Dataset Information

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

ABSTRACT: 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 NO3- 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.

SUBMITTER: Gann ER

PROVIDER: S-EPMC7109300 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Internal Nitrogen Pools Shape the Infection of <i>Aureococcus anophagefferens</i> CCMP 1984 by a Giant Virus.

Gann Eric R ER Hughes Brennan J BJ Reynolds Todd B TB Wilhelm Steven W SW

Frontiers in microbiology 20200325

The pelagophyte <i>Aureococcus anophagefferens</i> 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 ...[more]

PMID: 32269558

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Project description:The pelagophyte Aureococcus anophagefferens has caused recurrent brown tide blooms along the northeast coast of the United States since the mid-1980's, and more recently spread to other regions of the globe. These blooms, due to the high cell densities, are associated with severe light attenuation that destroys the sea grass beds which provide the basis for many fisheries. Data collected by transmission electron microscopy, PCR, and metatranscriptomic studies of the blooms, support the hypothesis that large dsDNA viruses play a role in bloom dynamics. While a large (~140 nm) icosahedral virus, with a 371 kbp genome, was first isolated more than a decade ago, the constraints imposed by environmental parameters on bloom infection dynamics by Aureococcus anophagefferens Virus, (AaV) remain unknown. To investigate the role light plays in infection by this virus, we acclimated A. anophagefferens to light intensities of 30 (low), 60 (medium) or 90 μmol photons m-2 s-1 (high) and infected cultures at these irradiance levels. Moreover, we completed light shift experiments where acclimated cultures were exposed to even lower light intensities (0, 5, and 15 μmol photons m-2 s-1) consistent with irradiance found during the peak of the bloom when cell concentrations are highest. The abundance of viruses produced per lytic event (burst size) was lower in the low irradiance acclimated cultures compared to the medium and high acclimated cultures. Transferring infected cultures to more-limiting light availabilities further decreased burst size and increased the length of time it took for cultures to lyse, regardless of acclimation irradiance level. A hypothetical mechanism for the reduced efficiency of the infection cycle in low light due to ribosome biogenesis was predicted from pre-existing transcriptomes. Overall, these studies provide a framework for understanding light effects on infection dynamics over the course of the summer months when A. anophagefferens blooms occur.

Project description:While viruses with distinct phylogenetic origins and different nucleic acid types can infect and lyse eukaryotic phytoplankton, "giant" dsDNA viruses have been found to be associated with important ecological processes, including the collapse of algal blooms. However, the molecular aspects of giant virus-host interactions remain largely unknown. Aureococcus anophagefferens virus (AaV), a giant virus in the Mimiviridae clade, is known to play a critical role in regulating the fate of brown tide blooms caused by the pelagophyte Aureococcus anophagefferens. To understand the physiological response of A. anophagefferens CCMP1984 upon AaV infection, we studied the transcriptomic landscape of this host-virus pair over an entire infection cycle using a RNA-sequencing approach. A massive transcriptional response of the host was evident as early as 5 min post-infection, with modulation of specific processes likely related to both host defense mechanism(s) and viral takeover of the cell. Infected Aureococcus showed a relative suppression of host-cell transcripts associated with photosynthesis, cytoskeleton formation, fatty acid, and carbohydrate biosynthesis. In contrast, host cell processes related to protein synthesis, polyamine biosynthesis, cellular respiration, transcription, and RNA processing were overrepresented compared to the healthy cultures at different stages of the infection cycle. A large number of redox active host-selenoproteins were overexpressed, which suggested that viral replication and assembly progresses in a highly oxidative environment. The majority (99.2%) of annotated AaV genes were expressed at some point during the infection cycle and demonstrated a clear temporal-expression pattern and an increasing relative expression for the majority of the genes through the time course. We detected a putative early promoter motif for AaV, which was highly similar to the early promoter elements of two other Mimiviridae members, indicating some degree of evolutionary conservation of gene regulation within this clade. This large-scale transcriptome study provides insights into the Aureococcus cells infected by a giant virus and establishes a foundation to test hypotheses regarding metabolic and regulatory processes critical for AaV and other Mimiviridae members.

Dataset Information

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

Publications

Internal Nitrogen Pools Shape the Infection of <i>Aureococcus anophagefferens</i> CCMP 1984 by a Giant Virus.

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