Abstract
ABSTRACTPrasinoviruses are large DNA viruses that infect diverse genera of green microalgae worldwide in aquatic ecosystems, but molecular knowledge of their life cycles is lacking. Several complete genomes of both these viruses and their marine algal hosts are now available and have been used to show the pervasive presence of these species in microbial metagenomes. We have analyzed the life cycle of Ostreococcus tauri virus 5 (OtV5), a lytic virus, using transcriptome sequencing (RNA-Seq) from 12 time points of healthy or infected Ostreococcus tauri cells over a day/night cycle in culture. In the day, viral gene transcription remained low while host nitrogen metabolism gene transcription was initially strongly repressed for two successive time points before being induced for 8 h, but during the night, viral transcription increased steeply while host nitrogen metabolism genes were repressed and many host functions that are normally reduced in the dark appeared to be compensated either by genes expressed from the virus or by increased expression of a subset of 4.4% of the host's genes. Some host cells underwent lysis progressively during the night, but a larger proportion were lysed the following morning. Our data suggest that the life cycles of algal viruses mirror the diurnal rhythms of their hosts.IMPORTANCE Prasinoviruses are common in marine environments, and although several complete genomes of these viruses and their hosts have been characterized, little is known about their life cycles. Here we analyze in detail the transcriptional changes occurring over a 27-h-long experiment in a natural diurnal rhythm, in which the growth of host cells is to some extent synchronized, so that host DNA replication occurs late in the day or early in the night and cell division occurs during the night. Surprisingly, viral transcription remains quiescent over the daytime, when the most energy (from light) is available, but during the night viral transcription activates, accompanied by expression of a few host genes that are probably required by the virus. Although our experiment was accomplished in the lab, cyclical changes have been documented in host transcription in the ocean. Our observations may thus be relevant for eukaryotic phytoplankton in natural environments.
Highlights
Prasinoviruses are large DNA viruses that infect diverse genera of green microalgae worldwide in aquatic ecosystems, but molecular knowledge of their life cycles is lacking
Several previous detailed reports on the life cycles of large DNA viruses infecting green microalgae have been done in continuous illumination [9, 32,33,34,35,36], which promotes rapid growth of the host and virus, but since all of these algae have evolved in a diurnal cycle, we decided to perform this study in a 12-h light and 12-h dark “day” and “night” cycle
Under these conditions, the general pattern of gene transcription is quite different in the daytime, when photosynthesis is in progress, and at night, when stored energy is being used, this rhythm being observed both in the laboratory [37] and in the environment [38]
Summary
Prasinoviruses are large DNA viruses that infect diverse genera of green microalgae worldwide in aquatic ecosystems, but molecular knowledge of their life cycles is lacking. The Mamiellophyceae is a class of eukaryotic unicellular green algae whose phylogenetically diverse members have been successful in colonizing the world’s oceans [1, 2] Their tiny cell sizes [3], global dispersion, and ease of laboratory culture [4, 5] render them attractive as models for interdisciplinary studies in marine biology. The complete genomes of several species in the genera Ostreococcus, Bathycoccus, and Micromonas have been characterized [6], permitting their detection in metagenomic data collected in microbial fractions of environmental seawater fractions [1] Numerous species in this group of algae are infected by prasinoviruses [1, 7], large double-stranded DNA (dsDNA) viruses in the family Phycod-. The best-characterized of these are Paramecium bursaria Chlorella virus 1 (PBCV-1), a species infecting freshwater Chlorella, which is a symbiont of the ciliate Paramecium bursaria [18], and Emiliania huxleyi viruses [19], which infect the marine haptophyte unicellular alga Emiliania huxleyi, well known for its extensive oceanic blooms
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
