A phylogenomic data-driven exploration of viral origins and evolution

Nasir, Arshan; Caetano‐Anollés, Gustavo

doi:10.1126/sciadv.1500527

Cited by 184 publications

(263 citation statements)

References 132 publications

(209 reference statements)

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“…As mentioned above, it is possible that RNAs encoding structural proteins associated with other viruses with segmented genomes had been lost by repeated cytoplasmic transmission. Additional analysis will be required to determine whether this is an outcome of horizontal cytoplasmic virus transfer or the bioinformatic methods used to detect structural protein genes, which are typically much less conserved than replication-related protein genes (88,89).…”

Section: Discussionmentioning

confidence: 99%

Identification of Diverse Mycoviruses through Metatranscriptomics Characterization of the Viromes of Five Major Fungal Plant Pathogens

Marzano

Nelson

Ajayi-Oyetunde

et al. 2016

J Virol

234

224

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Mycoviruses can have a marked effect on natural fungal communities and influence plant health and productivity. However, a comprehensive picture of mycoviral diversity is still lacking. To characterize the viromes of five widely dispersed plant-pathogenic fungi, Colletotrichum truncatum, Macrophomina phaseolina, Diaporthe longicolla, Rhizoctonia solani, and Sclerotinia sclerotiorum, a high-throughput sequencing-based metatranscriptomic approach was used to detect viral sequences. Total RNA and double-stranded RNA (dsRNA) from mycelia and RNA from samples enriched for virus particles were sequenced. Sequence data were assembled de novo, and contigs with predicted amino acid sequence similarities to viruses in the nonredundant protein database were selected. The analysis identified 72 partial or complete genome segments representing 66 previously undescribed mycoviruses. Using primers specific for each viral contig, at least one fungal isolate was identified that contained each virus. The novel mycoviruses showed affinity with 15 distinct lineages: Barnaviridae, Benyviridae, Chrysoviridae, Endornaviridae, Fusariviridae, Hypoviridae, Mononegavirales, Narnaviridae, Ophioviridae, Ourmiavirus, Partitiviridae, Tombusviridae, Totiviridae, Tymoviridae, and Virgaviridae. More than half of the viral sequences were predicted to be members of the Mitovirus genus in the family Narnaviridae, which replicate within mitochondria. Five viral sequences showed strong affinity with three families (Benyviridae, Ophioviridae, and Virgaviridae) that previously contained no mycovirus species. The genomic information provides insight into the diversity and taxonomy of mycoviruses and coevolution of mycoviruses and their fungal hosts. IMPORTANCEPlant-pathogenic fungi reduce crop yields, which affects food security worldwide. Plant host resistance is considered a sustainable disease management option but may often be incomplete or lacking for some crops to certain fungal pathogens or strains. In addition, the rising issues of fungicide resistance demand alternative strategies to reduce the negative impacts of fungal pathogens. Those fungus-infecting viruses (mycoviruses) that attenuate fungal virulence may be welcome additions for mitigation of plant diseases. By high-throughput sequencing of the RNAs from 275 isolates of five fungal plant pathogens, 66 previously undescribed mycoviruses were identified. In addition to identifying new potential biological control agents, these results expand the grand view of the diversity of mycoviruses and provide possible insights into the importance of intracellular and extracellular transmission in fungus-virus coevolution. R ecent metatranscriptomic and metagenomic studies of animals, fungi, insects, plants, and environmental samples have shown that mycoviruses are ubiquitous in nature (1-10). Analyses of viral metagenomes (i.e., viromes) of environmental samples suggest that the field of virology has discovered less than 1% of the existing viral diversity, and the rate of discovery by metage...

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Section: Discussionmentioning

confidence: 99%

Identification of Diverse Mycoviruses through Metatranscriptomics Characterization of the Viromes of Five Major Fungal Plant Pathogens

Marzano

Nelson

Ajayi-Oyetunde

et al. 2016

J Virol

234

224

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“…Currently, there were two major scenarios for evolution of Giant dsDNA viruses; the ‘reduction model’ and the ‘expansion model.’ The ‘reduction model’ is based on the idea that the viruses presumably emerged from much more complex organisms with larger sizes of genome, and reached to current status by genome simplifications (Raoult et al, 2004; Martin et al, 2010; Boyer et al, 2011; Nasir and Caetano-Anollés, 2015). In the ‘expansion model,’ the viruses are presumed to descend from common ancestor virus with much smaller genomes, and reaching to contemporary sizes and diversity by progressively acquiring genes (Yutin et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

Evolution and Phylogeny of Large DNA Viruses, Mimiviridae and Phycodnaviridae Including Newly Characterized Heterosigma akashiwo Virus

Maruyama

Ueki

2016

Front. Microbiol.

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Nucleocytoplasmic DNA viruses are a large group of viruses that harbor double-stranded DNA genomes with sizes of several 100 kbp, challenging the traditional concept of viruses as small, simple ‘organisms at the edge of life.’ The most intriguing questions about them may be their origin and evolution, which have yielded the variety we see today. Specifically, the phyletic relationship between two giant dsDNA virus families that are presumed to be close, Mimiviridae, which infect Acanthamoeba, and Phycodnaviridae, which infect algae, is still obscure and needs to be clarified by in-depth analysis. Here, we studied Mimiviridae–Phycodnaviridae phylogeny including the newly identified Heterosigma akashiwo virus strain HaV53. Gene-to-gene comparison of HaV53 with other giant dsDNA viruses showed that only a small proportion of HaV53 genes show similarities with the others, revealing its uniqueness among Phycodnaviridae. Phylogenetic/genomic analysis of Phycodnaviridae including HaV53 revealed that the family can be classified into four distinctive subfamilies, namely, Megaviridae (Mimivirus-like), Chlorovirus-type, and Coccolitho/Phaeovirus-type groups, and HaV53 independent of the other three groups. Several orthologs found in specific subfamilies while absent from the others were identified, providing potential family marker genes. Finally, reconstruction of the evolutionary history of Phycodnaviridae and Mimiviridae revealed that these viruses are descended from a common ancestor with a small set of genes and reached their current diversity by differentially acquiring gene sets during the course of evolution. Our study illustrates the phylogeny and evolution of Mimiviridae–Phycodnaviridae and proposes classifications that better represent phyletic relationships among the family members.

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“…The origin of viruses is still obscure (Nasir and Caetano-Anollés, 2015). So far, no common ancestor has been found.…”

Section: A Symbio-centric Ecological Speciation Frameworkmentioning

confidence: 99%

Bacterial Diversification in the Light of the Interactions with Phages: The Genetic Symbionts and Their Role in Ecological Speciation

et al. 2018

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Phages have a major impact on microbial populations. In this work, we discuss how predation, transduction, lysogeny, and phage domestication lead to symbio-centric genomic interactions between bacteria and phages, ranging from antagonistic to mutualistic. Furthermore, these interactions influence bacterial diversification and ecotype formation. We then propose an additional consideration in the form of a symbio-centric ecological speciation framework for bacteria. Our framework builds upon classical morphological and molecular taxonomy by also considering bacteria and their phages as a unit of evolutionary selection. This framework acknowledges the considerable effect that phage interaction has on bacterial genomic content, regulation, and evolution, and will advance our understanding of bacterial evolution.

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A phylogenomic data-driven exploration of viral origins and evolution

Abstract: A study of the evolution of the proteomic makeup of cells and viruses using protein structural and functional data.

Cited by 184 publications

References 132 publications

Identification of Diverse Mycoviruses through Metatranscriptomics Characterization of the Viromes of Five Major Fungal Plant Pathogens

Identification of Diverse Mycoviruses through Metatranscriptomics Characterization of the Viromes of Five Major Fungal Plant Pathogens

Evolution and Phylogeny of Large DNA Viruses, Mimiviridae and Phycodnaviridae Including Newly Characterized Heterosigma akashiwo Virus

Bacterial Diversification in the Light of the Interactions with Phages: The Genetic Symbionts and Their Role in Ecological Speciation

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