Widespread endogenization of giant viruses shapes genomes of green algae

Moniruzzaman, Mohammad; Weinheimer, Alaina R.; Martínez-Gutiérrez, Carolina A.; Aylward, Frank O.

doi:10.1038/s41586-020-2924-2

Cited by 107 publications

(129 citation statements)

References 67 publications

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“…The percent identity of these matches ranged from 19.4 - 93.2 (median 35.3), with only 4 greater than 90% identity suggesting that, if these represent gene exchanges between NCLDV and eukaryotes, the vast majority have not occurred recently. Although recent studies have revealed a dynamic gene exchange between NCLDV and eukaryotic lineages that can be used to link viruses to their hosts (Moniruzzaman et al, 2020b; Schulz et al, 2020), our analysis did not identify any clear signatures in the Asfarvirus MAGs that could be used for this purpose. It is possible that future work examining endogenous NCLDV signatures in eukaryotic genomes may be useful to better identify virus-host relationships.…”

Section: Resultscontrasting

confidence: 76%

Comparative Genomics and Environmental Distribution of Large dsDNA viruses in the familyAsfarviridae

Karki

Moniruzzaman

Aylward

2021

Preprint

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The Asfarviridae is a family of Nucleo-Cytoplasmic Large DNA Viruses (NCLDV) of which African swine fever virus (ASFV) is the most well-characterized. Recently the discovery of several Asfarviridae members other than ASFV has suggested that this family represents a diverse and cosmopolitan group of viruses, but the genomics and distribution of this family have not been studied in detail. To this end we analyzed five complete genomes and 35 metagenome-assembled genomes (MAGs) of viruses from this family to shed light on their evolutionary relationships and environmental distribution. The Asfarvirus MAGs derive from diverse marine, freshwater, and terrestrial habitats, underscoring the broad environmental distribution of this family. We present phylogenetic analyses using conserved marker genes and whole-genome comparison of pairwise average amino acid identity values, revealing a high level of genomic divergence across disparate Asfarviruses. Further, we found that Asfarviridae genomes encode genes with diverse predicted metabolic roles and detectable sequence homology to proteins in bacteria, archaea, and different eukaryotes, highlighting the genomic chimerism that is a salient feature of NCLDV. Our read mapping from Tara oceans metagenomic data also revealed that three Asfarviridae MAGs were present in multiple marine samples, indicating that they are widespread in the ocean. In one of these MAGs we identified four marker genes with >95% amino acid identity to genes sequenced from a virus that infects the dinoflagellate Heterocapsa circularisquama (HcDNAV). This suggests a potential host for this MAG, which would thereby represent a near-complete genome of a dinoflagellate-infecting giant virus. Together, these results show that Asfarviridae are ubiquitous, comprise similar sequence divergence as other NCLDV families, and include several members that are widespread in the ocean and potentially infect ecologically important protists.

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Section: Resultscontrasting

confidence: 76%

Comparative Genomics and Environmental Distribution of Large dsDNA viruses in the familyAsfarviridae

Karki

Moniruzzaman

Aylward

2021

Preprint

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“…For retroviruses, integration is an essential part of their replication cycles, but other viruses can also occasionally endogenize, for instance with the help of cellular retroelements 2 . Some green algal genomes even contain giant EVEs of several hundred kilobases (kb) in length 3 . Unlike prophages in bacteria and archaea, most eukaryotic EVEs are thought to be 'genomic fossils' and incapable of virion formation and horizontal transmission, although their genes may be co-opted for various host functions 4,5 .…”

Section: Introductionmentioning

confidence: 99%

Virophages and retrotransposons colonize the genomes of a heterotrophic flagellate

Hackl

Duponchel

Barenhoff

et al. 2020

Preprint

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Endogenous viral elements (EVEs) are frequently found in eukaryotic genomes, yet their integration dynamics and biological functions remain largely unknown. Unlike most other eukaryotic DNA viruses, the virophage mavirus integrates efficiently into the nuclear genome of its host, the marine heterotrophic flagellate Cafeteria burkhardae. Mavirus EVEs can reactivate upon superinfection with the lytic giant virus CroV and may act as an adaptive antiviral defense system, because mavirus increases host population survival during a coinfection with CroV. However, the prevalence of endogenous virophages in natural flagellate populations has not been explored. Here we report dozens of endogenous mavirus-like elements (EMALEs) in the nuclear genomes of four C. burkhardae strains. EMALEs were typically 20 kilobase pairs long and constituted 0.7% to 1.8% of each host genome. We analyzed 33 fully assembled EMALEs that fell into two main clusters and eight types based on GC-content, nucleotide similarity, and coding potential. Inter-strain comparison showed conservation of some EMALE insertion loci, whereas the majority of integration sites were unique to a given host strain. We also describe a group of tyrosine recombinase retrotransposons, some of which exhibited a strong preference for integration into EMALEs and represent yet another layer of parasitism in this microbial system. Our findings show that virophages are common, diverse, and dynamic genome components of the marine protist C. burkhardae, which implies important eco-evolutionary roles for these enigmatic viruses.

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“…The new DNA can even originate from other algae—indicating a gene transfer—can allow the algae to improve their survival and may help to increase diversity. Such interactions have been going on since the origins of life, and they will continue [ 76 ].…”

Section: Giant Virusesmentioning

confidence: 99%

“…Endosymbiosis, or symbiogenesis, can extend beyond “master and slave” relationships as for many endosymbionts, but may include mutual benefits and partnerships [ 83 ]. Endogenization has now been shown for giant viruses as well [ 76 ].…”

Section: Endosymbiosismentioning

confidence: 99%

Viroids and the Origin of Life

Moelling

Broecker²

2021

IJMS

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Viroids are non-coding circular RNA molecules with rod-like or branched structures. They are often ribozymes, characterized by catalytic RNA. They can perform many basic functions of life and may have played a role in evolution since the beginning of life on Earth. They can cleave, join, replicate, and undergo Darwinian evolution. Furthermore, ribozymes are the essential elements for protein synthesis of cellular organisms as parts of ribosomes. Thus, they must have preceded DNA and proteins during evolution. Here, we discuss the current evidence for viroids or viroid-like RNAs as a likely origin of life on Earth. As such, they may also be considered as models for life on other planets or moons in the solar system as well as on exoplanets.

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Widespread endogenization of giant viruses shapes genomes of green algae

Cited by 107 publications

References 67 publications

Comparative Genomics and Environmental Distribution of Large dsDNA viruses in the familyAsfarviridae

Comparative Genomics and Environmental Distribution of Large dsDNA viruses in the familyAsfarviridae

Virophages and retrotransposons colonize the genomes of a heterotrophic flagellate

Viroids and the Origin of Life

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