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Life cycle of Cotesia and bracovirus. Female Cotesia wasps lay eggs in larvae of moths such as Plutella xylostella and also inject bracovirus virion particles carrying DNA circles that integrate into the chromosomes of the parasitized larvae and favor development of the wasp larvae over the moth larvae. The bracovirus provirus is resident in the wasp genome and transmitted directly to offspring
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The common histones H2A, H2B, H3, and H4 are the characteristic components of eukaryotic nucleosomes, which function to wrap DNA and compact the genome as well as to regulate access to DNA for transcription and replication in all eukaryotes. In the past two decades, histones have also been found to be encoded in some DNA viruses, where their functi...
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... For example, H2B-H2A and H4-H3 doublets in marseilleviruses form eukaryotic-like nucleosomes essential for viral genome packaging [14][15][16] . Moreover, phylogenetic analyses place these histones between archaeal and eukaryotic homologues, prompting competing hypotheses about their origins 11,17 . In particular, whether these repeats, formed by post-hoc fusion between recently transferred eukaryotic histones, represent the viral progenitors of eukaryotic histones or were acquired following gene transfer from primordial eukaryotes remains unclear. ...
... To characterize viral histone diversity, we surveyed the predicted proteomes of NCVs, viruses known to encode histone proteins 17 . Using profile hidden Markov models representing the core eukaryotic histone families and archaeal histones, we searched predicted proteins derived from both NCV genomes (n = 205) and assembled NCV metagenomes (n = 2,074) 7 . ...
... This approach identified 258 complete histone genes from 168 viruses. Viral histones had longer predicted coding sequences relative to cellular homologues due to the presence of histone repeats such as doublets (n = 90), triplets (n = 32) and quadruplets (n = 13), as noted previously 11,12,17 (Fig. 1a,b). These histone repeats exhibited partially constrained domain orders, with H2A/H2B and H3/H4 nearly always a b Viral histone co-occurrence network Co-occurrence prop. ...
Nucleosomes are DNA–protein complexes composed of histone proteins that form the basis of eukaryotic chromatin. The nucleosome was a key innovation during eukaryotic evolution, but its origin from histone homologues in Archaea remains unclear. Viral histone repeats, consisting of multiple histone paralogues within a single protein, may reflect an intermediate state. Here we examine the diversity of histones encoded by Nucleocytoviricota viruses. We identified 258 histones from 168 viral metagenomes with variable domain configurations including histone singlets, doublets, triplets and quadruplets, the latter comprising the four core histones arranged in series. Viral histone repeats branch phylogenetically between Archaea and eukaryotes and display intermediate functions in Escherichia coli, self-assembling into eukaryotic-like nucleosomes that stack into archaeal-like oligomers capable of impacting genomic activity and condensing DNA. Histone linkage also facilitates nucleosome formation, promoting eukaryotic histone assembly in E. coli. These data support the hypothesis that viral histone repeats originated in stem-eukaryotes and that nucleosome evolution proceeded through histone repeat intermediates.
... Furthermore, numerous sequences assigned to NCLDV families exhibited significant similarity to various host proteins, including heat-shock proteins, tRNA synthetase, histone, and ubiquitin sequences, among others. Although these genes with eukaryotic homologs can potentially be encoded by NCLDV (66)(67)(68)(69)(70)(71), their abundance was significantly greater than those associated with the virus replication, which lack close homologs in the host genomes (72). This could hint in the direction of these hits representing host sequences in the samples, which could partly explain why a large part of the apparently more dominant viral families identified across the viromes were DNA viruses, contrary to the common consensus, which states that RNA viruses dominate invertebrate viromes (4,5). ...
Invertebrates constitute the majority of animal species on Earth, including most disease-causing agents or vectors, with more diverse viromes when compared to vertebrates. Recent advancements in high-throughput sequencing have significantly expanded our understanding of invertebrate viruses, yet this knowledge remains biased toward a few well-studied animal lineages. In this study, we analyze invertebrate DNA and RNA viromes for 31 phyla using 417 publicly available RNA-Seq data sets from diverse environments in the marine-terrestrial and marine-freshwater gradients. This study aims to (i) estimate virome compositions at the family level for the first time across the animal tree of life, including the first exploration of the virome in several phyla, (ii) quantify the diversity of invertebrate viromes and characterize the structure of invertebrate-virus infection networks, and (iii) investigate host phylum and habitat influence on virome differences. Results showed that a set of few viral families of eukaryotes, comprising Retroviridae, Flaviviridae, and several families of giant DNA viruses, were ubiquitous and highly abundant. Nevertheless, some differences emerged between phyla, revealing for instance a less diverse virome in Ctenophora compared to the other animal phyla. Compositional analysis of the viromes showed that the host phylum explained over five times more variance in composition than its habitat. Moreover, significant similarities were observed between the viromes of some phylogenetically related phyla, which could highlight the influence of co-evolution in shaping invertebrate viromes.
IMPORTANCE
This study significantly enhances our understanding of the global animal virome by characterizing the viromes of previously unexamined invertebrate lineages from a large number of animal phyla. It showcases the great diversity of viromes within each phylum and investigates the role of habitat shaping animal viral communities. Furthermore, our research identifies dominant virus families in invertebrates and distinguishes phyla with analogous viromes. This study sets the road toward a deeper understanding of the virome across the animal tree of life.
... In contrast, giant viruses encode clearly recognizable homologs 203 of the four eukaryotic core histones (H2A, H2B, H3, and H4) that assemble into nucleosome-like 204 particles that wrap ~130 bp of DNA 17,19 . Phylogenetic analysis suggests that these histones 205 diverged prior to the emergence of LECA 20,[42][43][44][45] . Instances of histone doublets (or even triplets 206 . ...
... ; https://doi.org/10.1101/2024.04.13.589364 doi: bioRxiv preprint and quadruplets) have been described in NCLDV, which enforce specific pairing of histones and 207 suggest a potential role in the origin of eukaryotic histone dimers/tetramers 2,9,45 . With some 208 NCLDV only encoding one doublet pair, it is possible that NCLDV histones doublets have 209 evolved independent functions in viral genome packaging; although it is unclear if these 210 independent functions were developed before or after complete sets of core histone singlets were 211 encoded in eukaryotes or even MM 44 . MM histones are placed at the root of most histone 212 phylogenetic trees, and thus add to new potential theories regarding nucleosome 213 evolution 5,12,16,20 . ...
The organization of DNA into nucleosomes is a ubiquitous and ancestral feature that was once thought to be exclusive to the eukaryotic domain of life. Intriguingly, several representatives of the Nucleocytoplasmic Large DNA Viruses (NCLDV) encode histone-like proteins that in Melbournevirus were shown to form nucleosome-like particles. Medusavirus medusae (MM), a distantly related giant virus, encodes all four core histone proteins and, unique amongst most giant viruses, a putative acidic protein with two domains resembling linker histone H1. Here we report the structure of nucleosomes assembled with Medusavirus histones and highlight similarities and differences with eukaryotic and Melbournevirus nucleosomes. Our structure provides insight into how variations in histone tail and loop lengths are accommodated within the context of the nucleosome. We show that Medusavirus histones assemble into tri-nucleosome arrays, and that the putative linker histone H1 does not function in chromatin compaction. These findings expand our understanding of viral histones and suggest that Medusavirus histones represent a snapshot in the evolutionary timeline of nucleosome architecture.
ONE SENTENCE SUMMARY
The four Medusavirus medusae core histones form nucleosome-like structures that combine features of eukaryotic and other viral nucleosomes.
... Our study delves into the realm of epigenetic modifications, focusing on histone acetylation and deacetylation, to understand how T. brontispae influences host gene expression. The bracovirus of C. plutellae offers a compelling case of host manipulation through epigenetic modifications, introducing a variant histone H4 with an extended N-terminal tail into the host nucleosome, facilitating transcriptional reprogramming within the host [43,44]. This example underscores the pivotal role of histone modifications in the intricate relationship between parasitoids and their hosts, setting the stage for our investigation into T. brontispae's epigenetic influence. ...
Endoparasitoids are insects that develop within other insects, employing unique strategies to enhance their offspring’s survival. They inject polydnavirus and/or venom into their hosts along with eggs, effectively suppressing the host’s immune system. Polydnavirus from Braconidae and Ichneumonidae wasps can integrate into the host’s genome to express viral genes using the host’s transcription systems. However, the ability of parasitoids without polydnavirus to manipulate host gene expression remains unclear. Lysine acetylation (LysAc), a post-translational modification critical for gene regulation, is hypothesized to be used by endoparasitoids lacking polydnavirus. We utilized the Chalcidoidea wasp Tetrastichus brontispae, which lacks polydnavirus, as an idiobiont endoparasitoid model to test this hypothesis, with pupae of the nipa palm hispid beetle Octodonta nipae as the host. Parasitism by T. brontispae resulted in the reduced expression of histone deacetylase Rpd3 and elevated levels of LysAc modification at histones H3.3K9 and H3.3K14 through proteomics and LysAc modification omics. The knockdown of Rpd3 increased the expression level of OnPPAF1 and OnPPO involved in the phenoloxidase cascade, leading to melanization in the host body whereby it resembled a mummified parasitized pupa and ultimately causing pupa death. This study enhances our understanding of how endoparasitoids employ histone acetylation to regulate immunity-related genes, offering valuable insights into their survival strategies.
... Histones are proteins that package genomic DNA into nucleosomes, the fundamental building block of chromatin, and they can undergo posttranslational modifications with at least eight different types of reversible changes that are carried out by various enzymes. 54 These modifications, which are carried out by enzymes called histone deacetylases (HDACs), histone acetyltransferases (HATs), and histone demethylases (HDMs), include acetylation, methylation, phosphorylation, and ubiquitination. 55 Histone modifications can affect the tightness of DNA packing and consequently the accessibility of transcription factors and subsequent gene expression. ...
Obesity is a major risk factor for morbidity and mortality because it has a close relationship to metabolic illnesses, such as diabetes, cardiovascular diseases, and some types of cancer. With no drugs available, the mainstay of obesity management remains lifestyle changes with exercise and dietary modifications. In light of the tremendous disease burden and unmet therapeutics, fresh perspectives on pathophysiology and drug discovery are needed. The development of epigenetics provides a compelling justification for how environmental, lifestyle, and other risk factors contribute to the pathogenesis of obesity. Furthermore, epigenetic dysregulations can be restored, and it has been reported that certain natural products obtained from plants, such as tea polyphenols, ellagic acid, urolithins, curcumin, genistein, isothiocyanates, and citrus isoflavonoids, were shown to inhibit weight gain. These substances have great antioxidant potential and are of great interest because they can also modify epigenetic mechanisms. Therefore, understanding epigenetic modifications to target the primary cause of obesity and the epigenetic mechanisms of anti‐obesity effects with certain phytochemicals can prove rational strategies to prevent the disease and develop novel therapeutic interventions. Thus, the current review aimed to summarize the epigenetic mechanisms and advances in therapies for obesity based on natural products to provide evidence for the development of several potential anti‐obesity drug targets.
... Notably, histones are also encoded within viral genomes (22,23). Phylogenetically, viral histones are currently positioned between eukaryotic and archaeal histones (24). While many characterized viral nucleosomal histones structurally resemble eukaryotic nucleosome-like structures (25,26), some stack into larger complexes that lack linker DNA, resembling archaeal hypernucleosomes (27). ...
... Histones, ther efor e, a ppear to be a unique case among virologs in that they are not necessarily involved in manipulation of the host during infection, but rather are used to preserve the integrity of viral DNA in virions. A recent review has comprehensively discussed the presence of histone subunits in both members of the Nucleocytoviricota as well as other viral lineages (Talbert et al. 2022 ). ...
The phylum Nucleocytoviricota includes the largest and most complex viruses known. These “giant viruses” have a long evolutionary history that dates back to the early diversification of eukaryotes, and over time they have evolved elaborate strategies for manipulating the physiology of their hosts during infection. One of the most captivating of these mechanisms involves the use of genes acquired from the host - referred to here as viral homologs or “virologs” - as a means of promoting viral propagation. The best-known examples of these are involved in mimicry, in which viral machinery “imitates” immunomodulatory elements in the vertebrate defense system. But recent findings have highlighted a vast and rapidly expanding array of other virologs that include many genes not typically found in viruses, such as those involved in translation, central carbon metabolism, cytoskeletal structure, nutrient transport, vesicular trafficking, and light harvesting. Unraveling the roles of virologs during infection as well as the evolutionary pathways through which complex functional repertoires are acquired by viruses are important frontiers at the forefront of giant virus research.
... However, functional constraints and the extinction of stem-eukaryotes have concealed how these dynamic systems evolved from simpler histone homologues in Archaea 3-5 . Viral histones have also previously been identified and are thought to reflect an ancestral state as they often comprise multiple histone paralogues arranged within a single protein, termed histone repeats [6][7][8][9][10][11] . Here, using viruses as an alternative source of variation, we expand the known diversity of histones and develop an empirical hypothesis for the origin of the nucleosome. ...
... surveying the proteomes of diverse NCVs, viruses known to encode histone proteins 6 . Using profile hidden Markov models representing each of the core eukaryotic histone families and archaeal histones, we searched predicted proteins derived from both NCV genomes (n = 205) and assembled NCV metagenomes (n = 2,074) 13 . ...
... This approach identified 258 complete histone genes from 168 viruses. These histones were significantly larger relative to cellular homologues, an effect explained by the presence of histone repeats such as doublets (n = 90), triplets (n = 32), and quadruplets (n = 13), as noted previously [6][7][8] (Fig. 1a, b). These histone repeats exhibited variable but constrained domain orders, with H2A/H2B and H3/H4 nearly always in series (Fig. 1b). ...
Nucleosomes are a core-component of eukaryotic nuclei, forming the structural basis of chromatin and co-ordinating processes from gene expression to chromosome segregation. Composed of a DNA-protein complex consisting of the four individual histones, H2A, H2B, H3, and H4, the nucleosome and its associated functions were key innovations during eukaryotic evolution. However, functional constraints and the extinction of stem-eukaryotes have concealed how these dynamic systems evolved from simpler histone homologues in Archaea. Viral histones have also previously been identified and are thought to reflect an ancestral state as they often comprise multiple histone paralogues arranged within a single protein, termed histone repeats. Here, using viruses as an alternative source of variation, we expand the known diversity of histones and develop an empirical hypothesis for the origin of the nucleosome. Our analysis identified hundreds of histones with variable domain repeat configurations including histone singlets, doublets, triplets, and quadruplets, the latter comprising the four core histones arranged in series. Viral histone repeats consistently branch between Archaea and eukaryotes in phylogenetic trees and display intermediate functions, self-assembling into eukaryotic-like nucleosomes that stack into archaeal-like oligomers capable of impacting genomic activity and condensing DNA. The linkers conjoining the histone repeats also facilitate nucleosome formation and can promote the assembly of eukaryotic nucleosomes in the bacterium, Escherichia coli. Combining these data, we hypothesize that viral histone repeats represent molecular relics acquired by viruses from stem-eukaryotes during eukaryogenesis and suggest that nucleosome evolution may have proceeded through histone repeat intermediates.
... Nuclear DNA viruses and retroviruses organize their genome into nucleosomes through eukaryotic histones, while others encode their own histone-like proteins [10]. Virus-encoded histone-like proteins are structurally distinct from eukaryotic histones, suggesting specialized functions [11]. For example, the insect polydnavirus CpBV encodes an orthologue of the insect histone H4, which can be incorporated into host nucleosomes to inhibit genes expression [12]. ...
Molecular mimicry is a commonly used mechanism by viruses to manipulate host cellular machinery and coordinate their life cycles. While histone mimicry is well studied, viruses also employ other mimicry strategies to affect chromatin dynamics. However, the relationship between viral molecular mimicry and host chromatin regulation is not well understood. This review summarizes recent advances in histone mimicry and explores how viral molecular mimicry influences chromatin dynamics. We also discuss how viral proteins interact with both intact and partially unfolded nucleosomes and compare the distinct mechanisms governing chromatin tethering. Finally, we address the role of viral molecular mimicry in regulating chromatin dynamics. This review provides new insights into viral molecular mimicry and its impact on host chromatin dynamics, paving the way for the development of novel antiviral strategies.
... This may be because viruses required various proteins to favor their own survival in ancient times when the fusions or integrations occurred. In this study, the sequences of histone-related genes of P. dulcis, C. congregata bracovirus and P. salinus are highly homologous to those of amphioxus, which could play an important role in the origin of the nucleus of modern eukaryotic cells [80]. Viral HFs were also searched for in genomes of Erpetoichthys calabaricus (Vertebrata), Aplidium turbinatum (Urochordata), Lytechinus variegatus (Echinodermata), Saccoglossus kowalevskii (Hemichordate), Drosophila melanogaster (Protostomia), Dendronephthya gigantea (Cnidaria) and Amphimedon queenslandica (Porifera) using discontiguous megablast of NCBI's BLASTN programs. ...
Amphioxus species are considered living fossils and are important in the evolutionary study of chordates and vertebrates. To explore viral homologous sequences, a high-quality annotated genome of the Beihai amphioxus (Branchiostoma belcheri beihai) was examined using virus sequence queries. In this study, 347 homologous fragments (HFs) of viruses were identified in the genome of B. belcheri beihai, of which most were observed on 21 genome assembly scaffolds. HFs were preferentially located within protein-coding genes, particularly in their CDS regions and promoters. A range of amphioxus genes with a high frequency of HFs is proposed, including histone-related genes that are homologous to the Histone H4 or Histone H2B domains of viruses. Together, this comprehensive analysis of viral HFs provides insights into the neglected role of viral integration in the evolution of amphioxus.
