Diel cycling and long-term persistence of viruses in the ocean's euphotic zone

Abstract

Viruses are fundamental components of marine microbial communities that significantly influence oceanic productivity, biogeochemistry, and ecosystem processes. Despite their importance, the temporal activities and dynamics of viral assemblages in natural settings remain largely unexplored. Here we report the transcriptional activities and variability of dominant dsDNA viruses in the open ocean's euphotic zone over daily and seasonal timescales. While dsDNA viruses exhibited some fluctuation in abundance in both cellular and viral size fractions, the viral assemblage was remarkably stable, with the most abundant viral types persisting over many days. More extended time series indicated that long-term persistence (>1 y) was the rule for most dsDNA viruses observed, suggesting that both core viral genomes as well as viral community structure were conserved over interannual periods. Viral gene transcription in host cell assemblages revealed diel cycling among many different viral types. Most notably, an afternoon peak in cyanophage transcriptional activity coincided with a peak in Prochlorococcus DNA replication, indicating coordinated diurnal coupling of virus and host reproduction. In aggregate, our analyses suggested a tightly synchronized diel coupling of viral and cellular replication cycles in both photoautotrophic and heterotrophic bacterial hosts. A surprising consequence of these findings is that diel cycles in the ocean's photic zone appear to be universal organizing principles that shape ecosystem dynamics, ecological interactions, and biogeochemical cycling of both cellular and acellular community components.

Keywords: diel cycles; marine bacteriophage; marine virus; oligotrophic gyre; phage gene expression.

Fig. 1.

Abundance and annotation of viral scaffolds recovered over different timescales. (A) Bubble plot of scaffold abundances over the diel time-course reported in this study. Bubble size is proportional to relative abundance of the scaffolds in both the cellular and viral fraction, and the color provides the log₁₀-scaled VC ratio. (B) Bubble plot of scaffold relative abundances in a 1.5-y monthly time-series conducted at Sta. ALOHA, as determined from fragment recruitment analysis. Bubble size is proportional to relative abundance of the scaffolds, and the color provides the average percent identity of the reads mapped. (C) Putative host specificity and taxonomic classifications of the scaffolds are shown in color bars, and scaffold lengths are provided in the bar plot. All scaffolds >15 Kbp in length are shown.

Fig. 2.

Diel timing and abundance of viral transcription. (A) The red line shows average transcripts per liter of total viral transcripts analyzed in this study, with error bars denoting SE. The histogram shows the peak time of aggregate viral transcripts for individual scaffolds, and the dotplot below it provides the peak times of all scaffolds, with significantly diel scaffolds in blue and all other scaffolds in gray. (B) Viral scaffolds abundant in the transcriptomes are shown on the y axis. The shape of the plot denotes the distribution of abundances recovered in all 44 time-points. The x axis shows transcripts per liter. The dotted red lines denote the upper and lower bounds of thresholds of detection. Colored dots next to the scaffolds denote putative host designations and scaffolds for which significantly diel transcription was determined.

Fig. 3.

Diel synchrony of cyanophage and Prochlorococcus activities. Temporal profiles for diel cyanophage aggregate transcription (red), Prochlorococcus DNA replication and cell division marker gene transcription (green), and two metrics for estimating the timing of Prochlorococcus DNA replication (iRep and bPTR; blue). Units for the transcriptional profiles are ×10⁵ transcripts per L. Night-time periods are shaded gray.