetic silencing and host genome evolution determine fate of viral insertions in Acanthamoeba DOI Open Access

Cédric Blais,

Morgan Colp,

Luke A. Sarre

et al.

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

Published: Nov. 3, 2024

ABSTRACT Acanthamoeba is a cosmopolitan freshwater amoebae known for its association with Nucleocytoplasmic Large DNA Viruses (NCLDVs). Previous studies have shown that spp. undergo lateral gene transfer (LGT) NCLDVs. Here we leveraged chromosome-scale assemblies of two strains castellanii , Neff and C3, to investigate the occurrence genomic context viral LGT in . We show ‘footprints’ C3 genomes are largely non-overlapping genes found disproportionately large sub-telomeric insertions. Multiple partial copies these insertions throughout genome, but they not expressed do encode functions their own mobility. Viral regions hyper-methylated highly condensed, suggesting expression recently acquired suppressed heterochromatic regions. propose three-step model origin fate sequences : (i) integration from giant viruses, (ii) epigenetic suppression DNAs, which allows them persist (iii) deterioration by point mutation intra- inter-chromosomal recombination. integrations transient may long-lasting effects on fitness host amoeba. Our work strengthens growing body showing widespread protists extends relevance silencing mechanisms evolution Amoebozoa highlight importance genome dynamics understanding endogenized elements.

Language: Английский

Annelid methylomes reveal ancestral developmental and aging-associated epigenetic erosion across Bilateria DOI Creative Commons
Kero Guynes, Luke A. Sarre, Allan M. Carrillo‐Baltodano

et al.

Genome biology, Journal Year: 2024, Volume and Issue: 25(1)

Published: Aug. 1, 2024

Abstract Background DNA methylation in the form of 5-methylcytosine (5mC) is most abundant base modification animals. However, 5mC levels vary widely across taxa. While vertebrate genomes are hypermethylated, invertebrates, concentrates on constantly and highly transcribed genes (gene body methylation; GbM) and, some species, transposable elements (TEs), a pattern known as “mosaic”. Yet, role developmental dynamics how these explain interspecies differences patterns remain poorly understood, especially Spiralia, large clade invertebrates comprising nearly half animal phyla. Results Here, we generate base-resolution methylomes for three species with distinct genomic features phylogenetic positions Annelida, major spiralian phylum. All possible occur annelids, from typical invertebrate intermediate mosaic distribution to hypermethylation loss. GbM common annelids 5mC, explained by taxon-specific transcriptional or presence intronic TEs. Notably, link between transcription decays during development, alongside gradual global, age-dependent demethylation adult stages. Additionally, reducing cytidine analogs early development impairs normal embryogenesis reactivates TEs annelid Owenia fusiformis . Conclusions Our study indicates that global epigenetic erosion aging an ancestral feature bilateral tight gene likely more important embryonic stages, 5mC-mediated TE silencing probably emerged convergently lineages.

Language: Английский

Citations

4
Multiple, diverse endogenous giant virus elements within the genome of a brown alga DOI Creative Commons
Dean Mckeown, Alexandre Cormier, Declan C. Schroeder

et al.

Virus Evolution, Journal Year: 2025, Volume and Issue: 11(1)

Published: Jan. 1, 2025

Abstract Endogenous viral elements (EVEs) have been found in diverse eukaryotic genomes. These are particularly frequent the genomes of brown algae (Phaeophyceae) because these seaweeds infected by viruses (Phaeovirus) phylum Nucleocytoviricota (NCV) that capable inserting into their host’s genome as part infective cycle. A search for inserted sequences freshwater alga Porterinema fluviatile identified seven large EVEs, including four complete or near-complete proviruses. The which all appear to derived from independent insertion events, correspond phylogenetically members Phaeovirus genus and include both B subgroups this genus. This latter observation is surprising two were thought different evolutionary strategies therefore not expected be same host. EVEs contain a number novel genes H4 histone-like sequence but only one possesses full set NCV core genes, indicating other six probably nonfunctional, degenerated majority within transcriptionally silent most small showed some transcriptional activity unknown function. However, existence active several containing introns suggests may undergoing degree endogenization host over time.

Language: Английский

Citations

0
Cryptic infection of a giant virus in a unicellular green alga DOI
Maria P. Erazo-Garcia, Uri Sheyn, Zachary K. Barth

et al.

Science, Journal Year: 2025, Volume and Issue: unknown

Published: April 10, 2025

Latency is a common strategy in wide range of viral lineages, but its prevalence giant viruses remains unknown. Here we describe 617 kbp integrated element the model green alga Chlamydomonas reinhardtii . We resolve genome using long-read sequencing, identify putative polinton-like integrase, and show that particles accumulate primarily during stationary growth phase. A diverse array viral-encoded selfish genetic elements expressed activity, including several Fanzor nuclease-encoding transposable elements. In addition, field isolates sp. harbor signatures endogenous related to C. virus exhibit similar infection dynamics, suggesting latency prevalent natural host communities. Our work describes an unusually large temperate unicellular eukaryote, substantially expanding scope cryptic infections virosphere.

Language: Английский

Citations

0
Cytosine Methylation is a marker of Viral Gene Transfer across the eukaryotes DOI Creative Commons
Luke A. Sarre, Gabriela P. Peralta, Pedro Romero Charria

et al.

Published: April 16, 2025

Abstract Cytosine DNA methylation patterns vary widely across eukaryotes, with its ancestral roles being understood to have included both transposable element silencing and host gene regulation. To further explore these claims, in this study, we reevaluate the evolutionary origins of methyltransferases characterise cytosine on underexplored lineages, including amoebozoan Acanthamoeba castellanii , glaucophyte Cyanophora paradoxa heterolobosean Naegleria gruberi . Our analysis methyltransferase evolution reveals a rich eukaryotic repertoire, several lineages likely subsequently acquiring enzymes through lateral transfer (LGT). In three species examined, is enriched young elements silenced genes, suggesting an repressive function, without transcription-linked body plants animals. Notably, closest homologues many silenced, methylated genes diverse eukaryotes belong viruses, giant viruses. Given widespread occurrence pattern groups, propose that was mechanism originally acquired from bacterial donors which used mitigate expression viral elements, function may persist creating permissive atmosphere for LGT lineages. These findings highlight importance epigenetic information annotate genomes, as it helps delimit potentially adaptive LGTs parasitic elements.

Language: Английский

Citations

0
Ancient Host-Virus Gene Transfer Hints at a Diverse Pre-LECA Virosphere DOI Creative Commons
Sangita Karki, Zachary K. Barth, Frank O. Aylward

et al.

Journal of Molecular Evolution, Journal Year: 2025, Volume and Issue: unknown

Published: April 29, 2025

Abstract The details surrounding the early evolution of eukaryotes and their viruses are largely unknown. Several key enzymes involved in DNA synthesis transcription shared between large phylum Nucleocytoviricota , but evolutionary relationships these genes remain unclear. In particular, previous studies eukaryotic RNA polymerases often show deep-branching clades indicative ancient gene exchange. Here, we performed updated phylogenetic analysis viral family B polymerases, multimeric mRNA-capping to explore relationships. Our results that form typically adjacent eukaryotes, suggesting they originate prior emergence Last Eukaryotic Common Ancestor (LECA). machinery for replication, transcription, mRNA capping all processes needed maintenance virus factories, which complex structures formed by many nucleocytoviruses during infection, indicating capable making ancient. These findings hint at a diverse pre-LECA virosphere indicate may encode proteins relics extinct proto-eukaryotic lineages.

Language: Английский

Citations

0
Ichthyosporea: a window into the origin of animals DOI Creative Commons
Victoria Shabardina, Jennah Dharamshi, Patricia S. Ara

et al.

Communications Biology, Journal Year: 2024, Volume and Issue: 7(1)

Published: July 29, 2024

Ichthyosporea is an underexplored group of unicellular eukaryotes closely related to animals. Thanks their phylogenetic position, genomic content, and development through a multinucleate coenocyte reminiscent some animal embryos, the members are being increasingly recognized as pivotal study origins. We delve into existing knowledge Ichthyosporea, identify gaps discuss life cycles, insights, development, potential be model organisms. also underestimated diversity ichthyosporeans, based on new environmental data analyses. This review will essential resource for researchers venturing ichthyosporeans. crucial understanding origins evolution. Review outlines history recent advancements in ichthyosporean biology, genomics, genetics, provides insight diversity.

Language: Английский

Citations

2
Latent infection of an active giant endogenous virus in a unicellular green alga DOI Creative Commons
Maria P. Erazo-Garcia, Uri Sheyn, Zachary K. Barth

et al.

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

Published: Sept. 3, 2024

Abstract Latency is a common strategy in wide range of viral lineages, but its prevalence giant viruses remains unknown. Here we describe the activity and production from 617 kbp integrated element model green alga Chlamydomonas reinhardtii . We resolve region using long-read sequencing show that particles are produced released otherwise healthy cultures. A diverse array viral-encoded selfish genetic elements expressed during GEVE reactivation produce proteins packaged virions. In addition, field isolates sp. harbor latent related to C. exhibit similar infection dynamics, demonstrating virus latency prevalent natural host communities. Our work reports largest temperate documented date first active identified unicellular eukaryote, substantially expanding known limits latency.

Language: Английский

Citations

2
Chromatin profiling identifies putative dual roles for H3K27me3 in regulating transposons and cell type-specific genes in choanoflagellates DOI Creative Commons
James M. Gahan, Lily W. Helfrich, Laura A. Wetzel

et al.

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

Published: May 30, 2024

Gene expression is tightly controlled during animal development to allow the formation of specialized cell types. Our understanding how animals evolved this exquisite regulatory control remains elusive, but evidence suggests that changes in chromatin-based mechanisms may have contributed. To investigate possibility, here we examine gene features closest relatives animals, choanoflagellates. Using Salpingoeca rosetta as a model system, examined chromatin accessibility and histone modifications at genome scale compared these expression. We first observed accessible regions are primarily associated with promoters found no distal elements resembling enhancers deploy regulate developmental Remarkably, modification deposited by polycomb repressive complex 2, H3 lysine 27 trimethylation (H3K27me3), appeared function similarly S. its role because decorated genes type-specific Additionally, H3K27me3 marked transposons, retaining what appears be an ancestral regulating elements. further uncovered putative new bivalent state consists 4 mono-methylation (H3K4me1). Together, our discoveries support scenario gene-associated states underpin emerged before evolution multicellularity.

Language: Английский

Citations

0
Epigenetic silencing and host genome evolution determine fate of viral insertions in Acanthamoeba DOI Open Access

Cédric Blais,

Morgan Colp,

Luke A. Sarre

et al.

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

Published: Nov. 3, 2024

ABSTRACT Acanthamoeba is a cosmopolitan freshwater amoebae known for its association with Nucleocytoplasmic Large DNA Viruses (NCLDVs). Previous studies have shown that spp. undergo lateral gene transfer (LGT) NCLDVs. Here we leveraged chromosome-scale assemblies of two strains castellanii , Neff and C3, to investigate the occurrence genomic context viral LGT in . We show ‘footprints’ C3 genomes are largely non-overlapping genes found disproportionately large sub-telomeric insertions. Multiple partial copies these insertions throughout genome, but they not expressed do encode functions their own mobility. Viral regions hyper-methylated highly condensed, suggesting expression recently acquired suppressed heterochromatic regions. propose three-step model origin fate sequences : (i) integration from giant viruses, (ii) epigenetic suppression DNAs, which allows them persist (iii) deterioration by point mutation intra- inter-chromosomal recombination. integrations transient may long-lasting effects on fitness host amoeba. Our work strengthens growing body showing widespread protists extends relevance silencing mechanisms evolution Amoebozoa highlight importance genome dynamics understanding endogenized elements.

Language: Английский

Citations

0