Cargando…

Closely related viruses of the marine picoeukaryotic alga Ostreococcus lucimarinus exhibit different ecological strategies

In marine ecosystems, viruses are major disrupters of the direct flow of carbon and nutrients to higher trophic levels. Although the genetic diversity of several eukaryotic phytoplankton virus groups has been characterized, their infection dynamics are less understood, such that the physiological an...

Descripción completa

Detalles Bibliográficos
Autores principales: Zimmerman, Amy E., Bachy, Charles, Ma, Xiufeng, Roux, Simon, Jang, Ho Bin, Sullivan, Matthew B., Waldbauer, Jacob R., Worden, Alexandra Z.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley & Sons, Inc. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6851583/
https://www.ncbi.nlm.nih.gov/pubmed/30924271
http://dx.doi.org/10.1111/1462-2920.14608
_version_ 1783469649405411328
author Zimmerman, Amy E.
Bachy, Charles
Ma, Xiufeng
Roux, Simon
Jang, Ho Bin
Sullivan, Matthew B.
Waldbauer, Jacob R.
Worden, Alexandra Z.
author_facet Zimmerman, Amy E.
Bachy, Charles
Ma, Xiufeng
Roux, Simon
Jang, Ho Bin
Sullivan, Matthew B.
Waldbauer, Jacob R.
Worden, Alexandra Z.
author_sort Zimmerman, Amy E.
collection PubMed
description In marine ecosystems, viruses are major disrupters of the direct flow of carbon and nutrients to higher trophic levels. Although the genetic diversity of several eukaryotic phytoplankton virus groups has been characterized, their infection dynamics are less understood, such that the physiological and ecological implications of their diversity remain unclear. We compared genomes and infection phenotypes of the two most closely related cultured phycodnaviruses infecting the widespread picoprasinophyte Ostreococcus lucimarinus under standard‐ (1.3 divisions per day) and limited‐light (0.41 divisions per day) nutrient replete conditions. OlV7 infection caused early arrest of the host cell cycle, coinciding with a significantly higher proportion of infected cells than OlV1‐amended treatments, regardless of host growth rate. OlV7 treatments showed a near‐50‐fold increase of progeny virions at the higher host growth rate, contrasting with OlV1's 16‐fold increase. However, production of OlV7 virions was more sensitive than OlV1 production to reduced host growth rate, suggesting fitness trade‐offs between infection efficiency and resilience to host physiology. Moreover, although organic matter released from OlV1‐ and OlV7‐infected hosts had broadly similar chemical composition, some distinct molecular signatures were observed. Collectively, these results suggest that current views on viral relatedness through marker and core gene analyses underplay operational divergence and consequences for host ecology.
format Online
Article
Text
id pubmed-6851583
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher John Wiley & Sons, Inc.
record_format MEDLINE/PubMed
spelling pubmed-68515832019-11-18 Closely related viruses of the marine picoeukaryotic alga Ostreococcus lucimarinus exhibit different ecological strategies Zimmerman, Amy E. Bachy, Charles Ma, Xiufeng Roux, Simon Jang, Ho Bin Sullivan, Matthew B. Waldbauer, Jacob R. Worden, Alexandra Z. Environ Microbiol Research Articles In marine ecosystems, viruses are major disrupters of the direct flow of carbon and nutrients to higher trophic levels. Although the genetic diversity of several eukaryotic phytoplankton virus groups has been characterized, their infection dynamics are less understood, such that the physiological and ecological implications of their diversity remain unclear. We compared genomes and infection phenotypes of the two most closely related cultured phycodnaviruses infecting the widespread picoprasinophyte Ostreococcus lucimarinus under standard‐ (1.3 divisions per day) and limited‐light (0.41 divisions per day) nutrient replete conditions. OlV7 infection caused early arrest of the host cell cycle, coinciding with a significantly higher proportion of infected cells than OlV1‐amended treatments, regardless of host growth rate. OlV7 treatments showed a near‐50‐fold increase of progeny virions at the higher host growth rate, contrasting with OlV1's 16‐fold increase. However, production of OlV7 virions was more sensitive than OlV1 production to reduced host growth rate, suggesting fitness trade‐offs between infection efficiency and resilience to host physiology. Moreover, although organic matter released from OlV1‐ and OlV7‐infected hosts had broadly similar chemical composition, some distinct molecular signatures were observed. Collectively, these results suggest that current views on viral relatedness through marker and core gene analyses underplay operational divergence and consequences for host ecology. John Wiley & Sons, Inc. 2019-05-13 2019-06 /pmc/articles/PMC6851583/ /pubmed/30924271 http://dx.doi.org/10.1111/1462-2920.14608 Text en © 2019 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd. This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Articles
Zimmerman, Amy E.
Bachy, Charles
Ma, Xiufeng
Roux, Simon
Jang, Ho Bin
Sullivan, Matthew B.
Waldbauer, Jacob R.
Worden, Alexandra Z.
Closely related viruses of the marine picoeukaryotic alga Ostreococcus lucimarinus exhibit different ecological strategies
title Closely related viruses of the marine picoeukaryotic alga Ostreococcus lucimarinus exhibit different ecological strategies
title_full Closely related viruses of the marine picoeukaryotic alga Ostreococcus lucimarinus exhibit different ecological strategies
title_fullStr Closely related viruses of the marine picoeukaryotic alga Ostreococcus lucimarinus exhibit different ecological strategies
title_full_unstemmed Closely related viruses of the marine picoeukaryotic alga Ostreococcus lucimarinus exhibit different ecological strategies
title_short Closely related viruses of the marine picoeukaryotic alga Ostreococcus lucimarinus exhibit different ecological strategies
title_sort closely related viruses of the marine picoeukaryotic alga ostreococcus lucimarinus exhibit different ecological strategies
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6851583/
https://www.ncbi.nlm.nih.gov/pubmed/30924271
http://dx.doi.org/10.1111/1462-2920.14608
work_keys_str_mv AT zimmermanamye closelyrelatedvirusesofthemarinepicoeukaryoticalgaostreococcuslucimarinusexhibitdifferentecologicalstrategies
AT bachycharles closelyrelatedvirusesofthemarinepicoeukaryoticalgaostreococcuslucimarinusexhibitdifferentecologicalstrategies
AT maxiufeng closelyrelatedvirusesofthemarinepicoeukaryoticalgaostreococcuslucimarinusexhibitdifferentecologicalstrategies
AT rouxsimon closelyrelatedvirusesofthemarinepicoeukaryoticalgaostreococcuslucimarinusexhibitdifferentecologicalstrategies
AT janghobin closelyrelatedvirusesofthemarinepicoeukaryoticalgaostreococcuslucimarinusexhibitdifferentecologicalstrategies
AT sullivanmatthewb closelyrelatedvirusesofthemarinepicoeukaryoticalgaostreococcuslucimarinusexhibitdifferentecologicalstrategies
AT waldbauerjacobr closelyrelatedvirusesofthemarinepicoeukaryoticalgaostreococcuslucimarinusexhibitdifferentecologicalstrategies
AT wordenalexandraz closelyrelatedvirusesofthemarinepicoeukaryoticalgaostreococcuslucimarinusexhibitdifferentecologicalstrategies