Light regulation of coccolithophore host–virus interactions

Thamatrakoln, Kimberlee; Talmy, David; Haramaty, Liti; Maniscalco, Christopher; Latham, Jason R.; Knowles, Ben; Natale, Frank; Coolen, Marco J. L.; Follows, Michael J.; Bidle, Kay D.

doi:10.1111/nph.15459

Cited by 33 publications

(29 citation statements)

References 61 publications

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“…4B and 4C). The delayed shutdown of chloroplast-encoded genes suggests the need for active chloroplasts in early stages of infection, which is in agreement with the recent finding that photosynthetic electron transport remained active during the initial phase of viral infection ( 26 ). In contrast to chloroplasts, the mitochondrial transcripts were maintained throughout the infection progression, consistent with the high requirement for energy and redox equivalents at all stages of infection.…”

Section: Main Textsupporting

confidence: 90%

Tracking infection dynamics at single-cell level reveals highly resolved expression programs of a large virus infecting algal blooms

Sheyn²,

Sebé-Pedrós

et al. 2019

Preprint

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27Nucleocytoplasmic large DNA viruses have the largest genomes among all viruses and 28 infect diverse eukaryotes across various ecosystems, but their expression regulation and 29 infection strategies are not well understood. We profiled single-cell transcriptomes of the 30 worldwide-distributed microalga Emiliania huxleyi and its specific coccolithovirus 31 responsible for massive bloom demise. Heterogeneity in viral transcript levels detected among 32 single cells was used to reconstruct the viral transcriptional trajectory and to map cells along a 33 continuum of infection states. This enabled identification of novel viral genetic programs, 34 which are composed of five kinetic classes with distinct promoter elements. The infection 35 substantially changed the host transcriptome, causing rapid shutdown of protein-encoding 36 nuclear transcripts at the onset of infection, while the plastid and mitochondrial 37 transcriptomes persisted to mid-and late stages, respectively. Single-cell transcriptomics 38 thereby opens the way for tracking host-pathogen infection dynamics at high resolution within 39 microbial communities in the marine environment. 40 41 42 Main text 43Nucleocytoplasmic large DNA viruses (NCLDVs) are the largest viruses known today 44 in both genome and virion size. They have been found in most major lineages of eukaryotes 45 across diverse habitats (1-4), especially in the marine environment (5, 6). Among the 46 NCLDVs of special ecological importance are members of the family Phycodnaviridae that 47 infect a wide range of key algal hosts (1). These include the cosmopolitan calcifying 48 eukaryotic alga Emiliania huxleyi (Haptophyta), which forms massive annual blooms in the 49 oceans that have a profound impact on the carbon and sulfur biogeochemical cycles (7). E. 50 huxleyi blooms are frequently terminated by a large dsDNA virus -EhV (8), which 51 enhances nutrient cycling and carbon export to the deep ocean (9, 10). This host-virus model 52 provides a trackable system for understanding viral life cycle strategies and host responses. 53High-throughput bulk RNA sequencing (RNA-seq) has been used for whole-genome 54 expression profiling of NCLDVs during infection, shedding light on gene prediction, 55 transcript structure, and changes in metabolic pathways (11)(12)(13). However, bulk RNA-seq 56 profiles average gene expression levels across many cells, whereas infection states can be 57 variable among single cells. To overcome this limitation, single-cell RNA-seq (scRNA-seq) 58 approaches have been developed to probe the transcriptomes of individual cells in a highly 59 parallel manner. These methods have revolutionized our understanding of various 60 developmental and immunological processes (14, 15), including host-virus interactions in 61 mammalian systems (16, 17). 62Here we employed scRNA-seq to study EhV infection of E. huxleyi at the single-cell 63 level, in order to characterize the temporal dynamics and regulation of viral and host 64 transcriptomes. E. huxleyi CCMP2090 cultures were in...

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Section: Main Textsupporting

confidence: 90%

Tracking infection dynamics at single-cell level reveals highly resolved expression programs of a large virus infecting algal blooms

Sheyn²,

Sebé-Pedrós

et al. 2019

Preprint

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“…The failure of P-HM2 to adsorb to MED4 in the dark indicates that adsorption could be directly modulated by light, as suggested by [36]. Light-dependent variation in adsorption has also been reported in cyanophage infecting Synechococcus [36,39] and Cocolithoviruses [48]. Notably, the work of [48] is most similar to our approach, in that it also used nonlinear models to identify light-driven variation in viral straits that impact virus-host population dynamics.…”

Section: Discussionmentioning

confidence: 54%

“…Light-dependent variation in adsorption has also been reported in cyanophage infecting Synechococcus [36,39] and Cocolithoviruses [48]. Notably, the work of [48] is most similar to our approach, in that it also used nonlinear models to identify light-driven variation in viral straits that impact virus-host population dynamics. For Prochlorococcus, there are multiple reasons why P-HM2 may have evolved such variation.…”

Section: Discussionmentioning

confidence: 57%

“…Here, we couple mathematical models, high-resolution (i.e., sub-daily) measurements, and model-data integration to explore the interactions between Prochlorococcus MED4 (a HL ecotype) with the cyanophage P-HM2 and P-SSP7 ( Figure 1b). The models extend the framework of nonlinear population dynamics of lytic viruses and their hosts [47] to an explicitly light-driven context (see the related work of [48] on Cocolithoviruses and their Emiliana huxleyi hosts given low-resolution (i.e., daily) measurements). Our results suggest that cyanophage have light-dependent and host growth-dependent infection patterns with different associated life history traits depending on the viral strain.…”

Section: Introductionmentioning

confidence: 99%

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Linking light-dependent life history traits with population dynamics forProchlorococcusand cyanophage

Demory

Liu

Chen

et al. 2019

Preprint

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Prochlorococcus grow in diurnal rhythms driven by diel cycles. Their ecology depends on light, nutrients, and top-down mortality processes including lysis by viruses. Cyanophage, viruses that infect cyanobacteria, are also impacted by light. For example, extracellular viability and intracell infection kinetics of some cyanophage vary between light and dark conditions. Nonetheless, it remains unclear if light-dependent viral life history traits scale-up to influence population-level dynamics. Here we examined the impact of diel-forcing on both cellular-and population-scale dynamics in multiple Prochlorococcus-phage systems. To do so, we developed a light-driven population model including both cellular growth and viral infection dynamics. We then tested the model against measurements of experimental infection dynamics with diel forcing to examine the extent to which population level changes in both viral and host abundances could be explained by light-dependent life history traits. Model-data integration reveals that light-dependent adsorption can improve fits to population dynamics for some virus-host pairs. However, light-dependent variation alone does not fully explain realized host and virus population dynamics. Instead, we show evidence of a previously unrecognized lysis saturation at relatively high virus to cell ratios. Altogether, our study represents a quantitative approach to integrate mechanistic models to reconcile Prochlorococcus-virus dynamics spanning cellular to population scales. chlorophyll a and b, and have only constitutive photosystem II light-harvesting complexes [23][24][25]. Prochlorococcus cells do not have a circadian rhythm but rather a diurnal rhythm that persists and can be synchronized under light-dark cycles [22,26,27]. This diurnal rhytm is divided into photosynthesis during the light phase and cell division associated with energy consuption during the dark phase [21,28].

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“…An important question for future research is how resource limitation affects these relationships. Nutrient or light limitation have been shown to reduce burst size and lengthen latent period (Wilson et al 1996, Maat and Brussard 2016, Thamatrakoln et al 2019), but the data analyzed here are from experiments under resource-replete conditions. It is possible that the advantage of large genome size is greater under resource limitation, due to a greater control of rate-limiting metabolic reactions.…”

Section: Figurementioning

confidence: 99%

Making sense of virus size and the tradeoffs shaping viral fitness

Edwards

Steward

Schvarcz

2020

Preprint

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Viruses span an impressive size range, with genome length varying more than a thousandfold and capsid volume nearly a millionfold. Physical constraints suggest that smaller viruses may have multiple fitness advantages, because a greater number of viral offspring can be created from limited host resources, and because smaller particles diffuse to encounter new hosts more rapidly. At the same time, a larger genome size allows for numerous additional functions that may increase fitness, such as better control of replication, transcription, translation, and host metabolism, and neutralization of host defenses. However, it is unclear whether important viral traits correlate with size, and whether this causes size to vary among host types or environmental contexts. Here we focus on viruses of aquatic unicellular organisms, which exhibit the greatest known range of virus size. We develop and synthesize theory, and analyze data where available, to consider how size affects the primary components of viral fitness. We suggest that the costs of larger size (lower burst size and diffusivity) are mitigated by the role of a larger genome in increasing infection efficiency, broadening host range, and potentially increasing attachment success and decreasing decay rate. These countervailing selective pressures may explain why such a breadth of sizes exist and can even coexist when infecting the same host populations. We argue that oligotrophic environments may be particularly enriched in unusually large or "giant" viruses, because environments with diverse, resourcelimited phagotrophic eukaryotes at persistently low concentrations may select for broader host range, better control of host metabolism, lower decay rate, and a physical size that mimics bacterial prey. Finally, we describe areas where further research is needed to understand the ecology and evolution of viral size diversity.

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Light regulation of coccolithophore host–virus interactions

Cited by 33 publications

References 61 publications

Tracking infection dynamics at single-cell level reveals highly resolved expression programs of a large virus infecting algal blooms

Tracking infection dynamics at single-cell level reveals highly resolved expression programs of a large virus infecting algal blooms

Linking light-dependent life history traits with population dynamics forProchlorococcusand cyanophage

Making sense of virus size and the tradeoffs shaping viral fitness

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