Algae Virus

A special issue of Viruses (ISSN 1999-4915). This special issue belongs to the section "Viruses of Plants, Fungi and Protozoa".

Deadline for manuscript submissions: closed (31 July 2018) | Viewed by 61006

Special Issue Editor

Nebraska Center for Virology, University of Nebraska-Lincoln, Lincoln, NE 68583-0900, USA
Interests: virus; giant virus; chlorovirus; aquatic ecology; symbiosis; host–virus interactions; 5 great questions
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Special Issue Information

Dear Colleagues,

We are celebrating 40 years of algal virus research. This celebration corresponds with the 80th year of Jim Van Etten’s life, a founding father of the field of algal virology. Initial observations were of virus-like particles associated with the zoochlorellae of Paramecium bursaria (Kawakami and Kawakami, 1978).  Over the years, algal virus research has blossomed, illuminating many significant findings, including:  i) their diversity (RNA and DNA viruses), distributions and abundances, ii) their role in ecosystems functions, iii) their place as founding members of the “giant viruses,” iv) the insights gained by the evaluation of their complex genome and virion structures, v) the many unusual and un-expected genes for a virus, and vi) the evolutionary connection of certain algal viruses to the nucleocytoplasmic large DNA viruses (NCLDVs). 

This Special Issue of Viruses focuses on “Algal Viruses”, and we have outlined the “Five Great Questions of Algal Virology” as the guiding principle for this issue. The Five Great Questions are:

  1. What is an algal virus?
  2. How do algal viruses move?
  3. How do algal viruses replicate?
  4. What are the consequences of algal virus infections?
  5. Why are algal viruses successful? 

We invite you to help us celebrate the exciting field of algal virology, as well as Jim Van Etten’s significant contributions to algal virology by submitting your current findings to this Special Issue and relate your studies to the Five Great Questions. We also encourage you to make any personal comments on your relationship with Jim Van Etten, and/or how his career may have impacted yours. This is an exciting time to be studying the algal viruses and we look forward to learning of your current research interests and sharing those findings through this Special Issue.   

Prof. David D. Dunigan
Guest Editor

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Keywords

  • algae
  • virus
  • phycodnavirus
  • Phycodnaviridae
  • Marnaviridae
  • aquatic virus

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Published Papers (12 papers)

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Research

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16 pages, 3624 KiB  
Article
Influence of Irradiance and Temperature on the Virus MpoV-45T Infecting the Arctic Picophytoplankter Micromonas polaris
by Gonçalo J. Piedade, Ella M. Wesdorp, Elena Montenegro-Borbolla, Douwe S. Maat and Corina P. D. Brussaard
Viruses 2018, 10(12), 676; https://doi.org/10.3390/v10120676 - 29 Nov 2018
Cited by 17 | Viewed by 5269
Abstract
Arctic marine ecosystems are currently undergoing rapid changes in temperature and light availability. Picophytoplankton, such as Micromonas polaris, are predicted to benefit from such changes. However, little is known about how these environmental changes affect the viruses that exert a strong mortality [...] Read more.
Arctic marine ecosystems are currently undergoing rapid changes in temperature and light availability. Picophytoplankton, such as Micromonas polaris, are predicted to benefit from such changes. However, little is known about how these environmental changes affect the viruses that exert a strong mortality pressure on these small but omnipresent algae. Here we report on one-step infection experiments, combined with measurements of host physiology and viability, with 2 strains of M. polaris and the virus MpoV-45T under 3 light intensities (5, 60 and 160 μmol quanta m−2 s−1), 2 light period regimes (16:8 and 24:0 h light:dark cycle) and 2 temperatures (3 and 7 °C). Our results show that low light intensity (16:8 h light:dark) delayed the decline in photosynthetic efficiency and cell lysis, while decreasing burst size by 46%. In contrast, continuous light (24:0 h light:dark) shortened the latent period by 5 h for all light intensities, and even increased the maximum virus production rate and burst size under low light (by 157 and 69%, respectively). Higher temperature (7 °C vs 3 °C) led to earlier cell lysis and increased burst size (by 19%), except for the low light conditions. These findings demonstrate the ecological importance of light in combination with temperature as a controlling factor for Arctic phytoplankton host and virus dynamics seasonally, even more so in the light of global warming. Full article
(This article belongs to the Special Issue Algae Virus)
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19 pages, 2750 KiB  
Article
Gene Gangs of the Chloroviruses: Conserved Clusters of Collinear Monocistronic Genes
by Phillip Seitzer, Adrien Jeanniard, Fangrui Ma, James L. Van Etten, Marc T. Facciotti and David D. Dunigan
Viruses 2018, 10(10), 576; https://doi.org/10.3390/v10100576 - 20 Oct 2018
Cited by 8 | Viewed by 3625
Abstract
Chloroviruses (family Phycodnaviridae) are dsDNA viruses found throughout the world’s inland waters. The open reading frames in the genomes of 41 sequenced chloroviruses (330 ± 40 kbp each) representing three virus types were analyzed for evidence of evolutionarily conserved local genomic “contexts”, [...] Read more.
Chloroviruses (family Phycodnaviridae) are dsDNA viruses found throughout the world’s inland waters. The open reading frames in the genomes of 41 sequenced chloroviruses (330 ± 40 kbp each) representing three virus types were analyzed for evidence of evolutionarily conserved local genomic “contexts”, the organization of biological information into units of a scale larger than a gene. Despite a general loss of synteny between virus types, we informatically detected a highly conserved genomic context defined by groups of three or more genes that we have termed “gene gangs”. Unlike previously described local genomic contexts, the definition of gene gangs requires only that member genes be consistently co-localized and are not constrained by strand, regulatory sites, or intervening sequences (and therefore represent a new type of conserved structural genomic element). An analysis of functional annotations and transcriptomic data suggests that some of the gene gangs may organize genes involved in specific biochemical processes, but that this organization does not involve their coordinated expression. Full article
(This article belongs to the Special Issue Algae Virus)
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7 pages, 2009 KiB  
Communication
Visualization of a Dinoflagellate-Infecting Virus HcDNAV and Its Infection Process
by Yoshihito Takano, Yuji Tomaru and Keizo Nagasaki
Viruses 2018, 10(10), 554; https://doi.org/10.3390/v10100554 - 11 Oct 2018
Cited by 6 | Viewed by 4138
Abstract
HcDNAV (a type species of Genus Dinodnavirus) is a large double-stranded DNA virus, which lytically infects the bloom-forming marine microalga Heterocapsa circularisquama Horiguchi (Dinophyceae). In the present study, detailed observation of the HcDNAV particle and its infection process was conducted via field [...] Read more.
HcDNAV (a type species of Genus Dinodnavirus) is a large double-stranded DNA virus, which lytically infects the bloom-forming marine microalga Heterocapsa circularisquama Horiguchi (Dinophyceae). In the present study, detailed observation of the HcDNAV particle and its infection process was conducted via field emission scanning electron microscopy (FE-SEM) and epifluorescence microscopy (EFM). Each five-fold vertex of the icosahedral virion was decorated with a protrusion, which may be related to the entry process of HcDNAV into the host. The transverse groove of host cells is proposed to be the main virus entry site. A visible DAPI-stained region, which is considered to be the viroplasm (virus factory), appeared in close proximity to the host nucleus at 11 h post infection (hpi); the putative viral DAPI signal was remarkably enlarged at 11–30 hpi. It was kidney-shaped at 13–15 hpi, horseshoe-shaped at 20 hpi, doughnut-shaped at 30 hpi, and changed into a three-dimensionally complicated shape at 51–53 hpi, by which time most parts of the host cell were occupied by the putative viral DAPI signal. While the virions were within the viroplasm, they were easily distinguishable by their vertex protrusions by FE-SEM. Full article
(This article belongs to the Special Issue Algae Virus)
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11 pages, 407 KiB  
Article
Quantitative Infection Dynamics of Cafeteria Roenbergensis Virus
by Bradford P. Taylor, Joshua S. Weitz, Corina P. D. Brussaard and Matthias G. Fischer
Viruses 2018, 10(9), 468; https://doi.org/10.3390/v10090468 - 31 Aug 2018
Cited by 3 | Viewed by 4288
Abstract
The discovery of giant viruses in unicellular eukaryotic hosts has raised new questions on the nature of viral life. Although many steps in the infection cycle of giant viruses have been identified, the quantitative life history traits associated with giant virus infection remain [...] Read more.
The discovery of giant viruses in unicellular eukaryotic hosts has raised new questions on the nature of viral life. Although many steps in the infection cycle of giant viruses have been identified, the quantitative life history traits associated with giant virus infection remain unknown or poorly constrained. In this study, we provide the first estimates of quantitative infection traits of a giant virus by tracking the infection dynamics of the bacterivorous protist Cafeteria roenbergensis and its lytic virus CroV. Leveraging mathematical models of infection, we quantitatively estimate the adsorption rate, onset of DNA replication, latency time, and burst size from time-series data. Additionally, by modulating the initial ratio of viruses to hosts, we also provide evidence of a potential MOI-dependence on adsorption and burst size. Our work provides a baseline characterization of giant virus infection dynamics relevant to ongoing efforts to understand the ecological role of giant viruses. Full article
(This article belongs to the Special Issue Algae Virus)
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24 pages, 1160 KiB  
Article
Genes for Membrane Transport Proteins: Not So Rare in Viruses
by Timo Greiner, Anna Moroni, James L Van Etten and Gerhard Thiel
Viruses 2018, 10(9), 456; https://doi.org/10.3390/v10090456 - 26 Aug 2018
Cited by 16 | Viewed by 4829
Abstract
Some viruses have genes encoding proteins with membrane transport functions. It is unknown if these types of proteins are rare or are common in viruses. In particular, the evolutionary origin of some of the viral genes is obscure, where other viral proteins have [...] Read more.
Some viruses have genes encoding proteins with membrane transport functions. It is unknown if these types of proteins are rare or are common in viruses. In particular, the evolutionary origin of some of the viral genes is obscure, where other viral proteins have homologs in prokaryotic and eukaryotic organisms. We searched virus genomes in databases looking for transmembrane proteins with possible transport function. This effort led to the detection of 18 different types of putative membrane transport proteins indicating that they are not a rarity in viral genomes. The most abundant proteins are K+ channels. Their predicted structures vary between different viruses. With a few exceptions, the viral proteins differed significantly from homologs in their current hosts. In some cases the data provide evidence for a recent gene transfer between host and virus, but in other cases the evidence indicates a more complex evolutionary history. Full article
(This article belongs to the Special Issue Algae Virus)
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11 pages, 3430 KiB  
Article
Rapidity of Genomic Adaptations to Prasinovirus Infection in a Marine Microalga
by Sheree Yau, Gaëtan Caravello, Nadège Fonvieille, Élodie Desgranges, Hervé Moreau and Nigel Grimsley
Viruses 2018, 10(8), 441; https://doi.org/10.3390/v10080441 - 19 Aug 2018
Cited by 4 | Viewed by 4111
Abstract
Prasinoviruses are large dsDNA viruses commonly found in aquatic systems worldwide, where they can infect and lyse unicellular prasinophyte algae such as Ostreococcus. Host susceptibility is virus strain-specific, but resistance of susceptible Ostreococcus tauri strains to a virulent virus arises frequently. In [...] Read more.
Prasinoviruses are large dsDNA viruses commonly found in aquatic systems worldwide, where they can infect and lyse unicellular prasinophyte algae such as Ostreococcus. Host susceptibility is virus strain-specific, but resistance of susceptible Ostreococcus tauri strains to a virulent virus arises frequently. In clonal resistant lines that re-grow, viruses are usually present for many generations, and genes clustered on chromosome 19 show physical rearrangements and differential expression. Here, we investigated changes occurring during the first two weeks after inoculation of the prasinovirus OtV5. By serial dilutions of cultures at the time of inoculation, we estimated the frequency of resistant cells arising in virus-challenged O. tauri cultures to be 10−3–10−4 of the inoculated population. Re-growing resistant cells were detectable by flow cytometry 3 days post-inoculation (dpi), visible re-greening of cultures occurred by 6 dpi, and karyotypic changes were visually detectable at 8 dpi. Resistant cell lines showed a modified spectrum of host-virus specificities and much lower levels of OtV5 adsorption. Full article
(This article belongs to the Special Issue Algae Virus)
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18 pages, 8169 KiB  
Article
Phaeoviral Infections Are Present in Macrocystis, Ecklonia and Undaria (Laminariales) and Are Influenced by Wave Exposure in Ectocarpales
by Dean A. McKeown, Joanna L. Schroeder, Kim Stevens, Akira F. Peters, Claudio A. Sáez, Jihae Park, Mark D. Rothman, John J. Bolton, Murray T. Brown and Declan C. Schroeder
Viruses 2018, 10(8), 410; https://doi.org/10.3390/v10080410 - 05 Aug 2018
Cited by 11 | Viewed by 4975
Abstract
Two sister orders of the brown macroalgae (class Phaeophyceae), the morphologically complex Laminariales (commonly referred to as kelp) and the morphologically simple Ectocarpales are natural hosts for the dsDNA phaeoviruses (family Phycodnaviridae) that persist as proviruses in the genomes of their hosts. [...] Read more.
Two sister orders of the brown macroalgae (class Phaeophyceae), the morphologically complex Laminariales (commonly referred to as kelp) and the morphologically simple Ectocarpales are natural hosts for the dsDNA phaeoviruses (family Phycodnaviridae) that persist as proviruses in the genomes of their hosts. We have previously shown that the major capsid protein (MCP) and DNA polymerase concatenated gene phylogeny splits phaeoviruses into two subgroups, A and B (both infecting Ectocarpales), while MCP-based phylogeny suggests that the kelp phaeoviruses form a distinct third subgroup C. Here we used MCP to better understand the host range of phaeoviruses by screening a further 96 and 909 samples representing 11 and 3 species of kelp and Ectocarpales, respectively. Sporophyte kelp samples were collected from their various natural coastal habitats spanning five continents: Africa, Asia, Australia, Europe, and South America. Our phylogenetic analyses showed that while most of the kelp phaeoviruses, including one from Macrocystispyrifera, belonged to the previously designated subgroup C, new lineages of Phaeovirus in 3 kelp species, Ecklonia maxima, Ecklonia radiata, Undaria pinnatifida, grouped instead with subgroup A. In addition, we observed a prevalence of 26% and 63% in kelp and Ectocarpales, respectively. Although not common, multiple phaeoviral infections per individual were observed, with the Ectocarpales having both intra- and inter-subgroup phaeoviral infections. Only intra-subgroup phaeoviral infections were observed in kelp. Furthermore, prevalence of phaeoviral infections within the Ectocarpales is also linked to their exposure to waves. We conclude that phaeoviral infection is a widely occurring phenomenon in both lineages, and that phaeoviruses have diversified with their hosts at least since the divergence of the Laminariales and Ectocarpales. Full article
(This article belongs to the Special Issue Algae Virus)
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Review

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14 pages, 886 KiB  
Review
Mimiviridae: An Expanding Family of Highly Diverse Large dsDNA Viruses Infecting a Wide Phylogenetic Range of Aquatic Eukaryotes
by Jean-Michel Claverie and Chantal Abergel
Viruses 2018, 10(9), 506; https://doi.org/10.3390/v10090506 - 18 Sep 2018
Cited by 54 | Viewed by 6504
Abstract
Since 1998, when Jim van Etten’s team initiated its characterization, Paramecium bursaria Chlorella virus 1 (PBCV-1) had been the largest known DNA virus, both in terms of particle size and genome complexity. In 2003, the Acanthamoeba-infecting Mimivirus unexpectedly superseded PBCV-1, opening the [...] Read more.
Since 1998, when Jim van Etten’s team initiated its characterization, Paramecium bursaria Chlorella virus 1 (PBCV-1) had been the largest known DNA virus, both in terms of particle size and genome complexity. In 2003, the Acanthamoeba-infecting Mimivirus unexpectedly superseded PBCV-1, opening the era of giant viruses, i.e., with virions large enough to be visible by light microscopy and genomes encoding more proteins than many bacteria. During the following 15 years, the isolation of many Mimivirus relatives has made Mimiviridae one of the largest and most diverse families of eukaryotic viruses, most of which have been isolated from aquatic environments. Metagenomic studies of various ecosystems (including soils) suggest that many more remain to be isolated. As Mimiviridae members are found to infect an increasing range of phytoplankton species, their taxonomic position compared to the traditional Phycodnaviridae (i.e., etymologically “algal viruses”) became a source of confusion in the literature. Following a quick historical review of the key discoveries that established the Mimiviridae family, we describe its current taxonomic structure and propose a set of operational criteria to help in the classification of future isolates. Full article
(This article belongs to the Special Issue Algae Virus)
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17 pages, 3639 KiB  
Review
Algal Viruses: The (Atomic) Shape of Things to Come
by Christopher T. Evans, Oliver Payton, Loren Picco and Michael J. Allen
Viruses 2018, 10(9), 490; https://doi.org/10.3390/v10090490 - 12 Sep 2018
Cited by 1 | Viewed by 4094
Abstract
Visualization of algal viruses has been paramount to their study and understanding. The direct observation of the morphological dynamics of infection is a highly desired capability and the focus of instrument development across a variety of microscopy technologies. However, the high temporal (ms) [...] Read more.
Visualization of algal viruses has been paramount to their study and understanding. The direct observation of the morphological dynamics of infection is a highly desired capability and the focus of instrument development across a variety of microscopy technologies. However, the high temporal (ms) and spatial resolution (nm) required, combined with the need to operate in physiologically relevant conditions presents a significant challenge. Here we present a short history of virus structure study and its relation to algal viruses and highlight current work, concentrating on electron microscopy and atomic force microscopy, towards the direct observation of individual algae–virus interactions. Finally, we make predictions towards future algal virus study direction with particular focus on the exciting opportunities offered by modern high-speed atomic force microscopy methods and instrumentation. Full article
(This article belongs to the Special Issue Algae Virus)
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27 pages, 1930 KiB  
Review
Viruses of Eukaryotic Algae: Diversity, Methods for Detection, and Future Directions
by Samantha R. Coy, Eric R. Gann, Helena L. Pound, Steven M. Short and Steven W. Wilhelm
Viruses 2018, 10(9), 487; https://doi.org/10.3390/v10090487 - 11 Sep 2018
Cited by 43 | Viewed by 8650
Abstract
The scope for ecological studies of eukaryotic algal viruses has greatly improved with the development of molecular and bioinformatic approaches that do not require algal cultures. Here, we review the history and perceived future opportunities for research on eukaryotic algal viruses. We begin [...] Read more.
The scope for ecological studies of eukaryotic algal viruses has greatly improved with the development of molecular and bioinformatic approaches that do not require algal cultures. Here, we review the history and perceived future opportunities for research on eukaryotic algal viruses. We begin with a summary of the 65 eukaryotic algal viruses that are presently in culture collections, with emphasis on shared evolutionary traits (e.g., conserved core genes) of each known viral type. We then describe how core genes have been used to enable molecular detection of viruses in the environment, ranging from PCR-based amplification to community scale “-omics” approaches. Special attention is given to recent studies that have employed network-analyses of -omics data to predict virus-host relationships, from which a general bioinformatics pipeline is described for this type of approach. Finally, we conclude with acknowledgement of how the field of aquatic virology is adapting to these advances, and highlight the need to properly characterize new virus-host systems that may be isolated using preliminary molecular surveys. Researchers can approach this work using lessons learned from the Chlorella virus system, which is not only the best characterized algal-virus system, but is also responsible for much of the foundation in the field of aquatic virology. Full article
(This article belongs to the Special Issue Algae Virus)
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18 pages, 829 KiB  
Review
Why Are Algal Viruses Not Always Successful?
by Elena L. Horas, Loukas Theodosiou and Lutz Becks
Viruses 2018, 10(9), 474; https://doi.org/10.3390/v10090474 - 05 Sep 2018
Cited by 14 | Viewed by 5332
Abstract
Algal viruses are considered to be key players in structuring microbial communities and biogeochemical cycles due to their abundance and diversity within aquatic systems. Their high reproduction rates and short generation times make them extremely successful, often with immediate and strong effects for [...] Read more.
Algal viruses are considered to be key players in structuring microbial communities and biogeochemical cycles due to their abundance and diversity within aquatic systems. Their high reproduction rates and short generation times make them extremely successful, often with immediate and strong effects for their hosts and thus in biological and abiotic environments. There are, however, conditions that decrease their reproduction rates and make them unsuccessful with no or little immediate effects. Here, we review the factors that lower viral success and divide them into intrinsic—when they are related to the life cycle traits of the virus—and extrinsic factors—when they are external to the virus and related to their environment. Identifying whether and how algal viruses adapt to disadvantageous conditions will allow us to better understand their role in aquatic systems. We propose important research directions such as experimental evolution or the resurrection of extinct viruses to disentangle the conditions that make them unsuccessful and the effects these have on their surroundings. Full article
(This article belongs to the Special Issue Algae Virus)
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Other

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4 pages, 187 KiB  
Opinion
Is the Virus Important? And Some Other Questions
by Ruth-Anne Sandaa and Gunnar Bratbak
Viruses 2018, 10(8), 442; https://doi.org/10.3390/v10080442 - 19 Aug 2018
Cited by 3 | Viewed by 3546
Abstract
The motivation for focusing on a specific virus is often its importance in terms of impact on human interests. The chlorella viruses are a notable exception and 40 years of research has made them the undisputed model system for large icosahedral dsDNA viruses [...] Read more.
The motivation for focusing on a specific virus is often its importance in terms of impact on human interests. The chlorella viruses are a notable exception and 40 years of research has made them the undisputed model system for large icosahedral dsDNA viruses infecting eukaryotes. Their status has changed from inconspicuous and rather odd with no ecological relevance to being the Phycodnaviridae type strain possibly affecting humans and human cognitive functioning in ways that remain to be understood. The Van Etten legacy is the backbone for research on Phycodnaviridae. After highlighting some of the peculiarities of chlorella viruses, we point to some issues and questions related to the viruses we choose for our research, our prejudices, what we are still missing, and what we should be looking for. Full article
(This article belongs to the Special Issue Algae Virus)
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