A Student’s Guide to Giant Viruses Infecting Small Eukaryotes: From Acanthamoeba to Zooxanthellae

Wilhelm, Steven W.; Bird, John; Bonifer, Kyle S.; Calfee, Benjamin C; Chen, Tian; Coy, Samantha R; Gainer, P. Jackson; Gann, Eric R.; Heatherly, Huston T; Lee, Jasper; Liang, Xiaolong; Liu, Jiang; Armes, April C; Moniruzzaman, Mohammad; Rice, Jeffrey H.; Stough, Joshua M. A.; Tams, Robert N.; Williams, Evan P.; LeCleir, Gary R.

doi:10.3390/v9030046

Cited by 46 publications

(46 citation statements)

References 145 publications

(168 reference statements)

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“…Most members of the to date isolated giant viruses of amoeba show a capsid specially composed by copies of an MCP related to the D13L of Vaccinia virus (14, 41). Pandoraviruses are an exception as they seem to lack a protein shell to protect their genomes (25).…”

Section: Discussionmentioning

confidence: 99%

A mysterious 80 nm amoeba virus with a near-complete “ORFan genome” challenges the classification of DNA viruses

Pvm

et al. 2020

Preprint

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Here we report the discovery of Yaravirus, a new lineage of amoebal virus with a puzzling origin and phylogeny. Yaravirus presents 80 nm-sized particles and a 44,924 bp dsDNA genome encoding for 74 predicted proteins. More than 90% (68) of Yaravirus predicted genes have never been described before, representing ORFans. Only six genes had distant homologs in public databases: an exonuclease/recombinase, a packaging-ATPase, a bifunctional DNA primase/polymerase and three hypothetical proteins. Furthermore, we were not able to retrieve viral genomes closely related to Yaravirus in 8,535 publicly available metagenomes spanning diverse habitats around the globe. The Yaravirus genome also contained six types of tRNAs that did not match commonly used codons. Proteomics revealed that Yaravirus particles contain 26 viral proteins, one of which potentially representing a novel capsid protein with no significant homology with NCLDV major capsid proteins but with a predicted double-jelly roll domain. Yaravirus expands our knowledge of the diversity of DNA viruses. The phylogenetic distance between Yaravirus and all other viruses highlights our still preliminary assessment of the genomic diversity of eukaryotic viruses, reinforcing the need for the isolation of new viruses of protists.Significance statementMost of the known viruses of amoeba have been seen to share many features that eventually prompted authors to classify them into common evolutionary groups. Here we describe Yaravirus, an entity that could represent either the first isolated virus of Acanthamoeba spp. out of the group of NCLDVs or, in alternative evolutive scenario, it is a distant and extremely reduced virus of this group. Contrary to what is observed in other isolated viruses of amoeba, Yaravirus is not represented by a large/giant particle and a complex genome, but at the same time carries an important number of previously undescribed genes, including one encoding a novel major capsid protein. Metagenomic approaches also testified for the rarity of Yaravirus in the environment.

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Section: Discussionmentioning

confidence: 99%

A mysterious 80 nm amoeba virus with a near-complete “ORFan genome” challenges the classification of DNA viruses

Pvm

et al. 2020

Preprint

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“…In fact, ~60% of the giant viral genomes were completed after 2013 (Table 1). Many more virus-host systems that were reported for the last 5 years, are still await isolation and characterization [77].…”

Section: The Emerging Ecological Viewmentioning

confidence: 99%

Giant Viruses – Big Surprises

Brandes

Linial

2019

Preprint

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Viruses are the most prevalent infectious agents, populating almost every ecosystem on earth. Most viruses carry only a handful of genes supporting their replication and the production of capsids. It came as a great surprise in 2003 when the first giant virus was discovered and found to have a >1Mbp genome encoding almost a thousand proteins. Following this first discovery, dozens of giant virus strains across several viral families have been reported. Here, we provide an updated quantitative and qualitative view on giant viruses and elaborate on their shared and variable features. We review the complexity of giant virus proteomes, which include functions traditionally associated only with cellular organisms. These unprecedented functions include components of the translation machinery, DNA maintenance, and metabolic enzymes. We discuss the possible underlying evolutionary processes and mechanisms that might have shaped the diversity of giant viruses and their genomes, highlighting their remarkable capacity to hijack genes and genomic sequences from their hosts and environments. This leads us to examine prominent theories regarding the origin of giant viruses. Finally, we present the emerging ecological view of giant viruses, found across widespread habitats and ecological systems, with respect to the environment and human health.

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“…Since the accidental discovery of the 'giant' Mimivirus, viruses with particle sizes and genome sizes larger than many prokaryotic organisms have been isolated and are believed to belong to a monophyletic group termed the Nucleocytoplasmic large dsDNA viruses (NCLDVs) (Wilhelm et al, 2017). The increased genetic potential within these genomes allows for less dependence on the host during the infection cycle.…”

Section: Introductionmentioning

confidence: 99%

Internal Nitrogen Pools Shape the Infection of Aureococcus anophagefferens CCMP 1984 by a Giant Virus

et al. 2020

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The pelagophyte Aureococcus anophagefferens blooms annually in shallow bays around the world, where it is hypothesized to outcompete other phytoplankton in part by using alternative nitrogen sources. The high proportion of natural populations that are infected during the late stages of the bloom suggest viruses cause bloom collapse. We hypothesized that the Aureococcus anophagefferens Virus (AaV) infection cycle would be negatively influenced in cultures acclimated to decreasing external nitrogen conditions, but that the real-time external nitrogen concentration would not influence the infection cycle. Cultures acclimated in NO − 3 concentrations (0.0147 mM; N:P = 0.1225) that showed reduced end point cell abundances, forward scatter (a proxy for size) and red fluorescence (a proxy for chlorophyll a), also produced fewer viruses per cell at a slower rate. Decreasing the external concentration of nitrogen post infection did not alter burst size or time to lysis. These data suggest that the nitrogen used for new viral progeny is present within host cells at the time of infection. Flow cytometric data of an infection cycle showed a reduction in red fluorescence around twelve hours post infection, consistent with degradation of nitrogen-rich chloroplasts during the infection cycle. Using cell and virus quota estimates, we determined that A. anophagefferens cells had sufficient nitrogen and carbon for the lower ranges of burst sizes determined but did not contain enough phosphorous. Consistent with this observation, expression of nitrate and sugar transporters did not increase in the publicly available transcriptome data of the infection cycle, while several phosphorus transporters were. Our data demonstrate that dynamics of viruses infecting Aureococcus over the course of a bloom is dictated by the host cell state upon infection, which is set a priori by external nutrient supplies.

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A Student’s Guide to Giant Viruses Infecting Small Eukaryotes: From Acanthamoeba to Zooxanthellae

Cited by 46 publications

References 145 publications

A mysterious 80 nm amoeba virus with a near-complete “ORFan genome” challenges the classification of DNA viruses

A mysterious 80 nm amoeba virus with a near-complete “ORFan genome” challenges the classification of DNA viruses

Giant Viruses – Big Surprises

Internal Nitrogen Pools Shape the Infection of Aureococcus anophagefferens CCMP 1984 by a Giant Virus

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A Student’s Guide to Giant Viruses Infecting Small Eukaryotes: From Acanthamoeba to Zooxanthellae

Cited by 46 publications

References 145 publications

A mysterious 80 nm amoeba virus with a near-complete “ORFan genome” challenges the classification of DNA viruses

A mysterious 80 nm amoeba virus with a near-complete “ORFan genome” challenges the classification of DNA viruses

Giant Viruses &ndash; Big Surprises

Internal Nitrogen Pools Shape the Infection of Aureococcus anophagefferens CCMP 1984 by a Giant Virus

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Giant Viruses – Big Surprises