Functional Genomic Analyses Reveal an Open Pan-genome for the Chloroviruses and a Potential for Genetic Innovation in New Isolates

Rodrigues, Rodrigo Araújo Lima; Queiroz, Victória Fulgêncio; Ghosh, Jayadri Sekhar; Dunigan, David D.; Etten, James L. Van

doi:10.1128/jvi.01367-21

Cited by 10 publications

(17 citation statements)

References 61 publications

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“…In future, combining trait data with genomic data (Jeanniard et al ., 2013; e.g. Rodrigues et al ., 2022) could allow the creation of a genotype-to-phenotype map to explore chlorovirus evolution (DeLong et al ., 2022).…”

Section: Discussionmentioning

confidence: 99%

“…Finally, we used phylogenetic ANOVAs to partition variance among the virus clades. This accounted for the paraphyletic nature of the NC64A viruses, which are divided into a PBCV-1 clade and an NY-2A clade by the Osy strain OSyNE-5 (Quispe et al ., 2017; Rodrigues et al ., 2022). For each series of ANOVAs, we corrected for multiple testing with Holm’s method (Holm, 1979).…”

Section: Methodsmentioning

confidence: 99%

“…4Here we assume that the group level corresponds to the species level, within which evolution can occur. The chlorovirus groups infect the same hosts and a high protein sequence similarity (≥ 92.6%, Jeanniard et al ., 2013; see also Rodrigues et al ., 2022), supporting this approach. Yet considering the paraphyletic nature of the NC64A viruses (Quispe et al ., 2017; Rodrigues et al ., 2022), it may be more accurate to use virus clade as a species proxy.…”

mentioning

confidence: 94%

“…The chlorovirus groups infect the same hosts and a high protein sequence similarity (≥ 92.6%, Jeanniard et al ., 2013; see also Rodrigues et al ., 2022), supporting this approach. Yet considering the paraphyletic nature of the NC64A viruses (Quispe et al ., 2017; Rodrigues et al ., 2022), it may be more accurate to use virus clade as a species proxy. This would not affect our conclusion, as we also found ample within-clade phenotypic variation.…”

mentioning

confidence: 94%

“…Virions are large ( ~ 190 nm, Yan et al ., 2000; Quispe et al ., 2017) and their decay is temperature-dependent (Van Etten et al ., 1983; Agarkova et al ., 2014). The chloroviruses are known to vary in genome content and plaque size (Van Etten et al ., 1988; Rodrigues et al ., 2022), for example, but the life cycle traits have almost exclusively been measured in the type strain PBCV-1 (exceptions: Van Etten et al ., 1988; Greiner et al ., 2009; Quispe et al ., 2017; Schiano di Visconte et al ., 2022).…”

Section: Introductionmentioning

confidence: 99%

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High life history diversity within a single genus of phytoplankton viruses

Lievens

Agarkova

Dunigan

et al. 2022

Preprint

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Microbial viruses affect the ecology and evolution of every environment on earth. Although these effects can play out on a grand scale, to understand them we need to zoom in to virus' life cycle traits. The values of these traits determine a virus' effect on the host population, the trait diversity provides the material for natural selection, and trade-offs between the traits are expected to constrain virus' evolutionary potential. However, due to the difficulty involved in measuring viral life history phenotypes, there are not many studies that characterize their diversity within clades of viruses. In this study, we quantified the life history of 35 chloroviruses from three host range groups (NC64A, Osy, and SAG viruses). We developed methods to efficiently measure adsorption rate, depolarization probability, lysis probability, lysis time, burst size, specific infectivity, and decay. The trait estimates varied between 5 and 75-fold across all the virus strains, with most traits varying substantially both within and across groups. We then used our largest virus group, the NC64A viruses (n = 20), to look for correlations that could signal trade-offs between traits. We found that viruses with high depolarization probabilities also had higher burst sizes, but lower lysis probabilities once depolarized. These correlations were strong, but their mechanistic underpinnings are unclear. We also found a strong correlation between growth rate and survival in the NC64A viruses. Finally, we discovered biphasic or 'tailing' decay in all the chlorovirus groups. The nature and diversity of these traits has large implications for the ecology and evolutionary potential of the chloroviruses, and confirm the importance of studying viral life cycle traits.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 94%

mentioning

confidence: 94%

Section: Introductionmentioning

confidence: 99%

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High life history diversity within a single genus of phytoplankton viruses

Lievens

Agarkova

Dunigan

et al. 2022

Preprint

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Genomic analysis of lumpy skin disease virus asian variants and evaluation of its cellular tropism

Xie,

Cui,

Liao

et al. 2024

npj Vaccines

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Lumpy skin disease virus (LSDV) is a poxvirus that mainly affects cattle and can lead to symptoms such as severe reduction in milk production as well as infertility and mortality, which has resulted in dramatic economic loss in affected countries in Africa, Europe, and Asia. In this study, we successfully isolated two strains of LSDV from different geographical regions in China. Comparative genomic analyses were performed by incorporating additional LSDV whole genome sequences reported in other areas of Asia. Our analyses revealed that LSDV exhibited an ‘open’ pan-genome. Phylogenetic analysis unveiled distinct branches of LSDV evolution, signifying the prevalence of multiple lineages of LSDV across various regions in Asia. In addition, a reporter LSDV expressing eGFP directed by a synthetic poxvirus promoter was generated and used to evaluate the cell tropism of LSDV in various mammalian and avian cell lines. Our results demonstrated that LSDV replicated efficiently in several mammalian cell lines, including human A549 cells. In conclusion, our results underscore the necessity for strengthening LSD outbreak control measures and continuous epidemiological surveillance.

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Efficient assays to quantify the life history traits of algal viruses

Lievens,

Agarkova,

Dunigan

et al. 2023

Appl Environ Microbiol

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Although viral life history traits—the traits that determine reproductive and survival success—are critical to understanding the population dynamics and impact of viruses, they are understudied compared to molecular traits. This discrepancy is partly due to the challenge of phenotyping viral life histories. We developed improved methods to quantify the life cycles of chloroviruses, which are lytic double-stranded DNA viruses that infect unicellular “chlorella-like” algae. We modified classical one-step growth and survival assays by including flow cytometry and kinetic modeling, and applied these to four chlorovirus strains. Together, the modified assays quantified the full life cycle, including adsorption rate, probability of depolarizing the host cell, probability of releasing progeny virions, time until lysis, burst size, specific infectivity, and mortality rate of infectious virions. We also discovered that biphasic or “tailing” decay can occur in chloroviruses, and measured the fraction of infectious virions that resisted decay. The modified assays are more efficient than existing techniques, quantify more traits, and are applicable to other lytic viruses with quantifiable virions. The modified one-step growth assay is suitable for viruses with mutual exclusion, superinfection exclusion, or superinfection immunity; the modified survival assay can be applied to any lytic virus with quantifiable virions. IMPORTANCE Viruses play a crucial role in microbial ecosystems by liberating nutrients and regulating the growth of their hosts. These effects are governed by viral life history traits, i.e., by the traits determining viral reproduction and survival. Understanding these traits is essential to predicting viral effects, but measuring them is generally labor intensive. In this study, we present efficient methods to quantify the full life cycle of lytic viruses. We developed these methods for viruses infecting unicellular Chlorella algae but expect them to be applicable to other lytic viruses that can be quantified by flow cytometry. By making viral phenotypes accessible, our methods will support research into the diversity and ecological effects of microbial viruses.

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Functional Genomic Analyses Reveal an Open Pan-genome for the Chloroviruses and a Potential for Genetic Innovation in New Isolates

Abstract: Chloroviruses are large dsDNA viruses that infect unicellular green algae distributed worldwide in freshwater environments. They comprise a genetically diverse group of viruses; however, a comprehensive investigation of the genomic evolution of these viruses is still missing.

Cited by 10 publications

References 61 publications

High life history diversity within a single genus of phytoplankton viruses

High life history diversity within a single genus of phytoplankton viruses

Genomic analysis of lumpy skin disease virus asian variants and evaluation of its cellular tropism

Efficient assays to quantify the life history traits of algal viruses

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