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

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 sug...

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Autores principales: Gann, Eric R., Hughes, Brennan J., Reynolds, Todd B., Wilhelm, Steven W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7109300/
https://www.ncbi.nlm.nih.gov/pubmed/32269558
http://dx.doi.org/10.3389/fmicb.2020.00492
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author Gann, Eric R.
Hughes, Brennan J.
Reynolds, Todd B.
Wilhelm, Steven W.
author_facet Gann, Eric R.
Hughes, Brennan J.
Reynolds, Todd B.
Wilhelm, Steven W.
author_sort Gann, Eric R.
collection PubMed
description 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 [Formula: see text] 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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spelling pubmed-71093002020-04-08 Internal Nitrogen Pools Shape the Infection of Aureococcus anophagefferens CCMP 1984 by a Giant Virus Gann, Eric R. Hughes, Brennan J. Reynolds, Todd B. Wilhelm, Steven W. Front Microbiol Microbiology 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 [Formula: see text] 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. Frontiers Media S.A. 2020-03-25 /pmc/articles/PMC7109300/ /pubmed/32269558 http://dx.doi.org/10.3389/fmicb.2020.00492 Text en Copyright © 2020 Gann, Hughes, Reynolds and Wilhelm. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Gann, Eric R.
Hughes, Brennan J.
Reynolds, Todd B.
Wilhelm, Steven W.
Internal Nitrogen Pools Shape the Infection of Aureococcus anophagefferens CCMP 1984 by a Giant Virus
title Internal Nitrogen Pools Shape the Infection of Aureococcus anophagefferens CCMP 1984 by a Giant Virus
title_full Internal Nitrogen Pools Shape the Infection of Aureococcus anophagefferens CCMP 1984 by a Giant Virus
title_fullStr Internal Nitrogen Pools Shape the Infection of Aureococcus anophagefferens CCMP 1984 by a Giant Virus
title_full_unstemmed Internal Nitrogen Pools Shape the Infection of Aureococcus anophagefferens CCMP 1984 by a Giant Virus
title_short Internal Nitrogen Pools Shape the Infection of Aureococcus anophagefferens CCMP 1984 by a Giant Virus
title_sort internal nitrogen pools shape the infection of aureococcus anophagefferens ccmp 1984 by a giant virus
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7109300/
https://www.ncbi.nlm.nih.gov/pubmed/32269558
http://dx.doi.org/10.3389/fmicb.2020.00492
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