Biology subjects

Barth, Z. K.

Publications and source records attributed to Barth, Z. K..

7 recordsLinked to original sources

bioRxiv2026

Multi-level mosaicism shapes the evolution of small eukaryotic DNA viruses

Eukaryote-infecting small dsDNA viruses, including those referred to as virophages, polintons, and their relatives, are major constituents of ecosystems across the globe as both agents of mortality and as integrated elements that shape host genome evolution. As the ubiquity of these viruses has become apparent, there have been efforts to organize their diversity into major lineages in order to better understand their biogeography, ecological impact, and evolution. Virophages, polintons, and polinton-like viruses were recently placed in the sub-phylum Polisuviricotina, though efforts to resolve relationships within this sub-phylum have been complicated by the vast diversity of these viruses and the existence of horizontal gene transfer between their genomes. To address these complications, we have used a gene profile occurrence based method of phylogenetic tree construction to aid in comparative genomic analysis of Polisuviricotina. We find that mosaicism is common within Polisuviricotina, in particular, reassociation of replication modules and morphogenic modules occurs throughout major Polisuviricotina groups. In addition to mosaic exchanges of full replication modules, we also observe extensive domain swapping within some replicases, indicating that mosaic recombination occurs on both the genome and subgenic level in these viruses. Analysis of individual replication modules suggests that they may be capable of some level of autonomous mobility, partially decoupling their evolution from the morphogenic module. This model helps explain the high levels of mosaicism in these viruses and has implications for the mechanisms through which small dsDNA viruses evolve.

microbiology↗

bioRxiv2024

Convergent evolution of viral-like Borg archaeal extrachromosomal elements and giant eukaryotic viruses

Borgs are huge extrachromosomal elements of anaerobic methane-oxidizing archaea. They exist in exceedingly complex microbiomes, lack cultivated hosts and have few protein functional annotations, precluding their classification as plasmids, viruses or other. Here, we used in silico structure prediction methods to investigate potential roles for [~]10,000 Borg proteins. Prioritizing analysis of multicopy genes that could signal importance for Borg lifestyles, we uncovered highly represented de-ubiquitination-like Zn-metalloproteases that may counter host targeting of Borg proteins for proteolysis. Also prevalent are clusters of multicopy genes for production of diverse glycoconjugates that could contribute to decoration of the host cell surface, or of putative capsid proteins that we predict multimerize into hexagonal arrays. Features including megabase-scale linear genomes with inverted terminal repeats, genomic repertoires for energy metabolism, central carbon compound transformations and translation, and pervasive direct repeat regions are shared with giant viruses of eukaryotes, although analyses suggest that these parallels arose via convergent evolution. If Borgs are giant archaeal viruses they would fill the gap in the tri(um)virate of giant viruses of all three domains of life. One Sentence SummaryProtein analyses, informed by in silico protein structure prediction, revealed that Borgs share numerous features with giant eukaryotic viruses, suggesting that Borgs have a viral-like lifestyle and evolutionary convergence of large extrachromosomal elements across the Domains of Life.

microbiology↗

bioRxiv2024

Latent infection of an active giant endogenous virus in a unicellular green alga

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

microbiology↗

bioRxiv2024

Chimeric Origin of Eukaryotes from Asgard Archaea and Ancestral Giant Viruses

The details surrounding the evolution of complex cells remain some of the most enduring mysteries in biology. Recent evidence has demonstrated that Asgard archaea are the closest cellular relatives of eukaryotes, but several eukaryotic enzymes involved in key cellular processes lack phylogenetic affinity with archaea. In particular, phylogenies of eukaryotic DNA and RNA polymerases often support a 3-domain topology that is not consistent with an archaeal origin. Here we present comprehensive phylogenetic analysis of eukaryotic family B DNA polymerases and multimeric RNA polymerases and show that these core subunits of these enzymes are derived from the ancestors of modern giant viruses (phylum Nucleocytoviricota). Specifically, we show that the eukaryotic delta polymerase (Pol{delta}), a key processive polymerase required for genome replication in all eukaryotes, clusters within an ancient viral clade, strongly supporting a viral origin. By contrast, the other eukaryotic processive polymerase (Pol{varepsilon}), clusters within an Asgard archaeal clade. Together, these observations provide a strong and direct link between early eukaryotes, Asgard archaea, and giant viruses. Lastly, we provide a comprehensive phylogenetic analysis of eukaryotic multimeric RNA polymerases to confirm that RNA polymerase II, which is responsible for mRNA transcription in eukaryotes, is also derived from the ancestors of modern giant viruses. In total, our results support a model of eukaryogenesis in which complex cells emerged from a genomic chimera of Asgard archaea and an ancient viral lineage.

evolutionary biology↗

bioRxiv2023

Polinton-like Viruses Associated with Entomopoxviruses Provide Insight into Replicon Evolution

Polinton-like viruses (PLVs) are a diverse group of small integrative dsDNA viruses that infect diverse eukaryotic hosts. Many PLVs are hypothesized to parasitize viruses in the phylum Nucleocytoviricota for their own propagation and spread. Here we analyze the genomes of novel PLVs associated with the occlusion bodies of entomopoxvirus (EV) infections of two separate lepidopteran hosts. The presence of these elements within EV occlusion bodies suggests that they are the first known hyperparasites of poxviruses. We find that these PLVs belong to two distinct lineages that are highly diverged from known PLVs. These PLVs possess mosaic genomes, and some essential genes share homology with mobile genes within EVs. Based on this homology and observed PLV mosaicism, we propose a mechanism to explain the turnover of PLV replication and integration genes.

genomics↗

bioRxiv2021

A chimeric nuclease substitutes CRISPR-Cas: A phage weaponizes laterally acquired specificity to destroy subviral parasites

Mobile genetic elements, elements that can move horizontally between genomes, have profound effects on their hosts fitness. The PLE is a mobile element that integrates into the chromosome of Vibrio cholerae and parasitizes the bacteriophage ICP1 to move between cells. This parasitism by PLE is such that it abolishes the production of ICP1 progeny and provides a defensive boon to the host cell population. In response to the severe parasitism imposed by PLE, ICP1 has acquired an adaptive CRISPR-Cas system that targets the PLE genome during infection. However, ICP1 isolates that naturally lack CRISPR-Cas are still able to overcome certain PLE variants, and the mechanism of this immunity against PLE has thus far remained unknown. Here we show that ICP1 isolates that lack CRISPR-Cas encode an endonuclease in the same locus, and that the endonuclease provides ICP1 with immunity to a subset of PLEs. Further analysis shows that this endonuclease is of chimeric origin, incorporating a DNA binding domain that is highly similar to some PLE replication origin binding proteins. This similarity allows the endonuclease to bind and cleave PLE origins of replication. The endonuclease appears to exert considerable selective pressure on PLEs and may drive PLE replication module swapping and origin restructuring as mechanisms of escape. This work demonstrates that new genome defense systems can arise through domain shuffling and provides a greater understanding of the evolutionary forces driving genome modularity and temporal succession in mobile elements.

microbiology↗

bioRxiv2020

A family of viral satellites manipulates invading virus gene expression and affects cholera toxin mobilization

Many viruses possess temporally unfolding gene expression patterns aimed at subverting host defenses, commandeering host metabolism, and ultimately producing a large number of progeny virions. High throughput -omics tools, such as RNA-seq, have dramatically enhanced resolution of expression patterns during infection. Less studied have been viral satellites, mobile genomes that parasitize viruses and have far reaching effects on host-cell fitness. By performing RNA-seq on infection time courses, we have obtained the first time-resolved transcriptomes for bacteriophage satellites during lytic infection. Specifically, we have acquired transcriptomes for the lytic Vibrio cholerae phage ICP1 and all five known variants of ICP1s parasite, the Phage Inducible Chromosomal Island-Like Elements (PLEs). PLEs rely on ICP1 for both DNA replication and mobilization, and abolish production of ICP1 progeny in infected cells. We investigated PLEs impact on ICP1 gene expression and found that PLEs did not broadly restrict or reduce ICP1 gene expression. A major exception occurred in ICP1s capsid morphogenesis operon, which was downregulated by each of the PLE variants. This transcriptional manipulation, conserved among PLEs, has also evolved independently in at least one other phage satellite, suggesting that viral satellites may be under strong selective pressure to reduce the capsid expression of their larger host viruses. Surprisingly, PLEs were also found to alter the gene expression of CTX{phi}, the integrative phage that encodes cholera toxin and is necessary for virulence of toxigenic V. cholerae. One PLE, PLE1, upregulated CTX{phi} genes involved in replication and integration, and boosted CTX{phi} mobility following induction of the SOS response. Our data show that PLEs exhibit conserved manipulation of their host-phages gene expression, but divergent effects on CTX{phi}, revealing that PLEs can influence both their hosts resistance to phage and the mobility of virulence encoding elements.

microbiology↗